search references by typing your topic here:

 

OptiPrep™ Reference List RV01

GROUP I VIRUSES

• The seven groups of the Baltimore classification system are defined by the type of viral genome and the replication method. Each group contains a variety of virus types defined by structural and biological features. The OptiPrep™ reference lists are based on the Baltimore system; within each group, viruses are listed alphabetically according to family, genus and species. Where necessary, references are further divided alphabetically according to research topic/sub-topic. 
• Publications are listed alphabetically by first author. ™Multiple entries from the same first author are listed chronologically.
• For detailed methodologies of Group I virus purfication see OptiPrep™ Application Sheets V07-V13. V06 is a methodological review of OptiPrep™ technology.

1 Adenoviridae
1a Adenovirus and adeno-associated virus

Aoki, N., Yamaguchi, S., Kitajima, T., Takehara, A., Katagari-Nakagawa, S., Matsui, R., Watanabe, D., Matsushima, T. and Homma, K.J. (2015) Critical role of the neural pathway from the intermediate medial mesopallium to the intermediate hyperpallium apicale in filial imprinting of domestic chicks (Gallus gallus domesticus) Neuroscience, 308, 115–124

Catani, J.P.P., Medrano, R.F.V., Hunger, A., Del Valle, P., Adjemian, S., Bertolini Zanatta, D., Kroemer, G., Costanzi-Strauss, E. and Strauss, B.E. (2016) Intratumoral immunization by p19Arf and interferon-β gene transfer in a heterotopic mouse model of lung carcinoma Translat. Oncol., 9, 565–574

De Luna Vieira, I., Tamura, R.E., Hunger, A. and Strauss, B.E. (2019) Distinct roles of direct transduction versus exposure to the tumor secretome on murine endothelial cells after melanoma gene therapy with interferon-β and p19Arf J. Interferon Cytokine Res., 39, 246-258

Dormond, E., Chahal, P., Bernier, A., Tran, R., Perrier, M. and Kamen, A. (2010) An efficient process for the purification of helper-dependent adenoviral vector and removal of helper virus by iodixanol ultracentrifugation J. Virol. Meth., 165, 83-89

El-Andaloussi, N., Bonifati, S., Kaufmann, J.K., Mailly, L., Daeffler, L., Deryckère, F., Nettelbeck, D.M., Rommelaere, J. and Marchini, A. (2012) Generation of an adenovirus-parvovirus chimera with enhanced oncolytic potential J. Virol., 86, 10418-10431

Farquhar, M.J., Harris, H.J., Diskar, M., Jones, S., Mee,, C.J., Nielsen, S.U., Brimacombe C.L., Molina, S., Toms, G.L. et al (2008) Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity J. Virol., 82, 8797-8811

Giacca, M. and Zacchigna, S. (2012) Virus-mediated gene delivery for human gene therapy J. Control. Release, 161, 377–388

Giménez-Alejandre, M., Gros, A. and Alemany, R. (2011) Construction of capsid-modified adenoviruses by recombination in yeast and purification by iodixanol-gradient In Methods Mol. Biol., 797, Oncolytic Viruses: Methods and Protocols, (ed. Kirn, D.H. et al.), Springer Science+Business Media, pp 21-34

Houldcroft, C.J., Roy, S., Morfopoulou, S., Margetts, B.K., Depledge, D.P., Cudini, J., Shah, D., Brown, J.R. et al (2018) Use of whole-genome sequencing of adenovirus in immunocompromised pediatric patients to identify nosocomial transmission and mixed-genotype infection J. Infect. Dis., 218, 1261-1271

Koivisto, E., Acosta, A.J., Moilanen, A-M., Tokola, H., Aro, J., Pennanen, H., Sakkinen, H., Käikkonen, L., Ruskoaho, H. and Rysä, J. (2014) Characterization of the regulatory mechanisms of activating transcription factor 3 by hypertrophic stimuli in rat cardiomyocytes PLoS One, 9: e105168

Laborda, E., Puig-Saus, C., Cascalló, M., Chillón, M. and Alemany, R. (2013) Adeno-associated virus enhances wild-type and oncolytic adenovirus spread Hum. Gene Ther. Methods 24, 372–380

Le Lay, S., Hajduch, E., Lindsay, M.R., Le Lièpvre, X., Thiele, C., Ferré, P., Parton, R.G., Kurzchalia, T., Simons, K. and Dugail, I. (2006) Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis Traffic, 7, 549-561

Mak, G.Z., Kavanaugh, G.M., Buschmann, M.M., Stickley, S.M., Koch, M., Goss, K.H., Waechter, H., Zuk, A. and Matlin, K.S. (2006) Regulated synthesis and functions of laminin 5 in polarized Madin-Darby canine kidney epithelial cells Mol. Biol. Cell, 17, 3664-3677

Manninen, A., Verkade, P., Le Jay, S., Torkko, J., Kasper, M., Fullerkrug, J. and Simons, K. (2005) Caveolin-1 is not essential for biosynthetic apical membrane transport Mol. Cell. Biol., 25, 10087-10096

Matsui, R., Tanabe, Y. and Watanabe, D. (2012) Avian adeno-associated virus vector efficiently transduces neurons in the embryonic and post-embryonic chicken brain PLoS One 7: e48730

Moilanen, A-M., Rysä, J., Kaikkonen, L., Karvonen, T., Mustonen, E., Serpi, R., Szabó, Z., Tenhunen, O., Bagyura, Z., et al (2015) WDR12, a member of nucleolar PeBoW complex, is up-regulated in failing hearts and causes deterioration of cardiac function PLoS One, 10: e0124907

Muretta, J.M., Romenskaia, I., Cassiday, P.A. and Mastick, C.C. (2007) Expression of a synapsin Iib site phosphorylation mutant in 3T3-L1 adipocytes inhibits basal intracellular retention of Glut4 J. Cell Sci., 120, 1168-1177

Musick, M.A., McConnell, K.I., Lue, J.K., Wei, F., Chen, C. and Suh, J. (2011) Reprogramming virus nanoparticles to bind metal ions upon activation with heat Biomacromolecules, 12, 2153–2158

Okada, H., Iizuka, T., Mochizuki, H., Nihira, T., Kamiya, K., Inoshita, A., Kasagi, H., Kasai, M. and Ikeda, K. (2012) Gene transfer targeting mouse vestibule using adenovirus and adeno-associated virus vectors Otol. Neurotol., 33, 655-659

Peng, H.H., Wu, S., Davis, J.J., Wang, L., Roth, J.A., Marini III, F.C. and Fang, B. (2006) A rapid and efficient method for purification of recombinant adenovirus with arginine–glycine–aspartic acid-modified fibers Anal. Biochem., 354, 140-147

Pozzuto, T., von Kietzell, K., Bock, T., Schmidt-Lucke, C., Poller, W., Zobel, T., Lassner, D., Zeichhardt, H. Weger, S. and Fechner, H. (2011) Transactivation of human parvovirus B19 gene expression in endothelial cells by adenoviral helper functions Virology 411, 50–64

Rognoni, E., Widmaier, M., , C., Mantwill, K., Holzmüller, R., Gansbacher, B., Kolk, A., Schuster, T., Schmid, R.M., Saur, D., Kaszubiak, A., Lage, H. and Holm, P.S. (2009) Adenovirus-based virotherapy enabled by cellular YB-1 expression in vitro and in vivo Cancer Gene Ther., 16, 753–763

Schaar, K., Geisler, A., Kraus, M., Pinkert, S., Pryshliak, M., Spencer, J.F., Tollefson, A.E., Ying, B. et al (2017) Anti-adenoviral artificial microRNAs expressed from AAV9 vectors inhibit human adenovirus infection in immunosuppressed Syrian hamsters Mol. Ther. Nucleic Acids, 8, 300-316

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

Sharon, D. and Kamen, A. (2018) Advancements in the design and scalable production of viral gene transfer vectors Biotech. Bioeng., 115, 25–40

Sztacho, M., Segeletz, S., Sanchez-Fernandez, M.A., Czupalla, C., Niehage, C. and Hoflack, B. (2016) BAR proteins PSTPIP112 regulate podosome dynamics and the resorption activity of osteoclasts PLoS One, 11, e0164829

Tamura, R.E., Hunger, A., Fernandes, D.C., Laurindo, F.R., Costanzi-Strauss, E. and Strauss, B.E. (2017) Induction of oxidants distinguishes susceptibility of prostate carcinoma cell lines to p53 gene transfer mediated by an improved adenoviral vector Hum. Gene Ther., 28, 639-653

Wu, P., Kudrolli, T.A., Chowdhury, W.H., Liu, M.M., Rodriguez, R. and Lupold, S.E. (2010) Adenovirus targeting to prostate-specific membrane antigen through virus-displayed, semirandom peptide library screening Cancer Res; 70, 9549–9553

Zou, X-H., Bib, Z-X., Guo, X-J., Zhang, Z., Zhao, Y., Wang, M., Zhu, Y-L., Jie, H-Y. et al (2018) DNA assembly technique simplifies the construction of infectious clone of fowl adenovirus J. Virol. Meth., 257, 85–92

2 Asfaviridae
2a African swine fever virus

Lithgow, P., Takamatsu, H., Werling, D., Dixon, L. and Chapman, D. (2014) Correlation of cell surface marker expression with African swine fever virus infection Vet. Microbiol., 168, 413-419

Zhang, F., Hopwood, P., Abrams, C.C., Downing, A., Murray, F., Talbot, R., Archibald, A., Lowden, S. and Dixon, L.K. (2006) Macrophage transcriptional responses following in vitro infection with a highly virulent African swine fever isolate J. Virol., 80, 10514-10521

2b Faustovirus

Klose, T., Reteno, D.G., Benamar, S., Hollerbach, A., Colson, P., La Scola, B. and Rossmann, M.G. (2016) Structure of faustovirus, a large dsDNA virus Proc. Natl. Acad. Sci. USA, 113, 6206-6211

3. Baculoviridae
Baculovirus vectors

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

Strauss, R., Hüser, A., Ni, S., Tuve, S., Kiviat, N., Sow, P.S., Hofmann, C. and Lieber, A. (2007) Baculovirusbased vaccination vectors allow for efficient induction of immune responses against Plasmodium falciparum circumsporozoite protein Mol. Ther., 15, 193-202

Thompson, C.M., Aucoin, M.G. and Kamen, A.A. (2016) Production of virus-like particles for vaccination In Baculovirus and Insect Cell Expression Protocols, Methods in Molecular Biology, vol. 1350 (ed. Murhammer, D.W.) Springer Science+Business Media New York, pp 3299-315

Wang, Q., Bosch, B-J., Vlak, J.M., van Oers, M.M., Rottier, P.J. and van Lent, J.W.M. (2016) Budded baculovirus particle structure revisited J. Invertebr. Pathol., 134, 15–22

4. Herpesviridae
4a. Cytomegalovirus

Poglitsch, M., Weichhart, T., Hecking, M., Werzowa, J., Katholnig, K., Antlanger, M., Krmpotic, A., Jonjic, S., Hörla, W.H., Zlabinger, J.G., Puchhammer, E. and Säemanna, M.D. (2012) CMV late phase-induced mTOR activation is essential or efficient virus replication in polarized human macrophages Am. J. Transplant., 12, 1458–1468

Rupp, B., Ruzsics, Z., Sacher, T. and Koszinowski, U.H. (2005) Conditional cytomegalovirus replication in vitro and in vivo J. Virol., 79, 486-494

Tsen, S-W.D., Kingsley, D.H., Poweleit, C., Achilefu, S., Soroka, D.S., Wu, T.C. and Tsen, K-T. (2014) Studies of inactivation mechanism of non-enveloped icosahedral virus by a visible ultrashort pulsed laser Virol. J., 11: 20

4b. Epstein-Barr virus

Campion, E.M., Hakimjavadi, R., Loughran, S.T., Phelan, S., Smith, S.M., D’Souza, B.N., Tierney, R.J., Bell, A.I., Cahill, P.A. and Walls, D. (2014) Repression of the proapoptotic cellular BIK/NBK bene by Epstein-Barr virus antagonizes transforming growth factor 1-induced B cell apoptosis J. Virol., 88, 5001–5013

Fitzsimmons, L., Bell, A. and Rowe, M., Tierney, R.J., Shannon-Lowe, C.D., (2015) Unexpected patterns of Epstein–Barr virus transcription revealed by a High throughput PCR array for absolute quantification of viral mRNA Virology 474, 117–130

Hernando, H., 1, Islam, A.B.M.M.K., Rodríguez-Ubreva, J., Forné, I., Ciudad, L., Imhof, A., Shannon-Lowe, C. and Ballestar, E. (2014) Epstein–Barr virus-mediated transformation of B cells induces global chromatin changes independent to the acquisition of proliferation Nucleic Acids Res., 42, 249–263

Long, H.M., Leese, A.M., Chagoury, O.L., Connerty, S.R., Quarcoopome, J., Quinn, L.L., Shannon-Lowe, C. and Rickinson, A.B. (2011) Cytotoxic CD4+ T cell responses to EBV contrast with CD8 responses in breadth of lytic cycle antigen choice and in lytic cycle recognition J. Immunol., 187, 92–101

Rowe, M., Raithatha, S. and Shannon-Lowe, C. (2014) Counteracting effects of cellular notch and Epstein-Barr virus EBNA2: implications for stromal effects on virus-host interactions J. Virol., 88, 12065–12076

Ruiss, R., Jochum, S., Wanner, G., Reisbach, G., Hammerschmidt, W. and Zeidler, R. (2011) A virus-like particle-based Epstein-Barr virus vaccine J. Virol., 85, 13105–13113

Shannon-Lowe, C., Adland, E., Bell, A.I., Delecluse, H-J., Rickinson, A.B. and Rowe, M. (2009) Features distinguishing Epstein-Barr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance, and genome amplification J. Virol., 83, 7749-7760

Shannon-Lowe, C. and Rowe, M. (2011) Epstein-Barr virus infection of polarized epithelial cells via the basolateral surface by memory B cell-mediated transfer infection Plos Pathog., 5: e1001338

Tierney, R.J., Kao, K-Y., Nagra, J.K. and Rickinson, A.B. (2011) Epstein-Barr virus BamHI W repeat number limits EBNA2/EBNA-LP coexpression in newly infected B cells and the efficiency of B-cell transformation: a rationale for the multiple W repeats in wild-type virus strains J. Virol., 85, 12362–12375

Tierney, R.J., Nagra, J., Rowe, M., Bell, A.I. and Rickinson, A.B. (2015) The Epstein-Barr virus BamHI C promoter is not essential for B cell immortalization in vitro, but it greatly enhances B cell growth transformation J. Virol., 89, 2483-2493

4c. Herpes simplex virus

Angiogenesis
Arafat, W.O., Casado, E., Wang, M., Alvarez, R.D., Siegal, G.P., Glorioso, J.C., Curiel, D.T. and GomezNavarro, J. (2000) Genetically modified CD34+ cells exert a cytotoxic bystander effect on human endothelial and cancer cells Clin. Cancer Res., 6, 4442-4448

Berto, E., Bozac, A., Volpi, I., Lanzoni, I., Vasquez, F., Melara, N., Manservigi, R. and Marconi, P. (2007) Antitumor effects of non-replicative herpes simplex vectors expressing antiangiogenic proteins and thymidine kinase on Lewis lung carcinoma establishment and growth Cancer Gene Ther., 14, 791-801

Gomez-Navarro, J.L., Contreras, J.L., Arafat, W., Jiang, X.L., Krisky, D., Oligino, T., Marconi, P., Hubbard, B., Glorioso, J.C., Curiel, D.T. and Thomas, J.M. (2000) Genetically modified CD34+ cells as cellular vehicles for gene delivery into areas of angiogenesis in a rhesus model Gene Ther., 7, 43-52

Shah, A.C., Price, K.H., Parker, J.N., Samuel, S.L., Meleth, S., Cassady, K.A., Gillespie, G.Y., Whitley, R.J. and Markert, J.M. (2006) Serial passage through human glioma xenografts selects for a 134.5 herpes simplex virus type 1 mutant that exhibits decreased neurotoxicity and prolongs survival of mice with experimental brain tumors J. Virol., 80, 7308-7315

Anti-neoplastic agents
Cassady, K.A., Bauer, D.F., Roth, J., Chambers, M.R., Shoeb, T., Coleman, J., Prichard, M., Gillespie, Y. and Markert, J.M. (2017) Pre-clinical Assessment of C134, a chimeric oncolytic herpes simplex virus, in mice and non-human primates Mol. Ther. Oncolytics, 5, 1-10

Assembly/cell interactions
Bosse, J.B., Bauerfeind, R., Popilka, L., Marcinowski, L., Taeglich, M., Jung, C., Striebinger, H. et al (2012) A beta-herpesvirus with fluorescent capsids to study transport in living cells PLoS One, 7: e40585

Jambunathan, N., Chowdhury, S., Subramanian, R., Chouljenko, V.N., Walker, J.D. and Kousoulas, K.G. (2011) Site-specific proteolytic cleavage of the amino terminus of herpes simplex virus glycoprotein K on virion particles inhibits virus entry J. Virol., 85, 12910–12918

Jambunathan, N., Charles, A-S., Subramanian, R., Saied, A.A., Naderi, M., Rider, P., Brylinski, M., Chouljenko, V.N. and Kousoulas, K.G. (2016) Deletion of a predicted -sheet domain within the amino terminus of herpes simplex virus glycoprotein K conserved among alphaherpesviruses prevents virus entry into neuronal axons J. Virol., 90, 2230-2239

Exosome secretion profiles
Heikkilä, O., Ryödi, E. and Hukkanen, V. (2016) The 134.5 neurovirulence gene of herpes simplex virus 1 modifies the exosome secretion profile in epithelial cells J. Virol., 90, 10981-10984

Gene expression/therapy
Goins, W.F., Huang, S., Hall, B., Marzulli, M., Cohen, J.B. and Glorioso, J.C. (2020) Engineering HSV-1 Vectors for Gene Therapy In Herpes Simplex Virus: Methods and Protocols, in Methods in Mol. Biol., vol. 2060 (Diefenbach, R.J. and Fraefel, C, eds.20 Springer Science+Business Media LLC New York, pp 73-90

Musarrat, F., Jambunathan, N., Rider, P.J.F., Chouljenko, V.N. and Kousoulas, K.G. (2018) The amino terminus of herpes simplex virus 1 glycoprotein K (gK) is required for gB binding to Akt, release of intracellular calcium, and fusion of the viral envelope with plasma membranes J. Virol., 92: e01842-17

St. Leger, A.J., Peters, B., Sidney, J., Sette, A. and Hendricks, R.L. (2011) Defining the herpes simplex virusspecific CD8+ T cell repertoire in C57BL/6 mice J. Immunol., 186, 3927–3933

Glycoprotein K
Jambunathan, N., Charles, A-S., Subramanian, R., Saied, A.A., Naderi, M., Rider, P., Brylinski, M., Chouljenko, V.N. and Kousoulas, K.G. (2016) Deletion of a predicted -sheet domain within the amino terminus of herpes simplex virus glycoprotein K conserved among alphaherpesviruses prevents virus entry into neuronal axons J. Virol., 90, 2230-2239

HIV infection, in

Caselli, E., Galavan, M., Cassai, E., Caruso, A., Sighinolfi, L. and Di Luca, D. (2005) Human herpesvirus 8 enhances human immunodeficiency virus replication in acutely infected cells and induces reactivation in latently infected cells Blood, 106, 2790-2797

HLA modification
Caselli, E., Campioni, D., Cavazzini, F., Gentili, V., Bortolotti, D., Cuneo, A., Di Luca, D. and Rizzo, R. (2015) Acute human herpesvirus-6A infection of human mesothelial cells modulates HLA molecules Arch. Virol., 160, 2141–2149

Host cell proteins
Hammarstedt, M., Ahlqvist, J., Jacobson, S., Garoff, H. and Fogdell-Hahn, A. (2007) Purification of infectious human herpesvirus 6A virions and association of host cell proteins Virol J. 4:101

Immunosurveillance
Frank, G.M., Lepisto, A.J., Freeman, M.L., Sheridan, B.S., Cherpes, T.L. and Hendricks, R.L. (2010) Early CD4+ T cell help prevents partial CD8+ T cell exhaustion and promotes maintenance of herpes simplex virus 1 latency J. Immunol., 184, 277-286

Frank, G.M., Buela, K-A.G., Maker, D.M., Harvey, S.A.K. and Hendricks, R.L. (2012) Early responding dendritic cells direct the local NK response to control herpes simplex virus 1 infection within the cornea J. Immunol., 188, 1350–1359

Infectivity studies
Ahlquist, J., Hammarstadt, M., Jacobson, S., Garoff, H. and Fogdell-Hahn, A. (2006) Identification of host cell proteins in purified infectious humanherpesvirus 6A (HHV-6A) viral particles J. Neuroimmunol., 178, Suppl. 1, 114

Avanzi, S., Leoni, V., Rotola, A., Alviano, F., Solimando2, L., Lanzoni, G., Bonsi, L., Di Luca, D., Marchionni, C., Alvisi, G. and Ripalti, A. (2013) Susceptibility of human placenta derived mesenchymal stromal/stem cells to human herpesviruses infection PLoS One, 8: e71412

Becerra-Artiles, A., Santoro, T. and Stern, L.J. (2018) Evaluation of a method to measure HHV-6B infection in vitro based on cell size Virol. J., 15: 4 Bozac, A., Berto, E., Vasquez, F., Grandi, P., Caputo, A., Manservigi, R., Ensoli, B. and Marconi, P. (2006) Expression of human immunodeficiency virus type 1 tat from a replication-deficient herpes simplex type 1 vector induces antigen-specific T cell responses Vaccine, 24, 7148-7158

Caselli, E., Fiorentini, S., Amici, C., Di Luca, D., Caruso, A. and Santoro, M.G. (2007) Human herpesvirus 8 acute infection of endothelial cells induces monocyte chemoattractant protein 1-dependent capillary-like structure formation: role of the IKK/NF-B pathway Blood, 109, 2718-2726

Caselli, E., Campioni, D., Cavazzini, F., Gentili, V., Bortolotti, D., Cuneo, A., Di Luca, D. and Rizzo, R. (2015) Acute human herpesvirus-6A infection of human mesothelial cells modulates HLA molecules Arch. Virol., 160, 2141–2149

Decman, V., Kinchington, P.R., Harvey, S.A. and Hendricks, R.L. (2005) Gamma interferon can block herpes simplex virus type 1 reactivation from latency, even in the presence of late gene expression J. Virol., 79, 10339-10347

Divito, S.J. and Hendricks, R.L. (2008) Activated inflammatory infiltrate in HSV-1-infected corneas without Herpes stromal keratitis Invest. Ophthalmol. Vis. Sci., 49, 1488-1495

Frank, G.M., Buela, K-A.G., Maker, D.M., Harvey, S.A.K. and Hendricks, R.L. (2012) Early responding dendritic cells direct the local NK response to control herpes simplex virus 1 infection within the cornea J. Immunol., 188, 1350–1359

Lepisto, A.J., Frank, G.M., Xu, M., Stuart, P.M. and Hendricks, R.L. (2006) CD8 T cells mediate transient Herpes stromal keratitis in CD4-deficient mice Invest. Ophthalmol. Vis. Sci., 47, 3400-3409

Lepisto, A.J., Xu, M., Yagita, H., Weinberg, A.D. and Hendricks, R.L. (2007) Expression and function of the OX40/OX40L costimulatory pair during herpes stromal keratitis J. Leukoc. Biol., 81, 766-774

Prabhakaran, K., Sheridan, B.S., Kinchington, P.R., Khann, K.M., Decman, V., Lathrop, K. and Hendricks, R.L. (2005) Sensory neurons regulate the effector functions of CD8+ T cells in controlling HSV-1 latency ex vivo Immunity, 23, 515-525

Sheridan, B.S., Khanna, K.M., Frank, G.M. and Hendricks, R.L. (2006) Latent virus influences the generation and maintenance of CD8+ T cell memory J. Immunol., 177, 8356-8364

Sheridan, B.S., Cherpes, T.L., Urban, J., Kalinski, P. and Hendricks, R.L. (2009) Reevaluating the CD8 T-cell response to herpes simplex virus type 1: involvement of CD8 T cells reactive to subdominant epitopes J. Virol., 83, 2237-2245

St. Leger, A.J., Jeon, S. and Hendricks, R.L. (2013) Broadening the repertoire of functional herpes simplex virus type 1–specific CD8+ T cells reduces viral reactivation from latency in sensory ganglia J. Immunol., 191, 2258–2265

Sun, L., St. Leger, A.J., Yu, C-R., He, C., Mahdi, R.M., Chan, C-C., Wang, H., Morse, III, H.C. and Egwuagu, C.E. (2016) Interferon regulator factor 8 (IRF8) limits ocular pathology during HSV-1 infection by restraining the activation and expansion of CD8+ T cells PLoS ONE 11(5): e0155420

Xu, M., Lepisto, A.J. and Hendricks, R.L. (2004) CD154 signaling regulates the Th1 response to herpes simplex virus-1 and inflammation in infected corneas J. Immunol., 173, 1232-1239

Interferon regulatory factor
Sun, L., St. Leger, A.J., Yu, C-R., He, C., Mahdi, R.M., Chan, C-C., Wang, H., Morse, III, H.C. and Egwuagu, C.E. (2016) Interferon regulator factor 8 (IRF8) limits ocular pathology during HSV-1 infection by restraining the activation and expansion of CD8+ T cells PLoS ONE 11(5): e0155420

Karposi’s sarcoma associated
Caselli, E., Fiorentini, S., Amici, C., Di Luca, D., Caruso, A. and Santoro, M.G. (2007) Human herpesvirus 8 acute infection of endothelial cells induces monocyte chemoattractant protein 1-dependent capillary-like structure formation: role of the IKK/NF-B pathway Blood, 109, 2718-2726

Garrigues, H.J., Rubinchikova, Y.E., DiPersio, C. and Rose, T.M. (2008) Integrin Vβ3 binds to the RGD motif of glycoprotein B of Kaposi’s sarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor J. Virol., 82, 1570-1580

Groûkopf,A.K., Ensser, A., Neipel, F., Jungnick, D., Schlagowski, S., Desrosiers, R.C. and Hahn, A.S. (2018) A conserved Eph family receptor-binding motif on the gH/gL complex of Kaposi’s sarcoma-associated herpesvirus and rhesus monkey rhadinovirus PLoS Pathog., 14: e1006912

Hahn, A.S., Kaufmann, J.K., Wies, E., Naschberger, E., Panteleev-Ivlev, J., Schmidt, K., Holzer, A., Schmidt, M., Chen, J. et al (2012) The ephrin receptor tyrosine kinase A2 is a cellular receptor for Kaposi’s sarcoma– associated herpesvirus Nat. Med., 18, 961-966

Muniraju, M., Mutsvunguma, L.Z., Foley, J., Escalante, G.M., Rodriguez, E., Nabiee, R., Totonchy, J., Mulama, D.H., Nyagol, J. et al (2019) Kaposi sarcoma-associated herpesvirus glycoprotein H is indispensable for infection of epithelial, endothelial, and fibroblast cell types J. Virol., 93: e00630-19

Latency, recovery from
Decman, V., Kinchington, P.R., Harvey, S.A. and Hendricks, R.L. (2005) Gamma interferon can block herpes simplex virus type 1 reactivation from latency, even in the presence of late gene expression J. Virol., 79, 10339-10347

Prabhakaran, K., Sheridan, B.S., Kinchington, P.R., Khann, K.M., Decman, V., Lathrop, K. and Hendricks, R.L. (2005) Sensory neurons regulate the effector functions of CD8+ T cells in controlling HSV-1 latency ex vivo Immunity, 23, 515-525

Sheridan, B.S., Khanna, K.M., Frank, G.M. and Hendricks, R.L. (2006) Latent virus influences the generation and maintenance of CD8+
T cell memory J. Immunol., 177, 8356-8364

Sheridan, B.S., Cherpes, T.L., Urban, J., Kalinski, P. and Hendricks, R.L. (2009) Reevaluating the CD8 T-cell response to herpes simplex virus type 1: involvement of CD8 T cells reactive to subdominant epitopes J. Virol., 83, 2237-2245

St. Leger, A.J., Jeon, S. and Hendricks, R.L. (2013) Broadening the repertoire of functional herpes simplex virus type 1–specific CD8+
T cells reduces viral reactivation from latency in sensory ganglia J. Immunol., 191, 2258–2265

Nerve growth factor/neurotrophic factor
Fradette, J., Wolfem D., Goins, W.F., Hunag, S., Flanigan, R.M. and Glorioso, J.C. (2005) HSV vectormediated transduction and GDNF secretion from adipose cells Gene Ther., 12, 48-58

Goins, W.F., Yoshimura, N., Phelan, M.W., Yokoyama, T., Fraser, M.O., Ozawa, H., Bennett, N., de Groat, W.C., Glorioso, J.C. and Chancellor, M.B. (2001) Herpes simplex virus mediated nerve growth factor expression in bladder and affererent neurons: potential treatment for diabetic bladder dysfunction J. Urol., 165, 1748-1754

Glorioso, J.C and Fink, D.J. (2002) Use of HSV vectors to modify the nervous system Curr. Opin. Drug Discov. Dev., 5:2 Marconi, P., Zucchini, S., Berto, E., Bozac, A., Paradiso, B., Bregola, G., Grassi, C., Volpi, I., Argani, R., Marzola, A., Manservigi, R. and Simonato, M. (2005) Effects of defective herpes simplex vectors expressing neurotrophic factors on the proliferation and differentiation of nervous cells in vivo Gene Ther., 12, 559-569

Sasaki K., Chancellor, M.B., Goins, W.F., Phelan, M.W., Glorioso, J.C., de Groat, W.C. and Yoshimura, N. (2004) Gene therapy using replication-defective herpes simplex virus vectors expressing nerve growth factor in a rat model of diabetic cystopathy Diabetes, 53, 2723-2730

Oncolytic viral therapy
Cassady, K.A., Bauer, D.F., Roth, J., Chambers, M.R., Shoeb, T., Coleman, J., Prichard, M., Gillespie, Y. and Markert, J.M. (2017) Pre-clinical Assessment of C134, a chimeric oncolytic herpes simplex virus, in mice and non-human primates Mol. Ther. Oncolytics, 5, 1-10

Ghonime, M.G., Jackson, J., Shah, A., Roth, J., Li, M., Saunders, U., Coleman, J., Gillespie, G.Y., Markert, J.M. and Cassady, K.A. (2018) Chimeric HCMV/HSV-1 and Δγ134.5 oncolytic herpes simplex virus elicit immune mediated antigliomal effect and antitumor memory Translat. Oncol., 11, 86–93

PD-L1 expression (corneal cells)
Jeon S., Rowe, A.M., Carroll, K.L., Harvey, S.A.K. and Hendricks, R.L. (2018) PD-L1/B7-H1 inhibits viral clearance by macrophages in HSV-1–infected corneas J. Immunol., 200, 3711–3719

Stromal keratitis
Divito, S.J. and Hendricks, R.L. (2008) Activated inflammatory infiltrate in HSV-1-infected corneas without Herpes stromal keratitis Invest. Ophthalmol. Vis. Sci., 49, 1488-1495

Frank, G.M., Divito, S.J., Maker, D.M., Xu, M. and Hendricks, R.L. (2010) A novel p40-independent function of IL-12p35 is required for progression and maintenance of herpes stromal keratitis Invest. Ophthalmol. Vis. Sci., 51, 3591–3598

Lepisto, A.J., Frank, G.M., Xu, M., Stuart, P.M. and Hendricks, R.L. (2006) CD8 T cells mediate transient Herpes stromal keratitis in CD4-deficient mice Invest. Ophthalmol. Vis. Sci., 47, 3400-3409

Lepisto, A.J., Xu, M., Yagita, H., Weinberg, A.D. and Hendricks, R.L. (2007) Expression and function of the OX40/OX40L costimulatory pair during herpes stromal keratitis J. Leukoc. Biol., 81, 766-774

Xu, M., Lepisto, A.J. and Hendricks, R.L. (2004) CD154 signaling regulates the Th1 response to herpes simplex virus-1 and inflammation in infected corneas J. Immunol., 173, 1232-1239

Yun, H., Rowe, A.M., Lathrop, K.L., Harvey, S.A.K. amd Hendricks, R.L. (2104) Reversible nerve damage and corneal pathology in murine herpes simplex stromal keratitis J. Virol., 88,. 7870–7880

Suicide gene delivery
Moriuchi, S., Glorioso, J.C., Maruno, M., Izumoto, S., Wolfe, D., Huang, S., Cohen, J.B. and Yoshimine, T. (2005) Combination gene therapy for glioblastoma involving herpes simplex virus vector-mediated codelivery of mutant IB and HSV thymidine kinase Cancer Gene Ther., 12, 487-496 (2005)

Targeting
Argnani, R., Boccafogli, L., Marconi, P.C. and Manservigi, R. (2003) Specific targeted binding of herpes simplex virus type 1 to hepatocytes via the human hepatitis B virus preS1 peptide Gene Ther., 11, 1087-1098

T-cell interactions
Sheridan, B.S., Khanna, K.M., Frank, G.M. and Hendricks, R.L. (2006) Latent virus influences the generation and maintenance of CD8+ T cell memory J. Immunol., 177, 8356-8364

Sheridan, B.S., Cherpes, T.L., Urban, J., Kalinski, P. and Hendricks, R.L. (2009) Reevaluating the CD8 T-cell response to herpes simplex virus type 1: involvement of CD8 T cells reactive to subdominant epitopes J. Virol., 83, 2237-2245

St. Leger, A.J., Peters, B., Sidney, J., Sette, A. and Hendricks, R.L. (2011) Defining the herpes simplex virusspecific CD8+ T cell repertoire in C57BL/6 mice J. Immunol., 186, 3927–3933

Trigeminal ganglia infection
Jeon, S., St. Leger, A.J., Cherpes, T.L., Sheridan, B.S. and Hendricks, R.L. (2013) PD-L1/B7-H1 regulates the survival but not the function of CD8+ T cells in herpes simplex virus type 1 latently infected trigeminal ganglia J. Immunol., 190, 6277–6286

Vaccination
Çuburu, N., Wang, K., Goodman, K.N., Pang, Y.Y., Thompson, C.D., Lowy, D.R., Cohen, J.I. and Schiller, J.T. (2015) Topical herpes simplex virus 2 (HSV-2) vaccination with human papillomavirus vectors expressing gB/gD ectodomains induces genital-tissue-resident memory CD8+ T cells and reduces genital disease and viral shedding after HSV-2 challenge J. Virol., 89, 83-96

Vector construction and gene delivery (see also “Virus production”)
Argnani, R., Boccafogli, L., Marconi, P.C. and Manservigi, R. (2003) Specific targeted binding of herpes simplex virus type 1 to hepatocytes via the human hepatitis B virus preS1 peptide Gene Ther., 11, 1087-1098

Bozac, A., Berto, E., Vasquez, F., Grandi, P., Caputo, A., Manservigi, R., Ensoli, B. and Marconi, P. (2006) Expression of human immunodeficiency virus type 1 tat from a replication-deficient herpes simplex type 1 vector induces antigen-specific T cell responses Vaccine, 24, 7148-7158

Burton, E.A., Huang, S., Goins, W.F. and Glorioso, J.C. (2003) Use of the herpes simplex viral genome to construct gene therapy vectors Methods Mol. Med., 76, 1-31

Fraefel, C., Marconi, P. and Epstein, A.L. (2011) Herpes simplex virus type 1-derived recombinant and amplicon vectors In.Viral Vectors for Gene Therapy: Methods and Protocols (eds Merten, O-W. and Al-Rubeai, M.), Methods Mol. Biol., 737, Springer Science+Business Media, pp 303-343

Goins, W.F., Krisky, D.M., Wolfe, D.P., Fink, D.J. and Glorioso, J.C. (2002) Development of replicationdefective herpes simplex virus vectors Methods Mol. Med., 69, 481-507

GoSharma, N., Flaherty, K., Lezgiyeva, K., Wagner, D.E., Klein, A.M. and Ginty, D.D. (2020) The emergence of transcriptional identity in somatosensory neurons Nature, 392, 392-398ins, W.F., Krisky, D.M., Wechuck,

J.B., Huang, S. and Glorioso, J.C. (2008) Construction and production of recombinant herpes simplex virus vestors In Methods Mol. Biol., 433 Production and in vivo applications of gene transfer (ed. Le Doux, J.M.), Humana Press, Totowa, NJ. pp 97-113

Goss, J.R., Natsume, A., Wolfe, D., mata, M., Glorioso, J.C. and Fink, D. (2004) Delivery of herpes simplex virus-based vectors to the nervous system Methods Mol. Biol., 246, 309-322 (2004)

Marconi, P. and Manservigi, R. (2014) Herpes simplex virus growth, preparation, and assay In Methods Mol. Biol., 1144, Herpes Simplex Virus: Methods and Protocols, (ed. Diefenbach, R.J. and Fraefel, C.) Springer Science+Business Media, New York pp 19-29

Marconi, P., Fraefel, C. and Epstein, A.L. (2015) Herpes simplex virus type 1 (HSV-1)-derived recombinant vectors for gene transfer and gene therapy In Methods in Molecular Biology, 1254 Neuronal Cell Death: Methods and Protocols (ed. Lossi, L. and Merighi,A.) Springer Science+Business Media New York 2015, pp 269-293

Moriuchi, S., Glorioso, J.C., Maruno, M., Izumoto, S., Wolfe, D., Huang, S., Cohen, J.B. and Yoshimine, T. (2005) Combination gene therapy for glioblastoma involving herpes simplex virus vector-mediated codelivery of mutant IB and HSV thymidine kinase Cancer Gene Ther., 12, 487-496 (2005)

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

Virus production
Kang, W., Wang, L., Harrell, H., Liu, J., Thomas, D.L., Mayfield, T.L., Scotti, M.M., Ye, G.J., Veres, G. and Knop, D.R. (2009) An efficient rHSV-based complementation system for the production of multiple rAAV vector serotypes Gene Ther., 16, 229-239

Mistry, A.R., De Alwis, M., Feudner, E., Ali, R.R. and Thrasher, A.J. (2002) High-titer stocks of adenoassociated virus from replicating amplicons and herpes vectors Methods Mol. Med., 69, 445-460

Toublanc, E., Benraiss, A., Bonnin, D., Blouin, V., Brument, N., Cartier, N., Epstein, A.L., Moullier, P. and Salvetti, A. (2004) Identification of a replication-defective herpes simplex virus for recombinant adenoassociated virus type 2 (rAAV2) particle assembly using stable producer cell lines J. Gene Med., 6, 555-564

Sutter, S.O., Marconi, P. and Meier, A.F. (2020) Herpes simplex virus growth, preparation, and assay In Herpes Simplex Virus: Methods and Protocols, in Methods in Mol. Biol., vol. 2060 (Diefenbach, R.J. and Fraefel, C, eds), Springer Science+Business Media LLC New York, pp 57-72

5. Iridoviridae

Jitrakorn, S., Gangnonngiw, W., Bunnontae, M., Manajit, O., Rattanarojpong, T., Chaivisuthangkura, P. Dong, H.T. and Saksmerprome, V. (2020) Infectious cell culture system for concurrent propagation and purification of Megalocytivirus ISKNV and nervous necrosis virus from Asian Sea bass (Lates calcarifer) Aquaculture, 520:734931

Wu, J., Chan, R., Wenk, M.R. and Hew, C-L. (2010) Lipidomic study of intracellular Singapore grouper iridovirus Virology 399, 248–256

6. Mimiviridae

Fridmann-Sirkis, Y., Milrot, E., Mutsafi, Y., Ben-Dor, S., Levin, Y., Savidor, A., Kartvelishvily, E. and Minsky, A. (2016) Efficiency in complexity: composition and dynamic nature of mimivirus replication factories J. Virol., 90, 10039-10047

7. Nimaviridae

Dantas-Lima, J.J., Corteel, M., Cornelissen, M., Bossier, P., Sorgeloos, P. and Nauwynck, H.J. (2013) Purification of white spot syndrome virus by iodixanol density gradient centrifugation J. Fish Dis., 36, 841–851

8. Nudiviridae

Palmer, W.H., Medd, N.C., Beard, P.M. and Obbard, D.J. (2018) Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses PLoS Pathog., 14: e1007050

Palmer, W.H., Joosten, J., Overheul, G.J., Jansen, P.W., Vermeulen, M., Obbard, D.J. and Van Rijc, R.P. (2019) Induction and suppression of NF-κB signalling by a DNA virus of Drosophila J. Virol., 93(3): e01443- 18

9. Rhadinovirus

Bruce, A.G., Bakke, A.M., Gravett, C.A., DeMaster, L.K., Bielefeldt-Ohmann, H., Burnside, K.L. and Rose, T.M. (2009) The ORF59 DNA polymerase processivity factor homologs of Old World primate RV2 rhadinoviruses are highly conserved nuclear antigens expressed in differentiated epithelium in infected macaques Virol. J., 6:205

10. Papillomaviridae

Papillomavirus
B-cell anergy reversal
Chackerian, B., Durfee, M.R. and Schiller, J.T. (2008) Virus-like display of a neo-self antigen reverses B cell anergy in a B cell receptor transgenic mouse model J. Immunol., 180, 5816-5825

Baculoviral vectors
Cho, H., Lee, H-J., Heo, Y-K., Cho, Y., Gwon, Y-D., Kim, M-G., Park, K.H., Oh, Y-K. and Kim, Y.B. (2014) Immunogenicity of a trivalent human papillomavirus L1 DNA-encapsidated, non-replicable baculovirus nanovaccine PLoS One, 9: e95961

Lee, H-J., Hur, Y-K., Cho, Y-D., Kim, M-G., Lee, H-T., Oh, Y-K. and Kim, Y.B. (2012) Immunogenicity of bivalent human papillomavirus DNA vaccine using human endogenous retrovirus envelope-coated baculoviral vectors in mice and pigs PLoS One, 7: e50296

Lee, H-J., Cho, H., Kim, M-G., Heo, Y-K., Cho, Y., Gwon, Y-D., Park, K.H., Jin, H., Kim, J., Oh, Y-K. and Kim, Y.B. (2015) Sublingual immunization of trivalent human papillomavirus DNA vaccine in baculovirus nanovector for protection against vaginal challenge PLoS One, 10: e0119408

Capsids and capsid protein:

Capsid assembly
Day, P.M., Thompson, C.D., Pang, Y.Y., Lowy, D.R. and Schiller, J.T. (2015) Involvement of nucleophosmin (NPM1/B23) in assembly of infectious HPV16 capsids Papillomavirus Res. 1, 74–89

DNA, separation from
Bzhalava, D., Johansson, H., Ekström, J., Faust, H., Möller, B., Eklund, C., Nordin, P., Stenquist, B., Paoli, J., Persson, B., Forslund, O. and Dillner, J. (2013) Unbiased approach for virus detection in skin lesions PLoS One, 8: e65953

Dynein interacting domains
Florin, L., Becker, K.A., Lambert, C., Nowak, T., Sapp, C., Strand, D., Streeck, R.E. and Sapp, M. (2006) Identification of a dynein interacting domain in the papillomavirus minor capsid protein L2 J. Virol., 80, 6691- 6696

L1 capsid protein
Ainouze, M., Rochefort, P., Parroche, P., Roblot, G., Tout, I., Briat, F., Zannetti, C., Marotel, M., Goutagny, N. et al (2018) Human papillomavirus type 16 antagonizes IRF6 regulation of IL-1β PLoS Pathog 14: e1007158

Bienkowska-Haba, M., Williams, C., Kim, S.M., Garcea, R.L. and Sapp, M. (2012) Cyclophilins facilitate dissociation of the human papillomavirus type 16 capsid protein L1 from the L2/DNA complex following virus entry J. Virol., 86, 9875-9887

Ishii, Y., Kondo, K., Matsumoto, T., Tanaka, K., Shinkai-Ouchi, F., Hagiwara, K. and Kanda, T. (2007) Thiolreactive reagents inhibits intracellular trafficking of human papillomavirus type 16 pseudovirions by binding to cysteine residues of major capsid protein L1 Virol. J., 4:110

Mistry, N., Wibom, C. and Evander, M. (2008) Cutaneous and mucosal human papillomaviruses differ in net surface charge, potential impact on tropism Virol. J., 5:118 10

Ryndock, E.J., Conway, M.J., Alam, S., Gul, S., Murad, S., Christensen, N.D. and Meyers, C. (2014) Roles for human papillomavirus type 16 L1 cysteine residues 161, 229, and 379 in genome encapsidation and capsid stability PLoS One, 9: e99488

Maturation
Buck, C.B., Thompson, C.D., Pang, Y-Y-s., Lowy, D.R. and Schiller, J.T. (2005) Maturation of papillomavirus capsids J. Virol., 79, 2839-2846

Cardone, G., Moyer, A.L., Cheng, N., Thompson, C.D., Dvoretzky, I., Lowy, D.R., Schiller, J.T., Steven, A.C., Buck, C.B. and Trus, B.L. (2014) Maturation of the human papillomavirus 16 capsid mBio, 5: e01104-14

Conway, M.J., Cruz, L., Alam, S., Christensen, N.D. and Meyers, C. (2011) Differentiation-dependent interpentameric disulfide bond stabilizes native human papillomavirus type 16 PLoS One, 6: e22427

Neutralization-sensitive epitopes
Culp, T.D., Spatz, C.M., Reed, C.A. and Christensen, N.D. (2007) Binding and neutralization efficiencies of monoclonal antibodies, Fab fragments and scFv specific for L1 epitopes on the capsid of infectious HPV particles Virology, 361, 435-446

Godi, A., Martinelli, M., Haque, M., Li, S., Zhao, Q., Xia, N., Cocuzza, C.E. and Beddows, S. (2018) Impact of naturally occurring variation in the human papillomavirus 58 capsid proteins on recognition by type-specific neutralizing antibodies J. Infect. Dis., 218, 1611-1621

Tumour cell binding
Kines, R.C., Cerio, R.J., Roberts, J.N., Thompson, C.D., de Los Pinos, E., Lowy, D.R. and Schiller, J.T. (2016) Human papillomavirus capsids preferentially bind and infect tumor cells Int. J. Cancer, 138, 901–911

Cell entry/targeting

Autophagy inhibition
Surviladze, Z., Sterk, R.T., DeHaro, S.A. and Ozbun, M.A. (2013) Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy J. Virol., 87, 2508–2517

Clathrin/caveolin
Spoden, G., Freitag, K., Husmann, M., Boller, K., Sapp, M., Lambert, C. and Florin, L. (2008) Clathrin- and caveolin-independent entry of human papillomavirus type 16 – involvement of tetraspanin-enriched microdomains (TEMs) PLoS One, 3:e3313

Cyclophilin receptors
Bienkowska-Haba, M., Patel, H.D. and Sapp, M. (2009) Target cell cyclophilins facilitate human papillomavirus type 16 infection PLoS Pathog., 5:e1000524

Cysteine proteases
Dabydeen, S.A. and Meneses, P.I. (2009) The role of NH4Cl and cysteine proteases in human papillomavirus type 16 infection Virol. J., 6:109

Dynamin inhibition
Abban, C.Y., Bradbury, N.A. and Meneses, P.I. (2008) HPV16 and BPV1 infection can be blocked by the dynamin inhibitor dynasore Am. J. Therapeut., 15, 304-311

Dynein light chain requirement
Schneider, M.A., Spoden, G.A., Florin, L. and Lambert, C. (2011) Identification of the dynein light chains required for human papillomavirus infection Cell. Microbiol., 13, 32–46

Focal adhesion kinase activation
Abban, C.Y. and Meneses, P.I. (2010) Usage of heparan sulfate, integrins, and FAK in HPV16 infection Virology 403, 1–16

Gene delivery vectors
Bayer, L., Gümpel, J., Hause, G., Müller, M. and Grunwald, T. (2018) Non-human papillomaviruses for gene delivery in vitro and in vivo PLoS One, 13: e0198996 11

Cerqueira, C., Thompson, C.D., Day, P.M., Pang, Y-Y.S., Lowy, D.R. and Schiller, J.T. (2017) Efficient production of papillomavirus gene delivery vectors in defined in vitro reactions Mol. Ther. Meth. Clin. Dev., 5, 165-179

Heparan sulphate receptors
Abban, C.Y. and Meneses, P.I. (2010) Usage of heparan sulfate, integrins, and FAK in HPV16 infection Virology 403, 1–16

Day, P.M., Lowy, D.R. and Schiller, J.T. (2008) Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids J. Virol., 82, 12565 12568

Donalisio, M., Rusnati, M., Civra, A., Bugatti, A., Allemand, D., Pirri, G., Giuliani, A., Landolfo, S. and Lembo, D. (2010) Identification of a dendrimeric heparan sulfate-binding peptide that inhibits infectivity of genital types of human papillomaviruses Anitmicrob. Agents Chemother., 54, 4290-4299

Johnson, K.M., Kines, R.C., Roberts, J.N., Lowy, D.R., Schiller, J.T. and Day, P.M. (2009) Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus J. Virol., 83, 2067-2074

Knappe, M., Bodevin, S., Selinka, H-C., Spillman, D., Streeck, R.E., Chen, X.S., Lindahl, U. and Sapp, M. (2007) Surface-exposed amino acid residues of HPV16L1 protein mediating interaction with cell surface heparan sulfate J. Biol. Chem., 282, 27913-27922

Selinka, H-C., Florin, L., Patel, H.D., Freitag, K., Schmidtke, M., Makarov, V.A. and Sapp, M. (2007) Inhibition of transfer to secondary receptors by heparin sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus J. Virol., 81, 10970-10980

Inhibition by thio-reactive agents
Ishii, Y., Kondo, K., Matsumoto, T., Tanaka, K., Shinkai-Ouchi, F., Hagiwara, K. and Kanda, T. (2007) Thiolreactive reagents inhibits intracellular trafficking of human papillomavirus type 16 pseudovirions by binding to cysteine residues of major capsid protein L1 Virol. J., 4:110

Laminin-5 binding
Culp, T.D., Budgeon, L.R., Marinkovich, M.P., Meneguzzi, G. and Christensen, N.D. (2006) Keratinocytesecreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells J. Virol., 80, 8940-8950

L1/L2 protein interactions (incl. asynchronous uptake)
Becker, M., Greune, L., Schmidt, A. and Schelhaas, M. (2018) Extracellular conformational changes in the capsid of human papillomaviruses contribute to asynchronous uptake into host cells J. Virol., 92: e02106-17

Buck, C.B., Cheng, N., Thompson, C.D., Lowy, D.R., Steven, A.C., Schiller, J.T. and Trus, B.L. (2008) Arrangement of L2 within the papillomavirus capsid J. Virol., 82, 5190-5197

Knappe, M., Bodevin, S., Selinka, H-C., Spillman, D., Streeck, R.E., Chen, X.S., Lindahl, U. and Sapp, M. (2007) Surface-exposed amino acid residues of HPV16L1 protein mediating interaction with cell surface heparan sulfate J. Biol. Chem., 282, 27913-27922

Zhang, P., Monteiro da Silva, G., Deatherage, C., Burd, C. and DiMaio, D. (2018) Cell-penetrating peptide mediates intracellular membrane passage of human papillomavirus L2 protein to trigger retrograde trafficking Cell, 175, 1465–1476

Microtubules, L2 interaction with
Schneider, M.A., Spoden, G.A., Florin, L. and Lambert, C. (2011) Identification of the dynein light chains required for human papillomavirus infection Cell. Microbiol., 13, 32–46

Phosphatidylinositol-3 kinase
Surviladze, Z., Sterk, R.T., DeHaro, S.A. and Ozbun, M.A. (2013) Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy J. Virol., 87, 2508–2517

PML expression
Day, P.M., Baker, C.C., Lowy, D.R. and Schiller, J.T. (2004) Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression Proc. Natl. Acad. Sci. USA, 101, 14252-14257

y-Secretase requirement
Huang, H-S., Buck, C.B. and Lambert, P.F. (2010) Inhibition of gamma secretase blocks HPV infection Virology 407, 391–396 12
Karanam, B., Peng, S., Li, T., Buck, C., Day, P.M. and Roden, R.B.S. (2010) Papillomavirus infection requires  secretase J. Virol., 84, 10661–10670

Tetraspannin-enriched domains
Scheffer, K.D., Gawlitza, A., Spoden, G.A., Zhang, X.A., Lambert, C., Berditchevski, F. and Florina, L. (2013) Tetraspanin CD151 mediates papillomavirus type 16 endocytosis J. Virol., 87, 3435–3446

Spoden, G., Freitag, K., Husmann, M., Boller, K., Sapp, M., Lambert, C. and Florin, L. (2008) Clathrin- and caveolin-independent entry of human papillomavirus type 16 – involvement of tetraspanin-enriched microdomains (TEMs) PLoS One, 3:e3313

Epithelial cell, expression in
Israr, M., Biryukov, J., Ryndock, E.J., Alam, S. and Meyers, C. (2016) Comparison of human papilloma-virus type16 replication in tonsil and foreskin epithelia Virology, 499, 82–90

Gene expression
Berg, M., Gambhira, R., Siracusa, M., Hoiczyk, E., Roden, R. and Ketner, G. (2007) HPV16L1 capsid protein expressed from viable adenovirus recombinant elicits neutralizing antibody in mice Vaccine, 25, 3501-3510

Genome

Amplification
Culp, T.D., Cladel, N.M., Balogh, K.K., Budgeon, L.R., Mejia, A.F. and Christensen, N.D. (2006) Papillomavirus particles assembled in 293TT cells are infectious in vivo J. Virol., 80, 11381-11384 (CTR)

Encapsidation
Pyeon, D., Lambert, P.F. and Ahlquist, P. (2005) Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation Proc. Natl. Acad. Sci. USA, 102, 9311-9316

Packaging
Cerqueira, C., Pang, Y-Y.S., Day, P.M., Thompson, C.D., Buck, C.B., Lowy, D.R. and Schiller, J.T. (2016) A cell-free assembly system for generating infectious human papillomavirus 16 capsids implicates a size discrimination mechanism for preferential viral genome packaging J. Virol., 90, 1096-1107

Immunogenicity
Kwag, H-L., Kim, H.J., Chang, D.Y. and Kim, H-J. (2012) The production and immunogenicity of human papillomavirus type 58 virus-like particles produced in Saccharomyces cerevisiae J. Microbiol., 50, 813-820

Lee, H-J., Hur, Y-K., Cho, Y-D., Kim, M-G., Lee, H-T., Oh, Y-K. and Kim, Y.B. (2012) Immunogenicity of bivalent human papillomavirus DNA vaccine using human endogenous retrovirus envelope-coated baculoviral vectors in mice and pigs PLoS One, 7: e50296

Infection

Anti-L1 antibodies
Hu, J., Budgeon, L.R., Cladel, N.M., Culp, T.A., Balogh, K.K. and Christensen, N.D. (2007) Detection of L1, infectious virions and anti-L1 antibody in domestic rabbits infected with cottontail rabbit papillomavirus J. Gen. Virol., 88, 3286-3293

Antivirals
Donalisio, M., Cagno, V., Civra, A., Gibellini, D., Musumeci, G., Rittà, M., Ghosh, M. and Lembo, D. (2018) The traditional use of Vachellia nilotica for sexually transmitted diseases is substantiated by the antiviral activity of its bark extract against sexually transmitted viruses J. Ethnopharmacol., 213, 403–408

Huang, H-S., Pyeon, D., Pearce, S.M., Lank, S.M., Griffin, L.M., Ahlquist, P., Lambert, P.F. (2012) Novel antivirals inhibit early steps in HPV infection Antiviral Res., 93, 280–287

Theisen, L.L., Erdelmeier, C.A.J., Spoden, G.A., Boukhallouk, F., Sausy, A., Florin, L. and Muller, C.P. (2014) Tannins from Hamamelis virginiana bark extract:characterization and improvement of the antiviral efficacy against influenza A virus and human papillomavirus PLoS One, 9: e88062

ARRDC3 gene
Takeuchi, F., Kukimoto, I., Li, Z., Li, S., Li, N., Hu, Z., Takahashi, A., Inoue, S., Yokoi, S. et al (2019) Genome-wide association study of cervical cancer suggests a role for ARRDC3 gene in human papillomavirus infection Hum. Mol. Genet., 28, 341–348 13

Cell cycle progression requirement
Pyeon, D., Pearce, S.M., Lank, S.M., Ahlquist, P. and Lambert, P.F. (2009) Establishment of human papillomavirus infection requires cell cycle progression PLoS Pathog., 5:e1000318

Dopachrome tautomerase
Aksoy, P. and Meneses, P.I. (2017) The role of DCT in HPV16 infection of HaCaTs PLoS One 12: e0170158

Heparan sulphate
Cagno, V., Donalisio, M., Bugatti, A., Civra, A., Cavalli, R., Ranucci, E., Ferruti, P., Rusnati, M. and Lembo, D. (2015) The agmatine-containing poly(amidoamine) polymer AGMA1 binds cell surface heparan sulfates and prevents attachment of mucosal human papillomaviruses Antimicrob. Agents Chemother., 59, 5250-5259

Huang, H-S. and Lambert, P.F. (2012) Use of an in vivo animal model for assessing the role of integrin 64 and Syndecan-1 in early steps in papillomavirus infection Virology, 433, 395–400

Johnson, K.M., Kines, R.C., Roberts, J.N., Lowy, D.R., Schiller, J.T. and Day, P.M. (2009) Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus J. Virol., 83, 2067-2074

Kines, R.C., Cerio, R.J., Roberts, J.N., Thompson, C.D., de Los Pinos, E., Lowy, D.R. and Schiller, J.T. (2016) Human papillomavirus capsids preferentially bind and infect tumor cells Int. J. Cancer, 138, 901–911

Kumar, A., Jacob, T., Abban, C.Y. and Meneses, P.I. (2014) Intermediate heparan sulfate binding during HPV-16 infection in HaCaTs Am. J. Therapeut., 21, 331–342

Lembo, D., Donalisio, M., Laine, C., Cagno, V., Civra, A., Bianchini, E.P., Zeghbib, N. and Bouchemal, K. (2014) Auto-associative heparin nanoassemblies: A biomimetic platform against the heparan sulfate-dependent viruses HSV-1, HSV-2, HPV-16 and RSV Eur. J. Pharm. Biopharm., 88, 275–282

Immunodeficiency
Pastrana, D.V., Peretti, A., Welch, N.L., Borgogna, C., Olivero, C., Badolato, R., Notarangelo, L.D., Gariglio, M., FitzGerald, P.C., McIntosh, C.E. et al (2018) Metagenomic discovery of 83 new human papillomavirus types in patients with immunodeficiency mSphere 6 e00645-18

Integrins
Aksoy, P., Abban, C.Y., Kiyashka, E., Qiang, W. and Meneses, P.I. (2014) HPV16 infection of HaCaTs is dependenton β4 integrin, and α6 integrin processing Virology, 449, 45–52

Huang, H-S. and Lambert, P.F. (2012) Use of an in vivo animal model for assessing the role of integrin 64 and Syndecan-1 in early steps in papillomavirus infection Virology, 433, 395–400

L2 Cysteine residues
Gambhira, R., Jagu, S., Karanam, B., Day, P.M. and Roden, R. (2009) Role of L2 cysteines in papillomavirus infection and neutralization Virol. J., 6: 176

Optical imaging
Kines, R.C., Kobayashi, H., Choyke, P.L. and Bernardo, M.L. (2013) Optical imaging of HPV infection in a murine model In Mol. Dermatol: Methods and Protocols (ed. Has, C. and Sitaru, C.) Springer Science+Business Media, LLC, pp 141-150

Restriction factors
Warren, C.J., Xu, T., Guo, K., Griffin, L.M., Westrich, J.A., Lee, D., Lambert, P.F,, Santiago, M.L. and Pyeona, D. (2015) APOBEC3A functions as a restriction factor of human papillomavirus J. Virol., 89, 688-702

y-Secretase requirement
Huang, H-S., Buck, C.B. and Lambert, P.F. (2010) Inhibition of gamma secretase blocks HPV infection Virology 407, 391–396

Karanam, B., Peng, S., Li, T., Buck, C., Day, P.M. and Roden, R.B.S. (2010) Papillomavirus infection requires  secretase J. Virol., 84, 10661–10670

Single particle tracking
Ewers, H. and Schelhaas, M. (2012) Analysis of virus entry and cellular membrane dynamics by single particle tracking Methods Enzymol., 506, 63-80 14

Skin/vaginal/wart lesions
Bzhalava, D., Johansson, H., Ekström, J., Faust, H., Möller, B., Eklund, C., Nordin, P., Stenquist, B., Paoli, J., Persson, B., Forslund, O. and Dillner, J. (2013) Unbiased approach for virus detection in skin lesions PLoS One, 8: e65953

Chu, T-Y., Chang, Y-C. and Ding, D.C. (2013) Cervicovaginal secretions protect from human papillomavirus infection: Effects of vaginal douching Taiwan. J. Obstet. Gynecol., 52, 241-245

Çuburu, N., Cerio, R.J., Thompson, C.D. and Day, P.M. (2015) Mouse model of cervicovaginal papillomavirus infection In Cervical Cancer: Methods and Protocols, Methods in Molecular Biology, vol. 1249 (eds. Keppler, D. and Lin, A.W. Springer Science+Business Media New York, pp 365-379

Handisurya, A., Day, P.M., Thompson, C.D., Buck, C.B., Kwak, K., Roden, R.B.S., Lowy, D.R. and Schiller, J.T. (2012) Murine skin and vaginal mucosa are similarly susceptible to infection by pseudovirions of different papillomavirus classifications and species Virology, 433, 385–394

Meyers, J.M., Uberoi, A., Grace, M., Lambert, P.F. and Munger, K. (2017) Cutaneous HPV8 and MmuPV1 E6 proteins target the NOTCH and TGF-β tumor suppressors to inhibit differentiation and sustain keratinocyte proliferation PLoS Pathog., 13: e1006171

Roberts, J.N., Kines, R.C., Katki, H.A., Lowy, D.R. and Schiller, J.T. (2011) Effect of pap smear collection and carrageenan on cervicovaginal human papillomavirus-16 infection in a rhesus macaque model J. Natl. Cancer Inst., 103, 737–743

Vinzón, S.E., Braspenning-Wesch, I., Müller, M., Geissler, E.K., Nindl, I., Gröne, H-J., Schäfer, K. and Rösl, F. (2014 ) Protective vaccination against papillomavirus-induced skin tumors under immuno-competent and immunosuppressive conditions: a preclinical study using a natural outbred animal model PLoS Pathog., 10: e1003924

Xue, X-Y., Majerciak, V., Uberoi, A., Kim, B-H., Gotte, D., Chen, X., Cam, M., Lambert, P.F. and Zheng, ZM. (2017) The full transcription map of mouse papillomavirus type 1 (MmuPV1) in mouse wart tissue PloS Pathog. 13: e1006715

Superinfection inclusion
Biryukov, J. and Meyers, C. (2018) Superinfection exclusion between two high-risk human papillomavirus types during a coinfection J. Virol., 92: e01993-17

Syndecan-1
Huang, H-S. and Lambert, P.F. (2012) Use of an in vivo animal model for assessing the role of integrin 64 and Syndecan-1 in early steps in papillomavirus infection Virology, 433, 395–400

YAP1 activation
He, C., Lv, X., Huang, C., Angeletti, P.C., Hua, G., Dong, J., Zhou, J., Wang, Z., Ma, B., Chen, X. et al (2019) A human papillomavirus-independent cervical cancer animal model reveals unconventional mechanisms of cervical carcinogenesis Cell Reports 26, 2636–2650

Infection inhibition

Carrageenen
Buck, C.B., Thompson, C.D., Roberts, J.N., Müller, M., Lowy, D.R. and Schiller, J.T. (2007) Carrageenan is a potent inhibitor of papillomavirus function Plos Pathog., 2:e69

Novetsky, A.P., Keller, M.J., Gradissimo, A., Chen, Z., Morgan, S.L., Xue, X., Strickler, H.D., FernándezRomero, J.A., Burk, R. and Einstein, M.H. (2016) In vitro inhibition of human papillomavirus following use of a carrageenan-containing vaginal gel Gynecol. Oncol., 143, 313–318

Cholesterol derivatives
Civra, A., Cagno, V., Donalisio, M., Biasi, F., Leonarduzzi, G., Poli, G. and Lembo, D. (2014) Inhibition of pathogenic non-enveloped viruses by 25-hydroxycholesterol and 27-hydroxycholesterol Sci. Rep., 4: 7487

y-Defensins
Buck, C.B., Day, P.M., Thompson, C.D., Lubkowski, J., Lu, W., Lowy, D.R. and Schiller, J.T. (2006) Human -defensins block papillomavirus infection Proc. Natl. Acad. Sci. USA, 103, 1516-1521

Gounder, A.P., Wiens, M.E., Wilson, S.S., Lu, W. and Smith, J.G. (2012) Critical determinants of human - defensin 5 activity against non-enveloped viruses J. Biol. Chem., 287, 24554–24562

Wiens, M.E. and Smith, J.G. (2015) Alpha-defensin HD5 inhibits furin cleavage of human papillomavirus 16 L2 to block infection J. Virol., 89, 2866-2874

Wiens, M.E. and Smith, J.G. (2017) -Defensin HD5 inhibits human papillomavirus 16 infection via capsid stabilization and redirection to the lysosome mBio, 8: e02304 16 15

E. coli sulphated polysaccharides
Lembo, D., Donalisio, M., Rusnati, M., Bugatti, A., Cornaglia, M., Cappello, P., Giovarelli, M., Oreste, P. and Landolfo, S. (2008) Sulfated K5 Escherichia coli polysaccharide derivatives as wide-range inhibitors of genital types of human papillomavirus Antimicrob. Agents Chemother., 52, 1374-1381

Genome, nuclear transport block
Ishii, Y., Tanaka, K., Kondo, K., Takeuchi, T., Mori, S. and Kanda, T. (2010) Inhibition of nuclear entry of HPV16 pseudovirus-packaged DNA by an anti-HPV16 L2 neutralizing antibody Virology 406, 181–188

Heparan sulphate binding
Cagno, V., Donalisio, M., Bugatti, A., Civra, A., Cavalli, R., Ranucci, E., Ferruti, P., Rusnati, M. and Lembo, D. (2015) The agmatine-containing poly(amidoamine) polymer AGMA1 binds cell surface heparan sulfates and prevents attachment of mucosal human papillomaviruses Antimicrob. Agents Chemother., 59, 5250-5259

Donalisio, M., Rusnati, M., Civra, A., Bugatti, A., Allemand, D., Pirri, G., Giuliani, A., Landolfo, S. and Lembo, D. (2010) Identification of a dendrimeric heparan sulfate-binding peptide that inhibits infectivity of genital types of human papillomaviruses Anitmicrob. Agents Chemother., 54, 4290-4299

High affinity ligands
Mauro, N., Ferruti, P., Ranucci, E., Manfredi, A., Berzi, A., Clerici, M., Cagno, V., Lembo, D., Palmioli, A. and Sattin, S. (2016) Linear biocompatible glycopolyamidoamines as dual action mode virus infection inhibitors with potential as broad-spectrum microbicides for sexually transmitted diseases Sci. Rep., 6: 33393

Interferon
Day, P.M., Thompson, C.D., Lowy, D.R. and Schiller, J.T. (2017) Interferon gamma prevents infectious entry of human papillomavirus 16 via an L2-dependent mechanism J. Virol., 91: e00168-17

L1/L2 effects
Day, P.M., Kines, R.C., Thompson, C.D., Jagu, S., Roden, R.B., Lowy, D.R. and Schiller, J.T. (2010) In vivo mechanisms of vaccine-induced protection against HPV infection Cell Host Microbe, 8, 260–270

Day, P.M., Thompson, C.D., Lowy, D.R. and Schiller, J.T. (2017) Interferon gamma prevents infectious entry of human papillomavirus 16 via an L2-dependent mechanism J. Virol., 91: e00168-17

Pouyanfard, S., Spagnoli, G., Bulli, L., Balz, K., Yang, F., Odenwald, C., Seitz, H. Mariz, F.C. et al (2018) Minor capsid protein L2 polytope induces broad protection against oncogenic and mucosal human papillomaviruses J. Virol., 92: e01930-17

L2 lipopeptide
Yan, H., Foo, S-S., Chen, W., Yoo, J-S., Shin, W-J., Wu, C. and Jung, J.U. (2019) Efficient inhibition of human papillomavirus infection by L2 minor capsid-derived lipopeptide mBio, 10: e01834-19

Mucins
Lieleg, O., Lieleg, C., Bloom, J., Buck, C.B. and Ribbeck, K. (2012) Mucin biopolymers as broad-spectrum antiviral agents Biomacromolecules, 13, 1724−1732

Infectious virus production
Müller, K.H., Spoden, G.A., Scheffer, K.D., Brunnhöfer, R., De Brabander, J.K., Maier, M.E., Florin, L. and Muller, C.P. (2014) Inhibition by cellular vacuolar ATPase impairs human papillomavirus uncoating and infection Antimicrob. Agents Chemother., 58, 2905–2911

Pyeon, D., Lambert, P.F. and Ahlquist, P. (2005) Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation Proc. Natl. Acad. Sci. USA, 102, 9311-9316

Intracellular assembly

L1/L2 proteins
Bissa, M., Zanotto, C., Pacchioni, S., Volonté, L., Venuti, A., Lembo, D., De Giuli Morghen, C. and Radaelli, A. (2015) The L1 protein of human papilloma virus 16 expressed by a fowlpox virus recombinant can assemble into virus-like particles in mammalian cell lines but elicits a non-neutralising humoral response Antiviral Res., 116, 67–75

Buck, C.B., Pastrana, D.V., Lowy, D.R. and Schiller, J.T. (2004) Efficient intracellular assembly of Papillomaviral vectors J. Virol., 78, 751-757 (B)

Buck, C.B., Cheng, N., Thompson, C.D., Lowy, D.R., Steven, A.C., Schiller, J.T. and Trus, B.L. (2008) Arrangement of L2 within the papillomavirus capsid J. Virol., 82, 5190-5197 16

Conway, M.J. and Meyers, C. (2009) Replication and assembly of human papillomaviruses Dent. Res., 88, 307-317 (CTR)

Day, P.M., Thompson, C.D., Lowy, D.R. and Schiller, J.T. (2017) Interferon gamma prevents infectious entry of human papillomavirus 16 via an L2-dependent mechanism J. Virol., 91: e00168-17

L2 cysteine residues
Conway, M.J., Alam, S., Christensen, N.D. and Meyers, C. (2009) Overlapping and independent structural roles for human papillomavirus type 16 L2 conserved cysteines Virology 393, 295–303

Gambhira, R., Jagu, S., Karanam, B., Day, P.M. and Roden, R. (2009) Role of L2 cysteines in papillomavirus infection and neutralization Virol. J., 6: 176

Redox gradient dependence
Conway, M.J., Alam, S., Ryndock, E.J., Cruz, L., Christensen, N.D., Roden, R.B.S. and Meyers, C. (2009) Tissue-spanning redox gradient-dependent assembly of native human papillomavirus type 16 virions J. Virol., 83, 10515-10526

Intracellular trafficking

Cysteine proteases
Dabydeen, S.A. and Meneses, P.I. (2009) The role of NH4Cl and cysteine proteases in human papillomavirus type 16 infection Virol. J., 6:109

Dynein interacting domain
Florin, L., Becker, K.A., Lambert, C., Nowak, T., Sapp, C., Strand, D., Streeck, R.E. and Sapp, M. (2006) Identification of a dynein interacting domain in the papillomavirus minor capsid protein L2 J. Virol., 80, 6691-6696

Endosomal trafficking
Gräßel, L., Fast, L.A., Scheffer, K.D., Boukhallouk, F., Spoden, G.A., Tenzer, S., Boller, K., Bago, R., Rajesh, S. et al (2016) The CD63-syntenin-1 complex controls post-endocytic trafficking of oncogenic human papillomaviruses Sci. Rep., 6: 32337

Popa, A., Zhang, W., Harrison, M.S., Goodner, K., Kazakov, T., Goodwin, E.C., Lipovsky, A., Burd, C.G. and DiMaio, D. (2015) Direct binding of retromer to human papillomavirus type 16 minor capsid protein L2 mediates endosome exit during viral infection PLoS Pathog., 11: e1004699

Genome, nuclear transport block
Ishii, Y., Tanaka, K., Kondo, K., Takeuchi, T., Mori, S. and Kanda, T. (2010) Inhibition of nuclear entry of HPV16 pseudovirus-packaged DNA by an anti-HPV16 L2 neutralizing antibody Virology 406, 181–188

Inhibition by thio-reactive agents
Ishii, Y., Kondo, K., Matsumoto, T., Tanaka, K., Shinkai-Ouchi, F., Hagiwara, K. and Kanda, T. (2007) Thiolreactive reagents inhibits intracellular trafficking of human papillomavirus type 16 pseudovirions by binding to cysteine residues of major capsid protein L1 Virol. J., 4:110

L2 capsid protein
Inoue, T., Zhang, P., Zhang, W., Goodner‑Bingham, K., Dupzyk, A., DiMaio, D. and Tsai, B. (2018) 1 γSecretase promotes membrane insertion of the human papillomavirus L2 capsid protein during virus infection J. Cell Biol., 217, 3545–3559

Kondo, K., Ishii, Y., Mori, S., Shimabukuro, S., Yoshikawa, H. and Kanda, T. (2009) Nuclear location of minor capsid protein L2 is required for expression of a reporter plasmid packaged in HPV51 pseudovirions Virology 394, 259–265

Mamoor, S., Onder, Z., Karanam, B., Kwak, K., Bordeaux, J., Crosby, L., Roden, R.B.S. and Moroianu, J. (2012) The high risk HPV16 L2 minor capsid protein has multiple transport signals that mediate its nucleocytoplasmic traffic Virology, 422, 413–424

PML expression
Day, P.M., Baker, C.C., Lowy, D.R. and Schiller, J.T. (2004) Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression Proc. Natl. Acad. Sci. USA, 101, 14252-14257 17

Polyethyleninimes
Spoden, G.A., Besold, K., Krauter, S., Plachter, B., Hanik, N., Kilbinger, A.F.M., Lambert, C. and Florina, L. (2012) Polyethylenimine is a strong inhibitor of human papillomavirus and cytomegalovirus infection Antimicrob. Agents Chemother., 56, 75-82

Keratinocyte/expression in/interactions
Brendle, S.A. and Christensen, N.D. (2015) HPV binding assay to Laminin-332/Integrin α6β4 on human keratinocytes In Cervical Cancer: Methods and Protocols, Methods in Molecular Biology, vol. 1249 (eds. Keppler, D. and Lin, A.W. Springer Science+Business Media New York, pp 53-66

McKinney, C.C., Kim, M.J., Chen, D. and McBride, A.A. (2016) Brd4 activates early viral transcription upon human papillomavirus 18 infection of primary keratinocytes mBio, 7: e01644-16

Tao, L., Pavlova, S.I., Gasparovich, S.R., Jin, L. and Schwartz, J. (2015) Alcohol metabolism by oral Streptococci and interaction with human papillomavirus leads to malignant transformation of oral keratinocytes In Advances in Experimental Medicine and Biology, 815 Biological Basis of Alcohol-Induced Cancer. (ed. Vasiliou, V. et al), Springer International Publishing Switzerland pp 239-264

Van Doorslaer, K., Porter, S., McKinney, C., Stepp, W.H. and McBride, A.A. (2016) Novel recombinant papillomavirus genomes expressing selectable genes Sci. Rep., 6: 37782

Langerhans cell activation
Da Silva, D.M., Movius, C.A., Raff, A.B., Brand, H.E., Skeate, J.G., Wong, M.K. and Kast, W.M. (2014) Suppression of Langerhans cell activation is conserved amongst human papillomavirus α and β genotypes, but not a  genotype Virology, 452-453, 279–286

Life cycle proteins
Bienkowska-Haba, M., Luszczek, W., Myers, J.E., Keiffer, T.R., DiGiuseppe, S., Polk, P., Bodily, J.M., Scott, R.S. and Sapp, M. (2018) A new cell culture model to genetically dissect the complete human papillomavirus life cycle PloS Pathog., 14: e1006846

Methodology
Buck, C.B., Pastrana, D.V., Lowy, D.R. and Schiller, J.T. (2004) Efficient intracellular assembly of Papillomaviral vectors J. Virol., 78, 751-757 (B)

Buck, C.B., Pastrana, D.V., Lowy, D.R. and Schiller, J.T (2005) Generation of HPV pseudovirions using transfection and their use in neutralization assays Methods Mol. Med., 119, 445-462

Neutralization assays
Buck, C.B., Pastrana, D.V., Lowy, D.R. and Schiller, J.T (2005) Generation of HPV pseudovirions using transfection and their use in neutralization assays Methods Mol. Med., 119, 445-462

Lamprecht, R.L., Kennedy, P., Huddy, S.M., Bethke, S., Hendrikse, M., Hitzeroth, I.I. and Rybicki, E.P. (2016) Production of human papillomavirus pseudovirions in plants and their use in pseudovirion-based neutralization assays in mammalian cells Sci. Rep., 6: 20431

Pastrana, D.V., Buck, C.B., Pang, Y-Y. S., Thompson, C.D., Castle, P.E., Fitzgerald, P.C., Kjaer, S.K., Lowy, D.R. and Schiller, J.T. (2004) Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18 Virology, 321, 205-216

Sehr, P., Rubio, I., Seitz, H., Putzker, K., Ribeiro-Müller, L., Pawlita, M. and Müller, M. (2013) Highthroughput pseudovirion-based neutralization assay for analysis of natural and vaccine-induced antibodies against human papillomaviruses PLoS One, 8: e75677

Steele, J., Collins, S., Wen, K., Ryan, G., Constandinou-Williams, C. and Woodman, C.B.J. (2008) Measurement of the humoral immune response following an incident human papillomavirus type 16 or 18 infection in young women by a pseudovirion-based neutralizing antibody assay Clin. Vaccine Immunol., 15, 1387-1390

Neutralizing antibodies

Capsid protein
Culp, T.D., Spatz, C.M., Reed, C.A. and Christensen, N.D. (2007) Binding and neutralization efficiencies of monoclonal antibodies, Fab fragments and scFv specific for L1 epitopes on the capsid of infectious HPV particles Virology, 361, 435-446 18

L1 epitopes
Carter, J.J., Wipf, G.C., Madelaine, M.M., Schwartz, S.M., Koutsky, L.A. and Galloway, D.A. (2006) Identification of human papillomavirus type 16 L1 surface loops required for neutralization by human sera J. Virol., 80, 4664-4672

Roth, S.D., Sapp, M., Streeck, R.E. and Selinka, H-C. (2006) Characterization of neutralizing epitopes within the major capsid protein of human papillomavirus type 33 Virol. J., 3:83

L2 epitopes
Kondo, K., Ishii, Y., Ochi, H., Matsumoto, T., Yoshikawa, H. and Kanda, T. (2007) Neutralization of HPV16, 18, 31, and 58 pseudovirions with antisera induced by immunizing rabbits with synthetic peptides representing segments of the HPV16 minor capsid protein L2 surface region Virology, 358, 266-272

Pastrana, D.V., Gambhira, R., Buck, C.B., Pang, Y-Y.S., Thompson, C.D., Culp, T.D., Christensen, N.D., Lowy, D.R., Schiller, J.T. and Roden, R.B.S. (2005) Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sea to the amino terminus of L2 Virology, 337, 365-372

Seitz, H., Schmitt, M., Böhmer, G., Kopp-Schneider, A. and Müller, M. (2013) Natural variants in the major neutralizing epitope of human papillomavirus minor capsid protein L2 Int. J. Cancer, 132, E139–E148

Oropharyngeal cancer
Conway, M.J. and Meyers, C. (2009) Replication and assembly of human papillomaviruses Dent. Res., 88, 307-317

Ovarian cancer therapy
Hung, C-F., Chiang, A.J., Tsai, H-H., Pomper, M.G., Kang, T.H., Roden, R.R. and Wu, T-C. (2012) Ovarian cancer gene therapy using HPV-16 pseudovirion carrying the HSV-tk gene PLoS One, 7: e40983

Kines, R.C., Cerio, R.J., Roberts, J.N., Thompson, C.D., de Los Pinos, E., Lowy, D.R. and Schiller, J.T. (2016) Human papillomavirus capsids preferentially bind and infect tumor cells Int. J. Cancer, 138, 901–911

Pichia pastoris infection
Gupta, G., Glueck, R. and Rishi, N. (2017) Physicochemical characterization and immunological properties of Pichia pastoris based HPV16L1 and 18L1 virus like particles Biologicals, 46, 11-22

Rao, N.H., Babu, P.B., Rajendra, L.., Sriraman, R., Pang, Y-Y.S., Schiller, J.T. and Srinivasan, V.A. (2011) Expression of codon optimized major capsid protein (L1) of human papillomavirus type 16 and 18 in Pichia pastoris; purification and characterization of the virus-like particles Vaccine, 29, 7326– 7334

Plants, production in
Lamprecht, R.L., Kennedy, P., Huddy, S.M., Bethke, S., Hendrikse, M., Hitzeroth, I.I. and Rybicki, E.P. (2016) Production of human papillomavirus pseudovirions in plants and their use in pseudovirion-based neutralization assays in mammalian cells Sci. Rep., 6: 20431

Proteoglycans
Huang, H-S. and Lambert, P.F. (2012) Use of an in vivo animal model for assessing the role of integrin 64 and Syndecan-1 in early steps in papillomavirus infection Virology, 433, 395–400

Pseudovirus production
Tintori, C., Iovenitti, G., Ceresola, E.R., Ferrarese, R., Zamperini, C., Brai, A., Poli, G., Dreassi, E., Cagno, V., Lembo, D., Canducci, F. and Botta, M. (2018) Rhodanine derivatives as potent anti-HIV and anti-HSV microbicides PLoS One, 13: e0198478

Recombinant viruses
Van Doorslaer, K., Porter, S., McKinney, C., Stepp, W.H. and McBride, A.A. (2016) Novel recombinant papillomavirus genomes expressing selectable genes Sci. Rep., 6: 37782

Serology
Bissett, S.L., Wilkinson, D., Tettmar, K.I., Jones, N., Stanford, E., Panicker, G., Faust, H., Borrow, R., Soldan, K., Unger, E.R., Dillner, J., Minor, P. and Beddows, S. (2012) Human papillomavirus antibody reference reagents for use in postvaccination surveillance serology Clin. Vaccin. Immunol., 19 449–451

Dillner, J. and Zhou, T. (2007) Meeting report of the WHO workshop and practical course on human papillomavirus (HPV) genotyping and HPV16/18 serology, Lusanne, Switzerland, June 2007 Faust, H., Knekt, P., Forslund, O. and Dillner, J. (2010) Validation of multiplexed human papillomavirus serology using pseudovirions bound to heparincoated beads J. Gen. Virol., 91, 1840–1848 19

SNARE/Syntaxin
Culp, T.D., Budgeon, L.R., Marinkovich, M.P., Meneguzzi, G. and Christensen, N.D. (2006) Keratinocytesecreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells J. Virol., 80, 8940-8950

Laniosz, V., Nguyen, K.C. and Meneses, P.I. (2007) Bovine papillomavirus type 1 infection is mediated by SNARE Syntaxin 18 J. Virol., 81, 7435-7448

Sublingual immunization
Lee, H-J., Cho, H., Kim, M-G., Heo, Y-K., Cho, Y., Gwon, Y-D., Park, K.H., Jin, H., Kim, J., Oh, Y-K. and Kim, Y.B. (2015) Sublingual immunization of trivalent human papillomavirus DNA vaccine in baculovirus nanovector for protection against vaginal challenge PLoS One, 10: e0119408

Surveillance
Louie, K.S., Dalel, J., Reuter, C., Bissett, S.L., Kleeman, M., Ashdown-Barr, L., Banwait, R., Godi, A. (2018) Evaluation of dried blood spots and oral fluids as alternatives to serum for human papillomavirus antibody surveillance mSphere 3: e00043-18

Survival
Ding, D-C., Chang, Y-C., Liu, H-W. and Chu, T-Y (2011) Long-term persistence of human papillomavirus in environments Gynecol. Oncol., 121, 148–151

Transfection
Buck, C.B., Pastrana, D.V., Lowy, D.R. and Schiller, J.T (2005) Generation of HPV pseudovirions using transfection and their use in neutralization assays Methods Mol. Med., 119, 445-462

UV radiation
Uberoi, A., Yoshida, S., Frazer, I.H., Pitot, H.C. and Lambert, P.F. (2016) Role of ultraviolet radiation in papillomavirus-induced disease PLoS Pathog., 12: e1005664

Vaccines/vaccination

A7/A9 species groups
Draper, E., Bissett, S.L., Howell-Jones, R., Edwards, D., Munslow, G., Soldan, K. and Beddows, S. (2011) Neutralization of non-vaccine human papillomavirus pseudoviruses from the A7 and A9 species groups by bivalent HPV vaccine sera Vaccine. 29, 8585– 8590

Antibody detection
Nie, J., Huang, W., Wu, X. and Wang, Y. (2014) Optimization and validation of a high throughput method for detecting neutralizing antibodies against human papillomavirus (HPV) based on pseudovirons J. Med. Virol., 86, 1542–1555

Wu, X., Ma, X., Li, Y., Xu, Y., Zheng, N., Xu, S. and Nawaz, W. (2019) Induction of neutralizing antibodies by human papillomavirus vaccine generated in mammalian cells Antibody Therapeut., 2, 45-53 Antibody neutralization assay Brady, A.M., Unger, E.R. and Panicker, G. (2017) Description of a novel multiplex avidity assay for evaluating HPV antibodies J. Immunol. Meth., 447, 31–36

Guan, J., Bywaters, S.M., Brendle, S.A., Lee, H., Ashley, R.E., Makhov, A.M., Conway, J.F., Christensen, N.D. and Hafenstein, S. (2015) Structural comparison of four different antibodies interacting with human papillomavirus 16 and mechanisms of neutralization Virology, 483, 253–263

Panicker, G., Rajbhandari, I., Gurbaxani, B.M., Querec, T.D. and Unger, E.R. (2015) Development and evaluation of multiplexed immunoassay for detection of antibodies to HPV vaccine types J. Immunol. Methods, 417, 107–114

Schellenbacher, C., Shafti-Keramat, S., Huber, B., Fink, D., Brandt, S. and Kirnbauer, R. (2015) Establishment of an in vitro equine papillomavirus type2 (EcPV2) neutralization assay and a VLP-based vaccine for protection of equids against EcPV2-associated genital tumors Virology, 486, 284–290 (E)

Sehr, P., Rubio, I., Seitz, H., Putzker, K., Ribeiro-Müller, L., Pawlita, M. and Müller, M. (2013) Highthroughput pseudovirion-based neutralization assay for analysis of natural and vaccine-induced antibodies against human papillomaviruses PLoS One, 8: e75677

Calreticulin
Kim, D., Gambhira, R., Karanam, B., Monie, A., Hung, C-F., Roden, R. and Wu, T-C. (2008) Generation and characterization of a preventative and therapeutic HPV DNA vaccine Vaccine, 26, 351-360 20

Capsid variants
Bissett, S.L., Godi, A., Fleury, M.J.J., Touze, A., Cocuzza, C. and Beddows, S. (2015) Naturally occurring capsid protein variants of human papillomavirus genotype 31 represent a single L1 serotype J. Virol., 89, 7748- 7757

Mejia, A.F., Culp, T.D., Cladel, N.M., Balogh, K.K., Budgeon, L.R., Buck, C.B. and Christensen, N.D. (2006) Preclinical model to test human papillomavirus virus (HPV) capsid vaccines in vivo using infectious HPV/cottontail rabbit papillomavirus chimeric papillomavirus particles J. Virol., 80, 12393-12397

Capsomer vaccines
Wu, W-H., Gersch, E., Kwak, K., Jagu, S., Karanam, B., Huh, W.K., Garcea, R.L. and Roden, R.B.R. (2011) Capsomer vaccines protect mice from vaginal challenge with human papillomavirus PLoS One 6: e27141

Caspase recruitment domain
Lee, D-K., Lee, E-Y., Kim, R-H., Kwak, H-W., Kim, J.Y., Kim, H., Kang, K-W., Lee, S-M. et al (2018) Effect of apoptosis-associated speck-like protein containing a caspase recruitment domain on vaccine efficacy: Overcoming the effects of its deficiency with aluminum hydroxide adjuvant Microbiol. Immunol., 62, 176–186 CD8+ memory T cells

Çuburu, N., Kim, R., Guittard, G.C., Thompson, C.D., Day, P.M., Hamm, D.E., Pang, Y-Y.S., Graham, B.S., Lowy, D.R. and Schiller, J.T. (2019) A prime-pull-amplify vaccination strategy to maximize induction of circulating and genital-resident intraepithelial CD8+ memory T cells J. Immunol., 202, 1250–1264

DNA vaccines
Graham, B.S., Kines, R.C., Corbett, K.S., Nicewonger, J., Johnson, T.R., Chen, M., LaVigne, D., Roberts, J.N., Cuburu. N., Schiller, J.T. and Buck, C.B. (2010) Mucosal delivery of human papillomavirus pseudovirusencapsidated plasmids improves the potency of DNA vaccination Mucosal Immunol., 5, 475-486

Kines, R.C., Zarnitsyn, V., Johnson, T.R., Pang, Y-Y.S., Corbett, K.S., Nicewonger, J.D., Gangopadhyay, A., Chen, M. et al (2015) Vaccination with human papillomavirus pseudovirus-encapsidated plasmids targeted to skin using microneedles PLoS One, 10: e0120797

Peng, S., Monie, A., Kang, T.H., Hung, C-F., Roden, R. and Wu, T-C. (2010) Efficient delivery of DNA vaccines using human papillomavirus pseudovirions Gene Ther., 17, 1453–1464

Yang, B., Yang, A., Peng, S., Pang, X., Roden, R.B.S., Wu, T-C. and Hung, C-F. (2015) Co-administration with DNA encoding papillomavirus capsid proteins enhances the antitumor effects generated by therapeutic HPV DNA vaccination Cell Biosci., 5:35

E2 epitopes
Qian, J., Dong, Y., Pang, Y-Y.s., Ibrahim, R., Berzofsky, J.A., Schiller, J.T. and Kheif, S.N. (2006) Combined prophylactic and therapeutic cancer vaccine: Enhancing CTL responses to HPV16 E2 using a chimeric VLP in HLA-A2 mice Int. J. Cancer, 118, 3022-3029

Fusion protein
Karanam, B., Gambhira, R., Peng, S.,Jagu, S., Kim, D.J., Ketner, G.W., Stern, P.L., Adams, R.J. and Roden, R.B.S. (2009) Vaccination with HPV16 L2E6E7 fusion protein in GPI-0100 adjuvant elicits protective humoral and cell-mediated immunity Vaccine 27, 1040–1049

Gardasil Ⓡ
Han, J.E., Kim, H.K., Park, S.A., Lee, S.J., Kim, H.J., Son, G.H., Kim, Y.T., Cho, Y.J., Kim, H-J. and Lee, N.G. (2010) A nontoxic derivative of lipopolysaccharide increases immune responses to Gardasil® HPV vaccine in mice Int. Immunopharmacol., 10, 169-176

Immunity and immune responses
Giannini, S.L., Hanon, E., Moris, P., Van Mechelen, M., Morel, S., Dessy, F., Fourneau, M.A., Colau, B., Suzich, J., Losonsky, G., Martin, M-T., Dubin, G. and Wettendorf, M.A. (2006) Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only Vaccine, 24, 5937-5949

Han, J.E., Kim, H.K., Park, S.A., Lee, S.J., Kim, H.J., Son, G.H., Kim, Y.T., Cho, Y.J., Kim, H-J. and Lee, N.G. (2010) A nontoxic derivative of lipopolysaccharide increases immune responses to Gardasil® HPV vaccine in mice Int. Immunopharmacol., 10, 169-176

Handisurya, A., Day, P.M., Thompson, C.D., Bonelli, M., Lowy, D.R. and Schiller, J.T. (2014) Strain-specific properties and T cells regulate the susceptibility to papilloma induction by Mus musculus papillomavirus 1 PLoS Pathog., 10: e1004314

Hassett, K.J., Meinerz, N.M., Semmelmann, F., Cousins, M.C., Garcea, R.L. and Randolph, T.W. (2015) Development of a highly thermostable, adjuvanted human papillomavirus vaccine Eur. J. Pharm. Biopharm., 94, 220–228

Huo, Z., Bissett, S.L., Giemza, R., Beddows, S., Oeser, C. and Lewis, D.J.M. (2012) Systemic and mucosal immune responses to sublingual or intramuscular human papilloma virus antigens in healthy female volunteers PLoS One, 7: e33736

Kim, H.J., Lim, S.J., Kwag, H-L. and Kim, H-J. (2012) The choice of resin-bound ligand affects the structure and immunogenicity of column-purified human papillomavirus type 16 virus-like particles PLoS One 7: e35893

Peng, S., Ma, B., Chen, S-H., Hung, C-F. and Wu, T.C. (2011) DNA vaccines delivered by human papillomavirus pseudovirions as a promising approach for generating antigen-specific CD8+T cell immunity Cell Biosci., 1: 26

Tam, J.C.H., Bidgood, S.R., McEwan, W.A. and James, L.C. (2014) Intracellular sensing of complement C3 activates cell autonomous immunity Science, 345: 1256070

Vinzón, S.E., Braspenning-Wesch, I., Müller, M., Geissler, E.K., Nindl, I., Gröne, H-J., Schäfer, K. and Rösl, F. (2014) Protective vaccination against papillomavirus-induced skin tumors under immuno-competent and immunosuppressive conditions: a preclinical study using a natural outbred animal model PLoS Pathog., 10: e1003924

Immunoassay

Panicker, G., Rajbhandari, I and Unger, E. (2012) Detection of antibodies to HPV vaccine types using a multiplexed immunoassay FASEB J., 26, 577.8

Panicker, G., Rajbhandari, I., Gurbaxani, B.M., Querec, T.D. and Unger, E.R. (2015) Development and evaluation of multiplexed immunoassay for detection of antibodies to HPV vaccine types J. Immunol. Methods, 417, 107–114

Immunogenicity enhancement
Cho, H., Lee, H-J., Heo, Y-K., Cho, Y., Gwon, Y-D., Kim, M-G., Park, K.H., Oh, Y-K. and Kim, Y.B. (2014) Immunogenicity of a trivalent human papillomavirus L1 DNA-encapsidated, non-replicable baculovirus nanovaccine PLoS One, 9: e95961

Chang, D.Y., Kim, H.J. and Kim, H-J. (2012) Effects of downstream processing on structural integrity and immunogenicity in the manufacture of papillomavirus type 16 L1 virus-like particles Biotechnol. Bioproc. Eng., 17, 755-763

Janitzek, C.M., Peabody, J., Thrane, S., Carlsen, P.H.R., Theander, T.G., Salanti, A., Chackerian, B., Nielsen, M.A. and Sander, A.F. (2019) A proof-of-concept study for the design of a VLP-based combinatorial HPV and placental malaria vaccine Sci. Rep., 9: 5260

Lee, H-J., Hur, Y-K., Cho, Y-D., Kim, M-G., Lee, H-T., Oh, Y-K. and Kim, Y.B. (2012) Immunogenicity of bivalent human papillomavirus DNA vaccine using human endogenous retrovirus envelope-coated baculoviral vectors in mice and pigs PLoS One, 7: e50296
Nieto, K., Weghofer, M., Sehr, P., Ritter, M., Sedlmeier, S., Karanam, B., Seitz, H., Müller, M., Kellner, M., Hörer, M., Michaelis, U., Roden, R.B.S., Gissmann, L., Kleinschmidt, J.A. (2012) Development of AAVLP(HPV16/31L2) particles as broadly protective HPV vaccine candidate PLoS One, 7: e39741

Schellenbacher, C., Roden, R. and Kirnbauer, R. (2009) Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines J. Virol., 83, 10085-10095

L1 antibodies
Baud, D., Ponci, F., Bobst, M., De Gandhi, P. and Nardelli-Haefliger, D. (2004) Improved efficiency of a Salmonella-based vaccine against human papillomavirus type 16 virus-like particles achieved by using a codonoptimized version of L1 J. Virol., 78, 12901-12909

Berg, M.G., Adams, R.J., Gambhira, R., Siracusa, M.C., Scott, A.L., Roden, R.B.S. and Ketner, G. (2014) Immune responses in macaques to a prototype recombinant adenovirus live oral human papillomavirus 16 vaccine Clin. Vaccine Immunol., 21, 1224–1231

Bissett, S.L., Godi, A., Fleury, M.J.J., Touze, A., Cocuzza, C. and Beddows, S. (2015) Naturally occurring capsid protein variants of human papillomavirus genotype 31 represent a single L1 serotype J. Virol., 89, 7748- 7757

Fraillery, D., Zosso, N. and Nardelli-Haefliger, D (2009) Rectal and vaginal immunization of mice with human papillomavirus L1virus-like particles Vaccine, 27. 2326–2334

Qian, J., Dong, Y., Pang, Y-Y.s., Ibrahim, R., Berzofsky, J.A., Schiller, J.T. and Kheif, S.N. (2006) Combined prophylactic and therapeutic cancer vaccine: Enhancing CTL responses to HPV16 E2 using a chimeric VLP in HLA-A2 mice Int. J. Cancer, 118, 3022-3029 22

Rao, N.H., Babu, P.B., Rajendra, L.., Sriraman, R., Pang, Y-Y.S., Schiller, J.T. and Srinivasan, V.A. (2011) Expression of codon optimized major capsid protein (L1) of human papillomavirus type 16 and 18 in Pichia pastoris; purification and characterization of the virus-like particles Vaccine, 29, 7326– 7334

Yang, B., Yang, A., Peng, S., Pang, X., Roden, R.B.S., Wu, T-C. and Hung, C-F. (2015) Co-administration with DNA encoding papillomavirus capsid proteins enhances the antitumor effects generated by therapeutic HPV DNA vaccination Cell Biosci., 5:35

L2 antibodies
Bywaters, S.M., Brendle, S.A., Biryukov, J., Wang, J.W., Walston, J., Milici, J., Roden, R.B., Meyers, C. and Christensen, N.D. (2018) Production and characterization of a novel HPV anti-L2 monoclonal antibody panel Virology, 524, 106–113

Conway, M.J., Cruz, L., Alam, S., Christensen, N.D., and Meyers, C. (2011) Cross-neutralization potential of native human papillomavirus N-terminal L2 epitopes PloS One 6: e16405

Jagu, S., Malandro, N., Kwak, K., Yuan, H., Schlegel, R., Palmer, K.E., Huh, W.K., Campo, M.S. and Roden, R.B.S. (2011) A multimeric L2 vaccine for prevention of animal papillomavirus infections Virology, 420, 43–50 (C, B)

Jagu, S., Kwak, K., Schiller, J.T., Lowy, D.R., Kleanthous, H., Kalnin, K., Wang, C., Wang, H-K., Chow, L.T., Huh, W.K., Jaganathan, K.S., Chivukula, S.V. and Roden, R.B.S. (2013) Phylogenetic considerations in designing a broadly protective multimeric L2 vaccine J. Virol., 87, 6127–6136

Jagu, S., Karanam, B., Wang, J.W., Zayed, H., Weghofer, M., Brendle, S.A., Balogh, K.K., Tossi, K.P., Roden, R.B.S. and Christensen, N.D. (2015) Durable immunity to oncogenic human papillomaviruses elicited by adjuvanted recombinant Adeno-associated virus-like particle immunogen displaying L2 17–36 epitopes Vaccine 33 (2015) 5553–5563

Kwak, K., Jiang, R., Wang, J.W., Jagu, S., Kirnbauer, R. and Roden, R.B.S. (2014) Impact of inhibitors and L2antibodies upon the infectivity of diverse alpha and beta human papillomavirus types PLoS One, 9: e97232

Longet, S., Schiller, J.T., Bobst, M., Jichlinski, P. and Nardelli-Haefliger, D. (2011) A murine genital-challenge model is a sensitive measure of protective antibodies against human papillomavirus infection J. Virol., 85, 13253–13259

Seitz, H., Schmitt, M., Böhmer, G., Kopp-Schneider, A. and Müller, M. (2013) Natural variants in the major neutralizing epitope of human papillomavirus minor capsid protein L2 Int. J. Cancer, 132, E139–E148

Yang, B., Yang, A., Peng, S., Pang, X., Roden, R.B.S., Wu, T-C. and Hung, C-F. (2015) Co-administration with DNA encoding papillomavirus capsid proteins enhances the antitumor effects generated by therapeutic HPV DNA vaccination Cell Biosci., 5:35

Yoon, S-W., Lee, T-Y., Kim, S-J., Lee, I-H., Sung, M-H., Park, J-S. and Poo, H. (2012) Oral administration of HPV-16 L2 displayed on Lactobacillus casei induces systematic and mucosal cross-neutralizing effects in Balb/c mice Vaccine, 30, 3286– 3294

LPS-derivative (non-toxic)
Han, J.E., Kim, H.K., Park, S.A., Lee, S.J., Kim, H.J., Son, G.H., Kim, Y.T., Cho, Y.J., Kim, H-J. and Lee, N.G. (2010) A nontoxic derivative of lipopolysaccharide increases immune responses to Gardasil® HPV vaccine in mice Int. Immunopharmacol., 10, 169-176

Measles-vectored vaccine
Gupta, G., Giannino, V., Rishi, N. and Glueck, R. (2016) Immunogenicity of next-generation HPV vaccines in non-human primates: Measles-vectored HPV vaccine versus Pichia pastoris recombinant protein vaccine Vaccine, 34, 4724–4731

Memory B cells
Scherer, E.M., Smith, R.A., Simonich, C.A., Niyonzima, N., Carter, J.J. and Galloway, D.A. (2014) Characteristics of memory B cells elicited by a highly efficacious HPV vaccine in subjects with no pre-existing immunity PLoS Pathog., 10: e1004461

MUC1 peptide – VLP conjugate
Pejawar-Gaddy, S., Rajawat, Y., Hilioti, Z., Xue, J., Gaddy, D.F., Finn. O.J., Viscidi, R.P. and Bossis, I. (2010) Generation of a tumor vaccine candidate based on conjugation of a MUC1 peptide to polyionic papillomavirus virus-like particles Cancer Immunol. Immunother. 59, 1685–1696 (B) 23

Placental malarial antigen
Thrane, S., Janitzek, C.M., Agerbæk, M.O., Ditlev, S.B., Resende, M., Nielsen, M.A., Theander, T.G., Salanti, A. and Sander, A.F. (2015) A novel virus-like particle based vaccine platform displaying the placental malaria antigen VAR2CSA PLoS One, 10: e0143071

Plants, virus production in
Matić, S., Masenga, V., Poli, A., Rinaldi, R., Milne, R.G., Vecchiati, M. and Noris, E. (2012) Comparative analysis of recombinant human papillomavirus 8 L1 production in plants by a variety of expression systems and purification methods Plant Biotechnol. J., 10, 410–421

Prophylactic immunization
Ahn, J., Peng, S., Hung, C-F., Roden, R.B.S. and Best, S.R. (2018) Prophylactic immunization with human papillomavirus vaccines induces oral immunity in mice Laryngoscope, 128, E16–E20

Salmonella-based
Baud, D., Ponci, F., Bobst, M., De Gandhi, P. and Nardelli-Haefliger, D. (2004) Improved efficiency of a Salmonella-based vaccine against human papillomavirus type 16 virus-like particles achieved by using a codonoptimized version of L1 J. Virol., 78, 12901-12909

Fraillery, D., Baud, D., Pang, S.Y-Y., Schiller, J., Bobst, M., Zosso, N., Ponci, F. and Nardelli-Haefliger, D. (2007) Salmonella enterica serovar typhi Ty21a expressing human papillomavirus type 16 L1 as a potential live vaccine against cervical cancer and typhoid fever Clin. Vaccine Immunol., 14, 1285-129

Thermostability
Hassett, K.J., Meinerz, N.M., Semmelmann, F., Cousins, M.C., Garcea, R.L. and Randolph, T.W. (2015) Development of a highly thermostable, adjuvanted human papillomavirus vaccine Eur. J. Pharm. Biopharm., 94, 220–228

Vaccination status
Grant, B.D., Smith, C.A., Castle, P.E., Scheurer, M.E. and Richards-Kortum, R. (2016) A paper-based immunoassay to determine HPV vaccination status at the point-of-care Vaccine, 34, 5656–5663

VLP-vaccines
Huber, B., Schellenbacher, C., Jindra, C., Fink, D. Shafti-Keramat, S. Kirnbauer, R. (2015) A chimeric 18L1- 45RG1 virus-like particle vaccine cross-protects against oncogenic alpha-7 human papillomavirus types PLoS One, 10: e0120152

Yeast-expressed
Kim, S.N., Jeong, H.S., Park, S.N. and Kim, H-J. (2007) Purification and immunogenicity study of human papillomavirus type 16 L1 protein in Saccharomyces cerevisiae J. Virol. Methods, 139, 24-30

Kwag, H-L., Kim, H.J., Chang, D.Y. and Kim, H-J. (2012) The production and immunogenicity of human  papillomavirus type 58 virus-like particles produced in Saccharomyces cerevisiae J. Microbiol., 50, 813-820

11. Phycodnaviridae (Chlorella viruses)

Dunigan, D.D., Cerny, R.L., Bauman, A.T., Roach, J.C., Lane, L.C., Agarkova, I.V., Wulser, K., Yanai-Balser, G.M., Gurnon, J.R., Vitek, J.C. et al (2012) Paramecium bursaria chlorella virus 1 proteome reveals novel architectural and regulatory features of a giant virus J. Virol., 86, 8821-8834

Dunigan, D.D., Al-Sammak, M., Al-Ameeli, Z., Agarkova, I.V., DeLong, J.P. and Van Etten, J.L. (2019) Chloroviruses lure hosts through long-distance chemical signaling J. Virol., 93: e01688-18

Petro, T.M., Agarkova, I.V., Zhou, Y., Yolken, R.H., Van Etten, J.L. and Dunigana, D.D. (2015) Response of mammalian macrophages to challenge with the chlorovirus Acanthocystis turfacea chlorella virus 1 J. Virol., 89, 12096-12107

Schatz, D., Shemi, A., Rosenwasser, S., Sabanay, H., Wolf, S.G., Ben-Dor, S. and Vardi, A. (2014) Hijacking of an autophagy-like process is critical for the life cycle of a DNA virus infecting oceanic algal blooms New Phytologist, 204, 854–863

Wulfmeyer, T., Polzer, C., Hiepler, G., Hamacher, K., Shoeman, R., Dunigan, D.D., Van Etten, J.L., Lolicato, M., Moroni, A., Thiel, G. and Meckel, T. (2012) Structural organization of DNA in chlorella viruses PLoS One, 7: e30133

 

12 Polyomaviridae (incl. polyomavirus, BK virus, JC virus, Merkel cell carcinoma and
Simian virus SV40)

Bagchi, P., Walczak, C.P. and Tsaia, B. (2015) The endoplasmic reticulum membrane J protein C18 executes a distinct role in promoting simian virus 40 membrane penetration J. Virol., 89, 4058-4068

Becker, M., Dominguez, M., Greune, L., Soria-Martinez, L., Pfleiderer, M.M., Schowalter, R., Buck, C.B., Blaum, B.S., Schmidt, M.A. and Schelhaasa, M. (2019) Infectious entry of Merkel cell polyomavirus J. Virol., 93: e02004-18

Buck, C.B., Phan, G.Q., Raiji, M.T., Murphy, P.M., McDermott, D.H. and McBride, A.A. (2012) Complete genome sequence of a tenth human polyomavirus J. Virol., 86, 10887

Burmeister, J.J., Pomerleau, F., Quintero, J.E., Huettl, P., Jakobsson, Y.A.J., Lundblad, M., Heuer, A., Slevin, J.T. and Gerhardt, G.A. (2018) In vivo electrochemical studies of optogenetic control of glutamate signaling measured using enzyme-based ceramic microelectrode arrays In Biochemical Approaches for Glutamatergic Neurotransmission, Neuromethods, vol. 130 (eds. Parrot, S. and Denoroy, L.) Springer Science+Business Media LLC, New York, pp 327-351

Catrice, E.V.B. and Sainsbury, F. (2015) Assembly and purification of polyomavirus-like particles from plants Mol. Biotechnol., 57, 904–913

Dupzyk, A. and Tsaia, B. (2018) Bag2 is a component of a cytosolic extraction machinery that promotes membrane penetration of a nonenveloped virus J. Virol, 92: e00607-18

Enomoto, T., Kukimoto, I., Kawano, M-a., Yamaguchi, Y., Berk, A.J. and Handa, H. (2011) In vitro reconstitution of SV40 particles that are composed of VP1/2/3 capsid proteins and nucleosomal DNA and direct efficient gene transfer Virology, 420, 1–9

Feng, H., Kwun, H.J., Liu, X., Gjoerup, O., Stolz, D.B., Chang, Y. and Moore, P.S. (2011) Cellular and viral factors regulating Merkel cell polyomavirus replication PLoS One, 6: e22468

Hamilton, R.S., Gravell, M. and Major, E.O. (1999) Comparison of antibody titers determined by hemagglutination inhibition and enzyme immunoassay for JC virus and BK virus J. Clin. Microbiol., 38, 105- 109

Ho, J., Jedrych, J.J., Feng, H., Natalie, A.A., Grandinetti, L., Mirvish, E., Crespo, M.M., Yadav, D., Fasanella, K.E., et al (2015) Human polyomavirus 7–associated pruritic rash and viremia in transplant recipients J. Infect. Dis., 211, 1560–1565

Hurdiss, D.L., Morgan, E.L., Thompson, R.F., Prescott, E.L., Panou, M.M., Macdonald, A. and Ranson, N.A. (2016) New structural insights into the genome and minor capsid proteins of BK polyomavirus using cryoelectron microscopy Structure, 24, 528–536

Inoue, T. and Tsai, B. (2011) A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol PLoS Pathog., 7: e1002037

Inoue, T., Dosey, A., Herbstman, J.F., Ravindran, M.S., Skiniotis, G. and Tsaia, B. (2015) ERdj5 reductase cooperates with protein disulfide isomerase to promote simian virus 40 endoplasmic reticulum membrane translocation J. Virol., 89, 8897–8908

Jilek, S., Jaquiéry, E., Hirsch, H.H., Lysandropoulos, A., Canales, M., Guignard, L., Schluep, M., Pantaleo, G., Du Pasquier, R.A. (2010) Immune responses to JC virus in patients with multiple sclerosis treated with natalizumab: a cross-sectional and longitudinal study Lancet Neurol., 9, 264–72

Kitai, Y., Fukuda, H., Enomoto, T., Asakawa, Y., Suzuki, T., Inouye, S. and Handa, H. (2011) Cell selective targeting of a simian virus 40 virus-like particle conjugated to epidermal growth factor J. Biotechnol., 155, 251– 256

Li, J., Wang, X., Diaz, J., Tsang, S.H., Buck, C.B. and You, J. (2013) Merkel cell polyomavirus large T antigen disrupts host genomic integrity and inhibits cellular proliferation J. Virol., 87, 9173–9188

Liu, W., Yang, R., Payne, A.S.,Schowalter, R.M., Spurgeon, M.E., Lambert, P.F., Xu, X., Buck, C.B. and You, J. (2016) Identifying the target cells and mechanisms of Merkel Ccll polyomavirus infection Cell Host Microbe, 19, 775–787

Liu, W., Krump, N.A., MacDonald, M. and You, J. (2018) Merkel cell polyomavirus infection of animal dermal fibroblasts J. Virol., 92: e01610-17
Maginnis, M.S., Ströh, L.J., Gee, G.V., O’Hara, B.A., Derdowski, A., Stehle, T. and Atwood, W.J. (2013) Progressive multifocal leukoencephalopathy-associated mutations in the JC polyomavirus capsid disrupt lactoseries tetrasaccharide c binding mBio, 4: e00247-13

Murata, H., Teferedegne, B., Lewis, A.M. and Peden, K. (2009) A quantitative PCR assay for SV40 neutralization adaptable for high-throughput applications J. Virol. Methods 162, 236–244

Murata, H., Macauley, J., Lewis Jr., A.M. and Peden, K. (2011) Plaque purification as a method to mitigate the risk of adventitious-agent contamination in influenza vaccine virus seeds Vaccine 29, 3155–3161

Nakanishi, A., Chapellier, B., Maekawa, N., Hiramoto, M., Kuge, T., Takahashi, R-u., Handa, H. and Imai, T. (2008) SV40 vectors carrying minimal sequence of viral origin with exchangeable capsids Virology, 379, 110- 117

Neu, U., Henge, H., Blaum, B.S., Schowalter, R.M., Macejak, D., Gilbert, M., Wakarchuk, W.W., Imamura, A., Ando, H. et al (2012) Structures of Merkel cell polyomavirus VP1 complexes define a sialic acid binding site required for infection PLoS Pathog., 8: e1002738

Neumann, F., Borchert, S., Schmidt, C., Reimer, R., Hohenberg, H., Fischer, N., and Grundhoff, A. (2011) Replication, gene expression and particle production by a consensus Merkel cell polyomavirus (MCPyV) genome PLoS One 6: e29112

Nguyen, K.D., Lee, E.E., Yue, Y., Stork, J., Pock, L., North, J.P., Vandergriff, T., Cockerell, C., Hosler, G.A. et al (2017) Human polyomavirus 6 and 7 are associated with pruritic and dyskeratotic dermatoses J. Am. Acad. Dermatol., 76, 932-940

Pastrana, D.V., Tolstov, Y.L., Becker, J.C., Moore, P.S., Chang, Y. and Buck, C.B. (2009) Quantitation of human seroresponsiveness to Merkel cell polyomavirus PLoS Pathog., 5: e1000578

Pastrana, D.V., Brennan, D.C., Cuburu, N., Storch, G.A., Viscidi, R.P., Randhawa, P.S. and Buck, C.B. (2012) Neutralization serotyping of BK polyomavirus infection in kidney transplant recipients PLoS Pathog., 8: e1002650

Pastrana, D.V., Pumphrey, K.A., Çuburu, N., Schowalter, R.M., Buck, C.B. (2010) Characterization of monoclonal antibodies specific for the Merkel cell polyomavirus capsid Virology 405 (2010) 20–25

Pastrana, D.V., Wieland, U., Silling, S., Buck, C.B. and Pfister, H. (2012) Positive correlation between Merkel cell polyomavirus viral load and capsid-specific antibody titer Med. Microbiol. Immunol., 201, 17–23

Pastrana, D.V., Ray, U., Magaldi, T.G., Schowalter, R.M., Çuburu, N. and Buck, C.B. (2013) BK polyomavirus genotypes represent distinct serotypes with distinct entry tropism J. Virol., 87, 10105–10113

Peretti, A., FitzGerald, P.C., Bliskovsky, V., Buck, C.B. and Pastrana, D.V. (2015) Hamburger polyomaviruses J. Gen. Virol., 96, 833–839

Peretti, A., Geoghegan, E.M., Pastrana, D.V., Smola, S., Feld, P., Sauter, M., Lohse, S., Ramesh, M., Lim, E.S. et al (2018) Characterization of BK polyomaviruses from kidney transplant recipients suggests a role for APOBEC3 in driving in-host virus evolution Cell Host Microbe 23, 628–635

Randhawa, P., Pastrana, D.V., Zeng, G., Huang, Y., Shapiro, R., Sood, P., Puttarajappa, C., Berger, M., Hariharan, S. and Buck, C.B. (2015) Commercially available immunoglobulins contain virus neutralizing antibodies against all major genotypes of polyomavirus BK Am. J. Transplant., 15, 1014–1020

Ray, U., Cinque, P., Gerevini, S., Longo, V., Lazzarin, A., Schippling, S., Martin, R., Buck, C.B. and Pastrana, D.V. (2015) JC polyomavirus mutants escape antibody- mediated neutralization Sci. Transl. Med. 7: 306ra151

Showalter, R.M., Reinhold, W.C. and Buck, C.B. (2012) Entry tropism of BK and Merkel cell polyomaviruses in cell culture PLoS One, 7: e42181

Schowalter, R.M., Pastrana, D.V., Pumphrey, K.A., Moyer, A.L. and Buck, C.B. (2010) Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin Cell Host Microbe, 7, 509–515

Schowalter, R.M., Pastrana, D.V. and Buck, C.B. (2011) Glycosaminoglycans and sialylated glycans sequentially facilitate Merkel cell polyomavirus infectious entry PLoS Pathog., 7: e1002161

Showalter, R.M., Reinhold, W.C. and Buck, C.B. (2012) Entry tropism of BK and Merkel cell polyomaviruses in cell culture PLoS One, 7: e42181

Schowalter, R.M. and Buck, C.B. (2013) The Merkel cell polyomavirus minor capsid protein PLoS Pathog., 9: e1003558

Sunyaev, S.R., Lugovskoy, A., Simon, K. and Gorelik, L. (2009) Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML) PLoS Genetics 5:e1000368

Tolstov, Y., Pastrana, D.V., Feng, H., Becker, J.C., Jenkins, F.J., Moschos, S., Chang, Y., Bick, C.B. and Moore, P.S. (2009) Human Merkel cell polyomavirus infection II. MCV is a common human infection that can be detected by conformational capsid epitope immunoassays Int. J. Cancer, 125, 1250-1256

Tsang, S.H., Wang, X., Li, J., Buck, C.B. and You, J. (2014) Host DNA damage response factors localize to Merkel cell polyomavirus DNA replication sites to support efficient viral DNA replication J. Virol., 88, 3285– 3297

Viscidi, R.P., Rollison, D.E., Sondak, V.K., Silver, B., Messina, J.L., Giuliano, A.R., Fulp, W., Ajidahun, A. and Rivanera, D. (2011) Age-specific seroprevalence of Merkel cell polyomavirus, BK virus, and JC virus Clin. Vaccine Immunol., 18, 1737–1743

Walczak, C.P., Ravindran, M.S., Inoue, T. and Tsai, B. (2014) A cytosolic chaperone complexes with dynamic membrane J-proteins and mobilizes a non-enveloped virus out of the endoplasmic reticulum PLoS Pathog., 10: e1004007

Yatawara, A., Gaidos, G., Rupasinghe, C.N., O’Hara, B.A., Pellegrini, M., Atwood, W.J. and Mierke, D.F. (2015) Small-molecule inhibitors of JC polyomavirus infection J. Pept. Sci., 21, 236–242

13. Poxviridae

13a. Molluscipoxvirus
Bugert, J.J. (2007) Genus molluscipoxvirus In Poxviruses (ed. Mercer, A., Schmidt, A. and Weber, O.) Birkhäuser Verlag, Basel, Switzerland, pp 89-112

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

13b. Vaccinia virus
Horita, K., Kurosaki, H., Nakatake, M., Kuwano, N., Oishi, T., Itamochi, H., Sato, S., Kono, H. et al (2019) lncRNA UCA1-mediated Cdc42 signaling promotes oncolytic vaccinia virus cell-to-cell spread in ovarian cancer Mol. Ther: Oncolytics, 13, 35-48

Krijnse-Locker, J., Kuehn, A., Schleich, S., Rutter, G., Hohenberg, H., Wepf, R. and Griffiths, G. (2000) Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV Mol. Biol. Cell, 11, 2497-2511

Parras-Moltó, M., Rodríguez-Galet, A., Suárez-Rodríguez, P. and López-Bueno, A. (2018) Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses Microbiome, 6: 119

Sancho, M.C., Schleich, S., Griffiths, G. and Krijinse-Locker, J. (2002) The block in assembly of modified vaccinia virus Ankara in HeLa cells reveals new insights into vaccinia virus morphogenesis J. Virol., 76, 8318- 8334

Sandbulte, M.R., Platt, R. and Roth, J.A. (2004) T cells from a high proportion of apparently naive cattle can be activated by modified vaccinia virus Ankara (MVA) Viral Immunol., 17, 39-49

Sandgren, K.J., Wilkinson, J., Miranda-Saksena, M., McInerney, G.M., Byth-Wilson, K., Robinson, P.J. and Cunningham, A.L. (2010) A differential role for macropinocytosis in mediating entry of the two forms of vaccinia virus into dendritic cells PLoS Pathogens, 6: e1000866

Scheckelhoff, M.R., Telford, S.R. and Hu, L.T. (2006) Protective efficacy of an oral vaccine to reduce carriage of Borrelia burgdorferi (strain N40) on mouse and tick reservoirs Vaccine, 24, 1949-1957

Van Diepen, M.T., Chapman, R., Douglass, N., Galant, S., Moore, P.L., Margolin, E., Ximba, P., Morris, L., Rybicki, E.P. and Williamson, A-L. (2019) Prime-boost immunizations with DNA, modified vaccinia virus ankara, and protein-based vaccines elicit robust HIV-1 tier 2 neutralizing antibodies against the CAP256 superinfecting virus J. Virol., 93: e02155-18

 

OptiPrepTM Reference List RV01: 2nd edition, January 2020

OptiPrep™ Reference List RV02-1

• PART A OF THIS REFERENCE LIST (pp 1-118) provides a comprehensive reference list of papers reporting the use of OptiPrep for rAAV purification.
• PART B of RV02-1 lists ALL other Group II virus papers (starting p118).
• IMPORTANT NOTE: The rAAV PAPERS RUN TO SEPT. 2018.
• THE COMPANION LIST (RV02-2) LISTS rAAV PAPERS AFTER SEPT. 2018.
• References are divided alphabetically into “Site of delivery” and/or “Research topic” sections. References in each section are listed alphabetically according to first author; multiple references by the same first author are presented chronologically.
• To aid selection, key words are highlighted in blue.
• For detailed methodologies of Group II virus purifications see OptiPrepTM Application Sheets V14-V16. V06 is a methodological review of all OptiPrepTM technology.

PART A

Adenovirus infections
Schaar, K., Geisler, A., Kraus, M., Pinkert, S., Pryshliak, M., Spencer, J.F., Tollefson, A.E., Ying, B. et al (2017) Anti-adenoviral artificial microRNAs expressed from AAV9 vectors inhibit human adenovirus infection in immunosuppressed Syrian hamsters Mol. Ther. Nucleic Acids, 8, 300-316

Adipose tissue delivery
Kallendrusch, S., Schopow, N., Stadler, S.J., Büning, H. and Hacker, U.T, (2016) Adeno-associated viral vectors transduce mature human adipocytes in three-dimensional slice cultures Hum. Gene Ther., 27, 171-173

Liu, X., Magee, D., Wang, C., McMurphy, T., Slater, A., During, M. and Cao, L. (2014) Adipose tissue insulin receptor knockdown via a new primate-derived hybrid recombinant AAV serotype Mol. Ther. Meth. Clin. Dev., 1: 8

Adrenal cortex delivery
Markmann, S., De, B.P., Reid, J., Jose, C.L., Rosenberg, J.B., Leopold, P.L., Kaminsky, S.M., Sondhi, D., Pagovich, O. and Crystal, R.G. (2018) Biology of the adrenal gland cortex obviates effective use of adenoassociated virus vectors to treat hereditary adrenal disorders Hum. Gene, Ther., 29, 403-412

AdV receptor (see “Coxsackie virus”)
Airway delivery (see “Respiratory system delivery”)

Amyotrophic lateral sclerosis
Ceballos-Diaz, C., Rosario, A.M., Park, H-J., Chakrabarty, P., Sacino, A., Cruz, P.E., Siemienski, Z., Lara, N. et al (2015) Viral expression of ALS-linked ubiquilin-2 mutants causes inclusion pathology and behavioral deficits in mice Mol. Neurodegener., 10 :25

Dirren, E., Aebischer, J., Rochat, C., Towne, C., Schneider, B.L. and Aebischer, P. (2015) SOD1 silencing in motoneurons or glia rescues neuromuscular function in ALS mice Ann. Clin. Transl. Neurol., 2, 167–184

Filézac de L’Etang, A., Maharjan, N., Braña, M.C., Ruegsegger, C., Rehmann, R., Goswami, A., Roos, A., Troost, D. et al (2015) Marinesco-Sjögren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS Nat. Neurosci., 18, 227-238

Foust, K.D., Poirier, A., Pacak, C.A., Mandel, R.J. and Flotte, T.R. (2008) Neonatal intraperitoneal or intravenous injections of recombinant adeno-associated virus type 8 transduce dorsal root ganglia and lower motor neurons Hum. Gene Ther., 19, 61-69

Foust, K.D., Flotte, T.R., Reier, P.J. and Mandel, R.J. (2008) Recombinant adeno-associated virus-mediated global anterograde delivery of glial cell line-derived neurotrophic factor to the spinal cord: comparison of rubrospinal and corticospinal tracts in the rat Hum. Gene Ther., 19, 71-81

Jara, J.H., Villa, S.R., Khan, N.A., Bohn, M.C., et al (2012) AAV2 mediated retrograde transduction of corticospinal motor neurons reveals initial and selective apical dendrite degeneration in ALS Neurobiol. Dis., 47, 174–183

Koerber, J.T., Klimczak, R., Jang, J-H., Dalkara, D., et al (2009) Molecular evolution of adeno-associated virus for enhanced glial gene delivery Mol. Ther., 17, 2088–2095

Kubodera, T., Yamada, H., Anzai, M., Ohira, S., et al (2011) In vivo application of an RNAi strategy for the selective suppression of a mutant allele Hum. Gene. Ther., 22, 27-34

Mancuso, R., Martínez-Muriana, A., Leiva, T., Gregorio, D., Ariza, L., Morell, M., Esteban-Pérez, J., GarcíaRedondo, A. et al (2016) Neuregulin-1 promotes functional improvement by enhancing collateral sprouting in SOD1G93A ALS mice and after partial muscle denervation Neurobiol. Dis., 95, 168–178

Stoica, L., Todeasa, S.H., Cabrera, G.T., Salameh, J.S., ElMallah, M.K., Mueller, C., Brown, Jr, R.H., and Sena-Esteves, M. (2016) Adeno-associated virus–delivered artificial microRNA extends survival and delays paralysis in an amyotrophic lateral sclerosis mouse model Ann. Neurol., 79, 687–700

Tatom, J.B., Wang, D.B., Dayton, R.D., Skalli, O., et al (2009) Mimicking aspects of frontotemporal lobar degeneration and Lou Gehrig’s disease in rats via TDP-43 overexpression Mol. Ther., 17, 607–613

Towne, C., Schneider, B.L., Kieran, D., Redmond, D.E., et al (2010) Efficient transduction of non-human primate motor neurons after intramuscular delivery of recombinant AAV serotype 6 Gene Ther., 17, 141–146

Uchida, A., Sasaguri, H., Kimura, N., Tajiri, M., et al (2012) Non-human primate model of amyotrophiclateral sclerosis with cytoplasmic mislocalization of TDP-43 Brain, 135, 833–846

Walker, C., Herranz-Martin, S., Karyka, E., Liao, C., Lewis, K., Elsayed, W., Lukashchuk, V. et al (2017) C9orf72 expansion disrupts ATM-mediated chromosomal break repair Nat. Neurosci., 20, 1225-1235

Xu, Y-F., Prudencio, M., Hubbard, J.M., Tong, J., et al (2013) The pathological phenotypes of human TDP-43 transgenic mouse models are independent of downregulation of mouse Tdp-43 PLoS One, 8: e69864

Anaphylaxis
Pagovich, O.E., Wang, B., Chiuchiolo, M.J., Kaminsky, S,M., Sondhi, D., Jose, C.L., Price, C.C., Brooks, S.F. et al (2016) Anti-hIgE gene therapy of peanut-induced anaphylaxis in a humanized murine model of peanut allergy J. Allergy Clin. Immunol., 138, 1652-1662

Anhedonia
Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E. and Malenka, R.C. (2012) Anhedonia requires MC4Rmediated synaptic adaptations in nucleus accumbens Nature, 487, 183-189

Anthrax toxin protection
De, B.P., Hackett, N.R., Crystal, R.G. and Boyer, J.L. (2008) Rapid/sustained anti-anthrax passive immunity mediated by co-administration of Ad/AAV Mol. Ther., 16, 203-209

Anti-angiogenesis (cancer therapy); see also “Tumour cells, effect on”
Batchu, R.B., Qazi, A.M., Seward, S., Haider, M., et al (2010) B cell transduction of capsid mutant (Y730F) adeno-associated virus-2 vectors with mage-A3 gene for immunotherapy of colorectal cancer J. Surg. Res., 158, 197

Hacker, U.T., Wingenfeld, L., Kofler, D. M., Schuhmann, N.K., et al (2005) Adeno-associated virus serotypes 1 to 5 mediated tumor cell directed gene transfer and improvement of transduction efficiency J. Gene Med., 7, 1429-1438

Igarashi, T., Miyake, K., Masuda, I., Takahashi, H. and Shimada, T. (2010) Adeno-associated vector (type 8)- mediated expression of soluble Flt-1 efficiently inhibits neovascularization in a murine choroidal neovascularization model Hum. Gene Ther., 21, 631-637

Isayeva, T., Ren, C. and Ponnazhagan, S. (2005) Recombinant adeno-associated virus 2-mediated antiangiogenic prevention in a mouse model of intraperitoneal ovarian cancer Clin. Cancer Res., 11, 1342-1347

Isayeva, T. and Ponnazhagan, S. (2007) Intraperitoneal gene therapy by rAAV provides long-term survival against epithelial ovarian cancer independently of survivin pathway Gene Ther., 14, 138-146

Isayeva, T., Chanda, D., Kallman, L., Eltoum, I-E.A. and Ponnazhagan, S. (2007) Effects of sustained antiangiogenic therapy in multistage prostate cancer in TRAMP model Cancer Res., 67, 5789-5797

Kuo, C-H., Chen, P-K., Chang, B-I., Sung, M-C., et al (2012) The recombinant lectin-like domain of thrombomodulin inhibits angiogenesis through interaction with Lewis Y antigen Blood, 119, 1302-1313

Kuo, C-H., Chang, B-I., Lee, F-T., Chen, P-K., Lee, J-s., Shi, G-Y. and Wu, H-L. (2015) Development of recombinant adeno-associated virus serotype 2/8 carrying kringle domains of human plasminogen for sustained expression and cancer therapy Hum. Gene Ther., 26, 603-613

Levy, H.C., Bowman, V.D., Govindasamy, L., McKenna, R., et al (2009) Heparin binding induces conformational changes in Adeno-associated virus serotype 2 J. Struct. Biol., 165 146–156

Mahendra, G., Kumar, S., Isayeva, T., Mahasreshti, P.J., et al (2005) Antiangiogenic cancer gene therapy by adeno-associated virus 2-mediated stable expression of the soluble FMS-like tyrosine kinase-1 receptor Cancer Gene Ther., 12, 26-34

McMahon, J.M., Conroy, S., Lyons, M., Greiser, U., O’Shea, C., Strappe, P., Howard, L., Murphy, M., Barry, F. and O’Brien, T. (2006) Gene transfer into rat mesenchymal stem cells: a comparative study of viral and nonviral vectors Stem Cell. Dev., 15, 87-96

Mu, W., Long, D.A., Ouyang, X., Agarwal, A., et al (2009) Angiostatin overexpression is associated with an improvement in chronic kidney injury by an anti-inflammatory mechanism Am. J. Physiol. Renal. Physiol., 296: F145–F152

Nieto, K., Stahl-Hennig, C., Leuchs, B., Müller, M., et al (2012) Intranasal vaccination with AAV5 and 9 vectors against human papillomavirus type 16 in rhesus mcaques Hum. Gene Ther., 23, 3–741

Ponnazhagan, S., Mahendra, G., Kumar, S., Shaw, D.R., et al (2004) Adeno-associated virus 2-mediated antiangiogenic cancer gene therapy: long-term efficacy of a vector encoding angiostatin and endostatin over vectors encoding a single factor Cancer Res., 64, 1781-1787

Ren, C., Kumar, S., Chanda, D., Kallman, L., et al (2008) Cancer gene therapy using mesenchymal stem cells expressing interferon-β in a mouse prostate cancer lung metastasis model Gene Therapy 15, 1446–1453

Ren, C., Kumar, S., Chanda, D., Chen, J., et al (2008) Therapeutic potential of mesenchymal stem cells producing interferon- in a mouse melanoma lung metastasis model Stem Cells, 26, 2332-2338

Shi, W., Teschendorf, C., Muzyczka, N. and Siemann, D. (2002) Adeno-associated virus-mediated gene transfer of endostatin inhibits angiogenesis and tumor growth in vivo Cancer Gene Ther., 9, 513-521

Shi, W., Teschendorf, C., Muzyczka, N. and Siemann, D.W. (2003) Gene therapy delivery of endostatin enhances the treatment efficacy of radiation Radiother. Oncol., 66, 1-9
Shi, W., Hemminki, A. and Bartlett, J.S. (2006) Capsid modifications overcome low heterogeneous expression of heparan sulfate proteoglycan that limits AAV2-mediated gene transfer and therapeutic efficacy in human ovarian carcinoma Gynecol. Oncol., 103, 1054-1062

Shi, W-F. and Bartlett, J.S. (2008) Estrogen plays a critical role in AAV2-mediated gene transfer in ovarian cancer Acta Pharmacol. Sin., 29, 1440-1450

Subramanian, I.V., Ghebre, R. and Ramakrishnan, S. (2005) Adeno-associated virus-mediated delivery of a mutant endostatin suppresses ovarian carcinoma growth in mice Gene Ther., 12, 30-38

Tahara, I., Miyake, K., Hanawa, H., Kurai, T., et al (2007) Systemic cancer gene therapy using adenoassociated virus type 1 vector expressing MDA-7/IL24 Mol Ther., 15, 1805-1811

Takei, Y., Mizukami, H., Saga, Y., Yoshimura, I., et al (2006) Suppression of ovarian cancer by musclemediated expression of soluble VEGFR-1/Flt-1 using adeno associated virus serotype 1-derived vector Int. J. Cancer, 120, 278-284

Teschendorf, C., Emons, B., Muzyczka, N., Graeven, U. and Schmiegel, W. (2010) Efficacy of recombinant adeno-associated viral vectors serotypes 1, 2, and 5 for the transduction of pancreatic and colon carcinoma cells Anticancer Res., 30, 1931-1936

Vanrell, L., Di Scala, M., Blanco, L., Otano, I., Gil-Farina, I., et al (2011) Development of a liver-specific TetOn inducible system for AAV vectors and its application in the treatment of liver cancer Mol. Ther., 19, 1245– 1253

Watanabe, M., Boyer, J.L. and Crystal, R.G. (2010) AAVrh.10-mediated genetic delivery of bevacizumab to the pleura to provide local anti-VEGF to suppress growth of metastatic lung tumors Gene Ther., 17, 1042–1051 Yanamandra, N., Kondraganti, S., Gondi, C.S., Gujrati, M., et al (2005) Recombinant adeno-associated virus (rAAV) expressing TFPI-2 inhibits invasion, angiogenesis and tumor growth in a human glioblastoma cell line Int. J. Cancer, 115, 998-1005

Yoo, J., Choi, S., Hwang, K-S., Cho, W-K., et al (2006) Adeno-associated virus-mediated gene transfer of a secreted form of TRAIL inhibits tumor growth and occurrence in an experimental tumor model J. Gene Med., 8, 163-174

Antibody response to
Calcedo, R. and Wilson, J.M. (2016) AAV natural infection induces broad cross-neutralizing antibody responses to multiple AAV serotypes in chimpanzees Hum. Gene Ther. Clin. Dev., 27, 79-82

Jungmann, A., Müller, O. and Rapti, K. (2017) Cell-based measurement of neutralizing antibodies against adeno-associated virus (AAV) In Cardiac Gene Therapy: Methods and Protocols, Methods Mol. Biol., 1521, (ed. Ishikawa, K.) Springer Science+Business Media, New York, pp 109-126

Antigen presentation/reactivity
Ashley, S.N., Somanathan, S., Hinderer, C., Arias, M., McMenamin, D., Draper, C. and Wilson, J.M. (2017) Alternative start sites downstream of non-sense mutations drive antigen presentation and tolerance induction to C-terminal epitopes J. Immunol., 198, 4581–4587

Huang, L-Y., Patel, A., Ng, R., Miller, E.B., Halder, S., McKenna, R., Asokan, A. and Agbandje-McKenna, M. (2016) Characterization of the adeno-associated virus 1 and 6 sialic acid binding site J. Virol., 90, 5219-6230

Perrin, G.Q., Zolotukhin, I., Sherman, A., Biswas, M., de Jong, Y.P., Terhorst, C., Davidoff, A.M. and Herzog, R.W. (2016) Dynamics of antigen presentation to transgene product-specific CD4+ T cells and of Treg induction upon hepatic AAV gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16083

Tseng, Y-S., Gurda, B.L., Chipman, P., McKenna, R., Afione, S., Chiorini, J.A., Muzyczka, N., Olson, N.H. et al (2015) Adeno-associated virus serotype 1 (AAV1)- and AAV5-antibody complex structures reveal evolutionary commonalities in parvovirus antigenic reactivity J. Virol., 89, 1794-1808

Anti-viral activity
Rothe, D., Gisela Wajant, G., Grunert, H-P., Zeichhardt, H., et al (2010) Rapid Construction of adenoassociated virus vectors expressing multiple short hairpin RNAs with high antiviral activity against echovirus 30 Oligonucleotides, 20, 191-198

Tartour, K., Nguyen, X-N., Appourchaux, R., Assil, S., Barateau, V., Bloyet, L-M., Gaillard, J.B., Confort, MP. et al (2017) Interference with the production of infectious viral particles and bimodal inhibition of replication are broadly conserved antiviral properties of IFITMs PLoS Pathog., 13: e1006610

Apolipoproteins (see “Lipoprotein metabolism-related disorders”)

Arsenic trioxide

Mitchell, A.M., Li, C. and Samulski, R.J. (2013) Arsenic trioxide stabilizes accumulations of adeno-associated virus virions at the perinuclear region, increasing transduction in vitro and in vivo J. Virol., 87, 4571–4583

Arthritic joint delivery
Adriaansen, J., Tas, S.W., Klarenbeek, P.L., Bakker, A.C., et al (2005) Enhanced gene transfer to arthritic joints using adeno-associated virus type 5: implications for intra-articular gene therapy Ann. Rheum. Dis., 64, 1677-1684

Grimstein, C., Choi, Y-K., Satoh, M., Lu, Y., et al (2010) Combination of alpha-1 antitrypsin and doxycycline suppresses collagen-induced arthritis J. Gene Med., 12, 35–44

Kay, J.D., Gouze, E., Oligino, T.J., Gouz, J-N., et al (20090 Intra-articular gene delivery and expression of interleukin-1Ra mediated by self-complementary adeno-associated virus J. Gene Med., 11, 605-614

Kyostio-Moore, S., Piraino, S., Berthelette, P., Moran, N., Serriello, J., Bendele, A., Sookdeo, C., Nambiar, B. et al (2015) Overexpression of cystatin C in synovium does not reduce synovitis or cartilage degradation in established osteoarthritis Arthritis Res. Ther., 17: 5

Tas, S.W., Adriaansen, J., Hajji, N., Bakker, A.C., et al (2006) Amelioration of arthritis by intraarticular dominant negative IKKβ gene therapy using adeno-associated virus type 5 Hum. Gene Ther., 17, 821-832

Watson, R.S., Broome, T.A., Levings, P.P., Rice, B.L., et al (2013) scAAV-mediated gene transfer of interleukin-1-receptor antagonist to synovium and articular cartilage in large mammalian joints Gene Ther., 20, 670–677

Atherosclerosis (see “Lipoprotein metabolism-related disorders”)

Baculovirus expression system
Buclez, P-O., Florencio, G.D., Relizani, K., Beley, C., Garcia, L. and Benchaouir, R. (2016) Rapid, scalable, and low-cost purification of recombinant adeno-associated virus produced by baculovirus expression vector system Mol. Ther. Meth. Clin. Dev., 3: 16035

Steel, M., Woodburn, K., Kniffin, T., Gebretsadik, K., Chan, J., Vijay, S., Chen, H., Chalberg, T.W. and Gasmi, N. (2015) In vitro and in vivo comparability assessment of an AAV vector manufactured by triple transfection in HEK293 cells or in the baculovirus expression system Hum. Gene Ther., 26, A70

Wu, Y., Jiang, L., Geng, H., Yang, T., Han, Z., He, X., Lin, K. and Xu, F. (2018) A recombinant baculovirus efficiently generates recombinant adeno-associated virus vectors in cultured insect cells and larvae Mol. Ther: Meth. Clin. Dev., 10, 38-47

Behavioural changes
Chen, J.L., Carta, S., Soldado-Magraner, J., Schneider, B.L. and Helmchen, F. (2013) Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex Nature, 499, 336-340

Muhia, M., Willadt, S., Yee, B.K., Feldon, J., Paterna, J-C., Schwendener, S., Vogt, K., Kennedy, M.B. and Knuese, I. (2012) Molecular and behavioral changes associated with adult hippocampus-specific SynGAP1 knockout Learn. Mem., 19, 268-281

Bile salt metabolism
Boesjes, M., Bloks, V.W., Hageman, J., Bos, T., van Dijk, T.H., Havinga, R., Wolters, H., Jonker, J.W., Kuipers, F. and Groen, A.K. (2014) Hepatic farnesoid X-receptor isoforms 2 and 4 differentially modulate bile salt and lipoprotein metabolism in mice PLoS One, 9: e115028

Blood-brain barrier
Foley, C.P., Rubin, D.G.., Santillan, A., Sondhi, D., Dyke, J.P., Gobin, Y.P., Crystal, R.G. and Ballon, D.J. (2014) Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption J. Control. Release, 196, 71–78

Body weight control (see “Obesity”)

Bone disorders
Dai, J. and Rabie, A.B.M. (2007) The use of recombinant adeno-associated virus for skeletal gene therapy Orthod. Craniofacial Res., 10, 1-14

Kumar, S., Mahendra, G., Nagy, T.R. and Ponnazhagan, S. (2004) Osteogenic differentiation of recombinant adeno-associated virus 2-transduced murine mesenchymal stem cells and development of an immunocomponent mouse model for ex vivo osteoporosis gene therapy Hum. Gene Ther., 15, 1197-1206

Kumar, S., Mahendra, G. and Ponnazhagan, S. (2005) Determination of osteoprogenitor-specific promoter activity in mouse mesenchymal stem cells by recombinant adeno-associated virus transduction Biochim. Biophys. Acta, 1731, 95-103

Kumar, S., Nagy, T.R. and Ponnazhagan, S. (2010) Therapeutic potential of genetically modified adult stem cells for osteopenia Gene Ther., 17, 105–116

Kumar, S., Wan, C., Ramaswamy, G., Clemens, T.L. and Ponnazhagan, S. (2010) Mesenchymal stem cclls expressing osteogenic and angiogenic factors synergistically enhance bone formation in a mouse model of segmental bone defect Mol. Ther., 18, 1026–1034

Shenegelegn Mern, D., Tschugg, A., Hartmann, S. and Thome, C. (2017) Self-complementary adenoassociated virus serotype 6 mediated knockdown of ADAMTS4 induces long-term and effective enhancement of aggrecan in degenerative human nucleus pulposus cells: A new therapeutic approach for intervertebral disc disorders PloS One, 12: e0172181

Caffeine, effect of
Lazarus, M., Shen, H-Y., Cherasse, Y., Qu, W-M., et al (2011) Arousal effect of caffeine depends on adenosine A2A receptors in the shell of the nucleus accumbens J. Neurosci., 31, 10067–10075

Capsid – assembly, target specificity, structure, peptide ligand insertion Agbandje-McKenna, M. and Kleinschmidt, J. (2011) AAV capsid structure and cell interactions In AdenoAssociated Virus: Methods and Protocols, Methods Mol. Biol., 807 (ed. Snyder, R.O. and Moullier, P.), Springer Science+Business Media, pp 47-92

Aslanidi, G.V., Rivers, A.E., Ortiz, L., Song, L., et al (2013) Optimization of the capsid of recombinant adenoassociated virus 2 (AAV2) vectors: the final threshold? PLoS One, 8: e59142

Aydemir, F., Salganik, M., Resztak, J., Singh, J., Bennett, A., Agbandje-McKenna, M. and Muzyczka, N. (2016) Mutants at the 2-fold interface of adeno-associated virus type 2 (AAV2) structural proteins suggest a role in viral transcription for AAV capsids J. Virol. 90, 7196-7204

Batchu, R.B., Gruzdyn, O.V., Kung, S.T., Weaver, D.W., et al (2014) Novel AAV-DJ capsid tyrosine mutants with enhanced transgene expression in a pancreatic cancer cell line J. Surg, Res., 186, 637-638

Bleker, S., Sonntag, F. And Kleinschmidt, J.A. (2005) Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity J. Virol., 79, 2528-2540

Boucas, J., Lux, K., Huber, A., Schievenbusch, S., et al (2009) Engineering adeno-associated virus serotype 2- based targeting vectors using a new insertion site-position 453-and single point mutations J. Gene Med., 11, 1103-1113

Büning, H., Perabo, L., Coutelle, O., Quadt-Humme, S. and Hallek, M. (2008) Recent developments in adenoassociated virus vector technology J. Gene Med., 10, 717 733

Büning, H., Bolyard, C.M., Hallek, M. and Bartlett, J.S. (2011) Modification and labeling of AAV vector particles In Adeno-Associated Virus: Methods and Protocols, Methods Mol. Biol., 807 (ed. Snyder, R.O. and Moullier, P.), Springer Science+Business Media, pp 273-300

Chan, K.Y., Jang, M.J., Yoo, B.B., Greenbaum, A., Ravi, N., Wu, W-L., Sánchez-Guardado, L., Lois, C., Mazmanian, S.K., Deverman, B.E. and Gradinaru, V. (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems Nat. Neurosci., 20, 1172-1179

Chandran, J.S., Sharp, P.S., Karyka, E., da Conceição Aves-Cruzeiro, J.M., Coldicott, I., Castelli, L.1, Hautbergue, G., Collins, M.O. and Azzouz, M. (2017) Site specific modification of adeno-associated virus enables both fluorescent imaging of viral particles and characterization of the capsid interactome Sci. Rep., 7:14766

Chen, C-L., Jensen, R.L., Schnepp, B.C., Connell, M.J., et al (2005) Molecular characterization of adenoassociated viruses infecting children J. Virol., 79, 14781-14792

Chen, Y.H., Claflin, K., Geoghegan, J.C. and Davidson, B.L. (2012) Sialic acid deposition impairs the utility of AAV9, but not peptide-modified AAVs for brain gene therapy in a mouse model of lysosomal storage disease Mol. Ther., 20, 1393-1399

Choudhury, S.R., Harris, A.F., Cabral, D.J., Keeler, A.M., Sapp, E., Ferreira, J.S., Gray-Edwards, H.L., Johnson, J.A. et al (2016) Widespread central nervous system gene transfer and silencing after systemic delivery of novel AAV-AS vector Mol. Ther., 24, 726-735

Choudhury, S.R., Fitzpatrick, Z., Harris, A.F., Maitland, S.A., Ferreira, J.S., Zhang, Y., Ma, S., Sharma, R.B. et al (2016) In vivo selection yields AAV-B1 capsid for central nervous system and muscle gene therapy Mol. Ther., 24, 1247–1257

DiPrimio, N., Asokan, A., Govindasamy, L., Agbandje-McKenna, M. and samulski, R.J. (2008) Surface loop dynamics in adeno-associated virus capsid assembly J. Virol., 82, 5178-5189

Drouin, L.M., Lins, B., Janssen, M., Bennett, A., Chipman, P., McKenna, R., Chen, W., Muzyczka, N., Cardone, G., Baker, T.S. and Agbandje-McKenna, M. (2016) Cryo-electron microscopy reconstruction and stability studies of the wild type and the R432A variant of adeno-associated virus type 2 reveal that capsid structural stability is a major factor in genome packaging J. Virol., 90, 8542-8541

Gabriel, N., Hareendran, S., Sen, D., Gadkari, R.A., et al (2013) Bioengineering of AAV2 capsid at specific serine, threonine, or lysine residues improves its transduction efficiency in vitro and in vivo Hum. Gene Ther. Methods, 24, 80–93

Gigout, L., Rebollo, P., Clement, N., Warrington, K.H., et al (2005) Altering AAV tropism with mosaic viral capsids Mol. Ther., 11, 856-865
Grieger, J.C. and Samulski, R.J. (2005) Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and post-entry steps J. Virol., 79, 9933-9944

Grieger, J.C., Snowdy, S. and Samulski, R.J. (2006) Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly J. Virol., 80, 5190-5210

Greieger, J.C., Johnson, J.S., Gurda-Whitaker, B., Agbandje-McKenna, M. and Samulski, R.J. (2007) Surfaceexposed adeno-associated virus Vp1-NLS capsid fusion protein rescues infectivity of noninfectious wild-type Vp2/Vp3 and Vp3 only capsids but not that of fivefold pore mutant virions J. Virol., 81, 7833-7843

Gurda, B.L., Raupp, C., Popa-Wagner, R., Naumer, M., et al (2012) Mapping a neutralizing epitope onto the capsid of adeno-associated virus serotype 8 J. Virol., 86, 7739–7751

Gurda, B.L., DiMattia, M.A., Miller, E.B., Bennett, A., et al (2013) Capsid antibodies to different adenoassociated virus serotypes bind common regions J. Virol., 87, 9111 9124

Horowitz, E.D., Rahman, K.S., Bower, B,D., Dismuke, D.J., et al (2013) Biophysical and ultrastructural characterization of adeno-associated virus capsid uncoating and genome release J. Virol., 87, 2994–3002

Huttner, N.A., Girod, A., Perabo, L., Edbauer, D., et al (2003) Genetic modifications of the adeno-associated virus type 2 capsid reduce the affinity and the neutralizing effects of human serum antibodies Gene Ther., 10, 2139-2147

Judd, J., Wei, F., Nguyen, P.Q., Tartaglia, L.J., et al (2012) Random insertion of mCherry into VP3 domain of adeno-associated virus yields fluorescent capsids with no loss of infectivity Mol. Ther. Nucleic Acids, 1, e54 Kern, A., Schmidt, K., Leder, C., Muller, O.J., et al (2003) Identification of a heparin-binding motif on adenoassociated virus type 2 capsids J. Virol., 77, 11072-11081

Kronenberger, S., Böttcher, B., von der Lieth, C.W., Bleker, S. and Kleinschmidt, J.A. (2005) A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini J. Virol., 79, 5296-5303

Krüger, L., Eskerski, H., Dinsart, C., Cornelis, J., et al (2008) Augmented transgene expression in transformed cells using a parvoviral hybrid vector Cancer Gene Ther., 15, 252-267

Ling, C., Li, B., Ma, W. and Srivastava, A. (2016) Development of optimized AAV serotype vectors for highefficiency transduction at further reduced doses Hum. Gene Ther. Meth., 27, 143-149

Lux, K., Goerlitz, N., Leike, K., Goldnau, D., et al (2004) Incorporation of the green fluorescent protein into the adeno-associated virus type 2 capsid Mol. Ther., 9, Suppl. 1 S8 Mays, L.E., Wang, L., Tenney, R., Bell, P., et al (2013) Cell activation to the immunogenic adeno-associated virus capsid from isolate rhesus 32.33 J. Virol., 87, 9473–9485

Michelfelder, S., Varadi, K., Raupp, C., Hunger, A., et al (2011) Peptide ligands incorporated into the threefold spike capsid domain to re-direct gene transduction of AAV8 and AAV9 in vivo PLoS One 6: e23101 942

Moreno, A.M., Fu, X., Zhu, J., Katrekar, D., Shih, Y-R.V., Marlett, J., Cabotaje, J., Tat, J., Naughton, J., et al (2018) In situ gene therapy via AAV-CRISPR-Cas9-mediated targeted gene regulation Mol. Ther.,26, 1818-1827

Nam, H-J., Gurda, B.L., McKenna, R., Potter, M., et al (2011) Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking J. Virol., 85, 11791–11799

Naumer, M., Ying, Y., Michelfelder, S., Reuter, A., et al (2012) Development and validation of novel AAV2 random libraries displaying peptides of diverse lengths and at diverse capsid positions Hum. Gene Ther., 23, 492–507

Naumer, M., Popa-Wagner, R. and Kleinschmidt, J.A. (2012) Impact of capsid modifications by selected peptide ligands on recombinant adeno-associated virus serotype 2-mediated gene transduction J. Gen. Virol., 93, 2131–2141

Nicolson, S.C. and Samulski, R.J. (2014) Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus J. Virol., 88, 4132–4144

Nony, P., Chadeuf, G., Tessier, J., Moullier, P. and Salvetti, A. (2003) Evidence for packaging of rep-cap sequences into adeno-associated virus (AAV) type 2 capsids in the absence of inverted terminal repeats: a model for generation of rep-positive AAV particles J. Virol., 77, 776-781

Opie, S.R., Warrington, K.H., Agbandje-McKenna, M., Zolotukhin, S. and Muzyczka, N. (2003) Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding J. Virol., 77, 6995-7006

Peden, C.S., Manfredsson, F.P., Reimsnider, S.K., Poirier, A.E., et al (2009) Striatal readministration of rAAV vectors reveals an immune response against AAV2 capsids that can be circumvented Mol. Ther., 17, 524–537

Popa-Wagner, R., Porwal, M., Kann, M., Reuss, M., et al (2012) Impact of VP1-specific protein sequence motifs on adeno-associated virus type 2 intracellular trafficking and nuclear entry J. Virol., 86, 9163-9174

Raupp, C., Naumer, M., Müller, O.J., Gurda, B.L., et al (2012) The threefold protrusions of adeno-associated virus type 8 are involved in cell surface targeting as well as post-attachment processing J. Virol., 86, 9396-9408

Salganik, M., Venkatakrishnan, B., Bennett, A., Lins, B., Yarbrough, J., et al (2012) Evidence for pHdependent protease activity in the adeno-associated virus capsid J. Virol., 86, 11877-11885

Salganik, M., Aydemir, F., Nam, H-J., McKenna, R., et al (2014) Adeno-associated virus capsid proteins may play a role in transcription and second-strand synthesis of recombinant genomes J. Virol., 88, 1071–1079

Sen, D., Gadkari, R.A., Sudha, G., Gabriel, N., (2013) Targeted modifications in adeno-associated virus serotype 8 capsid improves its hepatic gene transfer efficiency in vivo Hum. Gene Ther. Methods, 24, 104–116

Shi, W., Arnold, G.S. and Bartlett, J.S. (2001) Insertional mutagenesis of the adeno-associated virus type 2 (AAV2) capsid gene and generation of AAV2 vectors targeted to alternative cell-surface receptors Hum. Gene Ther., 12, 1697-1711

Stilwell, J.L. and Samulski, R.J. (2004) Role of viral vectors and virion shells in cellular gene expression Mol. Ther., 9, 337-346

Tse, L.V., Moller-Tank, S., Meganck, R.M. and Asokan, A. (2018) Mapping and engineering functional domains of the assembly-activating protein of adeno-associated viruses J. Virol, 92: e00393-18

Van Vliet, K., Blouin, V., Agbandje-McKenna, M. and Snyder, R.O. (2006) Proteolytic mapping of the adenoassociated virus capsid Mol. Ther., 14, 809-821

Van Vliet, K.M., Blouin, V., Brument, N., Agbandje-McKenna, M. and Snyder, R.O. (2008) The role of the adeno-associated virus capsid in gene transfer Methods Mol Biol., 437, 51-91

Wang, Y., Ling, C., Song, L., Wang, L., Aslanidi, G.V., et al (2012) Limitations of encapsidation of recombinant self-complementary adeno-associated viral genomes in different serotype capsids and their quantitation Hum. Gene Ther. Methods, 23, 225–233

Warrington, K.H., Gorbatyuk, O.S., Harrison, J.K., Opie, S.R., et al (2004) Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at its N terminus J. Virol., 78, 6595-6609

White, A.F., Mazur, M., Sorscher, E.J., Zinn, K.R. and Ponnazhagan, S. (2008) Genetic modification of adenoassociated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells Hum. Gene Ther., 19, 1407–1414

Wooley, D.P., Sharma, P., Weinstein, J.R., Narayan, P.K.L., Schaffer, D.V., Excoffon, K.J.D.A. (2017) A directed evolution approach to select for novel Adeno-associated virus capsids on an HIV-1 producer T cell line J. Virol. Meth., 250, 47–54

Wu, P., Xiao, W., Conlon, T., Hughes, J., et al (2000) Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism J. Virol., 74, 8635-8647

Zeng, C., Moller-Tank, S., Asokan, A. and Dragnea, B. (2017) Probing the link among genomic cargo, contact mechanics, and nanoindentation in recombinant adeno-associated vrus 2 J. Phys. Chem. B, 121, 1843-1853

Cardiac delivery and cardiomyocytes (see “Vascular smooth muscle delivery”)
Celiac artery delivery (see “Diabetes and other pancreatic disorders”)

Central nervous system
Addictive behaviours
Zweifel, L.S., Argilli, E., Bonci, A. and Palmiter, R.D. (2008) Role of NMDA receptors in dopamine neurons for plasticity and addictive behaviors Neuron, 59, 486-496

Adrenoleukodystrophy
Gong, Y., Mu, D., Prabhakar, S., Moser, A., Musolino, P., Ren, J-Q., Breakefield, X.O., Maguire, C.A. and Eichler, F.S. (2015) Adeno-associated virus serotype 9-mediated gene therapy for X-linked adrenoleukodystrophy Mol. Ther., 23, 824–834

Age-related effects
Bourdenx, M., Dovero, S., Engeln, M., Bido, S., Bastide, M.F., Dutheil, N., Vollenweider, I., Baud, L. et al (2015) Lack of additive role of ageing in nigrostriatal neurodegeneration triggered by α-synuclein overexpression Acta Neuropathologica Comm., 3: 46

Polinski, N.K., Gombash, S.E., Manfredsson, F.P., Lipton, J.W., Kemp, C.J., Cole-Strauss, A., Kanaan, N.M. et al (2015) Recombinant adeno-associated virus 2/5-mediated gene transfer is reduced in the aged rat midbrain Neurobiol. Aging, 36, 1110-1120

Aldehyde dehydrogenase
Mudannayake, J.M., Mouravlev, A., Fong, D.M. and Young, D. (2016) Transcriptional activity of novel ALDH1L1 promoters in the rat brain following AAV vector-mediated gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16075

Alzheimer’s disease (see also “Amyloid  precursor protein” and “Skeletal muscle delivery”) Alves, S., Bode, J., Bemelmans, A-P., von Kalle, C., Cartier, N. and Tews, B. (2016) Ultramicroscopy as a novel tool to unravel the tropism of AAV gene therapy vectors in the brain Sci. Rep., 6: 28272

Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S. and Ikezu, T. (2015) Depletion of microglia and inhibition of exosome synthesis halt tau propagation Nat. Neurosci., 18, 1584-1593

Bustos, F.J., Ampuero, E., Jury, N., Aguilar, R., Falahi, F., Toledo, J., Ahumada J., Lata, J., Cubillos, P. et al (2017) Epigenetic editing of the Dlg4/PSD95 gene improves cognition in aged and Alzheimer’s disease mice Brain, 140, 3252–3268

Chu, J., Giannopoulos, P.F., Ceballos-Diaz, C., Golde, T.E. and Pratico, D. (2012) Adeno-associated virusmediated brain delivery of 5-lipoxygenase modulates the AD like phenotype of APP mice Mol. Neurodegen., 7:1

Condello, C., Yuan, P., Schain, A. and Grutzendler, J. (2015) Microglia constitute a barrier that prevents neurotoxic protofibrillar Ab42 hotspots around plaques Nat. Commun., 6: 6176

Dayton, R.D., Wang, D.B., Cain, C.D., Schrott, L.M., et al (2012) Frontotemporal lobar degeneration-related proteins induce only subtle memory-related deficits when bilaterally overexpressed in the dorsal hippocampus Exp. Neurol., 233, 807–814

Fukuchi, K-i., Yang, J., Kou, J., Song, M., Lalonde, R., Planque, S.A. and Paul, S, (2018) Prophylactic and therapeutic applications of catalytic immunoglobulin gene delivery in a mouse model of Alzheimers disease Gowrishankar, S., Yuan, P., Wu, Y., Schrag, M., Paradise, S., Grutzendler, J., De Camilli, P. and Ferguson, S.M. (2015) Massive accumulation of luminal protease-deficient axonal lysosomes at Alzheimer’s disease amyloid plaques Proc. Natl. Acad. Sci. USA, 112, E3699–E3708

Hu, J., Liu, C-C., Chen, X-F., Zhang, Y-w., Xu, H. and Bu, G. (2015) Opposing effects of viral mediated brain expression of apolipoprotein E2 (apoE2) and apoE4 on apoE lipidation and Aβ metabolism in apoE4-targeted replacement mice Mol. Neurodegen., 10:6

Huang, Y-W.A., Zhou, B., Wernig, M. and Südhof, T.C. (2017) ApoE2, ApoE3, and ApoE4 differentially stimulate APP transcription and Ab secretion Cell 168, 427–441

Jaworski, T., Dewachter, I., Lechat, B., Croes, S., et al (2009) AAV-Tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice PLoS One, 4: e2780

Klein, R.L., Dayton, R.D., Tatom, J.B., Diaczynsky, C.G. and Salvatore, M.F. (2008) Tau expression levels from various adeno-associated virus vector serotypes produce graded neurodegenerative disease states Eur. J. Neurosci., 27, 1615-1625

Kou, J., Yang, J., Lim, J-E., Pattanayak, A., Song, M., Planque, S., Paul, S. and Fukuchi, K-i. (2015) Catalytic immunoglobulin gene delivery in a mouse model of Alzheimer’s disease: prophylactic and therapeutic applications Mol. Neurobiol., 51, 43–56

Lathuilière, A., Valdés, P., Papin, S., Cacquevel, M., Maclachlan, C., Knott, G.W., Muhs, A., Paganetti, P. and Schneider, B.L. (2017) Motifs in the tau protein that control binding to microtubules and aggregation determine pathological effects Sci, Rep., 7: 13556

Levites, Y., O’Nuallain, B., Puligedda, R.D., Ondrejcak, T., Adekar, S.P., Chen, C., Cruz, P.E., Rosario, A.M. et al (2015) A human monoclonal IgG that binds A assemblies and diverse amyloids exhibits anti-amyloid activities in vitro and in vivo J. Neurosci., 35, 6265- 6276

Liu, Y., Studzinski, C., Beckett, T., Murphy, M.P., Klein, R.L. and Hersh, L.B. (2010) Circulating neprilysin clears brain amyloid Mol. Cell. Neurosci., 45, 101–107

Ljungberg, M.C., Ali, Y.O., Zhu, J., Wu, C-S., et al (2012) CREB-activity and nmnat2 transcription are downregulated prior to neurodegeneration, while NMNAT2 over expression is neuroprotective, in a mouse model of human tauopathy Hum. Mol. Genet., 21, 251-267

Pascual-Lucas, M., da Silva, S.V., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C.M., Cuadrado-Tejedor, M. and Garcia-Osta, A. (2014) Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice EMBO Mol. Med., 6, 1246-1262

Ramirez, J.J., Poulton, W.E., Knelson, E., Barton, C., et al (2011) Focal expression of mutated tau in entorhinal cortex neurons of rats impairs spatial working memory Behav. Brain Res., 216, 332–340

Richter, M.C., Ludewig, S., Winschel, A., Abel, T., Bold, C., Salzburger, L.R., Klein, S., Han, K., Weyer. S.W. et al (2018) Distinct in vivo roles of secreted APP ectodomain variants APPsa and APPsb in regulation of spine density, synaptic plasticity, and cognition EMBO J., 37: e98335Rodríguez-Lebrón, E., Gouvion, C.M., Moore, S.A., Davidson, B.L. and Paulson, H.L. (2009) Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer’s disease Mol. Ther., 17, 1563–1573

Thinschmidt, J., López-Hernández, G.Y., Ren, K., King, M.A., et al (2008) Modulation of spontaneous hippocampal synaptic events with 5-hydroxyindole, 4OH-GTS-21, and rAAV-mediated α7 nicotinic receptor gene transfer Brain Res., 1203, 51-60

Wang, D.B., Dayton, R.D., Zweig, R.M. and Klein, R.L. (2010) Transcriptome analysis of a tau overexpression model in rats implicates an early pro-inflammatory response Exp. Neurol., 224, 197–206

Wang, X., Blanchard, J., Kohlbrenner, E., Clement, N., Linden, R.M., Radu, A., Grundke-Iqbal, I. and Iqbal, K. (2010) The carboxy-terminal fragment of inhibitor-2 of protein phosphatase-2A induces Alzheimer disease pathology and cognitive impairment FASEB J. 24, 4420–4432

Woodling, N.S., Colas, D., Wang, Q., Minhas, P., Panchal, M., Liang, X., Mhatre, S.D., Brown, H., Ko, N., Zagol-Ikapitte, I. et al (2016) Cyclooxygenase inhibition targets neurons to prevent early behavioural decline in Alzheimer’s disease model mice Brain, 139, 2063–2081

Yang, J., Pattanayak, A., Song, M., Kou, J., et al (2013) Muscle-directed anti-Aβ single-chain antibody delivery via AAV1 reduces cerebral Aβ load in an Alzheimer’s disease mouse model J. Mol. Neurosci., 49, 277–288

Yang, S., Cacquevel, M., Saksida, L.M., Bussey, T.J., Schneider, B.L., Aebischer, P., Melani, R. et al (2015) Perineuronal net digestion with chondroitinase restores memory in mice with tau pathology Exp. Neurol., 265, 48–58

Zhao, L., Gottesdiener, A.J., Parmar, M., Li, M., Kaminsky, S.M., Chiuchiolo, M.J., Sondhi, D., Sullivan, P.M., Holtzman, D.M., Crystal, R.G. and Paul, S.M. (2016) Intracerebral adeno-associated virus gene delivery of apolipoprotein E2 markedly reduces brain amyloid pathology in Alzheimer’s disease mouse models Neurobiol. Aging, 44, 159-172

AMPAR-synapse interactions
Han, K-S., Cooke, S.F. and Xu, W. (2017) Experience-dependent equilibration of AMPAR-mediated synaptic transmission during the critical period Cell Rep., 18, 892–904

Amygdal delivery
Bahi, A., Mineur, Y.S. and Picciotto, M.R. (2009) Blockade of protein phosphatase 2B activity in the amygdala increases anxiety- and depression-like behaviors in mice Biol. Psychiatry, 66, 1139-1146

Banerjee, A., Luong, J.A., Ho, A., Saib, A.O. and Ploski, J.E. (2016) Overexpression of Homer1a in the basal and lateral amygdala impairs fear conditioning and induces an autism-like social impairment Mol. Autism, 7:16

De Backer, M.W.A., Fitzsimons, C.P., Brans, M.A.D., Luijendijk, M.C.M., et al (2010) An adeno-associated viral vector transduces the rat hypothalamus and amygdala more efficient than a lentiviral vector BMC Neurosci., 11: 81

Del Boca, C., Lutz, P.E., Le Merrer, J., Koebal, P. and Kieffer, B.L. (2012) Cholecystokinin knock-down in the basolateral amygdala has anxiolytic and antidepressent-like effects in mice Neuroscience, 218, 185–195

De Solis, C.A., Holehonnur, R., Banerjee, A., Luong, J.A., Lella, S.K., Ho, A., Pahlavan, B. and Ploski, J.E. (2015) Viral delivery of shRNA to amygdala neurons leads to neurotoxicity and deficits in Pavlovian fear conditioning Neurobiol. Learn. Mem., 124, 34–47

De Solis, C.A., Hosek, M.P., Holehonnur, R., Ho, A., Banerjee, A., Luong, J.A., Jones, L.E., Chaturvedi, D. and Ploski, J.E. (2017) Adeno-associated viral serotypes differentially transduce inhibitory neurons within the rat amygdala Brain Res., 1672, 148–162

Holehonnur, R., Luong, J.A., Chaturvedi, D., Ho, A., et al (2014) Adeno-associated viral serotypes produce differing titers and differentially transduce neurons within the rat basal and lateral amygdala BMC Neurosci., 15: 28

Huang, Y.H., Ishikawa, M., Lee, B.R., Nakanishi, N., et al (2011) Searching for presynaptic NMDA receptors in the nucleus accumbens J. Neurosci., 31, 18453–18463

Jhang, J., Lee, H., Kang, M.S., Lee, H-S., Park, H. and Han, J-H. (2018) Anterior cingulate cortex and its input to the basolateral amygdala control innate fear response Nat. Comm., 9: 2744

Ji, G., Zhang, W., Mahimainathan, L., Narasimhan, M., Kiritoshi, T., Fan, X., Wang, J., Green, T.A. and Neugebauer, V. (2017) 5-HT2C receptor knockdown in the amygdala inhibits neuropathic-pain-related plasticity and behaviors J. Neurosci., 37, 1378 –1393

Kwon, J-T., Nakajima, R., Kim, H-S., Jeong, Y., Augustine, G.J. and Han, J-H. (2014) Optogenetic activation of presynaptic inputs in lateral amygdala forms associative fear memory Learn. Mem., 21, 627-633

Ma, Y-Y.,Wang, X., Huang, Y., Marie, H., Nestler, E.J., Schlüter, O.M. and Dong, Y. (2016) Re-silencing of silent synapses unmasks anti-relapse effects of environmental enrichment Proc. Natl. Acad. Sci. USA, 113, 5089–5094

Mineur, Y.S., Taylor, S.R. and Picciotto, M.R. (2014) Calcineurin downregulation in the amygdala is sufficient to induce anxiety-like and depression-like behaviors in C57BL/6J male mice Biol. Psychiatry, 75, 991–998

Tasan, R.O., Nguyen, N.K., Weger, S., Sartori, S.B., et al (2010) The central and basolateral amygdala are critical sites of neuropeptide Y/Y2 receptor-mediated regulation of anxiety and depression J. Neurosci., 30, 6282– 6290

Verma, D., Wood, J., Lach, G., Mietzsch, M., Weger, S., Heilbronn, R., Herzog, H., Bonaventure, P., Sperk, G. and Tasan, R.O. (2015) NPY Y2 receptors in the central amygdala reduce cued but not contextual fear Neuropharmacology, 99, 665-674

Amyloid ß precursor protein (see also “Alzheimer’s disease”)
Batista, A.R., Sena-Esteves, M. and Saraiva, M.J. (2013) Hepatic production of transthyretin L12P leads to intracellular lysosomal aggregates in a new somatic transgenic mouse model Biochim. Biophys. Acta, 1832, 1183–1193

Chakrabarty, P., Ceballos-Diaz, C., Beccard, A, Janus, C., et al (2010) IFN- promotes complement expression and attenuates amyloid plaque deposition in amyloid  precursor protein transgenic mice J. Immunol., 184, 5333-5343

Chu, J., Giannopoulos, P.F., Ceballos-Diaz, C., Golde, T.E. and Pratico, D. (2012) Adeno-associated virusmediated brain delivery of 5-lipoxygenase modulates the AD like phenotype of APP mice Mol. Neurodegen., 7:1

Fol1, R., Braudeau, J., Ludewig, S., Abel, T., Weyer, S.W., Roederer, J-P., Brod6, F., Audrain, M. et al (2016) Viral gene transfer of APPsα rescues synaptic failure in an Alzheimer’s disease mouse model Acta Neuropathol., 131, 247–266

Fukuchi, K-i., Tahara, K., Kim, H-D., Maxwell, A., et al. (2006) Anti-Aβ single-chain antibody delivery via adeno-associated virus for treatment of Alzheimer’s disease Neurobiol. Dis., 23, 502-511

Gong, Y., Meyer, E.M., Meyers, C.A., Klein, R.L., et al (2006) Memory-related deficits following selective hippocampal expression of Swedish mutation amyloid precursor protein in the rat Exp. Neurol., 200, 371-377

Hu, J., Liu, C-C., Chen, X-F., Zhang, Y-w., Xu, H. and Bu, G. (2015) Opposing effects of viral mediated brain expression of apolipoprotein E2 (apoE2) and apoE4 on apoE lipidation and Aβ metabolism in apoE4-targeted replacement mice Mol. Neurodegen., 10:6

Huang, Y-W.A., Zhou, B., Wernig, M. and Südhof, T.C. (2017) ApoE2, ApoE3, and ApoE4 differentially stimulate APP transcription and Ab secretion Cell 168, 427–441

Kim, J., Miller, V.M., Levites, Y., West, K.J., et al (2008) BRI2 (ITM2b) inhibits A deposition in vivo J. Neurosci., 28, 6030-6036

Latta, C.H., Sudduth, T.L., Weekman, E.M., Brothers, H.M., Abner, E.L., Popa, G.J., Mendenhall, M.D., Gonzalez-Oregon, F. Braun, K. and Wilcock, D.M. (2015) Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-β using BV2 microglial cells and APP/PS1 transgenic mice J. Neuroinflam., 12: 41

Lawlor, P.A., Bland, R.J., Das, P., Price, R.W., et al Novel rat Alzheimer’s disease models based on AAVmediated gene transfer to selectively increase hippocampal A levels Mol. Neurodegener., 2:11

Levites, Y., Jansen, K., Smithson, L.A., Dakin, R., et al (2006) Intracranial adeno-associated virus-mediated delivery of anti-pan amyloid, amyloid 40, and amyloid 42 single-chain variable fragments attenuates plaque pathology in amyloid precursor protein mice J. Neurosci., 26, 11923-11928

Levites, Y., O’Nuallain, B., Puligedda, R.D., Ondrejcak, T., Adekar, S.P., Chen, C., Cruz, P.E., Rosario, A.M. et al (2015) A human monoclonal IgG that binds A assemblies and diverse amyloids exhibits anti-amyloid activities in vitro and in vivo J. Neurosci., 35, 6265- 6276

Liu, Y., Studzinski, C., Beckett, T., Guan, H., et al (2009) Expression of neprilysin in skeletal muscle reduces amyloid burden in a transgenic mouse model of Alzheimer disease Mol. Ther., 17, 1381–1386

Liu, Y., Studzinski, C., Beckett, T., Murphy, M.P., et al (2010) Circulating neprilysin clears brain amyloid Mol. Cell. Neurosci., 45, 101–107

Ludwig, A., Blume, J., Diep, T-M., Yuan, J., et al (2009) Calsyntenins mediate TGN exit of APP in a kinesin-1- dependent manner Traffic, 10, 572–589

Meyer-Luehmann, M., Mielke, M., Spires-Jones, T.L., Stoothoff, W., et al (2009) A reporter of local dendritic translocation shows plaque-related loss of neural system function in APP-transgenic mice J. Neurosci., 29, 12636-12640

Mosser, S., Alattia, J-R., Dimitrov, M., Matz, A., Pascual, J., Schneider, B.L. and Fraering, P.C. (2015) The adipocyte differentiation protein APMAP is an endogenous suppressor of A production in the brain Hum. Mol. Genet., 24, 371–382

Richter, M.C., Ludewig, S., Winschel, A., Abel, T., Bold, C., Salzburger, L.R., Klein, S., Han, K., Weyer. S.W. et al (2018) Distinct in vivo roles of secreted APP ectodomain variants APPsa and APPsb in regulation of spine density, synaptic plasticity, and cognition EMBO J., 37: e98335

Rodríguez-Lebrón, E., Gouvion, C.M., Moore, S.A., Davidson, B.L., et al (2009) Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer’s disease Mol. Ther., 17, 1563–1573

Wang, X., Blanchard, J., Kohlbrenner, E., Clement, N., et al (2010) The carboxy-terminal fragment of inhibitor2 of protein phosphatase-2A induces Alzheimer disease pathology and cognitive impairment FASEB J. 24, 4420–4432

Weekman, E.M., Sudduth, T.L., Abner, E.L., Popa, G.J., Mendenhal, M.D., Brothers, H.M., Braun, K., Greenstein, A. and Wilcock, D.M. (2014) Transition from an M1 to a mixed neuroinflammatory phenotype increases amyloid deposition in APP/PS1 transgenic mice J. Neuroinflamm., 11: 127

Yang, J., Pattanayak, A., Song, M., Kou, J., et al (2013) Muscle-directed anti-Aβ single-chain antibody delivery via AAV1 reduces cerebral Aβ load in an Alzheimer’s disease mouse model J. Mol. Neurosci., 49, 277–288

Angelman syndrome
Daily, J.L., Nash, K., Jinwal, U., Golde, T., et al (2011) Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome PLoS One 6: e27221

Antidepressant effect
Del Boca, C., Lutz, P.E., Le Merrer, J., Koebal, P. and Kieffer, B.L. (2012) Cholecystokinin knock-down in the basolateral amygdala has anxiolytic and antidepressent-like effects in mice Neuroscience, 218, 185–195

Mineur, Y.S., Obayemi, A., Wigestrand, M.B., Fote, G.M., et al (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior Proc. Natl. Acad. Sci. USA, 110, 3573-3578

Anxiety
Mineur, Y.S., Obayemi, A., Wigestrand, M.B., Fote, G.M., et al (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior Proc. Natl. Acad. Sci. USA, 110, 3573-3578

Sink, K.S., Chung, A., Ressler, K.J., Davis, M., and Walker, D.L. (2013) Anxiogenic effects of CGRP within the BNST may be mediated by CRF acting at BNST CRFR1 receptors Behav. Brain Res., 243, 286– 293

Zhu, L-J., Li, T-Y., Luo, C-X., Jiang, N., Chang, L., Lin, Y-H., Zhou, H-H., Chen, C., Zhang, Y., Lu, W. et al. (2014) CAPON-nNOS coupling can serve as a target for developing new anxiolytics Nat. Med., 9, 1050-1054

Arcuate nucleus delivery
Benskey, M.J., Manfredsson, F.P., Lookingland, K.J. and Goudreau, J. L. (2015) The role of parkin in the differential susceptibility of tuberoinfundibular and nigrostriatal dopamine neurons to acute toxicant exposure Neurotoxicology, 46, 1–11

Astrocytes
Drinkut, A., Tereshchenko, Y., Schulz, J.B., Bähr, M., et al (2012) Efficient gene therapy for Parkinson’s disease using astrocytes as hosts for localized neurotrophic factor delivery Mol. Ther., 20, 534–543

Fong, D.M., Wu, A. and Young, D, (2018) Targeting transgene and DNA interference-based gene silencing sequences to astrocytes using viral vector-mediated appraches In Gene Therapy in Neurological Disorders Elsevier Inc. pp 41-61

Kostoula, C., Pascente, R., Ravizza, T., McCown, T., Schoch, S., Vezzani, A., Becker, A.J. and van Loo, K.M.J. (2018) Development of in vivo imaging tools for investigating astrocyte activation in epileptogenesis Mol. Neurobiol., 55, 4463–4472

Kunze, C., Börner, K., Kienle, E., Orschmann, T., Rusha, E., Schneider, M., Radivojkov-Blagojevic, M., Drukker, M. et al (2018) Synthetic AAV/CRISPR vectors for blocking HIV-1 expression in persistently infected astrocytes Glia. 66, 413–427

Li, K., Nicaise, C., Sannie, D., Hala, T.J., et al (2014) Overexpression of the astrocyte glutamate transporter GLT1 exacerbates phrenic motor neuron degeneration, diaphragm compromise, and forelimb motor dysfunction following cervical contusion spinal cord injury J. Neurosci., 34, 7622–7638

Mächler, P., Wyss, M.T., Elsayed, M., Stobart, J., Gutierrez, R., von Faber-Castell, A., Kaelin, V., Zuend, M., San Martín, A. et al (2016) In vivo evidence for a lactate gradient from astrocytes to neurons Cell Metabolism 23, 94–102

Meng, X., Yang, F., Ouyang, T., Liu, B., Wu, C. and Jiang, W. (2015) Specific gene expression in mouse cortical astrocytes is mediated by a 1740bp-GFAP promoter-driven combined adeno-associated virus Neurosci. Lett., 593, 45–50

Rincon, M.Y., de Vin, F., Duqué, S.I., Fripont, S., Castaldo, S.A., Bouhuijzen-Wenger, J. and Holt, M.G. (2018) Widespread transduction of astrocytes and neurons in the mouse central nervous system after systemic delivery of a selfcomplementary AAV-PHP.B vector Gene Ther., 25, 83–92

Shinohara, Y., Konno, A., Takahashi, N., Matsuzaki, Y., Kishi, S. and Hirai, H. (2016) Viral vector-based dissection of marmoset GFAP promoter in mouse and marmoset brains PLoS One, 11: e0162023

Taschenberger, G., Tereshchenko, J. and Kügler, S. (2017) A microRNA124 target sequence restores astrocyte
specificity of gfaABC1D-driven transgene expression in AAV-mediated gene transfer Mol. Ther. Nucl. Acids 8, 13-25

Weller, M.L., Stone, I.M., Goss, A., Rau, T., Rova, C. and Poulsen, D.J. (2008) Selective overexpression of excitatory amino acid transporter 2 (EAAT2) in astrocytes enhances neuroprotection from moderate but not severe hypoxia-ischemia Neuroscience, 155, 1204-1211

Young, D., Fong, D.M., Lawlor, P.A., Wu, A., Mouravlev, A., McRae, M., Glass, M., Dragunow, M. and During, M.J. (2014) Adenosine kinase, glutamine synthetase and EAAT2 as gene therapy targets for temporal lobe epilepsy Gene Ther., 21, 1029–1040

Autism
Banerjee, A., Luong, J.A., Ho, A., Saib, A.O. and Ploski, J.E. (2016) Overexpression of Homer1a in the basal and lateral amygdala impairs fear conditioning and induces an autism-like social impairment Mol. Autism, 7:

Benskey, M.J., Manfredsson, F.P., Lookingland, K.J. and Goudreau, J. L. (2015) The role of parkin in the differential susceptibility of tuberoinfundibular and nigrostriatal dopamine neurons to acute toxicant exposure Neurotoxicology, 46, 1–11

Rothwell, P.E., Fuccillo, M.V., Maxeiner, S., Hayton, S.J., Gokce, O., Lim, B.K., Fowler, S.C., Malenka, R.C. and Südhof, T.C. (2014) Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors Cell 158, 198–212

Axonal responses
Alves, J.N., Muir, E.M., Andrews, M.R., Ward, A., et al (2014) AAV vector-mediated secretion of chondroitinase provides a sensitive tracer for axonal arborisations J. Neurosci. Methods, 227 107–120

Kneynsberg A., Collier, T.J., Manfredsson, F.P. and Kanaan, N.M. (2016) Quantitative and semi-quantitative measurements of axonal degeneration in tissue and primary neuron cultures J. Neurosci. Meth., 266, 32–41

Van der Kallen, L.R., Eggers, R., Ehlert, E.M., Verhaagen, J., Smit, A.B. and van Kesteren, R.E. (2015) Genetic deletion of the transcriptional repressor NFIL3 enhances axon growth in vitro but not axonal repair in vivo PLoS One, 10: e0127163

Basal ganglia
Dardou, D., Monlezun, S., Foerch, P., Courade, J-P., et al (2013) A role for Sv2c in basal ganglia functions Brain Res., 1507, 61-73

Dodiya, H.B., Bjorklund, T., Stansell III, J., Mandel, R.J., et al (2010) Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates Mol. Ther., 18, 579–587

Blood-brain barrier
Dashkoff, J., Lerner, E.P., Truong, N., Klickstein, J.A., Fan, Z., Mu, D., Maguire, C.A., Hyman, B.T. and Hudry, E. (2016) Tailored transgene expression to specific cell types in the central nervous system after peripheral injection with AAV9 Mol. Ther. Meth. Clin. Devel., 3: 16081

Mendez-Gomez, H.R., Galera-Prat, A., Meyers, C., Chen, W., Singh, J., Carrion-Vazquez, M. and Muzyczka, N. (2015) Transcytosis in the blood–cerebrospinal fluid barrier of the mouse brain with an engineered receptor/ligand system Mol. Ther. Methods Clin. Dev., 2: 15037

Merkel, S.F., Andrews, A.M., Lutton, E.M., Mu, D., Hudry, E., Hyman, B.T., Maguire, C.A. and Ramirez, S.H. (2017) Trafficking of adeno-associated virus vectors across a model of the blood-brain barrier; a comparative study of transcytosis and transduction using primary human brain endothelial cells J. Neurochem., 140, 216- 230

Brain/CNS delivery
Dashkoff, J., Lerner, E.P., Truong, N., Klickstein, J.A., Fan, Z., Mu, D., Maguire, C.A., Hyman, B.T. and Hudry, E. (2016) Tailored transgene expression to specific cell types in the central nervous system after peripheral injection with AAV9 Mol. Ther. Meth. Clin. Devel., 3: 16081

Rincon, M.Y., de Vin, F., Duqué, S.I., Fripont, S., Castaldo, S.A., Bouhuijzen-Wenger, J. and Holt, M.G. (2018) Widespread transduction of astrocytes and neurons in the mouse central nervous system after systemic delivery of a selfcomplementary AAV-PHP.B vector Gene Ther., 25, 83–92

Brain ischaemia
Cabral-Miranda, F., Nicoloso-Simões, E., Adão-Novaes, J., Chiodo, V., Hauswirth, W.W., Linden, R., Barreto Chiarini, L. Petrs-Silva, H. (2017) rAAV8-733-Mediated gene transfer of CHIP/Stub-1 prevents hippocampal neuronal death in experimental brain ischemia Mol. Ther., 25, 392-400

Cardiac troponin T promoter
Chamberlain, K., Riyad, J.M., Garnett, T., Kohlbrenner, E., Mookerjee, A., Elmastour, F., Benard, L., Chen, J., VandenDriessche, T. et al (2018) A calsequestrin cis-regulatory motif coupled to a cardiac troponin T promoter improves cardiac adeno-associated virus serotype 9 transduction specificity Hum. Gene Ther., 29, 927-937

Capsid types
Chan, K.Y., Jang, M.J., Yoo, B.B., Greenbaum, A., Ravi, N., Wu, W-L., Sánchez-Guardado, L., Lois, C., Mazmanian, S.K., Deverman, B.E. and Gradinaru, V. (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems Nat. Neurosci., 20, 1172-1179

Choudhury, S.R., Fitzpatrick, Z., Harris, A.F., Maitland, S.A., Ferreira, J.S., Zhang, Y., Ma, S., Sharma, R.B. et al (2016) In vivo selection yields AAV-B1 capsid for central nervous system and muscle gene therapy Mol. Ther., 24, 1247–1257

Choudhury, S.R., Harris, A.F., Cabral, D.J., Keeler, A.M., Sapp, E., Ferreira, J.S., Gray-Edwards, H.L., Johnson, J.A. et al (2016) Widespread central nervous system gene transfer and silencing after systemic delivery of novel AAV-AS vector Mol. Ther., 24, 726-735

Caudate delivery
Dodiya, H.B., Bjorklund, T., Stansell III, J., Mandel, R.J., et al (2010) Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates Mol. Ther., 18, 579–587

Cerebellar delivery
El-Shamayleh, Y., Kojima, Y., Soetedjo, R. and Horwitz, G.D. (2017) Selective optogenetic control of Purkinje cells in monkey cerebellum Neuron, 95, 51–62

Huda, F., Fan, Y., Suzuki, M., Konno, A., Matsuzaki, Y., Takahashi, N., Chan, J.K.Y. and Hirai, H. (2016) Fusion of human fetal mesenchymal stem cells with degenerating cerebellar neurons in spinocerebellar ataxia Type 1 model mice PLoS One, 11: e0164202

Nitta, K., Matsuzaki, Y., Konno, A., and Hirai, H. (2017) Minimal Purkinje cell-specific PCP2/L7 promoter virally available for rodents and bon-human primates Mol. Ther. Meth. Clin. Dev., 6, 159-170

Roberts, M.S., Macauley, S.L., Wong, A.M., Yilmas, D., et al (2012) Combination small molecule PPT1 mimetic and CNS-directed gene therapy as a treatment for infantile neuronal ceroid lipofuscinosis J. Inherit. Metab. Dis., 35, 847–857

Shinohara, Y., Konno, A., Takahashi, N., Matsuzaki, Y., Kishi, S. and Hirai, H. (2016) Viral vector-based dissection of marmoset GFAP promoter in mouse and marmoset brains PLoS One, 11: e0162023

Sondhi, D., Scott, E.C., Chen, A., Hackett, N.R., Wong, A.M.S., Kubiak, A., Nelvagal, H.R., Pearse, Y., Cotman, S.L., Cooper, J.D. and Crystal, R.G. (2014) Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adeno-associated virus serotype rh.10 vector expressing the human CLN3 gene Hum. Gene Ther., 25, 223–239

Xiao, L., Bornmann, C., Hatstatt-Burklé, L. and Scheiffele, P. (2018) Regulation of striatal cells and goaldirected behavior by cerebellar outputs Nat. Comm., 9: 3133 Yoon, S.Y., Gay-Antaki, C., Ponde, D.E., Poptani, H., Vite, C.H. and Wolfe, J.H. (2014) Quantitative, noninvasive, in vivo longitudinal monitoring of gene expression in the brain by co-AAV transduction with a PET reporter gene Mol. Ther. Methods Clin. Dev., 1, 14016

Cerebral cortex delivery
Alves, J.N., Muir, E.M., Andrews, M.R., Ward, A., et al (2014) AAV vector-mediated secretion of chondroitinase provides a sensitive tracer for axonal arborisations J. Neurosci. Methods, 227 107–120

Bethge, P., Carta, S., Lorenzo, D.A., Egolf, L., Goniotaki, D., Madisen, L., Voigt, F.F., Chen, J.L. et al (2017) An R-CaMP1.07 reporter mouse for cell-type specific expression of a sensitive red fluorescent calcium indicator PLoS One, 12: e0179460

Boudreau, R.L., Martins, I. and Davidson, B.L. (2009) Artificial micro-RNAs as siRNA shuttles: improved safety as compared to shRNAs in vitro and in vivo Mol. Ther., 17, 169–175

Boudreau, R.L., Spengler, R.M. and Davidson, B.L. (2011) Rational design of therapeutic siRNAs: minimizing off-targeting potential to improve the safety of RNAi therapy for Huntington’s disease Mol. Ther., 19, 2169–2177

Cao, X., Li, L-P., Wang, Q., Wu, Q., et al (2013) Astrocyte-derived ATP modulates depressive-like behaviors Nat. Med., 19, 773-777

Chatterjee, S., Sullivan, H.A., MacLennan, B.J., Xu, R., Hou, Y.Y., Lavin, T.K., Lea, N.E., Michalski, J.E., Babcock, K.R. et al (2018) Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons Nat. Neurosci., 638, 638–646

Chen, J.L., Carta, S., Soldado-Magraner, J., Schneider, B.L. and Helmchen, F. (2013) Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex Nature, 499, 336-340

Chen, J.L., Margolis, D.J., Stankov, A., Sumanovski, L.T., Schneider, B.L. and Helmchen, F. (2015) Pathwayspecific reorganization of projection neurons in somatosensory cortex during learning Nat. Neurosci., 18, 1101-1108

Chu, J., Giannopoulos, P.F., Ceballos-Diaz, C., Golde, T.E. and Pratico, D. (2012) Adeno-associated virusmediated brain delivery of 5-lipoxygenase modulates the AD like phenotype of APP mice Mol. Neurodegen., 7:1

Dimidschstein, J., Chen, Q., Tremblay, R., Rogers, S.L., Saldi, G-A., Guo, L., Xu, Q., Liu, R., Lu, C., Chu, J., Grimley, J.S. et al (2016) A viral strategy for targeting and manipulating interneurons across vertebrate species Nat. Neurosci., 19, 1743-1749

Ellinwood, N.M., Ausseil, J., Desmaris, N., Bigou, S., et al (2011) Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes Mol. Ther., 19, 251–259

Huang, Y.H., Ishikawa, M., Lee, B.R., Nakanishi, N., et al (2011) Searching for presynaptic NMDA receptors in the nucleus accumbens J. Neurosci., 31, 18453–18463

Hutson, T.H., Verhaagen, J., Yáñez-Muñoz, R.J. and Moon, L.D.F. (2012) Corticospinal tract transduction: a comparison of seven adeno-associated viral vector serotypes and a non-integrating lentiviral vector Gene Ther., 19, 49–60

Janelidze, S., Nordström, U., Kügler, S. and Brundin, P. (2014) Pre-existing immunity to adeno-associated virus (AAV)2 limits transgene expression following intracerebral AAV2-based gene delivery in a 6- hydroxydopamine model of Parkinson’s disease J. Gene Med., 16, 300–308

Jara, J.H., Genc, B., Cox, G.A., Bohn, M.C., Roos, R.P., Macklis, J.D., Ulupinar, E. and Ozdinler, P.H. (2015) Corticospinal motor neurons are susceptible to increased ER stress and display profound degeneration in the absence of UCHL1 function Cerebral Cortex 25, 4259-4272

Jaworski, T., Dewachter, I., Lechat, B., Croes, S., et al (2009) AAV-Tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice PLoS One, 4: e2780

Leker, R.R., Soldner, F., Velasco, I., Gavin, D.K., et al (2007) Long-lasting regeneration after ischemia in the cerebral cortex Stroke, 38, 153-161

McBride, J.L., Pitzer, M.R., Boudreau, R.L., Dufour, B., et al (2011) Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington’s disease Mol. Ther., 19, 2152–2162

McCown, T.J. (2006) Adeno-associated virus-mediated expression and constitutive secretion of galanin suppresses limbic seizure activity in vivo Mol. Ther., 14, 63-68

Machado de Oliveira, R., Miranda, H.V., Francelle, L., Pinho, R., Szegö, E.M., Martinho, R., Munari, F., Lázaro, D.F., Moniot, S. et al (2017) The mechanism of sirtuin 2-mediated exacerbation of alpha-synuclein toxicity in models of Parkinson disease PLoS Biol., 15: e2000374

Mandel, R.J., Marmikon, D.J., Kirik, D., Chu, Y., Heindel, C., McCown, T., Gray, S.J. and Kordower, J. H. (2017) Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodemts and nonhuman primates Acta Neuropath. Comm., 5: 47

Mendez-Gomez, H.R., Galera-Prat, A., Meyers, C., Chen, W., Singh, J., Carrion-Vazquez, M. and Muzyczka, N. (2015) Transcytosis in the blood–cerebrospinal fluid barrier of the mouse brain with an engineered receptor/ligand system Mol. Ther. Methods Clin. Dev., 2: 15037

Meyer-Luehmann, M., Mielke, M., Spires-Jones, T.L., Stoothoff, W., et al (2009) A reporter of local dendritic translocation shows plaque-related loss of neural system function in APP-transgenic mice J. Neurosci., 29, 12636-12640

Nathanson, J.L., Yanagawa, Y., Obata, K. and Callaway, E.M. (2009) Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors Neuroscience, 161 441–450

Prabhakar, S., Goto, J., Zuang, X., Sena-Esteves, M., et al (2013) Stochastic model of Tsc1 lesions in mouse brain PLoS One, 8: e64224

Roberts, M.S., Macauley, S.L., Wong, A.M., Yilmas, D., et al (2012) Combination small molecule PPT1 mimetic and CNS-directed gene therapy as a treatment for infantile neuronal ceroid lipofuscinosis J. Inherit. Metab. Dis., 35, 847–857

Shinohara, Y., Konno, A., Takahashi, N., Matsuzaki, Y., Kishi, S. and Hirai, H. (2016) Viral vector-based dissection of marmoset GFAP promoter in mouse and marmoset brains PLoS One, 11: e0162023

Stoica, L., Todeasa, S.H., Cabrera, G.T., Salameh, J.S., ElMallah, M.K., Mueller, C., Brown, Jr, R.H., and Sena-Esteves, M. (2016) Adeno-associated virus–delivered artificial microRNA extends survival and delays paralysis in an amyotrophic lateral sclerosis mouse model Ann. Neurol., 79, 687–700

Suska, A., Lee, B.R., Huang, Y.H., Dong, Y. and Schlüter, O.M. (2013) Selective presynaptic enhancement of the prefrontal cortex to nucleus accumbens pathway by cocaine Proc. Natl. Acad. Sci. USA, 110, 710-718

Tan, E.M., Yamaguchi, Y., Horwitz. G.D., Gosgnach, S., et al (2006) Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor Neuron, 51, 157-170

Tardieu, M., Zérah, M., Husson, B., de Bournonville, S., Deiva, K., Adamsbaum, K., Vincent, F., Hocquemiller, M., Broissand, C., Furlan, V. et al (2014) Intracerebral administration of adeno-associated viral vector Serotype rh.10 carrying human SGSH and SUMF1 cDNAs in children with muco-polysaccharidosis type IIIA disease: results of a phase I/II trial Hum. Gene Ther., 25, 506–516

Wang, X., Blanchard, J., Kohlbrenner, E., Clement, N., et al (2010) The carboxy-terminal fragment of inhibitor2 of protein phosphatase-2A induces Alzheimer disease pathology and cognitive impairment FASEB J. 24, 4420–4432

Weekman, E.M., Sudduth, T.L., Abner, E.L., Popa, G.J., Mendenhal, M.D., Brothers, H.M., Braun, K., Greenstein, A. and Wilcock, D.M. (2014) Transition from an M1 to a mixed neuroinflammatory phenotype increases amyloid deposition in APP/PS1 transgenic mice J. Neuroinflamm., 11: 127

Winner, L.K., Beard, H., Hassiotis, S., Lau, A.A., Luck, A.J., Hopwood, J.J. and Hemsley, K.M. (2016) A preclinical study evaluating AAVrh10-based gene therapy for Sanfilippo syndrome Hum. Gene Ther., 27, 363-375

Zhang, S., Xu, M., Chang, W-C., Ma, C., Do, J.P.H., Jeong, D., Lei, T., Fan, J.L. and Dan, Y. (2016) Organization of long-range inputs and outputs of frontal cortex for top-down control Nat. Neurosci., 19, 1506-1512

Cerebrospinal fluid delivery
Hinderer, C., Katz, N., Louboutin, J-P., Bell, P., Yu, H., Nayal, M., Kozarsky, K., O’Brien, W.T., Goode, T. and Wilson, J.M. (2016) Delivery of an adeno-associated virus vector into cerebrospinal fluid attenuates central nervous system disease in mucopolysaccharidosis Type II Mice Hum. Gene Ther., 27, 906-915

Pasta, S., Akhile, O., Tabron, D., Ting, F., Shackleton, G. and Watson, G. (2015) Delivery of the 7- dehydrocholesterol reductase gene to the central nervous system using adeno-associated virus vector in a mouse model of Smith-Lemli-Opitz Syndrome Mol. Genet. Metab. Rep., 4, 92–98

Cerebroventricular delivery
Boender, A.J., Koning, N.A., van den Heuvel, J.K., Luijendijk, M.C.M., et al (2014) AAV-mediated gene transfer of the obesity-associated gene Etv5 in rat midbrain does not affect energy balance or motivated behavior PLoS One, 9: e94159

Carty, N., Berson, N., Tillack, K., Thiede, C., Scholz, D., Kottig, K., Sedaghat, Y., Gabrysiak, C. et al (2015) Characterization of HTT inclusion size, location, and timing in the zQ175 mouse model of Huntington´s disease: an in vivo high-content imaging study PLoS One, 10: e0123527

Ceballos-Diaz, C., Rosario, A.M., Park, H-J., Chakrabarty, P., Sacino, A., Cruz, P.E., Siemienski, Z., Lara, N. et al (2015) Viral expression of ALS-linked ubiquilin-2 mutants causes inclusion pathology and behavioral deficits in mice Mol. Neurodegener., 10 :25

Cook, C., Kang, S.S., Carlomagno, Y., Lin, W-L., Yue, M., Kurti, A., Shinohara, M., Jansen-West, K., Perkerson, E. et al (2015) Tau deposition drives neuropathological, inflammatory and behavioral abnormalities independently of neuronal loss in a novel mouse model Hum. Mol. Genet., 24. 6198-6212

Deczkowska, A., Matcovitch-Natan, O., Tsitsou-Kampeli, A., Ben-Hamo, S., Dvir-Szternfeld, R., Spinrad, A., Singer, O., David, E., Winter, D.R. et al (2017) Mef2C restrains microglial inflammatory response and is lost in brain ageing in an IFN-I-dependent manner Nat. Comm., 8: 717

Delenclos, M., Faroqi, A.H., Yue, M., Kurti, A., Castanedes-Casey, M., Rousseau, L., Phillips, V., Dickson, D.W., Fryer, J.D. and McLean, P.J. (2017) Neonatal AAV delivery of alpha-synuclein induces pathology in the adult mouse brain Acta Neuropath. Comm., 5: 51

Dirren, E., Towne, C.L., Setola, V., Redmond Jr. D.E., et al (2014) Intra-cerebroventricular injection of adenoassociated virus 6 and 9 vectors for cell type–specific transgene expression in the spinal cord Hum. Gene Ther., 25, 109–120

Golebiowski, D., van der Bom, I.M.J., Kwon, C-S., Miller, A.D., Petrosky, K., Bradbury, A.M., Maitland, S., Kühn, A.L., Bishop, N. et al (2017) Direct intracranial injection of AAVrh8 encoding monkey β-Nacetylhexosaminidase causes neurotoxicity in the primate brain Hum. Gene Ther., 28, 510-522

Gong, Y., Mu, D., Prabhakar, S., Moser, A., Musolino, P., Ren, J-Q., Breakefield, X.O., Maguire, C.A. and Eichler, F.S. (2015) Adeno-associated virus serotype 9-mediated gene therapy for X-linked adrenoleukodystrophy Mol. Ther., 23, 824–834

Kou, J., Yang, J., Lim, J-E., Pattanayak, A., Song, M., Planque, S., Paul, S. and Fukuchi, K-i. (2015) Catalytic immunoglobulin gene delivery in a mouse model of Alzheimer’s disease: prophylactic and therapeutic applications Mol. Neurobiol., 51, 43–56

Levites, Y., O’Nuallain, B., Puligedda, R.D., Ondrejcak, T., Adekar, S.P., Chen, C., Cruz, P.E., Rosario, A.M. et al (2015) A human monoclonal IgG that binds A assemblies and diverse amyloids exhibits anti-amyloid activities in vitro and in vivo J. Neurosci., 35, 6265- 6276

Odermatt, P., Trüb, J., Furrer, L., Fricker, R., Marti, A. and Schümperli, D. (2016) Somatic therapy of a mouse SMA model with a U7 snRNA gene correcting SMN2 splicing Mol. Ther., 1797–1805

Platt, T.L., Beckett, T.L., Kohleer, Niedowicz, K.D.M. and Murphy, M.P. (2016) Obesity, diabetes, and leptin resistance promote tau pathology in a mouse model of disease Neuroscience 315, 162–174

Prabhakar, S., Zhang, X., Goto, J., Han, S., Lai, C., Bronson, R., Sena-Esteves, M., Ramesh, V. et al (2015) Survival benefit and phenotypic improvement by hamartin gene therapy in a tuberous sclerosis mouse brain model Neurobiol. Dis., 82, 22–31

Rosario, A.M., Cruz, P.E., Ceballos-Diaz, C., Strickland, M.R., Siemienski, Z., Pardo, M., Schob, K-L., Li, A., Aslanidi, G.V. et al (2016) Microglia-specific targeting by novel capsid-modified AAV6 vectors Mol. Ther. Meth. Clin. Dev., 3: 16026

Sasaguri, H., Chew, J., Xu, Y-F., Gendron, T.F., Garrett, A., Lee, C.W., Jansen-West, K., Bauer, P.O. et al (2016) The extremeN-terminus of TDP-43 mediates the cytoplasmic aggregation of TDP-43 and associated toxicity in vivo Brain Res., 1647, 57–64

Cholecystokinin knock-down
Del Boca, C., Lutz, P.E., Le Merrer, J., Koebal, P. and Kieffer, B.L. (2012) Cholecystokinin knock-down in the basolateral amygdala has anxiolytic and antidepressent-like effects in mice Neuroscience, 218, 185–195

Cholinergic neuron regulation
Aldrin-Kirk, P., Davidsson, M., Holmqvist, S., Li, J-Y. and Björklund, T. (2014) Novel AAV based rat model of forebrain synucleinopathy shows extensive pathologies and progressive loss of cholinergic interneurons PLoS One, 9: e100869

Aldrin-Kirk, P., Heuer, A., Ottosson, D.R., Davidsson, M., Mattsson, B. and Björklund, T. (2018) Chemogenetic modulation of cholinergic interneurons reveals their regulating role on the direct and indirect output pathways from the striatum Neurobiol. Dis., 109, 148–162

Tomioka, T., Shimazaki, T., Yamauchi, T., Oki, T., et al (2014) LIM homeobox 8 (Lhx8) is a key regulator of the cholinergic neuronal function via a tropomyosin receptor kinase A (TrkA)-mediated positive feedback loop J. Biol. Chem., 289, 1000–1010

Chondroitinase
Alves, J.N., Muir, E.M., Andrews, M.R., Ward, A., et al (2014) AAV vector-mediated secretion of chondroitinase provides a sensitive tracer for axonal arborisations J. Neurosci. Methods, 227 107–120

Chronic social isolation stress
Zelikowsky, M., Hui, M., Karigo, T., Choe, A., Yang, B., Blanco, M.R., Beadle, K., Gradinaru, V., Deverman, B.E. and Anderson, D.J. (2018) The neuropeptide Tac2 controls a distributed brain state induced by chronic social isolation stress Cell, 173, 1265–1279

Circadian system
Enokia, R., Ono, D., Hasan, M.T., Honma, S. et al (2012) Single-cell resolution fluorescence imaging of circadian rhythms detected with a Nipkow spinning disk confocal system J. Neurosci. Methods, 207, 72– 79

Landgraf, D., Long, J.E., Proulx, C.D., Barandas, R., Malinow, R. and Welsh, D.K. (2016) Genetic disruption of circadian rhythms in the suprachiasmatic nucleus causes helplessness, behavioral despair, and anxiety-like behavior in mice Biol. Psych., 80, 827–835

Roybal, K., Theobold, D., Graham, A., DiNieri, J.A., et al (2007) Mania-like behaviour induced by disruption of CLOCK Proc. Natl. Acad. Sci. USA, 104, 6406-6411

Cisterna magna delivery
Hinderer, C., Bell, P., Vite, C.H., Louboutin, J-P., Grant, R., Bote, E., Yu, H., Pukenas, B., Hurst, R. and Wilson, J.M. (2014) Widespread gene transfer in the central nervous system of cynomolgus macaques following delivery of AAV9 into the cisterna magna Mol. Ther. Methods Clin. Dev., 1: 14051

Lukashchuk, V., Lewis, K.E., Coldicott, I., Grierson, A.J. and Azzouz, M. (2016) AAV9-mediated central nervous system–targeted gene delivery via cisterna magna route in mice Mol. Ther. Methods Clin. Dev., 3:15055

Yoon, S.Y., Bagel, J.H., O’Donnell, P., Vite, C.H. and Wolfe, J.H. (2016) Clinical improvement of alphamannosidosis cat following a single cisterna magna infusion of AAV1 Mol. Ther., 24, 26-33

CNS disease
Hinderer, C., Katz, N., Louboutin, J-P., Bell, P., Yu, H., Nayal, M., Kozarsky, K., O’Brien, W.T., Goode, T. and Wilson, J.M. (2016) Delivery of an adeno-associated virus vector into cerebrospinal fluid attenuates central nervous system disease in mucopolysaccharidosis Type II Mice Hum. Gene Ther., 27, 906-915

Cocaine
Chandra, R., Francis, T.C., Konkalmatt, P., Amgalan, A., Gancarz, A.M., Dietz, D.M. and Lobo, M.K. (2015) Opposing role for Egr3 in nucleus accumbens cell subtypes in cocaine action J. Neurosci., 35, 7927–7937

Harasta, A.E., Power, J.M., von Jonquieres, G., Karl, T., Drucker, D.J., Housley, G.D., Schneider, M. and Klugmann, M. (2015) Septal glucagon-like peptide 1 receptor expression determines suppression of cocaineinduced behavior Neuropsychopharmacology, 40, 1969–1978

Ma, Y-Y., Wang, X., Huang, Y., Marie, H., Nestler, E.J., Schlüter, O.M. and Dong, Y. (2016) Re-silencing of silent synapses unmasks anti-relapse effects of environmental enrichment Proc. Natl. Acad. Sci. USA, 113, 5089–5094

Murthya, V., Gao, Y., Geng, L., LeBrasseur, N.K., et al (2014) Physiologic and metabolic safety of butyrylcholinesterase gene therapy in mice Vaccine, 32, 4155–4162

Neumann, P.A., Wang, Y., Yan, Y., Wang, Y., Ishikawa, M., Cui, R., Huang, Y.H. et al (2016) Cocaineinduced synaptic alterations in thalamus to nucleus accumbens projection Neuropsychopharmacology, 41, 2399–2410

Suska, A., Lee, B.R., Huang, Y.H., Dong, Y. and Schlüter, O.M. (2013) Selective presynaptic enhancement of the prefrontal cortex to nucleus accumbens pathway by cocaine Proc. Natl. Acad. Sci. USA, 110, 710-718

Yu, J., Yan, Y., Li, K-L., Wang, Y., Huang, Y.H., Urban, N.N., Nestler, E.J., Schlüter, O.M. and Dong, Y. (2017) Nucleus accumbens feedforward inhibition circuit promotes cocaine self-administration Proc. Natl. Acad. Sci. USA, 114, E8750–E8759

Cognitive aging/defects
Bean, L.A., Kumar, A., Rani, A., Guidi, M., Rosario, A.M., Cruz, P.E., Golde, T.E. and Foster, T.C. (2015) Reopening the critical window for estrogen therapy J. Neurosci., 35, 16077–16093

Gerstein, H., Lindstrom, M.J. and Burger, C. (2013) Gene delivery of Homer1c rescues spatial learning in a rodent model of cognitive aging Neurobiol. Aging, 34, 1963 1970

Hall, H., Jewett, M., Landeck, N., Nilsson, N., Schagerlof, U., et al (2013) Characterization of cognitive deficits in rats overexpressing human alpha-synuclein in the ventral tegmental area and medial septum using recombinant adeno-associated viral vectors PLoS One 8: e64844

Corpus callosum
Francis, J.S., Wojtas, I., Markov, V., Gray, S.J., McCown, T.J., Samulski, R.J., Bilaniuk, L.T. Wang, D-J. et al (2016) N-acetylaspartate supports the energetic demands of developmental myelination via oligodendroglial aspartoacylase Neurobiol. Dis., 96, 323–334

Corticotropin-releasing hormone type 1 receptor
Bender, J., Engeholm, M., Ederer, M.S., Breu, J., Møller, T.C., Michalakis, S., Rasko, T. 5, Wanker, E.E. et al (2015) Corticotropin-releasing hormone receptor type 1 (CRHR1) clustering with MAGUKs is mediated via its C-terminal PDZ binding motif PLoS One, 10: e0136768

Cre
Bethge, P., Carta, S., Lorenzo, D.A., Egolf, L., Goniotaki, D., Madisen, L., Voigt, F.F., Chen, J.L. et al (2017) An R-CaMP1.07 reporter mouse for cell-type specific expression of a sensitive red fluorescent calcium indicator PLoS One, 12: e0179460

Deverman, B.E., Pravdo, P.L., Simpson, B.P., Kumar, S.R., Chan, K.Y., Banerjee, A., Wu, W-L., Yang, B., Huber, N., Pasca, S.P. and Gradinaru, V. (2016) Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain Nat. Biotech., 34, 204-209

Prabhakar, S., Goto, J., Zuang, X., Sena-Esteves, M., et al (2013) Stochastic model of Tsc1 lesions in mouse brain PLoS One, 8: e64224

Schindler, S.E., McCall, J.G., Yan, P., Hyrc, K.L., Li, M., Tucker, C.L., Lee, J-M., Bruchas, M.R. and Diamond, M.I. (2015) Photo-activatable Cre recombinase regulates gene expression in vivo Sci. Rep., 5: 13627

Werfel, S., Jungmann, A., Lehmann, L.., Ksienzyk, J., Bekeredjian, R., Kaya, Z., Leuchs, B., Nordheim, A., Backs, J., Engelhardt, S. et al (2014) Rapid and highly efficient inducible cardiac gene knockout in adultmice using AAV-mediated expression of Cre recombinase Cardiovasc. Res., 104, 15–23

CREB
Ljungberg, M.C., Ali, Y.O., Zhu, J., Wu, C-S., et al (2012) CREB-activity and NMAT2 transcription are downregulated prior to neurodegeneration, while NMNAT2 over expression is neuroprotective, in a mouse model of human tauopathy Hum. Mol. Genet., 21, 251-267

Cynomolgus CNS delivery
Hinderer, C., Bell, P., Vite, C.H., Louboutin, J-P., Grant, R., Bote, E., Yu, H., Pukenas, B., Hurst, R. and Wilson, J.M. (2014) Widespread gene transfer in the central nervous system of cynomolgus macaques following delivery of AAV9 into the cisterna magna Mol. Ther. Methods Clin. Dev., 1: 14051

Delivery and expression in the CNS – methodologies and reviews
Broekman, M.L.D., Comer, L.A., Hyman, B.T. and Sena-Esteves, M. (2006) Adeno-associated virus vectors serotyped with AAV8 capsid are more efficient than AAV-1 or –2 serotypes for widespread gene delivery to the neonatal mouse brain Neuroscience, 138, 501-510

Burger, C., Gorbatyuk, O.S., Velardo, M.J., Peden, C.S., et al (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2 and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system Mol. Ther., 10, 302-317

Dashkoff, J., Lerner, E.P., Truong, N., Klickstein, J.A., Fan, Z., Mu, D., Maguire, C.A., Hyman, B.T. and Hudry, E. (2016) Tailored transgene expression to specific cell types in the central nervous system after peripheral injection with AAV9 Mol. Ther. Meth. Clin. Devel., 3: 16081

Davis, A.S., Federici, T., Ray, W.C., Boulis, N.M., O’Connor, D., Clark, K.R. and Bartlett, J.S. (2015) Rational design and engineering of a modified adeno-associated virus (AAV1)-based vector system for enhanced retrograde gene delivery Neurosurgery, 76, 216-225

Dirren, E. and Schneider, B.L. (2014) Application of viral vectors to motor neuron disorders In Viral Vector Approaches in Neurobiology and Brain Diseases, Neuromethods, vol. 82, (ed. Brambilla, R.) Springer Science+Business Media, LLC, pp 221-242

Dutheil, N. and Bezard, E. (2014) Adeno-associated virus-based vectors In Viral Vector Approaches in Neurobiology and Brain Diseases, Neuromethods, vol. 82, (ed. Brambilla, R.) Springer Science+Business Media, LLC, pp 27-49

Hinderer, C., Bell, P., Katz, N., Vite, C.H., Louboutin, J-P., Bote, E., Yu, H., Zhu, Y., Casal, M.L., Bagel, J. (2018) Evaluation of intrathecal routes of administration for adeno-associated viral vectors in large animals Hum. Gene Ther., 29, 15-24

Gray, S.J., Kalburgi, S,N., McCown, T.J. and Samulski, R.J. (2013) Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates Gene Ther., 20, 450–459

Klein, R.L., Wang, D.B. and King, M.A. (2009) Versatile somatic gene transfer for modeling neurodegenerative diseases Neurotox. Res., 16, 329–342

Miyake, N., Miyake, K., Yamamoto, M., Hirai, Y. and Shimada, T. (2011) Global gene transfer into the CNS across the BBB after neonatal systemic delivery of single-stranded AAV vectors Brain Res., 1389, 19-26

Okada, T., Nomoto, T., Shimazaki, K., Lijun, W., et al (2002) Adeno-associated virus vectors for gene transfer to the brain Methods, 28, 237-247

Paterna, J-C. and Büeler, H. (2002) Recombinant adeno-associated virus vector design and gene expression in the mammalian brain Methods, 28, 208-218

Peden, C.S., Burger, C., Muzyczka, N. and Mandel, R.J. (2004) Circulating anti-wild type adeno-associated virus type 2 (AAV2) antibodies inhibit recombinant AAV2 (rAAV2)-mediated, but not rAAV5-mediated, gene transfer in the brain J. Virol., 78, 6344-6359

Peel, A.L. and Klein, R.L. (2000) Adeno-associated virus vectors: activity and applications in the CNS J. Neurosci. Meth., 98, 95-104

Ruitenberg, M.J., Eggers, R., Boer, G.J. and Verhaagen, J. (2002) Adeno-associated viral vectors as agents for gene delivery: application in disorders and trauma of the central nervous system Methods, 28, 182-194

Tang, W., Ehrlich, I., Wolff, S.B.E., Michalski, A-M., Wölfl, S., et al (2009) Faithful expression of multiple proteins via 2A-peptide self-processing: a versatile and reliable method for manipulating brain circuits J. Neurosci., 29, 8621– 8629

Volpicelli-Daley, L.A., Kirik, D., Stokya, L.E., Standaert, D.G. and Hartms A.S., J. Neurochem. (2016) How can rAAV--synuclein and the fibril -synuclein models advance our understanding of Parkinson’s disease? J. Neurochem., 139 (Suppl. 1), 131–155

Van der Perren, A., Toelen, J., Taymans, J-M.and Baekelandt, V. (2012) Using recombinant adeno-associated viral vectors for gene expression in the brain In Controlled Genetic Manipulations, Neuromethods, vol. 65 (Ed. Morozov, A.) Springer Science+Business Media, pp 47-68

Wang, C., Wang, C-M., Clark, K.R. and Sferra, T.J. (2003) Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain Gene Ther., 10, 1528-1534

Dementia
Levites, Y., O’Nuallain, B., Puligedda, R.D., Ondrejcak, T., Adekar, S.P., Chen, C., Cruz, P.E., Rosario, A.M. et al (2015) A human monoclonal IgG that binds A assemblies and diverse amyloids exhibits anti-amyloid activities in vitro and in vivo J. Neurosci., 35, 6265- 6276

Nicholson, A.M., Zhou, X., Perkerson, R.B., Parsons, T.M., Chew, J., Brooks, M., DeJesus-Hernandez, M., Finch, N.A., Matchett, B.J. et al (2018) Loss of Tmem106b is unable to ameliorate frontotemporal dementia-like phenotypes in an AAV mouse model of C9ORF72-repeat induced toxicity Acta Neuropathol. Commun., 6: 42

Depression (see also “Amygdal delivery”)
Dogra, S., Kumar, A., Umrao, D., Sahasrabuddhe, A.A. and Yadav, P.M. (2016) Chronic Kappa opioid receptor activation modulates NR2B: Implication in treatment resistant depression Sci. Rep., 6: 33401

Landgraf, D., Long, J.E., Proulx, C.D., Barandas, R., Malinow, R. and Welsh, D.K. (2016) Genetic disruption of circadian rhythms in the suprachiasmatic nucleus causes helplessness, behavioral despair, and anxiety-like behavior in mice Biol. Psych., 80, 827–835

Knowland, D., Lilascharoen, V., Pham Pacia, C., Shin, S., Wang, E.H-J. and Lim, B.K. (2017) Distinct ventral pallidal neural populations mediate separate symptoms of depression Cell, 170, 284-297

Mineur, Y.S., Taylor, S.R. and Picciotto, M.R. (2014) Calcineurin downregulation in the amygdala is sufficient to induce anxiety-like and depression-like behaviors in C57BL/6J male mice Biol. Psychiatry, 75, 991–998

Song, L., Wang, H., Wang, Y-J., Wang, J-L., Zhu, Q., Wu, F., Zhang, W. and Jiang, B. (2018) Hippocampal PPARα is a novel therapeutic target for depression and mediates the antidepressant actions of fluoxetine in mice Br. J. Pharmacol., 175, 2968–2987

DNA bar-code
Marsic, D., Méndez-Gómez, H.R. and Zolotukhin, S. (2015) High-accuracy biodistribution analysis of adenoassociated virus variants by double barcode sequencing Mol. Ther. Methods Clin. Dev., 2:15041

Dopamine/Dopaminergic neurons
Cederfjäll, E., Sahin, G., Kirik, D. and Björklund, T. (2012) Design of a single AAV vector for co-expression of TH and GCH1 to establish continuous DOPA synthesis in a rat model of Parkinson’s disease Mol. Ther., 20, 1315–1326

Crook, Z.R. and Housman, D.E. (2012) Dysregulation of dopamine receptor D2 as a sensitive measure for Huntington disease pathology in model mice Proc. Natl. Acad. Sci. USA, 109, 7487–7492

Decressac, M., Mattsson, B. and Björklund, A. (2012) Comparison of the behavioural and histological characteristics of the 6-OHDA and α-synuclein rat models of Parkinson’s disease Exp. Neurol., 235, 306–315

Doucet-Beaupré, H., Gilbert, C., Profes, M.S., Chabrat, A., Pacelli, C., Giguère, N., Rioux, V., Charest, J., Deng, Q. et al (2016) Lmx1a and Lmx1b regulate mitochondrial functions and survival of adult midbrain dopaminergic neurons Proc. Natl. Acad. Sci. USA, 111, E4387-E4396

Gong, Y., Meyer, E.M., Meyers, C.A., Klein, R.L., et al (2006) Memory-related deficits following selective hippocampal expression of Swedish mutation amyloid precursor protein in the rat Exp. Neurol., 200, 371-377

Gordon, R., Neal, M.L., Luo, J., Langley, M.R., Harischandra, D.S., Panicker, N., Charli, A., Jin, H., Anantharam, V. et al (2016) Prokineticin-2 upregulation during neuronal injury mediates a compensatory protective response against dopaminergic neuronal degeneration Nat. Comm., 7: 12932

Grieder, T.E., Herman, M.A., Contet, C., Tan, L.A., Vargas-Perez, H., Cohen, A., Chwalek, M., Maal-Bared, G. et al (2014) VTA CRF neurons mediate the aversive effects of nicotine withdrawal and promote intake escalation Nat. Neurosci., 17, 1751-1758

Khodr, C.E., Pedapati, J., Han, Y. and Bohn, M.C. (2012) Inclusion of a portion of the native SNCA 30UTR reduces toxicity of human S129A SNCA on striatal-projecting dopamine neurons in rat substantia nigra Develop. Neurobiol., 72, 906–917

Klein, R.L., Dayton, R.D., Leidenheimer, N.J., Jansen, K., et al (2006) Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins Mol. Ther., 13, 517-527

Liu, C., Kershberg, L., Wang, J., Schneeberger, S, and Kaeser, P.S. (2018) Dopamine secretion is mediated by sparse active zone-like release sites Cell, 172, 706–718

McFarland, N.R., Dimant, H., Kibuuka, L., Ebrahimi-Fakhari, D., et al (2014) Chronic treatment with novel small molecule Hsp90 inhibitors rescues striatal dopamine levels but not -synuclein-induced neuronal cell loss PLoS One, 9: e86048

Dorsal root ganglia
Enomoto, M., Hirai, T., Kaburagi, H. and Yokota, T. (2016) Efficient gene suppression in dorsal root ganglia and spinal cord using adeno-associated virus vectors encoding short-hairpin RNA In SiRNA Delivery Methods: Methods and Protocols, Methods in Molecular Biology, vol. 1364 (eds. Shum, K. and Rossi, J.) Springer Science+Business Media New York, pp 277-290

Fischer, G., Pan, B., Vilceanu, D., Hogan, Q.H. and Yu, H. (2014) Sustained relief of neuropathic pain by AAVtargeted expression of CBD3 peptide in rat dorsal root ganglion Gene Ther., 21, 44–51

Foust, K.D., Poirier, A., Pacak, C.A., Mandel, R.J. and Flotte, T.R. (2008) Neonatal intraperitoneal or intravenous injections of recombinant adeno-associated virus type 8 transduce dorsal root ganglia and lower motor neurons Hum. Gene Ther., 19, 61-69

Hinderer, C., Bell, P., Katz, N., Vite, C.H., Louboutin, J-P., Bote, E., Yu, H., Zhu, Y., Casal, M.L., Bagel, J. (2018) Evaluation of intrathecal routes of administration for adeno-associated viral vectors in large animals Hum. Gene Ther., 29, 15-24

Iwamoto, N., Watanabe, A., Yamamoto, M., Miyake, N., et al (2009) Global diffuse distribution in the brain and efficient gene delivery to the dorsal root ganglia by intrathecal injection of adeno-associated viral vector serotype 1 J. Gene Med., 11, 498-505

Jacques, S.J., Ahmed, Z., Forbes, A., Douglas, M.R., et al (2012) AAV8gfp preferentially targets large diameter dorsal root ganglion neurones after both intra-dorsal root ganglion and intrathecal injection Mol. Cell. Neurosci., 49, 464–474

Machida, A., Kuwahara, H., Mayra, A., Kubodera, T., et al (2013) Intraperitoneal administration of AAV9- shRNA inhibits target gene expression in the dorsal root ganglia of neonatal mice Mol. Pain, 9:36

Sakai, A., Saitow, F., Miyake, N., Miyake, K., et al (2013) miR-7a alleviates the maintenance of neuropathic pain through regulation of neuronal excitability Brain: 136, 2738–2750

Van der Kallen, L.R., Eggers, R., Ehlert, E.M., Verhaagen, J., Smit, A.B. and van Kesteren, R.E. (2015) Genetic deletion of the transcriptional repressor NFIL3 enhances axon growth in vitro but not axonal repair in vivo PLoS One, 10: e0127163

Xiang, H., Liu, Z., Wang, F., Xu, H., Roberts, C., Fischer, G., Stucky, C.L., Dean, C., Pan, B., Hogan, Q.H. and Yu, H. (2017) Primary sensory neuron-specific interference of TRPV1 signaling by adeno-associated virusencoded TRPV1 peptide aptamer attenuates neuropathic pain Mol.Pain, 13, 1–18

Xiang, H., Xu, H., Fan, F., Shin, S-M., Hogan, Q.H. and Yu, H. (2018) Glial fibrillary acidic protein promoter determines transgene expression in satellite glial cells following intraganglionic adeno-associated virus delivery in adult rats J. Neuro. Res., 96, 436–448

Down syndrome
Ortiz-Abalia, J., Sahún, I., Altafaj, X., Andreu, N., Estivill, X., Dierssen, M. and Fillat, C. (2008) Targeting Dyrk1A with AAVshRNA attenuates motor alterations in TgDyrk1A, a mouse model of Down syndrome Am. J. Hum. Genet., 83, 479-488

Early life stress
Shin, S., Pribiag, H., Lilascharoen, V., Knowland, D., Wang, X-Y. and Lim, B.K. (2018) Drd3 signaling in the lateral septum mediates early life stress-induced social dysfunction Neuron, 97, 195–208

Embryonic mesencephalon
Lehtonen, E., Bonnaud, F., Melas, C., Lubansu, A., et al (2002) AAV2 vectors mediate efficient and sustained transduction of rat embryonic ventral mesencephalon Neuroreport, 13, 1503-1507

Entorhinal cortex
Liu, X., Zeng, K., Li, M., Wang, Q., Liu, R., Zhang, B., Wang, J-Z., Shu, X. and Wang, X. (2017) Expression of P301L-hTau in mouse MEC induces hippocampus-dependent memory deficit Sci. Rep., 7: 3914

Ramirez, J.J., Poulton, W.E., Knelson, E., Barton, C., et al (2011) Focal expression of mutated tau in entorhinal cortex neurons of rats impairs spatial working memory Behav. Brain Res., 216, 332–340

Tanninen, S.E., Nouriziabari, B., Morrissey, M.D., Bakir, R., Dayton, R.D., Klein, R.L. and TakeharaNishiuchi, K. (2017) Entorhinal tau pathology disrupts hippocampal prefrontal oscillatory coupling during associative learning Neurobiol. Aging, 58, 151-162

Epilepsy
Theofilas, P., Brar, S., Stewart, K-A., Shen, H-Y., et al (2011) Adenosine kinase as a target for therapeutic antisense strategies in epilepsy Epilepsia, 52, 589–601

Young, D., Fong, D.M., Lawlor, P.A., Wu, A., Mouravlev, A., McRae, M., Glass, M., Dragunow, M. and During, M.J. (2014) Adenosine kinase, glutamine synthetase and EAAT2 as gene therapy targets for temporal lobe epilepsy Gene Ther., 21, 1029–1040

ER stress
Filézac de L’Etang, A., Maharjan, N., Braña, M.C., Ruegsegger, C., Rehmann, R., Goswami, A., Roos, A., Troost, D. et al (2015) Marinesco-Sjögren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS Nat. Neurosci., 18, 227-238

Jara, J.H., Genc, B., Cox, G.A., Bohn, M.C., Roos, R.P., Macklis, J.D., Ulupinar, E. and Ozdinler, P.H. (2015) Corticospinal motor neurons are susceptible to increased ER stress and display profound degeneration in the absence of UCHL1 function Cerebral Cortex 25, 4259-4272

Exosome delivery
Hudry, E., Martin, C., Gandhi, S., György, B., Scheffer, D.I., Mu, D., Merkel, S.F., Mingozzi, F., Fitzpatrick, Z. et al (2016) Exosome-associated AAV vector as a robust and convenient neuroscience tool Gene Ther., 23, 380–392

Expression efficiency
Choi, J-H., Yu, N-K., Baek, G-C., Bakes, J., et al (2014) Optimization of AAV expression cassettes to improve packaging capacity and transgene expression in neurons Mol. Brain, 7: 17

Familial amyloidotic polyneuropathy
Batista, A.R., Gianni, D., Ventosa, M., Coelho, A.V., Almeida, M.R., Sena-Esteves, M. and Saraiva1, M.J. (2014) Gene therapy approach to FAP: in vivo influence of T119M in TTR deposition in a transgenic V30M mouse model Gene Ther., 21, 1041–1050

Fear/fear memory
De Solis, C.A., Holehonnur, R., Banerjee, A., Luong, J.A., Lella, S.K., Ho, A., Pahlavan, B. and Ploski, J.E. (2015) Viral delivery of shRNA to amygdala neurons leads to neurotoxicity and deficits in Pavlovian fear conditioning Neurobiol. Learn. Mem., 124, 34–47

Ho, M.L., Judd, J., Kuypers, B.E., Yamagami, M., Wong, F.F. and Suh, J. (2014) Efficiency of proteaseactivatable virus nanonodes tuned through incorporation of wild type capsid subunits Cell. Mol. Bioeng., 7, 334–343

Klaus, F., Paterna, J-C., Marzorati, E., Sigrist, H., Götze, L., Schwendener, S., Bergamini, G., Jehli, E., Azzinnari, D. et al (2016) Differential effects of peripheral and brain tumor necrosis factor on inflammation, sickness, emotional behavior and memory in mice Brain Behav. Immun., 58, 310–326

Verma, D., Wood, J., Lach, G., Mietzsch, M., Weger, S., Heilbronn, R., Herzog, H., Bonaventure, P., Sperk, G. and Tasan, R.O. (2015) NPY Y2 receptors in the central amygdala reduce cued but not contextual fear Neuropharmacology, 99, 665-674

Fluorescent proteins, use of
Alves, S., Bode, J., Bemelmans, A-P., von Kalle, C., Cartier, N. and Tews, B. (2016) Ultramicroscopy as a novel tool to unravel the tropism of AAV gene therapy vectors in the brain Sci. Rep., 6: 28272

Heindorf, M. and Hasan, M.T. (2015) Fluorescent calcium indicator protein expression in the mouse brain using recombinant adeno-associated viruses Cold Spring Harb Protoc; doi: 10.1101/pdb.prot087635

Harvey, A.R., Ehlert, E., de Wit, J., Drummond, E.S., et al (2009) Use of GFP to analyze morphology, connectivity and function of cells in the central nervous system In Methods in Molecular Biology, Viral Applications of Green Fluorescent Protein, vol. 515 (ed.. Hicks B.W.), Humana Perss, Totowa, NJ, pp 63-95

Lux, K., Goerlitz, N., Leike, K., Goldnau, D., et al (2004) Incorporation of the green fluorescent protein into the adeno-associated virus type 2 capsid Mol. Ther., 9, Suppl. 1 S8

Lux, K., Goerlitz, N., Schlemminger, S., Perabo, L., et al (2005) Green fluorescent protein-tagged adenoassociated virus particles allow the study of cytosolic and nuclear trafficking J. Virol., 79, 11776-11787

Marshall, J.D., Li, J.Z., Zhang, Y., Gong, Y., St-Pierre, F., Lin, M.Z. and Schnitzer, M.J. (2016) Cell-typespecific optical recording of membrane voltage dynamics in freely moving mice Cell, 167, 1650–1662

Marsic, D., Méndez-Gómez, H.R. and Zolotukhin, S. (2015) High-accuracy biodistribution analysis of adenoassociated virus variants by double barcode sequencing Mol. Ther. Methods Clin. Dev., 2:15041

Fragile X Mental Retardation Protein
Tabeta, R., Moutin, E., Becker, J.A.J., Heintz, D., Fouillen, L., Flatter, E., Kręzel, E., Alunni, V., Koebel, P. et al (2016) Fragile X Mental Retardation Protein (FMRP) controls diacylglycerol kinase activity in neurons Proc. Natl. Acad. Sci. USA, 113, E3619–E3628

FTO gene
van Gestel, M.A., Sanders, L.E., de Jong, J.W., Luijendijk, M.C.M. and Adan, J.A.H. (2014) FTO knockdown in rat ventromedial hypothalamus does not affect energy balance Physiol. Rep., 2: e12152

GABA receptors/GABAergic neurons
Aoto, J., Földy, C., Ciurea Ilcus, S.M., Tabuchi, K. and Südhof, T.C. (2015) Distinct circuit-dependent functions of presynaptic neurexin-3 at GABAergic and glutamatergic synapses Nat. Neurosci., 18, 997-1007

Dimidschstein, J., Chen, Q., Tremblay, R., Rogers, S.L., Saldi, G-A., Guo, L., Xu, Q., Liu, R., Lu, C., Chu, J., Grimley, J.S. et al (2016) A viral strategy for targeting and manipulating interneurons across vertebrate species Nat. Neurosci., 19, 1743-1749

Hausrat, T.J., Muhia, M., Gerrow, K., Thomas, P., Hirdes, W., Tsukita, S., Heisler, F.F., Herich, L., Dubroqua, S. (2015) Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and shortterm memory Nat. Commun., 6: 6872

Ito, T., Hioki, H., Sohn, J., Okamoto, S., Kaneko, T., Iino, S. and Oliver, D.L. (2015) Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons J. Comp. Neurol., 523, 2277–2296

Gene switch – vifepristone-regulated Maddalena, A., Tereshchenko, J., Bähr, M. and Kügler, S. (2013) Adeno-associated virus-mediated,
vifepristone-regulated transgene expression in the brain Mol. Ther. Nucleic Acids 2: e106

Genetic mosaicism
Kim, J-Y., Ash, R.T., Ceballos-Diaz, C., Levites, Y., et al (2013) Viral transduction of the neonatal brain delivers controllable genetic mosaicism for visualising and manipulating neuronal circuits in vivo Eur. J. Neurosci., 37, 1203–1220

Ghrelin
Romero-Picó, A., Vázquez, M.J., González-Touceda, D., Folgueira, C., et al (2013) Hypothalamic -opioid receptor modulates the orexigenic effect of ghrelin Neuropsychopharmacology, 38, 1296–1307

Glial/glioma/glioblastoma cells (see “Cultured cell and tissue delivery”)

Glutamate metabolism
Aoto, J., Földy, C., Ciurea Ilcus, S.M., Tabuchi, K. and Südhof, T.C. (2015) Distinct circuit-dependent functions of presynaptic neurexin-3 at GABAergic and glutamatergic synapses Nat. Neurosci., 18, 997-1007

Burmeister, J.J., Pomerleau, F., Quintero, J.E., Huettl, P., Jakobsson, Y.A.J., Lundblad, M., Heuer, A., Slevin, J.T. and Gerhardt, G.A. (2018) In vivo electrochemical studies of optogenetic control of glutamate signaling measured using enzyme-based ceramic microelectrode arrays In Biochemical Approaches for Glutamatergic Neurotransmission, Neuromethods, vol. 130 (eds. Parrot, S. and Denoroy, L.) Springer Science+Business Media LLC, New York, pp 327-351

Fitzsimons, H.L., Riban, V., Bland, R.J., Wendelken, J.L., et al (2010) Biodistribution and safety assessment of AAV2-GAD following intrasubthalamic injection in the rat J. Gene Med., 12, 385–398

Konno, A., Shuvaev, A.N., Miyake, N., Miyake, K., et al (2014) Mutant ataxin-3 with an abnormally expanded polyglutamine chain disrupts dendritic development and metabotropic glutamate receptor signaling in mouse cerebellar Purkinje cells Cerebellum, 13, 29–41

Green fluorescent protein techniques (see “Fluorescent proteins, use of”)

Heat-shock proteins
Jung, A.E., Fitzsimons, H.L., Bland, R.J., During, M.J. and Young, D. (2008) HSP70 and constitutively active HSF1 mediate protection against CDCrel-1-mediated toxicity Mol. Ther., 16, 1048-1055

Hindbrain delivery
Kanoski, S.E., Zhao, S., Guarnieri, D.J., DiLeone, R.J., et al (2012) Endogenous leptin receptor signaling in the medial nucleus tractus solitarius affects meal size and potentiates intestinal satiation signals Am. J. Physiol. Endocrinol. Metab., 303, E496–E503

Van der Peet, P.L., Gunawan, C., Abdul-Ridha, A., Ma, S., Scott, D.J., Gundlach, A.L., Bathgate, R.A.D., White, J.M. and Williams, S.J. (2018) Gram scale preparation of clozapine N-oxide (CNO), a synthetic small molecule actuator for muscarinic acetylcholine DREADDs MethodsX, 5, 257–267

Hippocampal basket cells
Ledri, M., Nikitidou, L., Erdelyi, F., Szabo, G., et al (2012) Altered profile of basket cell afferent synapses in hyper-excitable dentate gyrus revealed by optogenetic and two-pathway stimulations Eur. J. Neurosci., 36, 1971–1983

Hippocampal cells and delivery
Anderson, G.R., Maxeiner, S., Sando, R., Tsetsenis, T., Malenka, R.C. and Südhof, T.C. (2017) Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly J. Cell Biol., 216, 3831–3846

Aoto, J., Martinelli, D.C., Malenka, R.C., Tabuchi, K. and Südhof, T.C. (2013) Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking Cell, 154, 75–88

Aoto, J., Földy, C., Ciurea Ilcus, S.M., Tabuchi, K. and Südhof, T.C. (2015) Distinct circuit-dependent functions of presynaptic neurexin-3 at GABAergic and glutamatergic synapses Nat. Neurosci., 18, 997-1007

Auffenberg, E., Jurik, A., Mattusch, C., Stoffel, R., Genewsky, A., Namendorf, C., Schmid, R.M. Rammes, G. et al (2016) Remote and reversible inhibition of neurons and circuits by small molecule induced potassium channel stabilization Sci. Rep., 6: 19293

Bean, L.A., Kumar, A., Rani, A., Guidi, M., Rosario, A.M., Cruz, P.E., Golde, T.E. and Foster, T.C. (2015) Reopening the critical window for estrogen therapy J. Neurosci., 35, 16077–16093

Cabral-Miranda, F., Nicoloso-Simões, E., Adão-Novaes, J., Chiodo, V., Hauswirth, W.W., Linden, R., Barreto Chiarini, L. Petrs-Silva, H. (2017) rAAV8-733-Mediated gene transfer of CHIP/Stub-1 prevents hippocampal neuronal death in experimental brain ischemia Mol. Ther., 25, 392-400

Cao, X., Li, L-P., Wang, Q., Wu, Q., et al (2013) Astrocyte-derived ATP modulates depressive-like behaviors Nat. Med., 19, 773-777

Crawford, D.C., Ramirez, D.M.O., Trauterman, B., Monteggia, L.M. and Kavalali E.T. (2017) Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy Nat. Comm., 8: 14436

Crowther, A.J., Lim, S-A., Asrican, B., Albright, B.H., Wooten, J., Yeh, C-Y., Bao, H., Cerri, D.H., Hu, J. et al (2018) An adeno-associated virus-based toolkit for preferential targeting and manipulating quiescent neural stem cells in the adult hippocampus Stem Cell Rep., 10, 1146–1159

Daily, J.L., Nash, K., Jinwal, U., Golde, T., et al (2011) Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome PLoS One 6: e27221

Dayton, R.D., Wang, D.B., Cain, C.D., Schrott, L.M., et al (2012) Frontotemporal lobar degeneration-related proteins induce only subtle memory-related deficits when bilaterally overexpressed in the dorsal hippocampus Exp. Neurol., 233, 807–814

Elagabani, M.N., Brisevac, D., Kintscher, M., Pohle, J., Köhr, G., Schmitz, D. and Kornau, H-C. (2016) Subunit-selective N-methyl-D-aspartate (NMDA) receptor signaling through brefeldin A-resistant Arf guanine nucleotide exchange factors BRAG1 and BRAG2 during synapse maturation J. Biol. Chem., 291, 9105–9118

Favuzzi, E., Marques-Smith, A., Deogracias, R., Winterflood, C.M., Sánchez-Aguilera, A., Mantoan, L., Maeso, P., Fernandes, C., Ewers, H. and Rico, B. (2017) Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein Brevican Neuron, 95, 639–655

Fenno, L.E., Mattis, J., Ramakrishnan, C., Hyun, M., Lee, S.Y., He, M., Tucciarone, J., Selimbeyoglu, A., Berndt, A., Grosenick, L. et al (2014) Targeting cells with single vectors using multiple-feature Boolean logic Nature Meth., 11, 762-772

Fol1, R., Braudeau, J., Ludewig, S., Abel, T., Weyer, S.W., Roederer, J-P., Brod6, F., Audrain, M. et al (2016) Viral gene transfer of APPsα rescues synaptic failure in an Alzheimer’s disease mouse model Acta Neuropathol., 131, 247–266

Fukuchi, K-i., Tahara, K., Kim, H-D., Maxwell, A., et al (2006) Anti-Aβ single-chain antibody delivery via adeno-associated virus for treatment of Alzheimer’s disease Neurobiol. Dis., 23, 502-511

Gerstein, H., O’Riordan, K., Osting, S., Schwarz, M., Burger, C. (2012) Rescue of synaptic plasticity and spatial learning deficits in the hippocampus of Homer1 knockout mice by recombinant adeno-associated viral gene delivery of Homer1c Neurobiol. Learn. Mem., 97, 17–29

Gerstein, H., Lindstrom, M.J. and Burger, C. (2013) Gene delivery of Homer1c rescues spatial learning in a rodent model of cognitive aging Neurobiol. Aging, 34, 1963-1970

Gong, Y., Meyer, E.M., Meyers, C.A., Klein, R.L., et al (2006) Memory-related deficits following selective hippocampal expression of Swedish mutation amyloid precursor protein in the rat Exp. Neurol., 200, 371-377

Haberman, R.P., Samulski, R.J. and McCown, T.J. (2003) Attenuation of seizures and neuronal death by adeno-associated virus vector galanin expression and secretion Nat. Med., 9, 1076-1080

Hausrat, T.J., Muhia, M., Gerrow, K., Thomas, P., Hirdes, W., Tsukita, S., Heisler, F.F., Herich, L., Dubroqua, S. (2015) Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and shortterm memory Nat. Commun., 6: 6872

Kanter-Schlifke, I., Georgievska, B., Kirik, D. and Kokaia, M. (2007) Brain area, age and viral vector-specific glial cell-line-derived neurotrophic factor expression and transport in rat Neuroreport, 18, 845-850

Kanter-Schlifke, I., Georgievska, B., Kirik, D. and Kokaia, M. (2007) Seizure suppression by GDNF gene therapy in animal models of epilepsy Mol. Ther., 15, 1106-1113

Klein, R.L., Lin, W-L., Dickson, D.W., Lewis, J., et al (2004) Rapid neurofibrillary tangle formation after localized gene transfer of mutated Tau Am. J. Pathol., 164, 347-353

Klein, R.L., Dayton, R.D., Leidenheimer, N.J., Jansen, K., et al (2006) Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins Mol. Ther., 13, 517-527

Klein, R.L., Dayton, R.D., Tatom, J.B., Henderson, K.M., et al (2008) AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method Mol. Ther., 16, 89-96

Latta, C.H., Sudduth, T.L., Weekman, E.M., Brothers, H.M., Abner, E.L., Popa, G.J., Mendenhall, M.D., Gonzalez-Oregon, F. Braun, K. and Wilcock, D.M. (2015) Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-β using BV2 microglial cells and APP/PS1 transgenic mice J. Neuroinflam., 12: 41

Ledri, M., Nikitidou, L., Erdelyi, F., Szabo, G., et al (2012) Altered profile of basket cell afferent synapses in hyper-excitable dentate gyrus revealed by optogenetic and two-pathway stimulations Eur. J. Neurosci., 36, 1971–1983

Lee, Y-S., Ehninger, D., Zhou, M., Oh, J-Y., Kang, M., Kwak, C., Ryu, H-H., Butz, D., et al (2014) Mechanism and treatment for learning and memory deficits in mouse models of Noonan syndrome Nat. Neurosci., 17, 1736-1743

Lin, W-C., Davenport, C.M., Mourot, A., Vytla, D., Smith, C.M., Medeiros, K.A., Chambers, J.J. and Kramer, R.H. (2014) Engineering a light-regulated GABAA receptor for optical control of neural inhibition ACS Chem. Biol., 9, 1414−1419

Malmevik, J., Petri, R., Klussendorf, T., Knauff, P., Åkerblom, M., Johansson, J., Soneji, S. and Jakobsson, J. (2015) Identification of the miRNA targetome in hippocampal neurons using RIP-seq Sci. Rep., 5:12609

Malmevik, J., Petri, R., Knauff, P., Brattås. P.L., Åkerblom, M. and Jakobsson, J. (2016) Distinct cognitive effects and underlying transcriptome changes upon inhibition of individual miRNAs in hippocampal neurons Sci. Rep., 6: 19879

Mineur, Y.S., Obayemi, A., Wigestrand, M.B., Fote, G.M., et al (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior Proc. Natl. Acad. Sci. USA, 110, 3573-3578

Mosser, S., Alattia, J-R., Dimitrov, M., Matz, A., Pascual, J., Schneider, B.L. and Fraering, P.C. (2015) The adipocyte differentiation protein APMAP is an endogenous suppressor of A production in the brain Hum. Mol. Genet., 24, 371–382

Mudannayake, J.M., Mouravlev, A., Fong, D.M. and Young, D. (2016) Transcriptional activity of novel ALDH1L1 promoters in the rat brain following AAV vector-mediated gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16075

Muhia, M., Willadt, S., Yee, B.K., Feldon, J., et al (2012) Molecular and behavioral changes associated with adult hippocampus-specific SynGAP1 knockout Learn. Mem., 19, 268-281

Mustroph, M.L., King, M.A., Klein, R.L. and Ramirez, J.J. (2012) Adult-onset focal expression of mutated human tau in the hippocampus impairs spatial working memory of rats Behav. Brain Res., 233, 141-148

Oksman, M., Wisman, L.A., Jiang, H., Miettinen, P.,.et al (2013) Transduced wild-type but not P301S mutated human tau shows hyperphosphorylation in transgenic mice overexpressing A30P mutated human alphasynuclein Neurodegenerative Dis., 12, 91–102

O’Riordan, K., Gerstein, H., Hullinger, R. and Burger, C. (2014) The role of Homer1c in metabotropic glutamate receptor-dependent long-term potentiation Hippocampus, 24, 1-6

Paradiso, B., Marconi, P., Zucchini, S., Berto, E., et al (2009) Localized delivery of fibroblast growth factor–2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model Proc. Natl. Acad. Sci. USA, 106, 7191–7196

Pascual-Lucas, M., da Silva, S.V., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C.M. et al (2014) Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice EMBO Mol. Med., 6, 1246-1262

Pietropaolo, S., Paterna, J-C., Büeler, H., Feldon, J. and Yee, B.K. (2007) Bidirectional changes in water-maze learning following recombinant adenovirus-associated viral vector (rAAV)-mediated brain-derived neurotrophic factor expression in the rat hippocampus Behav. Pharmacol., 18, 533-547

Ren, K., Thinschmidt, J., Liu, J., Ai, L., et al (2007) 7 Nicotinic receptor gene delivery into mouse hippocampal neurons leads to functional receptor expression, improved spatial memory-related performance and tau hyperphosphorylation Neuroscience, 145, 314-322

Roberts, M.S., Macauley, S.L., Wong, A.M., Yilmas, D., et al (2012) Combination small molecule PPT1 mimetic and CNS-directed gene therapy as a treatment for infantile neuronal ceroid lipofuscinosis J. Inherit. Metab. Dis., 35, 847–857

Rodríguez-Lebrón, E., Gouvion, C.M., Moore, S.A., Davidson, B.L.,. et al (2009) Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer’s disease Mol. Ther., 17, 1563–1573

Rosario, A.M., Cruz, P.E., Ceballos-Diaz, C., Strickland, M.R., Siemienski, Z., Pardo, M., Schob, K-L., Li, A., Aslanidi, G.V. et al (2016) Microglia-specific targeting by novel capsid-modified AAV6 vectors Mol. Ther. Meth. Clin. Dev., 3: 16026

Rost, B.R., Schneider, F., Grauel, M.K., Wozny, C., Bentz, C.G., Blessing, A., Rosenmund, T., Jentsch, T.J. et al (2015) Optogenetic acidification of synaptic vesicles and lysosomes Nat. Neurosci., 18, 1845-1852

Schindler, S.E., McCall, J.G., Yan, P., Hyrc, K.L., Li, M., Tucker, C.L., Lee, J-M., Bruchas, M.R. and Diamond, M.I. (2015) Photo-activatable Cre recombinase regulates gene expression in vivo Sci. Rep., 5: 13627

Sim, S-E., Lim, C-S., Kim, J-I., Seo, D., Chun, H., Yu, N-K., Lee, J., Kang, S.J., Ko, H-G., Choi, J-H. et al (2016) The brain-enriched microRNA miR-9-3p regulates synaptic plasticity and memory J. Neurosci., 36, 8641– 8652

Sondhi, D., Scott, E.C., Chen, A., Hackett, N.R., et al (2014) Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adenoassociated virus serotype rh.10 vector expressing the human CLN3 gene Hum. Gene Ther., 25, 223–239

Song, L., Wang, H., Wang, Y-J., Wang, J-L., Zhu, Q., Wu, F., Zhang, W. and Jiang, B. (2018) Hippocampal PPARα is a novel therapeutic target for depression and mediates the antidepressant actions of fluoxetine in mice Br. J. Pharmacol., 175, 2968–2987

Sun, H-S., Jackson, M.F., Martin, L.J., Jansen, K., et al (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia Nat. Neurosci., 12, 1300-1307

Theofilas, P., Brar, S., Stewart, K-A., Shen, H-Y., et al (2011) Adenosine kinase as a target for therapeutic antisense strategies in epilepsy Epilepsia, 52, 589–601

Thinschmidt, J., López-Hernández, G.Y., Ren, K., King, M.A., et al (2008) Modulation of spontaneous hippocampal synaptic events with 5-hydroxyindole, 4OH-GTS-21, and rAAV-mediated α7 nicotinic receptor gene transfer Brain Res., 1203, 51-60

Traunmüller, L., Bornmann, C. and Scheiffele, P. (2014) Alternative splicing coupled nonsense-mediated decay generates neuronal cell type-specific expression of SLM proteins J. Neurosci., 34, 16755–16761

Vullhorst, D., Ahmad, T., Karavanova, I., Keating, C. and Buonanno, A. (2017) Structural similarities between neuregulin 1–3 isoforms determine their subcellular distribution and signaling mode in central neurons J. Neurosci., 37, 5232–5249

Weekman, E.M., Sudduth, T.L., Abner, E.L., Popa, G.J., Mendenhal, M.D., Brothers, H.M., Braun, K., Greenstein, A. and Wilcock, D.M. (2014) Transition from an M1 to a mixed neuroinflammatory phenotype increases amyloid deposition in APP/PS1 transgenic mice J. Neuroinflamm., 11: 127

Weinberg, M.S., Blake, B.L. and McCown, T.J. (2013) Opposing actions of hippocampus TNFα receptors on limbic seizure susceptibility Exp. Neurol., 247, 429–437

Woldemichael, B.T., Jawaid, A., Kremer, E.A., Gaur, N., Krol, J., Marchais, A. and Mansuy, I.M. (2016) The microRNA cluster miR-183/96/182 contributes to long-term memory in a protein phosphatase 1-dependent manner Nat. Comm., 7: 12594

Woodling, N.S., Colas, D., Wang, Q., Minhas, P., Panchal, M., Liang, X., Mhatre, S.D., Brown, H., Ko, N., Zagol-Ikapitte, I. et al (2016) Cyclooxygenase inhibition targets neurons to prevent early behavioural decline in Alzheimer’s disease model mice Brain, 139, 2063–2081

Xu, W., Morishita, W., Buckmaster, P.S., Pang, Z.P., et al (2012) Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic trans-mission Neuron, 73, 990-1001

Yoon, S.Y., Gay-Antaki, C., Ponde, D.E., Poptani, H., et al (2014) Quantitative, noninvasive, in vivo longitudinal monitoring of gene expression in the brain by co-AAV transduction with a PET reporter gene Mol. Ther. Methods Clin. Dev., 1, 14016

Young, D., Fong, D.M., Lawlor, P.A., Wu, A., Mouravlev, A., McRae, M., Glass, M., Dragunow, M. and During, M.J. (2014) Adenosine kinase, glutamine synthetase and EAAT2 as gene therapy targets for temporal lobe epilepsy Gene Ther., 21, 1029–1040

Zeier, Z., Kumar, A., Bodhinathan, K., Feller, J.A., et al (2009) Fragile X mental retardation protein replacement restores hippocampal synaptic function in a mouse model of fragile X syndrome Gene Ther., 16, 1122–1129

Zhu, L-J., Li, T-Y., Luo, C-X., Jiang, N., Chang, L., Lin, Y-H., Zhou, H-H., Chen, C., Zhang, Y., Lu, W. et al. (2014) CAPON-nNOS coupling can serve as a target for developing new anxiolytics Nat. Med., 9, 1050-1054

Hippocampus dentate gyrus delivery
Bustos, F.J., Ampuero, E., Jury, N., Aguilar, R., Falahi, F., Toledo, J., Ahumada J., Lata, J., Cubillos, P. et al (2017) Epigenetic editing of the Dlg4/PSD95 gene improves cognition in aged and Alzheimer’s disease mice Brain, 140, 3252–3268

Cho, H-Y., Kim, M. and Han, J-H. (2017) Specific disruption of contextual memory recall by sparse additional activity in the dentate gyrus Neurobiol. Learn. Mem., 145, 190–198

Hippocampus: neural; stem cells
Crowther, A.J., Lim, S-A., Asrican, B., Albright, B.H., Wooten, J., Yeh, C-Y., Bao, H., Cerri, D.H., Hu, J. et al (2018) An adeno-associated virus-based toolkit for preferential targeting and manipulating quiescent neural stem cells in the adult hippocampus Stem Cell Rep., 10, 1146–1159

Histone deacetylases
Mahgoub, M., Adachi, M., Suzuki, K., Liu, X., Kavalali, E.T., Chahrour, M.H. and Monteggia, L.M. (2016) MeCP2 and histone deacetylases 1 and 2 in dorsal striatum collectively suppress repetitive behaviors Nat. Neurosci., 19, 1506-1512

Homer 1, 1a, 1c
Banerjee, A., Luong, J.A., Ho, A., Saib, A.O. and Ploski, J.E. (2016) Overexpression of Homer1a in the basal and lateral amygdala impairs fear conditioning and induces an autism-like social impairment Mol. Autism, 7:

Gerstein, H., O’Riordan, K., Osting, S., Schwarz, M., Burger, C. (2012) Rescue of synaptic plasticity and spatial learning deficits in the hippocampus of Homer1 knockout mice by recombinant adeno-associated viral gene delivery of Homer1c Neurobiol. Learn. Mem., 97, 17–29

Gerstein, H., Lindstrom, M.J. and Burger, C. (2013) Gene delivery of Homer1c rescues spatial learning in a rodent model of cognitive aging Neurobiol. Aging, 34, 1963-1970

Hsp90
McFarland, N.R., Dimant, H., Kibuuka, L., Ebrahimi-Fakhari, D., et al (2014) Chronic treatment with novel small molecule Hsp90 inhibitors rescues striatal dopamine levels but not -synuclein-induced neuronal cell loss PLoS One, 9: e86048

Huntingdon’s disease
Alto, L.T., Chen, X., Ruhn, K.A., Trevino. I. and Tansey, M.G. (2014) AAV-dominant negative tumor necrosis factor (DN-TNF) gene transfer to the striatum does not rescue medium spiny neurons in the YAC128 mouse model of Huntington’s disease PLoS One, 9: e96544

Agustín-Pavón, C., Mielcarek, M., Marriga-Canut, M. and Isalan, M. (2016) Deimmunization for gene therapy: host matching of synthetic zinc finger constructs enables long-term mutant Huntingtin repression in mice Mol. Neurodegen., 11: 64

Boudreau, R.L., Spengler, R.M. and Davidson, B.L. (2011) Rational design of therapeutic siRNAs: minimizing off-targeting potential to improve the safety of RNAi therapy for Huntington’s disease Mol. Ther., 19, 2169–2177

Carty, N., Berson, N., Tillack, K., Thiede, C., Scholz, D., Kottig, K., Sedaghat, Y., Gabrysiak, C. et al (2015) Characterization of HTT inclusion size, location, and timing in the zQ175 mouse model of Huntington´s disease: an in vivo high-content imaging study PLoS One, 10: e0123527

Cheng, S., Tereshchenko, J., Zimmer, V., Vachey, G., Pythoud, C., Rey, M., Liefhebber, J., Raina, A., Streit, F. (2018) Therapeutic efficacy of regulable GDNF expression for Huntington’s and Parkinson’s disease by a highinduction, background-free “GeneSwitch” Vector Exp. Neurol., 309, 79–90

Crook, Z.R. and Housman, D.E. (2012) Dysregulation of dopamine receptor D2 as a sensitive measure for Huntington disease pathology in model mice Proc. Natl. Acad. Sci. USA, 109, 7487–7492

Gabery, S., Sajjad, M.U., Hult, S., Soylu, R., et al (2012) Characterization of a rat model of Huntington’s disease based on targeted expression of mutant huntingtin in the forebrain using adeno-associated viral vectors Eur. J. Neurosci., 36, 2789–2800

Garriga-Canut, M., Agustín-Pavón, C., Herrmann, F., Sánchez, A., et al (2012) Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice Proc. Natl. Acad. Sci. USA, E3136- E3145

Kim, S-H., Shahani, N, Bae, BII, Sbodio, J.I., Chung, Y., Nakaso, K., Paul, B.D. and Sawa, A. (2016) Allelespecific regulation of mutant Huntingtin by Wig1, a downstream target of p53 Hum. Mol. Genet., 25, 2514–2524

McBride, J.L., Pitzer, M.R., Boudreau, R.L., Dufour, B., et al (2011) Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington’s disease Mol. Ther., 19, 2152–2162

Rodriguez-Lebron, E., Denovan-Wright, E.M., Nash, K., Lewin, A.S. and Mandel, R.J. (2005) Intrastriatal rAAV-mediated delivery of anti-huntingtin shRNAs induces partial reversal of disease progression in R6/1 Huntington’s disease transgenic mice Mol. Ther., 12, 618-633

Southwell, A.L., Ko, J. and Patterson, P.H. (2009) Intrabody gene therapy ameliorates motor, cognitive, and neuropathological symptoms in multiple mouse models of Huntington’s disease J. Neurosci., 29, 13589 –13602

Tang, T-S., Guo, C., Wang, H., Chen, X. and Bezprozvanny, I. (2009) Neuroprotective effects of inositol 1,4,5- trisphosphate receptor C-terminal fragment in a Huntington’s disease mouse model J. Neurosci., 29, 1257–1266

Wu, A., Fong, D.M. and Young, D. (2015) Gene therapy for Huntington’s disease In Neuromethods, 98, Gene Delivery and Therapy for Neurological Disorders (ed. Bo, X. and Verhaagen, J.) Springer Science+Business Media New York, pp 121-151

Hypertension
He, D., Pan, Q., Chen, Z., Sun, C., Zhang, P., Mao, A., Zhu, Y., Li, H., Lu, C. et al (2017) Treatment of hypertension by increasing impaired endothelial TRPV4-KCa2.3 interaction EMBO Mol. Med., 9, 1491-1502

Shi, P., Diez-Freire, C., Jun, J.Y., Qi, Y., et al (2010) Brain microglial cytokines in neurogenic hypertension Hypertension, 56, 297-303

Hypoglossal neuron delivery
ElMallah, M.K., Falk, D.J., Lane, M.A., Conlon, T.J., et al (2012) Retrograde gene delivery to hypoglossal motoneurons using adeno-associated virus serotype 9 Hum. Gene Ther. Methods, 23, 148–156

Hypothalamus delivery
De Backer, M.W.A., Brans, M.A.D., Luijendijk, M.C., Garner, K.M., et al (2010) Optimization of adenoassociated viral vector-mediated gene delivery to the hypothalamus Hum. Gene Ther., 21, 673–682

De Backer, M.W.A., Fitzsimons, C.P., Brans, M.A.D., Luijendijk, M.C.M., et al (2010) An adeno-associated viral vector transduces the rat hypothalamus and amygdala more efficient than a lentiviral vector BMC

Neurosci., 11: 81
De Backer, M.W.A., Brans, M.A.D., van Rozen, A.J., van der Zwaal, E.M., et al (2010) Suppressor of cytokine signaling 3 knockdown in the mediobasal hypothalamus: counterintuitive effects on energy balance J. Mol. Endocrinol., 45, 341–353

Gabery, S., Sajjad, M.U., Hult, S., Soylu, R., et al (2012) Characterization of a rat model of Huntington’s disease based on targeted expression of mutant huntingtin in the forebrain using adeno-associated viral vectors Eur. J. Neurosci., 36, 2789–2800

Ganella, D.E., Callander, G.E., Ma, S., Bye, C.R., et al (2013) Modulation of feeding by chronic rAAV expression of a relaxin-3 peptide agonist in rat hypothalamus Gene Ther., 20, 703–716

Kim, J.D., Toda, C., D’Agostino, G., Zeiss, C.J., DiLeone, R.J., Elsworth, J.D., Kibbey, R.G., Chan, O., Harvey, B.K., Richie, C.T. et al (2014) Hypothalamic prolyl endopeptidase (PREP) regulates pancreatic insulin and glucagon secretion in mice Proc. Natl. Acad. Sci. USA, 111, 11876–11881

Liu, M., Blanco-Centurion, C., Konadhode, R., Begum, S., et al (2011) Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice J. Neurosci., 31, 6028–6040

Qi, Y., Purtell, L., Fu, M., Zhang, L., Zolotukhin, S., Campbell, L. and Herzog, H. (2017) Hypothalamus Specific re-introduction of SNORD116 into otherwise Snord116 deficient mice increased energy expenditure J. Neuroendocrinol., 29: 10.1111/jne.12457

Rodríguez, S.S., Schwerdt, J.I., Barbeito, C.G., Flamini, M.A., Han, Y., Bohn, M.C. and Goya, R.G. (2013) Hypothalamic IGF-I gene therapy prolongs estrous cyclicity and protects ovarian structure in middle-aged female rats Endocrinology, 154, 2166–2173

Romero-Picó, A., Vázquez, M.J., González-Touceda, D., Folgueira, C., et al (2013) Hypothalamic -opioid receptor modulates the orexigenic effect of ghrelin Neuropsychopharmacology, 38, 1296–1307

Van Gestel, M.A, van Erp, S., Sanders, L.E., Brans, M.A.D., Luijendijk, M.C.M., Merkestein, M., Pasterkamp, R.J. and Adan, R.A.H. (2014) shRNA-induced saturation of the microRNA pathway in the rat brain Gene Ther., 21, 205–211

Van Gestel, M.A., Boender, A.J., de Vrind, V.A.J., Garner, K.M., et al (2014) Recombinant adeno-associated virus: efficient transduction of the rat VMH and clearance from blood PLoS One, 9: e97639

Van Gestel, M.A., Sanders, L.E., de Jong, J.W., Luijendijk, M.C.M. and Adan, J.A.H. (2014) FTO knockdown in rat ventromedial hypothalamus does not affect energy balance Physiol. Rep., 2: e12152

Hypoxia-ischaemia
Weller, M.L., Stone, I.M., Goss, A., Rau, T., Rova, C. and Poulsen, D.J. (2008) Selective overexpression of excitatory amino acid transporter 2 (EAAT2) in astrocytes enhances neuroprotection from moderate but not severe hypoxia-ischemia Neuroscience, 155, 1204-1211

Immune responses
Mendoza, S.D., El-Shamayleh, Y. and Horwitz, G.D. (2017) AAV-mediated delivery of optogenetic constructs to the macaque brain triggers humoral immune responses J. Neurophysiol., 117, 2004–2013

Inflammation
Humbert-Claude, M., Duc, D., Dwir, D., Thieren, L., Sandstrom von Tobel, J., Begka, C., Legueux, F. et al (2016) Tollip, an early regulator of the acute inflammatory response in the substantia nigra J. Neuroinflamm., 13: 303

Wang. Y., Gao. Y., Tian. Q., Deng, Q., Wang, Y., Zhou, T., Liu, Q., Mei, K. Wang, Y. (2018) TRPV1 SUMOylation regulates nociceptive signaling in models of inflammatory pain Nat. Comm., 9: 1529

Zhuang, G.Z., Keeler, B., Grant, J., Bianchi, L., Fu, E.S., Zhang, Y.P., Erasso, D.M., Cui, J-G., Wiltshire, T. et al (2015) Carbonic anhydrase-8 regulates inflammatory pain by inhibiting the ITPR1-cytosolic free calcium pathway PLoS One, 10: e0118273

Insulin growth factor
Pascual-Lucas, M., da Silva, S.V., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C.M., Cuadrado-Tejedor, M. and Garcia-Osta, A. (2014) Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice EMBO Mol. Med., 6, 1246-1262

Interneuronal DISC1
Seshadri, S., Faust, T., Ishizuka, K., Delevich, K., Chung, Y., Kim, S-H., Cowles, M., Niwa, M. et al (2015) Interneuronal DISC1 regulates NRG1-ErbB4 signalling and excitatory–inhibitory synapse formation in the mature cortex Nat. Commun., 6: 10118

Intracisternal delivery
Sinnett, S.E., Hector, R.D., Gadalla, K.K.E., Heindel, C., Chen, D., Zaric, V., Bailey, M.E.S., Cobb, S.R. and Gray, S.J. (2017) Improved MECP2 gene therapy extends the survival of MeCP2-null mice without apparent toxicity after intracisternal delivery Mol. Ther. Meth. Clin. Dev., 5, 106-115

Intramuscular injection
Benkhelifa-Ziyyat, S., Besse, A., Roda, M., Duque, S., et al (2013) Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice Mol. Ther., 21, 282–290

Intraventricular injection
Filézac de L’Etang, A., Maharjan, N., Braña, M.C., Ruegsegger, C., Rehmann, R., Goswami, A., Roos, A., Troost, D. et al (2015) Marinesco-Sjögren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS Nat. Neurosci., 18, 227-238

Huang, X., Stodieck, S.K., Goetze, B., Cui, L., Wong, M.H., Wenzel, C., Hosang, L. Dong, Y., Löwel, S. and Schlüter, O.M. (2015) Progressive maturation of silent synapses governs the duration of a critical period Proc. Natl. Acad. Sci. USA, E3131–E3140

Kim, J-Y., Ash, R.T., Ceballos-Diaz, C., Levites, Y., et al (2013) Viral transduction of the neonatal brain delivers controllable genetic mosaicism for visualising and manipulating neuronal circuits in vivo Eur. J. Neurosci., 37, 1203–1220

Valluy, J., Bicker, S., Aksoy-Aksel, A., Lackinger, M., Sumer, S., Fiore, R., Wüst, T., Seffer, D. et al (2015) A coding-independent function of an alternative Ube3a transcript during neuronal development Nat. Neurosci., 18, 666-673

Xu, Y-F., Prudencio, M., Hubbard, J.M., Tong, J., et al (2013) The pathological phenotypes of human TDP-43 transgenic mouse models are independent of downregulation of mouse Tdp-43 PLoS One, 8: e69864

Invasive glioblastoma
Crommentuijn, M.H.W., Maguire, C.A., Niers, J.M., Vandertop, W.P., Badr, C.E., Wurdinger, T. and Tannous, B.A. (2016) Intracranial AAV-sTRAIL combined with lanatoside C prolongs survival in an orthotopic xenograft mouse model of invasive glioblastoma Mol. Oncol., 10, 625-634

Kappa opioid receptor
Dogra, S., Kumar, A., Umrao, D., Sahasrabuddhe, A.A. and Yadav, P.M. (2016) Chronic Kappa opioid receptor activation modulates NR2B: Implication in treatment resistant depression Sci. Rep., 6: 33401

Lateral lemniscus nuclei
Ito, T., Hioki, H., Sohn, J., Okamoto, S., Kaneko, T., Iino, S. and Oliver, D.L. (2015) Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons J. Comp. Neurol., 523, 2277–2296

Lateral septum delivery
Harasta, A.E., Power, J.M., von Jonquieres, G., Karl, T., Drucker, D.J., Housley, G.D., Schneider, M. and Klugmann, M. (2015) Septal glucagon-like peptide 1 receptor expression determines suppression of cocaineinduced behavior Neuropsychopharmacology, 40, 1969–1978

Shin, S., Pribiag, H., Lilascharoen, V., Knowland, D., Wang, X-Y. and Lim, B.K. (2018) Drd3 signaling in the lateral septum mediates early life stress-induced social dysfunction Neuron, 97, 195–208

Lateral ventricle delivery
Klaus, F., Paterna, J-C., Marzorati, E., Sigrist, H., Götze, L., Schwendener, S., Bergamini, G., Jehli, E., Azzinnari, D. et al (2016) Differential effects of peripheral and brain tumor necrosis factor on inflammation, sickness, emotional behavior and memory in mice Brain Behav. Immun., 58, 310–326

Learning
Chen, J.L., Margolis, D.J., Stankov, A., Sumanovski, L.T., Schneider, B.L. and Helmchen, F. (2015) Pathwayspecific reorganization of projection neurons in somatosensory cortex during learning Nat. Neurosci., 18, 1101-1108

Tanninen, S.E., Nouriziabari, B., Morrissey, M.D., Bakir, R., Dayton, R.D., Klein, R.L. and TakeharaNishiuchi, K. (2017) Entorhinal tau pathology disrupts hippocampal prefrontal oscillatory coupling during associative learning Neurobiol. Aging, 58, 151-162

Lipofuscinosis
Cabrera-Salazar, M.A., Roskelley, E.M., Bu, J., Hodges, B.L., et al (2007) Timing of therapeutic intervention determines functional and survival outcomes in a mouse model of late infantile Batten disease Mol. Ther., 15, 1782-1788

Foley, C.P., Rubin, D.G.., Santillan, A., Sondhi, D., Dyke, J.P., Gobin, Y.P., Crystal, R.G. and Ballon, D.J. (2014) Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption J. Control. Release, 196, 71–78

Griffey, M., Bible, E., Vogler, C., Levy, B., et al (2004) Adeno-associated virus 2-mediated gene therapy decreases autofluorescent storage material and increases brain mass in a murine model of infantile neuronal ceroid lipofuscinosis Neurobiol. Dis., 16, 360-369

Hackett, N.R., Redmond, D.E., Sondhi, D., Giannaris, E.L., et al (2005) Safety of direct administration of AAV2CUhCLN2, a candidate treatment for the central nervous system manifestations of late infantile neuronal ceroid lipofuscinosis, to brain of rats and nonhuman primates Hum. Gene Ther., 16, 1484-1503

Lojewski, X., Staropoli, J.F., Biswas-Legrand, S., Simas, A.M., et al (2014) Human iPSC models of neuronal ceroid lipofuscinosis capture distinct effects of TPP1 and CLN3 mutations on the endocytic pathway Hum. Mol. Genet., 23, 2005–2022

Passini, M.A., Dodge, J.C., Bu, J., Yang, W., et al (2006) Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis J. Neurosci., 26, 1334-1342

Roberts, M.S., Macauley, S.L., Wong, A.M., Yilmas, D., et al (2012) Combination small molecule PPT1 mimetic and CNS-directed gene therapy as a treatment for infantile neuronal ceroid lipofuscinosis J. Inherit. Metab. Dis., 35, 847–857

Sondhi, D., Peterson, D.A., Giannaris, E.L., Sanders, C.T., et al (2005) AAV2-mediated CLN2 gene transfer to rodent and non-human primate brain results in long-term TPP-I expression compatible with therapy for LINCL Gene Ther., 12, 1618-1632

Sondhi, D., Johnson, L., Purpura, K., Monette, S., et al (2012) Long-term expression and safety of administration of AAVrh.10hCLN2 to the brain of rats and nonhuman primates for the treatment of late infantile neuronal ceroid lipofuscinosis Hum. Gene Ther. Methods, 23, 324–335

Lumbar sensory neurons
Yu, H., Fischer, G., Ferhatovic, L., Fan, F., et al (2013) Intraganglionic AAV6 results in efficient and long-term gene transfer to peripheral sensory nervous system in adult rats PLoS One, 8: e61266

Major depressive disorder
Cao, X., Li, L-P., Wang, Q., Wu, Q., et al (2013) Astrocyte-derived ATP modulates depressive-like behaviors Nat. Med., 19, 773-777

Kang, H.J., Voleti, B., Hajszan, T., Rajkowska, G., et al (2012) Decreased expression of synapse-related genes and loss of synapses in major depressive disorder Nat. Med., 18, 1413-1419

Marmoset CNS transduction
Matsuzaki, Y., Konno, A., Mukai, R., Honda, F., Hirato, M., Yoshimoto, Y. and Hirai, H. (2017) Transduction profile of the marmoset central nervous system using adeno-associated virus Serotype 9 vectors Mol. Neurobiol., 54, 1745–1758

Mechanosensory C fibres
Vrontou, S., Wong, A.M., Rau, K.K., Koerber, R. and Anderson, D.J. (2013) Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo Nature, 493, 669-673

MECP2 gene
Gadalla, K.K.E., Bailey, M.E.S., Spike, R.C., Ross, P.D., et al (2013) Improved survival and reduced phenotypic severity following AAV9/MECP2 gene transfer to neonatal and juvenile male Mecp2 knockout mice Mol. Ther., 21, 18–30

Mahgoub, M., Adachi, M., Suzuki, K., Liu, X., Kavalali, E.T., Chahrour, M.H. and Monteggia, L.M. (2016) MeCP2 and histone deacetylases 1 and 2 in dorsal striatum collectively suppress repetitive behaviors Nat. Neurosci., 19, 1506-1512

Medial entorhinal cortex delivery
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S. and Ikezu, T. (2015) Depletion of microglia and inhibition of exosome synthesis halt tau propagation Nat. Neurosci., 18, 1584-1593

Medial septum delivery
Hall, H., Jewett, M., Landeck, N., Nilsson, N., et al (2013) Characterization of cognitive deficits in rats overexpressing human alpha-synuclein in the ventral tegmental area and medial septum using recombinant adeno-associated viral vectors PLoS One 8: e64844

Klein, R.L., Lin, W-L., Dickson, D.W., Lewis, J., et al (2004) Rapid neurofibrillary tangle formation after localized gene transfer of mutated Tau Am. J. Pathol., 164, 347-353

Tomioka, T., Shimazaki, T., Yamauchi, T., Oki, T., et al (2014) LIM homeobox 8 (Lhx8) is a key regulator of the cholinergic neuronal function via a tropomyosin receptor kinase A (TrkA)-mediated positive feedback loop J. Biol. Chem., 289, 1000–1010

Wu, K., Meyer, E.M., Bennett, J.A., Meyers, C.A., et al (2005) AAV2/5-mediated NGF gene delivery protects septal cholinergic neurons following axotomy Brain Res., 1061, 107-113

Memory, working
Hausrat, T.J., Muhia, M., Gerrow, K., Thomas, P., Hirdes, W., Tsukita, S., Heisler, F.F., Herich, L., Dubroqua, S. (2015) Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and shortterm memory Nat. Commun., 6: 6872

Liu, X., Zeng, K., Li, M., Wang, Q., Liu, R., Zhang, B., Wang, J-Z., Shu, X. and Wang, X. (2017) Expression of P301L-hTau in mouse MEC induces hippocampus-dependent memory deficit Sci. Rep., 7: 3914

Mustroph, M.L., King, M.A., Klein, R.L. and Ramirez, J.J. (2012) Adult-onset focal expression of mutated human tau in the hippocampus impairs spatial working memory of rats Behav. Brain Res., 233, 141-148

Sim, S-E., Lim, C-S., Kim, J-I., Seo, D., Chun, H., Yu, N-K., Lee, J., Kang, S.J., Ko, H-G., Choi, J-H. et al (2016) The brain-enriched microRNA miR-9-3p regulates synaptic plasticity and memory J. Neurosci., 36, 8641– 8652

Woldemichael, B.T., Jawaid, A., Kremer, E.A., Gaur, N., Krol, J., Marchais, A. and Mansuy, I.M. (2016) The microRNA cluster miR-183/96/182 contributes to long-term memory in a protein phosphatase 1-dependent manner Nat. Comm., 7: 12594

Microglia
Condello, C., Yuan, P., Schain, A. and Grutzendler, J. (2015) Microglia constitute a barrier that prevents neurotoxic protofibrillar Ab42 hotspots around plaques Nat. Commun., 6: 6176

Deczkowska, A., Matcovitch-Natan, O., Tsitsou-Kampeli, A., Ben-Hamo, S., Dvir-Szternfeld, R., Spinrad, A., Singer, O., David, E., Winter, D.R. et al (2017) Mef2C restrains microglial inflammatory response and is lost in brain ageing in an IFN-I-dependent manner Nat. Comm., 8: 717

Latta, C.H., Sudduth, T.L., Weekman, E.M., Brothers, H.M., Abner, E.L., Popa, G.J., Mendenhall, M.D., Gonzalez-Oregon, F. Braun, K. and Wilcock, D.M. (2015) Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-β using BV2 microglial cells and APP/PS1 transgenic mice J. Neuroinflam., 12: 41

Mid-brain delivery
Blits, B., Derks, S., Twisk, J., Ehlert, E., et al (2010) Adeno-associated viral vector (AAV)-mediated gene transfer in the red nucleus of the adult rat brain: Comparative analysis of the transduction properties of seven AAV serotypes and lentiviral vectors J. Neurosci. Meth., 185, 257–263

Eslamboli, A., Romero-Ramos, M., Burger, C., Bjorklund, T., et al (2007) Long-term consequences of human alpha-synuclein overexpression in the primate ventral midbrain Brain, 130, 799-815

Hayes, M.R., Skibicka, K.P., Leichner, T.M., Guarnieri, D.J., et al (2010) Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation Cell Metab., 11, 77–83

Hommel, J.D., Sears, R.M., Georgescu, D., Simmoms, D.L. and DiLeone, R.J. (2003) Local gene knowdown in the brain using viral-mediated RNA interference Nat. Med., 9, 1539-1544

Polinski, N.K., Gombash, S.E., Manfredsson, F.P., Lipton, J.W., Kemp, C.J., Cole-Strauss, A., Kanaan, N.M. et al (2015) Recombinant adenoassociated virus 2/5-mediated gene transfer is reduced in the aged rat midbrain Neurobiol. Aging, 36, 1110-1120

Motor coordination
Bosch, M.K., Carrasquillo, Y., Ransdell, J.L., Kanakamedala, A., Ornitz, D.M. and Nerbonne, J.M. (2015) Intracellular FGF14 (iFGF14) is required for spontaneous and evoked firing in cerebellar Purkinje neurons and for motor coordination and balance J. Neurosci., 35, 6752– 6769

Muscle-neuron delivery
ElMallah, M.K., Falk, D.J., Lane, M.A., Conlon, T.J., et al (2012) Retrograde gene delivery to hypoglossal motoneurons using adeno-associated virus serotype 9 Hum. Gene Ther. Methods, 23, 148–156

Myelin/MBP-deficient neurons
Aggarwal1, S., Snaidero, N., Pähler, G., Frey, S., et al (2013) Myelin membrane assembly is driven by a phase transition of myelin basic proteins into a cohesive protein meshwork PLoS Biol., 11: e1001577

Lutz, D., Loers, G., Kleene, R., Oezen, I., et al (2014) Myelin basic protein cleaves cell adhesion molecule L1 and promotes neuritogenesis and cell survival J. Biol. Chem., 289, 13503–13518

Myenteric neuron delivery
Buckinx, R., Van Remoortel, S., Gijsbers, R., Waddington, S.N. and Timmermans, J-P. (2016) Proof-ofconcept: neonatal intravenous injection of adenoassociated virus vectors results in successful transduction of myenteric and submucosal neurons in the mouse small and large intestine Neurogastroenterol. Motil., 28, 299–305

Narcolepsy
Liu, M., Blanco-Centurion, C., Konadhode, R., Begum, S., et al (2011) Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice J. Neurosci., 31, 6028–6040

Neocortical cells
Allen, W.E., Kauvar, I.V., Chen, M.Z., Richman, E.B., Yang, S.J., Chan, K., Gradinaru, V., Deverman, B.E. Luo, L. and Deisseroth, K. (2017) Global representations of goal-directed behavior in distinct cell types of mouse neocortex Neuron, 94, 891–907

Neonatal – Forebrain
Pilpel, N., Landeck, N., Klugmann, M., Seeburg, P.H. and Schwarz, M.K. (2009) Rapid, reproducible transduction of select forebrain regions by targeted recombinant virus injection into the neonatal mouse brain J. Neurosci. Methods, 182, 55–63

Neonatal – Intracerebroventricular
Wolf, D.A., Lenander, A.W., Nan, Z., Belur, L.R., et al (2011) Direct gene transfer to the CNS prevents emergence of neurologic disease in a murine model of mucopolysaccharidosis type I Neurobiol. Dis., 43, 123–133

Neuregulins
Seshadri, S., Faust, T., Ishizuka, K., Delevich, K., Chung, Y., Kim, S-H., Cowles, M., Niwa, M. et al (2015) Interneuronal DISC1 regulates NRG1-ErbB4 signalling and excitatory–inhibitory synapse formation in the mature cortex Nat. Commun., 6: 10118

Vullhorst, D., Ahmad, T., Karavanova, I., Keating, C. and Buonanno, A. (2017) Structural similarities between neuregulin 1–3 isoforms determine their subcellular distribution and signaling mode in central neurons J. Neurosci., 37, 5232–5249

Neurexins
Aoto, J., Martinelli, D.C., Malenka, R.C., Tabuchi, K. and Südhof, T.C. (2013) Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking Cell, 154, 75–88

Aoto, J., Földy, C., Ciurea Ilcus, S.M., Tabuchi, K. and Südhof, T.C. (2015) Distinct circuit-dependent functions of presynaptic neurexin-3 at GABAergic and glutamatergic synapses Nat. Neurosci., 18, 997-1007

Neuritogenesis
Lutz, D., Loers, G., Kleene, R., Oezen, I., et al (2014) Myelin basic protein cleaves cell adhesion molecule L1 and promotes neuritogenesis and cell survival J. Biol. Chem., 289, 13503–13518

Neurodegenerative model
Cook, C., Kang, S.S., Carlomagno, Y., Lin, W-L., Yue, M., Kurti, A., Shinohara, M., Jansen-West, K., Perkerson, E. et al (2015) Tau deposition drives neuropathological, inflammatory and behavioral abnormalities independently of neuronal loss in a novel mouse model Hum. Mol. Genet., 24. 6198-6212

Huda, F., Konno, A., Matsuzaki, Y., Goenawan, H., Miyake, K., Shimada, T. and Hirai, H. (2014) Distinct transduction profiles in the CNS via three injection routes of AAV9 and the application to generation of a neurodegenerative mouse model Mol. Ther. Methods Clin. Dev., 1: 14032

Leiva-Rodríguez, T., Romeo-Guitart, D., Marmolejo-Martínez-Artesero, S., Herrando-Grabulosa, M., Bosch, A., Forés, J. and Casas, C. (2018) ATG5 overexpression is neuroprotective and attenuates cytoskeletal and vesicle-trafficking alterations in axotomized motoneurons Cell Death Dis., 9: 626

Shumar, S.A., Fagone, P., Alfonso-Pecchio, A., Gray, J.T., Rehg, J.E., Jackowski, S. and Leonardi, R. (2015) Induction of neuron-specific degradation of coenzyme A models pantothenate kinase-associated neurodegeneration by reducing motor coordination in mice PLoS One, 10: e0130013

Neuroendocrine responses
Bender, J., Engeholm, M., Ederer, M.S., Breu, J., Møller, T.C., Michalakis, S., Rasko, T. 5, Wanker, E.E. et al (2015) Corticotropin-releasing hormone receptor type 1 (CRHR1) clustering with MAGUKs is mediated via its C-terminal PDZ binding motif PLoS One, 10: e0136768

Neuroglobin expression
Yu, Z., Liu, N., Li, Y., Xu, J. and Wang, X. (2013) Neuroglobin overexpression inhibits oxygen–glucose deprivation-induced mitochondrial permeability transition pore opening in primary cultured mouse cortical neurons Neurobiol. Dis., 56, 95–103

Neuroinflammation
Humbert-Claude, M., Duc, D., Dwir, D., Thieren, L., Sandstrom von Tobel, J., Begka, C., Legueux, F., Velin, D., Maillard, M.H., Do, K.Q., Monnet-Tschudi, F. and Tenenbaum, L. (2016) Tollip, an early regulator of the acute inflammatory response in the substantia nigra J. Neuroinflamm., 13: 303

Latta, C.H., Sudduth, T.L., Weekman, E.M., Brothers, H.M., Abner, E.L., Popa, G.J., Mendenhall, M.D., Gonzalez-Oregon, F. Braun, K. and Wilcock, D.M. (2015) Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-β using BV2 microglial cells and APP/PS1 transgenic mice J. Neuroinflam., 12: 41

Weekman, E.M., Sudduth, T.L., Abner, E.L., Popa, G.J., Mendenhal, M.D., Brothers, H.M., Braun, K., Greenstein, A. and Wilcock, D.M. (2014) Transition from an M1 to a mixed neuroinflammatory phenotype increases amyloid deposition in APP/PS1 transgenic mice J. Neuroinflamm., 11: 1

Neuroligin-3
Rothwell, P.E., Fuccillo, M.V., Maxeiner, S., Hayton, S.J., Gokce, O., Lim, B.K., Fowler, S.C., Malenka, R.C. and Südhof, T.C. (2014) Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors Cell 158, 198–212

Neuronal communication/circuits/transmission
Auffenberg, E., Jurik, A., Mattusch, C., Stoffel, R., Genewsky, A., Namendorf, C., Schmid, R.M. Rammes, G. et al (2016) Remote and reversible inhibition of neurons and circuits by small molecule induced potassium channel stabilization Sci. Rep., 6: 19293

Crawford, D.C., Ramirez, D.M.O., Trauterman, B., Monteggia, L.M. and Kavalali E.T. (2017) Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy Nat. Comm., 8: 14436

Del Pino, I., Koch, D., Schemm, R., Qualmann, B., Betz, H. and Paarmann, I. (2014) Proteomic analysis of glycine receptor  Subunit (GlyR)-interacting proteins – evidence for syndapin I regulating synaptic glycone receptors J. Biol. Chem., 289, 1396–11409

Frühbeis, C., Fröhlich, D., Kuo, W.P., Amphornrat, J., Thilemann, S., Saab, A.S., Kirchhoff, F., Möbius, W., Goebbels, S., Nave, K-A., Schneider, A., Simons, M., Klugmann, M., Trotter, J., Krämer-Albers, E-M., (2013) Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte–neuron communication PLoS Biol., 11: e1001604

Patzke, C., Acuna, C., Giam, L.R., Wernig, M. and Südhof, T.C. (2016) Conditional deletion of L1CAM in human neurons impairs both axonal and dendritic arborization and action potential generation J. Exp. Med. 213, 499–515

Traunmüller, L., Bornmann, C. and Scheiffele, P. (2014) Alternative splicing coupled nonsense-mediated decay generates neuronal cell type-specific expression of SLM proteins J. Neurosci., 34, 16755–16761

Neuronal differentiation
Zheng, D., Sabbagh, J.J., Blair, L.J., Darling, A.L., Wen, X. and Dickey, C.A. (2016) MicroRNA-511 binds to FKBP5 mRNA, which encodes a chaperone protein, and regulates neuronal differentiation J. Biol. Chem., 291, 17897–17906

Neuropathic pain
Fischer, G., Pan, B., Vilceanu, D., Hogan, Q.H. and Yu, H. (2014) Sustained relief of neuropathic pain by AAVtargeted expression of CBD3 peptide in rat dorsal root ganglion Gene Ther., 21, 44–51

Ji, G., Zhang, W., Mahimainathan, L., Narasimhan, M., Kiritoshi, T., Fan, X., Wang, J., Green, T.A. and Neugebauer, V. (2017) 5-HT2C receptor knockdown in the amygdala inhibits neuropathic-pain-related plasticity and behaviors J. Neurosci., 37, 1378 –1393

Xiang, H., Liu, Z., Wang, F., Xu, H., Roberts, C., Fischer, G., Stucky, C.L., Dean, C., Pan, B., Hogan, Q.H. and Yu, H. (2017) Primary sensory neuron-specific interference of TRPV1 signaling by adeno-associated virusencoded TRPV1 peptide aptamer attenuates neuropathic pain Mol.Pain, 13, 1–18

Neuropeptide function
Aoki, M., Watanabe, Y., Yoshimoto, K., Tsujimura, A., Yamamoto, T., Kanamura, N. and Tanaka, M. (2016) Involvement of serotonin 2C receptor RNA editing in accumbal neuropeptide Y expression and behavioural despair Eur. J. Neurosci., 43, 1219–1228

Callander, G.E., Ma, S., Ganella, D.E., Wimmer, V.C., Gundlach, A.L., Thomas, W.G. and Bathgate, R.A.D. (2012) Silencing relaxin-3 in nucleus incertus of adult rodents: a viral vector-based approach to investigate neuropeptide function PLoS One, 7: e42300

Ledri, M., Nikitidou, L., Erdelyi, F., Szabo, G., Kirik, D., Deisseroth, K. and Kokaia, M. (2012) Altered profile of basket cell afferent synapses in hyper-excitable dentate gyrus revealed by optogenetic and two-pathway stimulations Eur. J. Neurosci., 36, 1971–1983

Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E. and Malenka, R.C. (2012) Anhedonia requires MC4Rmediated synaptic adaptations in nucleus accumbens Nature, 487, 183-189

Neurotrophic factors
Barroso-Chinea, P., Cruz-Muros, I., Afonso-Oramas, D., Castro-Hernández, J., Salas-Hernández, J., Chtarto, A., Luis-Ravelo, D., Humbert-Claude, M., Tenenbaum, L. and González-Hernández, T. (2016) Long-term controlled GDNF over-expression reduces dopamine transporter activity without affecting tyrosine hydroxylase expression in the rat mesostriatal system Neurobiol. Dis., 88, 44–54

Chtarto, A., Bockstael, O., Gebara, E., Vermoesen, K., Melas, C., Pythoud, C., Levivier, M., De Witte, O., Luthi-Carter, R., Clinkers, R. and Tenenbaum, L. (2013) An adeno-associated virus-based intracellular sensor of pathological nuclear factor-B activation for disease-inducible gene transfer PLoS One, 8: e53156

Drinkut, A., Tereshchenko, Y., Schulz, J.B., Bähr, M. and Kügler, S. (2012) Efficient gene therapy for Parkinson’s disease using astrocytes as hosts for localized neurotrophic factor delivery Mol. Ther., 20, 534–543

Gombash, S.E., Lipton, J.W., Collier, T.J., Madhavan, L., Steece-Collier, K., Cole-Strauss, A., Terpstra, B.T., Spieles-Engemann, A.L., Daley, B.F., Wohlgenant, S.L., Thompson, V.B., Manfredsson, F.P., Mandel, D.J. and Sortwell, C.E. (2012) Striatal pleiotrophin overexpression provides functional and morphological neuroprotection in the 6-hydroxydopamine model Mol. Ther., 20, 544–554

Osborne, A., Wang, A.X.Z., Tassoni, A., Widdowson, P.S. and Martin, K.R. (2018) Design of a novel gene therapy construct to achieve sustained brain-derived neurotrophic factor signaling in neurons Hum. Gene Ther., 29, 828-841

Tereshchenko, J., Maddalena, A., Bähr, M. and Kügler, S. (2014) Pharmacologically controlled, discontinuous GDNF gene therapy restores motor function in a rat model of Parkinson’s disease Neurobiol. Dis., 65, 35–42

Tronci, E., Napolitano, F., Muñoz, A., Fidalgo, C., Rossi, F., Björklund, A., Usiello, A. and Carta, M. (2017) BDNF over-expression induces striatal serotonin fiber sprouting and increases the susceptibility to L-DOPA induced dyskinesia in 6-OHDA lesioned rats Exp. Neurol., 297, 73–81

Neurovascular delivery
Körbelin, J., Dogbevia, G., Michelfelder, S., Ridder, D.A., Hunger, A., Wenze, J., Seismann, H., Lampe, M., Bannach, J. et al (2016) A brain microvasculature endothelial cell-specific viral vector with the potential to treat neurovascular and neurological diseases EMBO Mol. Med., 8, 609-625

Niemann-Pick disease
Markmann, S., Christie-Reid, J.J., Rosenberg, J.B., De, B.P., Kaminsky, S.M., Crystal, R.G. and Sondhi, D. (2018) Attenuation of the Niemann-Pick type C2 disease phenotype by intracisternal administration of an AAVrh.10 vector expressing Npc2 Exp. Neurol., 306, 22–33

Nigro-striatal delivery
Dalkara, D., Kolstad, K.D., Guerin, K.I., Hoffmann, N.V., et al (2011) AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa Mol. Ther., 19, 1602–1608

Furler, S., Paterna, J-C., Weibel, M. and Büeler, H. (2001) Recombinant AAV vectors containing the foot and mouth disease virus 2A sequence confer efficient bicistronic gene expression in cultured cells and rat substantia nigra neurons Gene Ther., 8, 864-873

Gustafsson, E., Andsberg, G., Darsalia, V., Mohapel, P., et al (2003) Anterograde delivery of brain-derived neurotrophic factor to striatum via nigral transduction of recombinant adeno-associated virus increases neuronal death but promotes neurogenic response following stroke Eur. J. Neurosci., 17, 2667-2678

Klein, R.L., King, M.A., Hamby, M.E. and Meyer, E.M. (2002) Dopaminergic cell loss induced by human A30P -synuclein gene transfer to the rat substantia nigra Hum. Gene Ther., 13, 605-612

Klein, R.L., Dayton, R.D., Lin, W-L. and Dickson, D.W. (2005) Tau gene transfer, but not alpha-synuclein, induces both progressive dopamine neuron degeneration and rotational behavior in the rat Neurobiol. Dis., 20, 64-73

Klein, R.L., Dayton, R.D., Henderson, K.M. and Petrucelli, L. (2006) Parkin is protective for substantia nigra dopamine neurons in a tau gene transfer neurodegeneration model Neurosci. Lett., 401, 130-135

Klein, R.L., Dayton, R.D., Tatom, J.B., Diaczynsky, C.G., et al (2008) Tau expression levels from various adeno-associated virus vector serotypes produce graded neurodegenerative disease states Eur. J. Neurosci., 27, 1615-1625

Klein, R.L., Dayton, R.D., Terry, T.L., Vascoe, C., et al (2009) PET imaging in rats to discern temporal onset differences between 6-hydroxydopamine and tau gene vector neurodegeneration models Brain Res., 1259, 113-122

McFarland, N.R., Lee, J-S., Hyman, B.T. and McLean, P.J. (2009) Comparison of transduction efficiency of recombinant AAV serotypes 1, 2, 5 and 8 in the rat nigrostriatal system J. Neurochem., 109, 838–845

McFarland, N.R., Fan, Z., Xu, K., Schwarzschild, M.A., et al (2009) -Synuclein S129 phosphorylation mutants do not alter nigrostriatal toxicity in a rat model of Parkinson disease J. Neuropathol. Exp. Neurol., 68, 515-524

Manfredsson, F.P., Burger, C., Sullivan, L.F., Muzyczka, N., et al (2007) rAAV-mediated nigral human parkin over-expression partially ameliorates motor deficits via enhanced dopamine neurotransmission in a rat model of Parkinson’s disease Exp. Neurol., 207, 289-301

Manfredsson, F.P., Tumer, N., Erdos, B., Landa, T., et al (2009) Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity Mol. Ther., 17, 980-991

Paterna, J-C., Feldon, J. and Büeler, H. (2004) Transduction profiles of recombinant adeno-associated virus vectors derived from serotypes 2 and 5 in the nigrostriatal system of rats J. Virol., 78, 6808-6817

Seo, B.B., Nakamura-Ogiso, E., Flotte, T.R., Matsuno-Yagi, A. and Yagi, T. (2006) In vivo complementation of complex I by the yeast Ndi enzyme J. Biol. Chem.,281, 14250-14255

Tatom, J.B., Wang, D.B., Dayton, R.D., Skalli, O., et al (2009) Mimicking aspects of frontotemporal lobar degeneration and Lou Gehrig’s disease in rats via TDP-43 overexpression Mol. Ther., 17, 607–613

Ulusoy, A., Sahin, G., Björklund, T., Aebischer, P. and Kirik, D. (2009) Dose optimization for long-term rAAVmediated RNA interference in the nigrostriatal projection neurons Mol. Ther., 17, 1574-1584

Yasuda, T., Miyachi, S., Kitagawa, R., Wada, K., et al (2007) Neuronal specificity of α-synuclein toxicity and effect of Parkin co-expression in primates Neuroscience., 144, 743-753

Yasuda, T., Nihira, T., Ren, Y-R., Cao, X-Q., et al (2009) Effects of UCH-L1 on -synuclein over-expression mouse model of Parkinson’s disease J. Neurochem., 108, 932–944

NMDA receptors
Elagabani, M.N., Brisevac, D., Kintscher, M., Pohle, J., Köhr, G., Schmitz, D. and Kornau, H-C. (2016) Subunit-selective N-methyl-D-aspartate (NMDA) receptor signaling through brefeldin A-resistant Arf guanine nucleotide exchange factors BRAG1 and BRAG2 during synapse maturation J. Biol. Chem., 291, 9105–9118

Huang, Y.H., Ishikawa, M., Lee, B.R., Nakanishi, N., Schlüter, O.M. and Dong, Y. (2011) Searching for presynaptic NMDA receptors in the nucleus accumbens J. Neurosci., 31, 18453–18463

Vullhorst, D., Mitchell, R.M., Keating, C., Roychowdhury, S., Karavanova, I., Tao-Cheng, J-H. and Buonanno, A. (2015) A negative feedback loop controls NMDA receptor function in cortical interneurons via neuregulin 2/ErbB4 signalling Nat. Commun., 6: 7222

Non-invasive gene therapy
Chan, K.Y., Jang, M.J., Yoo, B.B., Greenbaum, A., Ravi, N., Wu, W-L., Sánchez-Guardado, L., Lois, C., Mazmanian, S.K., Deverman, B.E. and Gradinaru, V. (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems Nat. Neurosci., 20, 1172-1179

Noonan syndrome
Lee, Y-S., Ehninger, D., Zhou, M., Oh, J-Y., Kang, M., Kwak, C., Ryu, H-H., Butz, D., et al (2014) Mechanism and treatment for learning and memory deficits in mouse models of Noonan syndrome Nat. Neurosci., 17, 1736-1743

Nucleus accumbens
Aoki, M., Watanabe, Y., Yoshimoto, K., Tsujimura, A., Yamamoto, T., Kanamura, N. and Tanaka, M. (2016) Involvement of serotonin 2C receptor RNA editing in accumbal neuropeptide Y expression and behavioural despair Eur. J. Neurosci., 43, 1219–1228

Chandra, R., Francis, T.C., Konkalmatt, P., Amgalan, A., Gancarz, A.M., Dietz, D.M. and Lobo, M.K. (2015) Opposing role for Egr3 in nucleus accumbens cell subtypes in cocaine action J. Neurosci., 35, 7927–7937

Dölen, G., Darvishzadeh, A., Huang, K.W. and Malenka, R.C. (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin Nature, 501, 179-184

Huang, Y.H., Ishikawa, M., Lee, B.R., Nakanishi, N., et al (2011) Searching for presynaptic NMDA receptors in the nucleus accumbens J. Neurosci., 31, 18453–18463

Lazarus, M., Shen, H-Y., Cherasse, Y., Qu, W-M., et al (2011) Arousal effect of caffeine depends on adenosine A2A receptors in the shell of the nucleus accumbens J. Neurosci., 31, 10067–10075

Liefhebber, J.M.P., Hague, C.V., Zhang, Q., Wakelam, M.J.O. and McLauchlan, J. (2014) Modulation of triglyceride and cholesterol ester synthesis impairs assembly of infectious hepatitis C virus J. Biol. Chem., 289, 21276-21288

Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E. and Malenka, R.C. (2012) Anhedonia requires MC4Rmediated synaptic adaptations in nucleus accumbens Nature, 487, 183-189

Neumann, P.A., Wang, Y., Yan, Y., Wang, Y., Ishikawa, M., Cui, R., Huang, Y.H. et al (2016) Cocaineinduced synaptic alterations in thalamus to nucleus accumbens projection Neuropsychopharmacology, 41, 2399–2410

Reker. A.N., Oliveros, A., Sullivan III, J.M., Nahar, L., Hinton, D.J., Kim, T., Bruner, R.C., Choi, D-S., Goeders, N.E. and Nam, H.W. (2018) Neurogranin in the nucleus accumbens regulates NMDA receptor tolerance and motivation for ethanol seeking Neuropharmacology, 131, 58-67

Rothwell, P.E., Fuccillo, M.V., Maxeiner, S., Hayton, S.J., Gokce, O., Lim, B.K., Fowler, S.C., Malenka, R.C. and Südhof, T.C. (2014) Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors Cell 158, 198–212

Suska, A., Lee, B.R., Huang, Y.H., Dong, Y. and Schlüter, O.M. (2013) Selective presynaptic enhancement of the prefrontal cortex to nucleus accumbens pathway by cocaine Proc. Natl. Acad. Sci. USA, 110, 710-718

Yu, J., Yan, Y., Li, K-L., Wang, Y., Huang, Y.H., Urban, N.N., Nestler, E.J., Schlüter, O.M. and Dong, Y. (2017) Nucleus accumbens feedforward inhibition circuit promotes cocaine self-administration Proc. Natl. Acad. Sci. USA, 114, E8750–E8759

Nucleus incertus
Callander, G.E., Ma, S., Ganella, D.E., Wimmer, V.C., Gundlach, A.L., et al (2012) Silencing relaxin-3 in nucleus incertus of adult rodents: a viral vector-based approach to investigate neuropeptide function PLoS One, 7: e42300

Oestrous cycle maintenance
Rodríguez, S.S., Schwerdt, J.I., Barbeito, C.G., Flamini, M.A., et al (2013) Hypothalamic IGF-I gene therapy prolongs estrous cyclicity and protects ovarian structure in middle-aged female rats Endocrinology, 154, 2166–2173

Olfactory bulb
Suzuki, Y., Kiyokage, E., Sohn, J., Hioki, H. and Toida, K. (2015) Structural basis for serotonergic regulation of neural circuits in the mouse olfactory bulb J. Comp. Neurol., 523, 262–280

Oligodendroglia
Francis, J.S., Wojtas, I., Markov, V., Gray, S.J., McCown, T.J., Samulski, R.J., Bilaniuk, L.T. Wang, D-J. et al (2016) N-acetylaspartate supports the energetic demands of developmental myelination via oligodendroglial aspartoacylase Neurobiol. Dis., 96, 323–334

Mandel, R.J., Marmikon, D.J., Kirik, D., Chu, Y., Heindel, C., McCown, T., Gray, S.J. and Kordower, J. H. (2017) Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates Acta Neuropath. Comm., 5: 47

Mitew, S., Gobius, I., Fenlon, L.R., McDougall, S.J., Hawkes, D., Xing, Y.L., Bujalka, H., Gundlach, A.L., Richards, L.J. et al (2018) Pharmacogenetic stimulation of neuronal activity increases myelination in an axonspecific manner Nat. Comm., 9: 306

Powell, S.K., Khan, N., Parker, C.L., Samulski, R.J., Matsushima, G., Gray, S.J. 1,4,8 and McCown, T.J. (2016) Characterization of a novel adeno-associated viral vector with preferential oligodendrocyte tropism Gene Ther., 23, 807–814

Opioid system
Romero-Picó, A., Vázquez, M.J., González-Touceda, D., Folgueira, C., et al (2013) Hypothalamic -opioid receptor modulates the orexigenic effect of ghrelin Neuropsychopharmacology (2013) 38, 1296–1307

Parkinson’s disease
Angot, E., Steiner, J.A., Lema Tomé, C.M., Ekström, P., et al (2012) Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo PLoS One, 7: e39465

Arawaka, S., Fukushima, S., Sato, H., Sasaki, A., et al (2014) Zonisamide attenuates -synuclein neurotoxicity by an aggregation-independent mechanism in a rat model of familial Parkinson’s disease PLoS One, 9: e89076

Arcuri, L., Viaro, R., Bido, S., Longo, F., Calcagno, M., Fernagut, P-O., Zaveri, N.T., Calò, G., Bezard, E. and Morari, M. (2016) Genetic and pharmacological evidence that endogenous nociceptin/orphanin FQ contributes to dopamine cell loss in Parkinson’s disease Neurobiol. Dis., 89, 55–64

Barroso-Chinea, P., Cruz-Muros, I., Afonso-Oramas, D., Castro-Hernández, J., Salas-Hernández, J., Chtarto, A., Luis-Ravelo, D. et al (2016) Long-term controlled GDNF over-expression reduces dopamine transporter activity without affecting tyrosine hydroxylase expression in the rat mesostriatal system Neurobiol. Dis., 88, 44–

Benskey, M.J., Manfredsson, F.P., Lookingland, K.J. and Goudreau, J. L. (2015) The role of parkin in the differential susceptibility of tuberoinfundibular and nigrostriatal dopamine neurons to acute toxicant exposure Neurotoxicology, 46, 1–11

Bido, S., Soria, F.N., Fan, R.Z., Bezard, E. and Tieu, K. (2017) Mitochondrial division inhibitor-1 is neuroprotective in the A53T-α-synuclein rat model of Parkinson’s disease Sci. Rep., 7: 7495

Björklund, T., Carlsson, T., Cederfjäll, E.A., Carta, M. and Kirik, D. (2010) Optimized adeno-associated viral vector-mediated striatal DOPA delivery restores sensorimotor function and prevents dyskinesias in a model of advanced Parkinson’s disease Brain, 133, 496–511

Brys, I., Nunes, J. and Fuentes, R. (2017) Motor deficits and beta oscillations are dissociable in an alphasynuclein model of Parkinson’s disease Eur. J. Neurosci., 46, 1906–1917

Buck, K., Landeck, N., Ulusoy, A., Majbour, N.K., El-Agnaf, O.M.A. and Kirik, D. (2015) Ser129 phosphorylation of endogenous α-synuclein induced by overexpression of polo-like kinases 2 and 3 in nigral dopamine neurons is not detrimental to their survival and function Neurobiol. Dis., 78, 100–114

Cederfjäll, E., Sahin, G., Kirik, D. and Björklund, T. (2012) Design of a single AAV vector for co-expression of TH and GCH1 to establish continuous DOPA synthesis in a rat model of Parkinson’s disease Mol. Ther., 20, 1315–1326

Cederfjäl, E., Nilsson, N., Sahin, G., Chu, Y., et al (2013) Continuous DOPA synthesis from a single AAV: dosing and efficacy in models of Parkinson’s disease Sci. Rep., 3: 2157

Chansel-Debordeaux, L., Bourdenx, M., Dovero, S., Grouthier, V., Dutheil, N., Espana, A., Groc, L., Jimenez, C., Bezard, E. and Dehay, B. (2017) In utero delivery of rAAV2/9 induces neuronal expression of the transgene in the brain: towards new models of Parkinson’s disease Gene Ther., 24, 801–809

Cheng, S., Tereshchenko, J., Zimmer, V., Vachey, G., Pythoud, C., Rey, M., Liefhebber, J., Raina, A., Streit, F. (2018) Therapeutic efficacy of regulable GDNF expression for Huntington’s and Parkinson’s disease by a highinduction, background-free “GeneSwitch” Vector Exp. Neurol., 309, 79–90

Chtarto, A., Humbert-Claude, M., Bockstael, O., Das, A.T., Boutry, S., Breger, L.S., Klaver, B., Melas, C., Barroso-Chinea, P. et al (2016) A regulatable AAV vector mediating GDNF biological effects at clinicallyapproved sub-antimicrobial doxycycline doses Mol. Ther. Meth. Clin. Dev., 5: 16027

Danzer, K.M., Kranich, L.R., Ruf, W.P., Cagsal-Getkin, O., et al (2012) Exosomal cell-to-cell transmission of alpha synuclein oligomers Mol. Neurodegener., 7: 42

Decressac, M., Ulusoy, A., Mattsson, B., Georgievska, B., et al (2011) GDNF fails to exert neuroprotection in a rat a-synuclein model of Parkinson’s disease Brain, 134, 2302–2311

Decressac, M., Mattsson, B., Lundblad, M., Weikop, P. and Björklund, A. (2012) Progressive neurodegenerative and behavioural changes induced by AAV-mediated overexpression of α-synuclein in midbrain dopamine neurons Neurobiol. Dis., 45, 939–953

Decressac, M., Mattsson, B. and Björklund, A. (2012) Comparison of the behavioural and histological characteristics of the 6-OHDA and α-synuclein rat models of Parkinson’s disease Exp. Neurol., 235, 306–315

Decressac, M., Mattssona, B., Weikop, P., Lundblad, M., et al (2013) FEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity Proc. Soc. Natl. Acad. Sci. USA, E1817–E1826

Drinkut, A., Tereshchenko, Y., Schulz, J.B., Bähr, M. and Kügler, S. (2012) Efficient gene therapy for Parkinson’s disease using astrocytes as hosts for localized neurotrophic factor delivery Mol. Ther., 20, 534–543

Febbraro, F., Andersen, K.J., Sanchez-Guajardo, V., Tentillier, A., et al (2013) Chronic intranasal deferoxamine ameliorates motor defects and pathology in the α-synuclein rAAV Parkinson’s model Exp. Neurol., 247, 45–58

Febbraro, F., Sahin, G., Farran, A., Soares, S., et al (2013) Ser129D mutant alpha-synuclein induces earlier motor dysfunction while S129A results in distinctive pathology in a rat model of Parkinson’s disease Neurobiol. Dis., 56, 47–58

Fitzsimons, H.L., Riban, V., Bland, R.J., Wendelken, J.L., et al (2010) Biodistribution and safety assessment of AAV2-GAD following intrasubthalamic injection in the rat J. Gene Med., 12, 385–398

Garrido, M., Tereshchenko, Y., Zhevtsova, Z., Taschenberger, G., et al (2011) Glutathione depletion and overproduction both initiate degeneration of nigral dopaminergic neurons Acta Neuropathol., 121, 475–485

Gombash, S.E., Lipton, J.W., Collier, T.J., Madhavan, L., et al (2012) Striatal pleiotrophin overexpression provides functional and morphological neuroprotection in the 6-hydroxydopamine model Mol. Ther., 20, 544–554

Gordon, R., Neal, M.L., Luo, J., Langley, M.R., Harischandra, D.S., Panicker, N., Charli, A., Jin, H., Anantharam, V. et al (2016) Prokineticin-2 upregulation during neuronal injury mediates a compensatory protective response against dopaminergic neuronal degeneration Nat. Comm., 7: 12932

Hasegawa, K., Yasuda, T., Shiraishi, C., Fujiwara, K., Przedborski, S., Mochizuki, H. and Yoshikawa, K. (2016) Promotion of mitochondrial biogenesis by necdin protects neurons against mitochondrial insults Nat. Comm., 7: 10943

Humbert-Claude, M., Duc, D., Dwir, D., Thieren, L., Sandstrom von Tobel, J., Begka, C., Legueux, F., Velin, D., Maillard, M.H., Do, K.Q., Monnet-Tschudi, F. and Tenenbaum, L. (2016) Tollip, an early regulator of the acute inflammatory response in the substantia nigra J. Neuroinflamm., 13: 303

Janelidze, S., Nordström, U., Kügler, S. and Brundin, P. (2014) Pre-existing immunity to adeno-associated virus (AAV)2 limits transgene expression following intracerebral AAV2-based gene delivery in a 6-hydroxydopamine model of Parkinson’s disease J. Gene Med., 16, 300–308

Jung, A.E., Fitzsimons, H.L., Bland, R.J., During, M.J. and Young, D. (2008) HSP70 and constitutively active HSF1 mediate protection against CDCrel-1-mediated toxicity Mol. Ther., 16, 1048-1055

Kang, S.S., Zhang, Z., Liu, X., Manfredsson, F.P., He, L., Iuvone, P.N., Cao, X., Sun, Y.E., Jin, L. and Ye, K. (2017) α-Synuclein binds and sequesters PIKE-L into Lewy bodies, triggering dopaminergic cell death via AMPK hyperactivation Proc. Natl. Acad. Sci. Usa, 114, 1183–1188

Khodr, C.E., Sapru, M.K., Pedapati, J., Han, Y., et al (2011) An alpha-synuclein AAV gene silencing vector ameliorates a behavioral deficit in a rat model of Parkinson’s disease, but displays toxicity in dopamine neurons Brain Res., 1395, 94-107

Khodr, C.E., Pedapati, J., Han, Y. and Bohn, M.C. (2012) Inclusion of a portion of the native SNCA 30UTR reduces toxicity of human S129A SNCA on striatal-projecting dopamine neurons in rat substantia nigra Develop. Neurobiol., 72, 906–917

Klein, R.L., King, M.A., Hamby, M.E. and Meyer, E.M. (2002) Dopaminergic cell loss induced by human A30P -synuclein gene transfer to the rat substantia nigra Hum. Gene Ther., 13, 605-612

Klein, R.L., Dayton, R.D., Henderson, K.M. and Petrucelli, L. (2006) Parkin is protective for substantia nigra dopamine neurons in a tau gene transfer neurodegeneration model Neurosci. Lett., 401, 130-135

Koprich, J.B., Johnston, T.H., Reyes, M.G., Sun, X. and Brotchie, J.M. (2010) Expression of human A53T alpha-synuclein in the rat substantia nigra using a novel AAV1/2 vector produces a rapidly evolving pathology with protein aggregation, dystrophic neurite architecture and nigrostriatal degeneration with potential to model the pathology of Parkinson’s disease Mol. Neurodegener., 5 :43

Korecka, J.A., Moloney, E.B., Eggers, R., Hobo, B., Scheffer, S., Ras-Verloop, N., Pasterkamp, R.J., Swaab, D.F., Smit, A.B. et al (2017) Repulsive guidance molecule a (RGMa) induces neuropathological and behavioral changes that closely resemble Parkinson’s disease J. Neurosci., 37, 9361–9379

Krumova, P., Meulmeester, E., Garrido, M., Tirard, M., et al (2011) Sumoylation inhibits -synuclein aggregation and toxicity J. Cell Biol., 194, 49–60

Landeck, N., Hall, H., Ardah, M.T., Majbour, N.K., El-Agnaf, O.M.A., Halliday, G. and Kirik, D. (2016) A novel multiplex assay for simultaneous quantification of total and S129 phosphorylated human alpha-synuclein Mol. Neurodegen., 11: 61

Landeck, N., Buck, K. and Kirik, D. (2017) Toxic effects of human and rodent variants of alpha-synuclein in vivo Eur. J. Neurosci., 45, 536–547

Leriche, L., Björklund, T., Breysse, N., Besret, L., et al (2009) Positron emission tomography imaging demonstrates correlation between behavioral recovery and correction of dopamine neurotransmission after gene therapy J. Neurosci., 29, 1544 –1553

Lee, B., Lee, H., Nam, Y.R., Oh, J.H., et al (2005) Enhanced expression of glutamate decarboxylase 65 improves symptoms of rat parkinsonian models Gene Ther.,12, 1215-1222

McFarland, N.R., Fan, Z., Xu, K., Schwarzschild, M.A., et al (2009) -Synuclein S129 phosphorylation mutants do not alter nigrostriatal toxicity in a rat model of Parkinson disease J. Neuropathol. Exp. Neurol., 68, 515-524

Machado de Oliveira, R., Miranda, H.V., Francelle, L., Pinho, R., Szegö, E.M., Martinho, R., Munari, F., Lázaro, D.F., Moniot, S. et al (2017) The mechanism of sirtuin 2-mediated exacerbation of alpha-synuclein toxicity in models of Parkinson disease PLoS Biol., 15: e2000374

Manfredsson, F.P., Burger, C., Sullivan, L.F., Muzyczka, N., et al (2007) rAAV-mediated nigral human parkin over-expression partially ameliorates motor deficits via enhanced dopamine neurotransmission in a rat model of Parkinson’s disease Exp. Neurol., 207, 289-301

Manfredsson, F.P., Tumer, N., Erdos, B., Landa, T., et al (2009) Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity Mol. Ther., 17, 980-991

Manfredsson, F.P., Luk, K.C., Benskey, M.J., Gezer, A., Garcia, J., Kuhn, N.C., Sandoval, I.M., Patterson, J.R. et al (2018) Induction of alpha-synuclein pathology in the enteric nervous system of the rat and non-human primate results in gastrointestinal dysmotility and transient CNS pathology Neurobiol. Dis., 112, 106–118

Mendez-Gomez, H.R., Singh, J., Meyers, C., Chen, W., Gorbatyuk, O.S. and Muzyczka, N. (2018) The lipase activity of phospholipase D2 is responsible for nigral neurodegeneration in a rat model of Parkinson’s disease Neuroscience, 377, 174–183

Novell, S., Arcuri, L., Dovero, S., Dutheil, N., Shimshek, D.R., Bezard, E. and Morari, M. (2018) G2019S LRRK2 mutation facilitates α-synuclein neuropathology in aged mice Neurobiol. Dis., 120, 21–33

Saal, K.A., Koch, J.C., Tatenhorst, L., Szegő, E.M., Toledo Ribas, V., Michel, U., Bähr, M., Tönges, L. and Lingor, P. (2015) AAV.shRNA-mediated downregulation of ROCK2 attenuates degeneration of dopaminergic neurons in toxin-induced models of Parkinson’s disease in vitro and in vivo Neurobiol. Dis., 73, 150–162

Sanchez-Guajardo, V., Febbraro, F., Kirik, D. and Romero-Ramos, M. (2010) Microglia acquire distinct activation profiles depending on the degree of -synuclein neuropathology in a rAAV based model of Parkinson’s disease PLoS One, 5: e8784

Sato, H., Arawaka, S., Hara, S., Fukushima, S., et al (2011) Authentically phosphorylated -synuclein at Ser129 accelerates neurodegeneration in a rat model of familial Parkinson’s disease J. Neurosci., 31, 16884 –16894

Tereshchenko, J., Maddalena, A., Bähr, M. and Kügler, S. (2014) Pharmacologically controlled, discontinuous GDNF gene therapy restores motor function in a rat model of Parkinson’s disease Neurobiol. Dis., 65, 35–42

Torra, A., Parent, A., Cuadros, T., Rodríguez-Galván, B., Ruiz-Bronchal, E., Ballabio, A., Bortolozzi, A., Vila, M. and Bové, J. (2018) Overexpression of TFEB drives a pleiotropic neurotrophic effect and prevents Parkinson’s disease-related neurodegeneration Mol. Ther., 26, 1552-1567

Tronci, E., Napolitano, F., Muñoz, A., Fidalgo, C., Rossi, F., Björklund, A., Usiello, A. and Carta, M. (2017) BDNF over-expression induces striatal serotonin fiber sprouting and increases the susceptibility to L-DOPA induced dyskinesia in 6-OHDAlesioned rats Exp. Neurol., 297, 73–81

Ulusoy, A., Bjorklund, T., Hermening, S. and Kirik, D. (2008) In vivo delivery for development of mammalian models for Parkinson’s disease Exp. Neurol., 209, 89-100

Ulusoy, A., Febbraro, F., Jensen, P.H., Kirik, D., et al (2010) Co-expression of C-terminal truncated alphasynuclein enhances full-length alpha-synuclein-induced pathology Eur. J. Neurosci., 32, 409–422

Ulusoy, A., Björklund, T., Buck, K. and Kirik, D. (2012) Dysregulated dopamine storage increases the vulnerability to α-synuclein in nigral neurons Neurobiol. Dis., 47, 367–377

Van der Perren, A., Toelen, J., Carlon, M., Van den Haute, C., et al (2011) Efficient and stable transduction of dopaminergic neurons in rat substantia nigra by rAAV 2/1, 2/2, 2/5, 2/6.2, 2/7, 2/8 and 2/9 Gene Ther., 18, 517–527

Van Rompuy, A-S., Lobbestael, E., Van der Perren, A., Van den Haute, C., et al (2014) Long-term overexpression of human wild-type and T240R mutant parkin in rat substantia nigra induces progressive dopaminergic neurodegeneration J. Neuropathol. Exp. Neurol., 73, 159-174

Volpicelli-Daley, L.A., Kirik, D., Stokya, L.E., Standaert, D.G. and Hartms A.S., J. Neurochem. (2016) How can rAAV--synuclein and the fibril -synuclein models advance our understanding of Parkinson’s disease? J. Neurochem., 139 (Suppl. 1), 131–155

Xue, Y-Q., Ma, B-F., Zhao, L-R., Tatom, J.B., et al (2010) AAV9-mediated erythropoietin gene delivery into the brain protects nigral dopaminergic neurons in a rat model of Parkinson’s disease Gene Ther., 17, 83–94

Yang, C., Yang, W-H., Chen, S-S., Ma, B-F., et al (2013) Pre-immunization with an intramuscular injection of AAV9-human erythropoietin vectors reduces the vector-mediated transduction following re-administration in rat bain PLoS One, 8: e63876

Yasuda, T., Nihira, T., Ren, Y-R., Cao, X-Q., et al (2009) Effects of UCH-L1 on -synuclein over-expression mouse model of Parkinson’s disease J. Neurochem., 108, 932–944

Yasuda, T., Hayakawa, H., Nihira, T., Ren, Y-R., et al (2011) Parkin-mediated protection of dopaminergic neurons in a chronic MPTP-minipump mouse model of Parkinson disease J. Neuropathol. Exp. Neurol., 70, 686-697

Zhang, Z., Kang, S.S., Liu, X., Ahn E.E., Zhang, Z., He, L., Iuvone, P.M., Duong, D.M., Seyfried, N.T. et al (2017) Asparagine endopeptidase cleaves α-synuclein and mediates pathologic activities in Parkinson’s disease Nat. Struct. Mol. Biol., 24, 632-642

Parvalbumin interneurons
Favuzzi, E., Marques-Smith, A., Deogracias, R., Winterflood, C.M., Sánchez-Aguilera, A., Mantoan, L., Maeso, P., Fernandes, C., Ewers, H. and Rico, B. (2017) Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein Brevican Neuron, 95, 639–655

Peripheral nervous system
Chan, K.Y., Jang, M.J., Yoo, B.B., Greenbaum, A., Ravi, N., Wu, W-L., Sánchez-Guardado, L. et al (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems Nat. Neurosci., 20, 1172-1179

Chu, Q., Moreland, R., Yew, N.S., Foley, J., et al (2008) Systemic insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy Mol. Ther., 16, 1400-1408

Pleticha, J., Jeng-Singh, C., Rezek, R., Zaibak, M. and Beutler, A.S. (2014) Intraneural convection enhanced delivery of AAVrh20 for targeting primary sensory neurons Mol. Cell. Neurosci., 60, 72–80

Yu, H., Fischer, G., Ferhatovic, L., Fan, F., et al (2013) Intraganglionic AAV6 Results in efficient and long-term gene transfer to peripheral sensory nervous system in adult rats PLoS One, 8: e61266

PET imaging
Yoon, S.Y., Gay-Antaki, C., Ponde, D.E., Poptani, H., et al (2014) Quantitative, noninvasive, in vivo longitudinal monitoring of gene expression in the brain by co-AAV transduction with a PET reporter gene Mol. Ther. Methods Clin. Dev., 1, 14016

Post-synaptic efficacy
Crawford, D.C., Ramirez, D.M.O., Trauterman, B., Monteggia, L.M. and Kavalali E.T. (2017) Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy Nat. Comm., 8: 14436

Potassium channels
Auffenberg, E., Jurik, A., Mattusch, C., Stoffel, R., Genewsky, A., Namendorf, C., Schmid, R.M. Rammes, G. et al (2016) Remote and reversible inhibition of neurons and circuits by small molecule induced potassium channel stabilization Sci. Rep., 6: 19293

Sakai, A., Saitow, F., Maruyama, M., Miyake, N., Miyake, K., Shimada, T., Okada, T. and Suzuki, H. (2017) MicroRNA cluster miR-17-92 regulates multiple functionally related voltage-gated potassium channels in chronic neuropathic pain Nat. Comm., 8: 16079

PreBötzinger nuclei
Tan, W., Pagliardini, S., Yang, P., Janczewski, W.A. and Feldman, J.L. (2011) Projections of preBötzinger complex neurons in adult rats J. Comp. Neurol., 518, 1862–1878

Precursor cells, expression in
Bockstael, O., Melas, C., Pythoud, C., Levivier, M., et al (2012) Rapid transgene expression in multiple precursor cell types of adult rat subventricular zone mediated by adeno-associated type 1 vectors Hum.Gene Ther., 23, 742–753

Pre-frontal cortex
Kang, H.J., Voleti, B., Hajszan, T., Rajkowska, G., et al (2012) Decreased expression of synapse-related genes and loss of synapses in major depressive disorder Nat. Med., 18, 1413-1419

Seshadri, S., Faust, T., Ishizuka, K., Delevich, K., Chung, Y., Kim, S-H., Cowles, M., Niwa, M. et al (2015) Interneuronal DISC1 regulates NRG1-ErbB4 signalling and excitatory–inhibitory synapse formation in the mature cortex Nat. Commun., 6: 10118

Presynaptic dysfunction
Zhou, L., McInnes, J., Wierda, K., Holt, M., Herrmann, A.G., Jackson, R.J., Wang, Y-C., Swerts, J., Beyens, J., Miskiewicz, K. et al (2017) Tau association with synaptic vesicles causes presynaptic dysfunction Nat. Comm., 8: 15295

Projection neurons
Gowanlock, D., Tervo, R., Hwang, B-Y., Viswanathan, S., Gaj, T., Lavzin, M., Ritola, K.D., Lindo, S., Michael, S. et al (2016) A designer AAV variant permits efficient retrograde access to projection neurons Neuron 92, 372–382

Purkinje neurons
Bosch, M.K., Nerbonne, J.M., Ornitz, D.M. (2014) Dual transgene expression in murine cerebellar Purkinje neurons by viral transduction in vivo. PloS One, 9: e104062

Bosch, M.K., Carrasquillo, Y., Ransdell, J.L., Kanakamedala, A., Ornitz, D.M. and Nerbonne, J.M. (2015)Intracellular FGF14 (iFGF14) is required for spontaneous and evoked firing in cerebellar Purkinje neurons and for motor coordination and balance J. Neurosci., 35, 6752– 6769

Boudreau, R.L., Martins, I. and Davidson, B.L. (2009) Artificial micro-RNAs as siRNA shuttles: improved safety as compared to shRNAs in vitro and in vivo Mol. Ther., 17, 169–175

Chen, K.A., Cruz. P.E., Lanuto, D.J., Flotte, T.R., et al (2011) Cellular fusion for gene delivery to SCA1 affected Purkinje neurons Mol. Cell. Neurosci., 47, 61–70

El-Shamayleh, Y., Kojima, Y., Soetedjo, R. and Horwitz, G.D. (2017) Selective optogenetic control of Purkinje cells in monkey cerebellum Neuron, 95, 51–62

Kim, J-Y., Ash, R.T., Ceballos-Diaz, C., Levites, Y., et al (2013) Viral transduction of the neonatal brain delivers controllable genetic mosaicism for visualising and manipulating neuronal circuits in vivo Eur. J. Neurosci., 37, 1203–1220

Konno, A., Shuvaev, A.N., Miyake, N., Miyake, K., et al (2014) Mutant ataxin-3 with an abnormally expanded polyglutamine chain disrupts dendritic development and metabotropic glutamate receptor signaling in mouse cerebellar Purkinje cells Cerebellum, 13, 29–41

Nitta, K., Matsuzaki, Y., Konno, A., and Hirai, H. (2017) Minimal Purkinje cell-specific PCP2/L7 promoter virally available for rodents and bon-human primates Mol. Ther. Meth. Clin. Dev., 6, 159-170

Sawada, Y., Konno, A., Nagaoka, J. and Hirai, H. (2016) Inflammation-induced reversible switch of the neuron-specific enolase promoter from Purkinje neurons to Bergmann glia Sci. Rep., 6: 27758

Retrograde delivery
ElMallah, M.K., Falk, D.J., Lane, M.A., Conlon, T.J., et al (2012) Retrograde gene delivery to hypoglossal motoneurons using adeno-associated virus serotype 9 Hum. Gene Ther. Methods, 23, 148–156

Retro-orbital injection
Allen, W.E., Kauvar, I.V., Chen, M.Z., Richman, E.B., Yang, S.J., Chan, K., Gradinaru, V., Deverman, B.E. Luo, L. and Deisseroth, K. (2017) Global representations of goal-directed behavior in distinct cell types of mouse neocortex Neuron, 94, 891–907

Rett syndrome
Gadalla, K.K.E., Bailey, M.E.S., Spike, R.C., Ross, P.D., et al (2013) Improved survival and reduced phenotypic severity following AAV9/MECP2 gene transfer to neonatal and juvenile male Mecp2 knockout mice Mol. Ther., 21, 18–30

Sinnett, S.E., Hector, R.D., Gadalla, K.K.E., Heindel, C., Chen, D., Zaric, V., Bailey, M.E.S., Cobb, S.R. and Gray, S.J. (2017) Improved MECP2 gene therapy extends the survival of MeCP2-null mice without apparent toxicity after intracisternal delivery Mol. Ther. Meth. Clin. Dev., 5, 106-115

Sciatic nerve/Schwann cells
Homs, J., Ariza, L., Pagès, G., Udina, E., et al (2011) Schwann cell targeting via intrasciatic injection of AAV8 as gene therapy strategy for peripheral nerve regeneration Gene Ther., 18, 622–630

Homs, J., Pagès, G., Ariza, L., Casas, C., et al (2014) Intrathecal administration of IGF-I by AAVrh10 improves sensory and motor deficits in a mouse model of diabetic neuropathy Mol. Ther. Methods Clin. Dev., 1: 7

Prabhakar, S., Taherian, M., Gianni, D., Conlon, T.J., et al (2013) Regression of schwannomas induced by adeno-associated virus-mediated delivery of caspase-1 Hum. Gene Ther., 24, 152–162

Sasaki, Y., Hackett, A.R., Kim, S., Strickland, A. and Milbrandt, J. (2018) Dysregulation of NAD+ metabolism induces a Schwann cell dedifferentiation program J. Neurosci., 38, 6546–6562

Unzu, C., Sampedro, A., Mauleón, I., Alegre, M., et al (2011) Sustained enzymatic correction by rAAVmediated liver gene therapy protects against induced motor neuropathy in acute porphyria mice Mol. Ther., 19, 243–250

Zhuang, G.Z., Keeler, B., Grant, J., Bianchi, L., Fu, E.S., Zhang, Y.P., Erasso, D.M., Cui, J-G., Wiltshire, T. et al (2015) Carbonic anhydrase-8 regulates inflammatory pain by inhibiting the ITPR1-cytosolic free calcium pathway PLoS One, 10: e0118273

Seizures
Ledri, M., Nikitidou, L., Erdelyi, F., Szabo, G., et al (2012) Altered profile of basket cell afferent synapses in hyper-excitable dentate gyrus revealed by optogenetic and two-pathway stimulations Eur. J. Neurosci., 36, 1971–1983

Serotonin
Aoki, M., Watanabe, Y., Yoshimoto, K., Tsujimura, A., Yamamoto, T., Kanamura, N. and Tanaka, M. (2016) Involvement of serotonin 2C receptor RNA editing in accumbal neuropeptide Y expression and behavioural despair Eur. J. Neurosci., 43, 1219–1228

Dölen, G., Darvishzadeh, A., Huang, K.W. and Malenka, R.C. (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin Nature, 501, 179-184

Suzuki, Y., Kiyokage, E., Sohn, J., Hioki, H. and Toida, K. (2015) Structural basis for serotonergic regulation of neural circuits in the mouse olfactory bulb J. Comp. Neurol., 523, 262–280

Somatosensory neurons
Mächler, P., Wyss, M.T., Elsayed, M., Stobart, J., Gutierrez, R., von Faber-Castell, A., Kaelin, V., Zuend, M., San Martín, A. et al (2016) In vivo evidence for a lactate gradient from astrocytes to neurons Cell Metabolism 23, 94–102

Vrontou, S., Wong, A.M., Rau, K.K., Koerber, R. and Anderson, D.J. (2013) Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo Nature, 493, 669-673

Spinal cord
Ahmed S.G., Waddington S.N., Boza-Morán M.G. and Yáñez-Muñoz R.J. (2018) High-efficiency transduction of spinal cord motor neurons by intrauterine delivery of integration-deficient lentiviral vectors J. Control. Rel. 273, 99–107

Benkhelifa-Ziyyat, S., Besse, A., Roda, M., Duque, S., et al (2013) Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice Mol. Ther., 21, 282–290

Burger, C., Gorbatyuk, O.S., Velardo, M.J., Peden, C.S., et al (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2 and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system Mol. Ther., 10, 302-317

Challagundla, M., Koch, J.C., Ribas, V.T., Michel, U., Kugler, S., Ostendorf, T., Bradke, F., Muller, H.W., Bahr, M. and Lingor, P. (2015) AAV-mediated expression of BAG1 and ROCK2shRNA promote neuronal survival and axonal sprouting in a rat model of rubrospinal tract injury J. Neurochem., 134, 261-275

Cheah, M., Andrews, M.R., Chew, D.J., Moloney, E.B., Verhaagen, J., Fässler, R. and Fawcett, J.W. (2016) Expression of an activated integrin promotes long-distance sensory axon regeneration in the spinal cord J. Neurosci., 36, 7283–7297

Chen, J., Lee, H.J., Jakovcevski, I., Shah, R., et al (2010) The extracellular matrix glycoprotein tenascin-C is beneficial for spinal cord regeneration Mol. Ther., 18, 1769–1777

Dirren, E., Towne, C.L., Setola, V., Redmond Jr. D.E., et al (2014) Intra-cerebroventricular injection of adeno-associated virus 6 and 9 vectors for cell type–specific transgene expression in the spinal cord Hum. Gene Ther., 25, 109–120

Dirren, E., Aebischer, J., Rochat, C., Towne, C., Schneider, B.L. and Aebischer, P. (2015) SOD1 silencing in motoneurons or glia rescues neuromuscular function in ALS mice Ann. Clin. Transl. Neurol., 2, 167–184

Dominguez, E., Marais, T., Chatauret, N., Benkhelifa-Ziyyat, S., et al (2011) Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice Hum. Mol. Genet., 20, 681–693

Eaton, M.J., Blits, B., Ruitenberg, M.J., Verhaagen, J. and Oudega, M. (2002) Amelioration of chronic neuropathic pain after partial nerve injury by adeno-associated viral (AVV) vector-mediated over-expression of BDNF in the rat spinal cord Gene Ther., 9, 1387-1395

Ehlert, E.M., Eggers, R., Niclou, S.P. and Verhaagen, J. (2010) Cellular toxicity following application of adeno associated viral vector-mediated RNA interference in the nervous system BMC Neurosci., 11:20

Enomoto, M., Hirai, T., Kaburagi, H. and Yokota, T. (2016) Efficient gene suppression in dorsal root ganglia and spinal cord using adeno-associated virus vectors encoding short-hairpin RNA In SiRNA Delivery Methods:

Methods and Protocols, Methods in Molecular Biology, vol. 1364 (eds. Shum, K. and Rossi, J.) Springer Science+Business Media New York, pp 277-290

Filézac de L’Etang, A., Maharjan, N., Braña, M.C., Ruegsegger, C., Rehmann, R., Goswami, A., Roos, A., Troost, D. et al (2015) Marinesco-Sjögren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS Nat. Neurosci., 18, 227-238

Foust, K.D., Poirier, A., Pacak, C.A., Mandel, R.J. and Flotte, T.R. (2008) Neonatal intraperitoneal or intravenous injections of recombinant adeno-associated virus type 8 transduce dorsal root ganglia and lower motor neurons Hum. Gene Ther., 19, 61-69

Foust, K.D., Flotte, T.R., Reier, P.J. and Mandel, R.J. (2008) Recombinant adeno-associated virus-mediated global anterograde delivery of glial cell line-derived neurotrophic factor to the spinal cord: comparison of rubrospinal and corticospinal tracts in the rat Hum. Gene Ther., 19, 71-81

Homs, J., Pagès, G., Ariza, L., Casas, C., et al (2014) Intrathecal administration of IGF-I by AAVrh10 improves sensory and motor deficits in a mouse model of diabetic neuropathy Mol. Ther. Methods Clin. Dev., 1: 7

Hinderer, C., Bell, P., Katz, N., Vite, C.H., Louboutin, J-P., Bote, E., Yu, H., Zhu, Y., Casal, M.L., Bagel, J. (2018) Evaluation of intrathecal routes of administration for adeno-associated viral vectors in large animals Hum. Gene Ther., 29, 15-24

Hutson, T.H., Verhaagen, J., Yáñez-Muñoz, R.J. and Moon, L.D.F. (2012) Corticospinal tract transduction: a comparison of seven adeno-associated viral vector serotypes and a non-integrating lentiviral vector Gene Ther., 19, 49–60

Ito, N., Sakai, A., Miyake, N., Maruyama, M., Iwasaki, H., Miyake, K., Okada, T., Sakamoto, A. and Suzuki, H. (2017) miR-15b Mediates oxaliplatin-induced chronic neuropathic pain through BACE1 downregulation Br. J. Pharmacol., 174, 386–395

Jara, J.H., Villa, S.R., Khan, N.A., Bohn, M.C. and Özdinler, P.H. (2012) AAV2 mediated retrograde transduction of corticospinal motor neurons reveals initial and selective apical dendrite degeneration in ALS Neurobiol. Dis., 47, 174–183

Leiva-Rodríguez, T., Romeo-Guitart, D., Marmolejo-Martínez-Artesero, S., Herrando-Grabulosa, M., Bosch, A., Forés, J. and Casas, C. (2018) ATG5 overexpression is neuroprotective and attenuates cytoskeletal and vesicle-trafficking alterations in axotomized motoneurons Cell Death Dis., 9: 626

Li, K., Nicaise, C., Sannie, D., Hala, T.J., Javed, E., Parker, J.L., Putatunda, R., Regan, K.A., Suain, V., Brion, J-P., Rhoderick, F., Wright, M.C., Poulsen, D.J. and Lepore, A.C. (2014) Overexpression of the astrocyte glutamate transporter GLT1 exacerbates phrenic motor neuron degeneration, diaphragm compromise, and forelimb motor dysfunction following cervical contusion spinal cord injury J. Neurosci., 34, 7622–7638

Li, K., Hala, T.J., Seetharam, S., Poulsen, D.J., Wright, M.C. and Lepore, A.C. (2015) GLT1 over-expression in SOD1G93A mouse cervical spinal cord does not preserve diaphragm function or extend disease Neurobiol. Dis., 78, 12–23

Mason, M.R.J., Ehlert, E.M.E., Eggers, R., Pool, C.W., et al (2010) Comparison of AAV serotypes for gene delivery to dorsal root ganglion neurons Mol. Ther., 18, 715–724

Miyake, N., Miyake, K., Yamamoto, M., Hirai, Y., et al (2011) Global gene transfer into the CNS across the BBB after neonatal systemic delivery of single-stranded AAV vectors Brain Res., 1389, 19-26

Qiu, K., Falk, D.J., Reier, P.R., Byrne, B.J. and Fuller, D.D. (2012) Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice Mol. Ther., 20, 21–27

Sakai, A., Saitow, F., Miyake, N., Miyake, K., et al (2013) miR-7a alleviates the maintenance of neuropathic pain through regulation of neuronal excitability Brain: 136, 2738–2750

Romeo-Guitart, R., Forés, J., Herrando-Grabulosa, M., Valls, R., Leiva-Rodríguez, T., Galea, E., GonzálezPérez, F., Navarro, X. et al (2018) Neuroprotective drug for nerve trauma revealed using artificial intelligence Sci. Rep., 8:1879

Ruitenberg, M.J., Plant, G.W., Christensen, C.L., Blits, B., et al (2002) Viral vector-mediated gene expression in olfactory ensheathing glia implants in the lesioned rat spinal cord Gene Ther., 9, 135-146

Ruitenberg, M.J., Eggers, R., Boer, G.J. and Verhaagen, J. (2002) Adeno-associated viral vectors as agents for gene delivery: application in disorders and trauma of the central nervous system Methods, 28, 182-194

Siu, J.J., Queen, N.J., Huang, W., Yin, F.Q., Liu. X., Wang, C., McTigue, D.M. and Cao, L. (2017) Improved gene delivery to adult mouse spinal cord through the use of engineered hybrid adeno-associated viral serotypes Gene Ther., 24, 361–369

Soderblom, C., Lee, D-H., Dawood, A., Carballosa, M., Santamaria, A.J., Benavides, F.D., Jergova, S.. Grumbles, R.M., Thomas, C.K. et al (2015) 3D Imaging of axons in transparent spinal cords from rodents and nonhuman primates e-Neuro, 2: 0001-15

Theis, T., Yoo, M., Park, C.S., Chen, J., Kügler, S., Gibbs, K.M. and Schachner, M. (2017) Lentiviral delivery of miR-133b improves functional recovery after spinal cord injury in mice Mol. Neurobiol., 54, 4659–4671

Towne, C., Schneider, B.L., Kieran, D., Redmond, D.E., et al (2010) Efficient transduction of non-human primate motor neurons after intramuscular delivery of recombinant AAV serotype 6 Gene Ther., 17, 141–146

Uchida, A., Sasaguri, H., Kimura, N., Tajiri, M., et al (2012) Non-human primate model of amyotrophiclateral sclerosis with cytoplasmic mislocalization of TDP-43 Brain, 135, 833–846

Urakami, A., Sakurai, A., Ishikawa, M., Yap, M.L., Flores-Garcia, Y., Haseda, Y., Aoshi, T., Zavala, F.P. et al (2017) Development of a novel virus-like particle vaccine platform that mimics the immature form of alphavirus Clin. Vacc. Immunol., 24: e00090-17

Villmann, C., Oertel, J., Ma-Högemeier, Z-L., Hollmann, M., et al (2009) Functional complementation of Glra1spd-ot, a glycine receptor subunit mutant, by independently expressed C-terminal domains J. Neurosci., 29, 2440 –2452

Yu, H., Fischer, G., Ferhatovic, L., Fan, F., et al (2013) Intraganglionic AAV6 Results in efficient and long-term gene transfer to peripheral sensory nervous system in adult rats PLoS One, 8: e61266

Spinal muscular atrophy
Odermatt, P., Trüb, J., Furrer, L., Fricker, R., Marti, A. and Schümperli, D. (2016) Somatic therapy of a mouse SMA model with a U7 snRNA gene correcting SMN2 splicing Mol. Ther., 1797–1805

Spinocerebellar ataxia
Huda, F., Fan, Y., Suzuki, M., Konno, A., Matsuzaki, Y., Takahashi, N., Chan, J.K.Y. and Hirai, H. (2016) Fusion of human fetal mesenchymal stem cells with degenerating cerebellar neurons in spinocerebellar ataxia Type 1 model mice PLoS One, 11: e0164202

Konno, A., Shuvaev, A.N., Miyake, N., Miyake, K., et al (2014) Mutant ataxin-3 with an abnormally expanded polyglutamine chain disrupts dendritic development and metabotropic glutamate receptor signaling in mouse cerebellar Purkinje cells Cerebellum, 13, 29–41

Splicing regulators
Traunmüller, L., Bornmann, C. and Scheiffele, P. (2014) Alternative splicing coupled nonsense-mediated decay generates neuronal cell type-specific expression of SLM proteins J. Neurosci., 34, 16755–16761

Stress responses
Bender, J., Engeholm, M., Ederer, M.S., Breu, J., Møller, T.C., Michalakis, S., Rasko, T. 5, Wanker, E.E. et al (2015) Corticotropin-releasing hormone receptor type 1 (CRHR1) clustering with MAGUKs is mediated via its C-terminal PDZ binding motif PLoS One, 10: e0136768

Strial terminalis (bed nucleus)
Sink, K.S., Chung, A., Ressler, K.J., Davis, M., et al (2013) Anxiogenic effects of CGRP within the BNST may be mediated by CRF acting at BNST CRFR1 receptors Behav. Brain Res., 243, 286– 293

Striatal delivery
Agustín-Pavón, C., Mielcarek, M., Marriga-Canut, M. and Isalan, M. (2016) Deimmunization for gene therapy: host matching of synthetic zinc finger constructs enables long-term mutant Huntingtin repression in mice Mol. Neurodegen., 11: 64

Ahn, J-H., McAvoy, T., Rakhilin, S.V., Nishi, A., et al (2007) Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56 subunit Proc. Natl. Acad. Sci. USA, 104, 2979-2984

Aldrin-Kirk, P., Davidsson, M., Holmqvist, S., Li, J-Y., et al (2014) Novel AAV based rat model of forebrain synucleinopathy shows extensive pathologies and progressive loss of cholinergic interneurons PLoS One, 9: e100869

Auffenberg, E., Jurik, A., Mattusch, C., Stoffel, R., Genewsky, A., Namendorf, C., Schmid, R.M. Rammes, G. et al (2016) Remote and reversible inhibition of neurons and circuits by small molecule induced potassium channel stabilization Sci. Rep., 6: 19293

Arcuri, L., Viaro, R., Bido, S., Longo, F., Calcagno, M., Fernagut, P-O., Zaveri, N.T., Calò, G., Bezard, E. and Morari, M. (2016) Genetic and pharmacological evidence that endogenous nociceptin/orphanin FQ contributes to dopamine cell loss in Parkinson’s disease Neurobiol. Dis., 89, 55–64

Barroso-Chinea, P., Cruz-Muros, I., Afonso-Oramas, D., Castro-Hernández, J., Salas-Hernández, J., Chtarto, A., Luis-Ravelo, D. et al (2016) Long-term controlled GDNF over-expression reduces dopamine transporter activity without affecting tyrosine hydroxylase expression in the rat mesostriatal system Neurobiol. Dis., 88, 44–54

Benavides, D.R., Quinn, J.J., Zhong, P., Hawasli, A.H., et al (2007) Cdk5 modulates cocaine reward, motivation and striatal neuron excitability J. Neurosci., 27, 12967-12976

Björklund, T., Carlsson, T., Cederfjäll, E.A., Carta, M. and Kirik, D. (2010) Optimized adeno-associated viral vector-mediated striatal DOPA delivery restores sensorimotor function and prevents dyskinesias in a model of advanced Parkinson’s disease Brain, 133, 496–511

Bockstael, O., Melas, C., Pythoud, C., Levivier, M., et al (2012) Rapid transgene expression in multiple precursor cell types of adult rat subventricular zone mediated by adeno-associated type 1 vectors Hum.Gene Ther., 23, 742–753

Carty, N., Berson, N., Tillack, K., Thiede, C., Scholz, D., Kottig, K., Sedaghat, Y., Gabrysiak, C. et al (2015) Characterization of HTT inclusion size, location, and timing in the zQ175 mouse model of Huntington´s disease: an in vivo high-content imaging study PLoS One, 10: e0123527

Cederfjäll, E., Sahin, G., Kirik, D. and Björklund, T. (2012) Design of a single AAV vector for co-expression of TH and GCH1 to establish continuous DOPA synthesis in a rat model of Parkinson’s disease Mol. Ther., 20, 1315–1326

Cederfjäll, E., Nilsson, N., Sahin, G., Chu, Y., et al (2013) Continuous DOPA synthesis from a single AAV: dosing and efficacy in models of Parkinson’s disease Sci. Rep., 3: 2157

Chtarto, A., Yang, X., Bockstael, O., Melas, C., et al (2007) Controlled delivery of glial cell line-derived neurotrophic factor by a single tetracycline-inducible AAV vector Exp. Neurol., 204, 387-399

Crommentuijn, M.H.W., Maguire, C.A., Niers, J.M., Vandertop, W.P., Badr, C.E., Wurdinger, T. and Tannous, B.A. (2016) Intracranial AAV-sTRAIL combined with lanatoside C prolongs survival in an orthotopic xenograft mouse model of invasive glioblastoma Mol. Oncol., 10, 625-634

Crook, Z.R. and Housman, D.E. (2012) Dysregulation of dopamine receptor D2 as a sensitive measure for Huntington disease pathology in model mice Proc. Natl. Acad. Sci. USA, 109, 7487–7492

Decressac, M., Ulusoy, A., Mattsson, B., Georgievska, B., et al (2011) GDNF fails to exert neuroprotection in a rat a-synuclein model of Parkinson’s disease Brain, 134, 2302–2311

Dodiya, H.B., Bjorklund, T., Stansell III, J., Mandel, R.J., et al (2010) Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates Mol. Ther., 18, 579–587

Drinkut, A., Tereshchenko, Y., Schulz, J.B., Bähr, M., et al (2012) Efficient gene therapy for Parkinson’s disease using astrocytes as hosts for localized neurotrophic factor delivery Mol. Ther., 20, 534–543

Gabery, S., Sajjad, M.U., Hult, S., Soylu, R., et al (2012) Characterization of a rat model of Huntington’s disease based on targeted expression of mutant huntingtin in the forebrain using adeno-associated viral vectors Eur. J. Neurosci., 36, 2789–2800

Gaj, T., Staahl, B.T., Rodrigues, G.M.C., Limsirichai, P., Ekman, F.K., Doudna, J.A. and Schaffer, D.V. (2017) Targeted gene knock-in by homology-directed genome editing using Cas9 ribonucleoprotein and AAV donor delivery Nucleic Acids Res., 45: e98

Garriga-Canut, M., Agustín-Pavón, C., Herrmann, F., Sánchez, A., et al (2012) Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice Proc. Natl. Acad. Sci. USA, E3136-E3145

Gombash, S.E., Lipton, J.W., Collier, T.J., Madhavan, L., et al (2012) Striatal pleiotrophin overexpression provides functional and morphological neuroprotection in the 6-hydroxydopamine model Mol. Ther., 20, 544–554

Gordon, R., Neal, M.L., Luo, J., Langley, M.R., Harischandra, D.S., Panicker, N., Charli, A., Jin, H., Anantharam, V. et al (2016) Prokineticin-2 upregulation during neuronal injury mediates a compensatory protective response against dopaminergic neuronal degeneration Nat. Comm., 7: 12932

Hicks, M.J., Chiuchiolo, M.J., Ballon, D., Dyke, J.P., Aronowitz, E., Funato, K., Tabar, V., Havlicek, D. et al (2016) Anti-epidermal growth factor receptor gene therapy for glioblastoma PLoS One, 10: 1371

Kornum, B.R., Stott, S.R.W., Mattsson, B., Wisman, L., et al (2010) Adeno-associated viral vector serotypes 1 and 5 targeted to the neonatal rat and pig striatum induce widespread transgene expression in the forebrain Exp. Neurol., 222, 70–85

Landeck, N., Hall, H., Ardah, M.T., Majbour, N.K., El-Agnaf, O.M.A., Halliday, G. and Kirik, D. (2016) A novel multiplex assay for simultaneous quantification of total and S129 phosphorylated human alpha-synuclein Mol. Neurodegen., 11: 61

Lehtonen, E., Bonnaud, F., Melas, C., Lubansu, A., et al (2002) AAV2 vectors mediate efficient and sustained transduction of rat embryonic ventral mesencephalon Neuroreport, 13, 1503-1507

Leriche, L., Björklund, T., Breysse, N., Besret, L., et al (2009) Positron emission tomography imaging demonstrates correlation between behavioral recovery and correction of dopamine neurotransmission after gene therapy J. Neurosci., 29, 1544 –1553

Liu, M., Blanco-Centurion, C., Konadhode, R., Begum, S., et al (2011) Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice J. Neurosci., 31, 6028–6040

Maddalena, A., Tereshchenko, J., Bähr, M. and Kügler, S. (2013) Adeno-associated virus-mediated, vifepristone-regulated transgene expression in the brain Mol. Ther. Nucleic Acids 2: e106

Mahgoub, M., Adachi, M., Suzuki, K., Liu, X., Kavalali, E.T., Chahrour, M.H. and Monteggia, L.M. (2016) MeCP2 and histone deacetylases 1 and 2 in dorsal striatum collectively suppress repetitive behaviors Nat. Neurosci., 19, 1506-1512

Mandel, R.J., Marmikon, D.J., Kirik, D., Chu, Y., Heindel, C., McCown, T., Gray, S.J. and Kordower, J. H. (2017) Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodemts and nonhuman primates Acta Neuropath. Comm., 5: 47

Marshall, J.D., Li, J.Z., Zhang, Y., Gong, Y., St-Pierre, F., Lin, M.Z. and Schnitzer, M.J. (2016) Cell-typespecific optical recording of membrane voltage dynamics in freely moving mice Cell, 167, 1650–1662

Marsic, D., Méndez-Gómez, H.R. and Zolotukhin, S. (2015) High-accuracy biodistribution analysis of adenoassociated virus variants by double barcode sequencing Mol. Ther. Methods Clin. Dev., 2:15041

Matalon, R., Surendran S., Rady, P.L., Quast, M.J., et al (2008) Targeting Dyrk1A with AAVshRNA attenuates motor alterations in TgDyrk1A, a mouse model of Down syndrome Am. J. Hum. Genet., 83, 479-488

Mudannayake, J.M., Mouravlev, A., Fong, D.M. and Young, D. (2016) Transcriptional activity of novel ALDH1L1 promoters in the rat brain following AAV vector-mediated gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16075

Peden, C.S., Ezell, E.L., Muzyczka, N. and Mandel, R.J. (2003) Adeno-asociated virus-mediated aspartoacylase gene transfer to the brain of knockout mouse for canavan disease Mol. Ther., 7, 580-587

Peden, C.S., Manfredsson, F.P., Reimsnider, S.K., Poirier, A.E., et al (2009) Striatal readministration of rAAV vectors reveals an immune response against AAV2 capsids that can be circumvented Mol. Ther., 17, 524–537

Piguet, F., Sondhi, D., Piraud, M., Fouquet, F., et al (2012) Correction of brain oligodendrocytes by AAVrh.10 intracerebral gene therapy in metachromatic leukodystrophy mice Hum. Gene Ther., 23, 903–914

Polinski, N.K., Manfredsson, F.P., Benskey, M.J., Fischer, D.L., Kemp, C.J., Steece-Collier, K., Sandova, I.M., Paumier, K.L. and Sortwell, C.E. (2016) Impact of age and vector construct on striatal and nigral transgene expression Mol. Ther. Meth. Clin. Devel., 3: 16082

Rothwell, P.E., Fuccillo, M.V., Maxeiner, S., Hayton, S.J., Gokce, O., Lim, B.K., Fowler, S.C., Malenka, R.C. and Südhof, T.C. (2014) Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors Cell 158, 198–212

Saal, K.A., Koch, J.C., Tatenhorst, L., Szegő, E.M., Toledo Ribas, V., Michel, U., Bähr, M., Tönges, L. and Lingor, P. (2015) AAV.shRNA-mediated downregulation of ROCK2 attenuates degeneration of dopaminergic neurons in toxin-induced models of Parkinson’s disease in vitro and in vivo Neurobiol. Dis., 73, 150–162

Sohn, J., Takahashi, M., Okamoto, S., Ishida, Y., Furuta, T. and Hioki, H. (2017) A single vector platform for high-level gene transduction of central neurons: adeno-associated virus vector equipped with the Tet-off system PLoS One, 12: e0169611

Sondhi, D., Johnson, L., Purpura, K., Monette, S., et al (2012) Long-term expression and safety of administration of AAVrh.10hCLN2 to the brain of rats and nonhuman primates for the treatment of late infantile neuronal ceroid lipofuscinosis Hum. Gene Ther. Methods, 23, 324–335

Sondhi, D., Scott, E.C., Chen, A., Hackett, N.R., et al (2014) Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adenoassociated virus serotype rh.10 vector expressing the human CLN3 gene Hum. Gene Ther., 25, 223–239

Tabeta, R., Moutin, E., Becker, J.A.J., Heintz, D., Fouillen, L., Flatter, E., Kręzel, E., Alunni, V., Koebel, P. et al (2016) Fragile X Mental Retardation Protein (FMRP) controls diacylglycerol kinase activity in neurons Proc. Natl. Acad. Sci. USA, 113, E3619–E3628

Tang, T-S., Guo, C., Wang, H., Chen, X. and Bezprozvanny, I. (2009) Neuroprotective effects of inositol 1,4,5- trisphosphate receptor C-terminal fragment in a Huntington’s disease mouse model J. Neurosci., 29, 1257–1266

Taschenberger, G., Tereshchenko, J. and Kügler, S. (2017) A microRNA124 target sequence restores astrocyte specificity of gfaABC1D-driven transgene expression in AAV-mediated gene transfer Mol. Ther. Nucl. Acids 8, 13-25

Tereshchenko, J., Maddalena, A., Bähr, M. and Kügler, S. (2014) Pharmacologically controlled, discontinuous GDNF gene therapy restores motor function in a rat model of Parkinson’s disease Neurobiol. Dis., 65, 35–42

Tronci, E., Napolitano, F., Muñoz, A., Fidalgo, C., Rossi, F., Björklund, A., Usiello, A. and Carta, M. (2017) BDNF over-expression induces striatal serotonin fiber sprouting and increases the susceptibility to L-DOPA induced dyskinesia in 6-OHDA lesioned rats Exp. Neurol., 297, 73–81

White, E., Bienemann, A., Sena-Esteves, M., Taylor, H., et al (2011) Evaluation and optimization of the administration of recombinant adeno-associated viral vectors (serotypes 2/1, 2/2, 2/rh8, 2/9, and 2/rh10) by convection-enhanced delivery to the striatum Hum. Gene Ther., 22, 237–251

Xiao, L., Bornmann, C., Hatstatt-Burklé, L. and Scheiffele, P. (2018) Regulation of striatal cells and goaldirected behavior by cerebellar outputs Nat. Comm., 9: 3133

Yang, C., Yang, W-H., Chen, S-S., Ma, B-F., et al (2013) Pre-immunization with an intramuscular injection of AAV9-human erythropoietin vectors reduces the vector-mediated transduction following re-administration in rat bain PLoS One, 8: e63876

Subarachnoid space
Condello, C., Yuan, P., Schain, A. and Grutzendler, J. (2015) Microglia constitute a barrier that prevents neurotoxic protofibrillar Ab42 hotspots around plaques Nat. Commun., 6: 6176

Submucosal neuron delivery
Buckinx, R., Van Remoortel, S., Gijsbers, R., Waddington, S.N. and Timmermans, J-P. (2016) Proof-ofconcept: neonatal intravenous injection of adenoassociated virus vectors results in successful transduction of myenteric and submucosal neurons in the mouse small and large intestine Neurogastroenterol. Motil., 28, 299–305

Suboccipital puncture/lumbar puncture
Hinderer, C., Bell, P., Vite, C.H., Louboutin, J-P., Grant, R., Bote, E., Yu, H., Pukenas, B., Hurst, R. and Wilson, J.M. (2014) Widespread gene transfer in the central nervous system of cynomolgus macaques following delivery of AAV9 into the cisterna magna Mol. Ther. Methods Clin. Dev., 1: 14051

Hinderer, C., Bell, P., Louboutin, J-P., Zhu, Y., Yu, H., Lin, G., Choa, R., Gurda, B.L. et al (2015) Neonatal systemic AAV induces tolerance to CNS gene therapy in MPS I dogs and nonhuman primates Mol. Ther., 23, 1298-1307

Substantia nigra delivery (see also “α-Synuclein expression”)
Angot, E., Steiner, J.A., Lema Tomé, C.M., Ekström, P., et al (2012) Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo PLoS One, 7: e39465

Arcuri, L., Viaro, R., Bido, S., Longo, F., Calcagno, M., Fernagut, P-O., Zaveri, N.T., Calò, G., Bezard, E. and Morari, M. (2016) Genetic and pharmacological evidence that endogenous nociceptin/orphanin FQ contributes to dopamine cell loss in Parkinson’s disease Neurobiol. Dis., 89, 55–64

Barkholt, P., Sanchez-Guajardo, V., Kirik, D. and Romero-Ramos, M. (2012) Long-term polarization of microglia upon -synuclein overexpression in nonhuman primates Neuroscience, 208, 85–96

Benskey, M.J., Manfredsson, F.P., Lookingland, K.J. and Goudreau, J. L. (2015) The role of parkin in the differential susceptibility of tuberoinfundibular and nigrostriatal dopamine neurons to acute toxicant exposure Neurotoxicology, 46, 1–11

Bourdenx, M., Dovero, S., Engeln, M., Bido, S., Bastide, M.F., Dutheil, N., Vollenweider, I., Baud, L. et al (2015) Lack of additive role of ageing in nigrostriatal neurodegeneration triggered by α-synuclein overexpression Acta Neuropathologica Comm., 3: 46

Brys, I., Bobela, W., Schneider, B.L., Aebischer, P. and Fuentes, R. (2017) Spinal cord stimulation improves forelimb use in an alpha-synuclein animal model of Parkinson’s Disease Int. J. Neurosci., 127, 28–36

Brys, I., Nunes, J. and Fuentes, R. (2017) Motor deficits and beta oscillations are dissociable in an alphasynuclein model of Parkinson’s disease Eur. J. Neurosci., 46, 1906–1917

Buck, K., Landeck, N., Ulusoy, A., Majbour, N.K., El-Agnaf, O.M.A. and Kirik, D. (2015) Ser129 phosphorylation of endogenous α-synuclein induced by overexpression of polo-like kinases 2 and 3 in nigral dopamine neurons is not detrimental to their survival and function Neurobiol. Dis., 78, 100–114

Burger, C., Gorbatyuk, O.S., Velardo, M.J., Peden, C.S., et al (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2 and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system Mol. Ther., 10, 302-317

Decressac, M., Ulusoy, A., Mattsson, B., Georgievska, B., et al (2011) GDNF fails to exert neuroprotection in a rat a-synuclein model of Parkinson’s disease Brain, 134, 2302–2311

Decressac, M., Mattsson, B., Lundblad, M., Weikop, P. and Björklund, A. (2012) Progressive neurodegenerative and behavioural changes induced by AAV-mediated overexpression of α-synuclein in midbrain dopamine neurons Neurobiol. Dis., 45, 939–953

Decressac, M., Mattsson, B. and Björklund, A. (2012) Comparison of the behavioural and histological characteristics of the 6-OHDA and α-synuclein rat models of Parkinson’s disease Exp. Neurol., 235, 306–315

Decressac, M., Mattssona, B., Weikop, P., Lundblad, M., et al (2013) FEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity Proc. Soc. Natl. Acad. Sci. USA, E1817–E1826

Dodiya, H.B., Bjorklund, T., Stansell III, J., Mandel, R.J., et al (2010) Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates Mol. Ther., 18, 579–587

Dong, Z., Ferger, B., Feldon, J. and Büeler, H. (2002) Overexpression of Parkinson’s disease-associated - SynucleinA53T by recombinant adeno-associated virus in mice does not increase the vulnerability of dopaminergic neurons to MPTP J. Neurobiol., 53, 1-10

Eslamboli, A., Romero-Ramos, M., Burger, C., Bjorklund, T., et al (2007) Long-term consequences of human alpha-synuclein overexpression in the primate ventral midbrain Brain, 130, 799-815

Furler, S., Paterna, J-C., Weibel, M. and Büeler, H. (2001) Recombinant AAV vectors containing the foot and mouth disease virus 2A sequence confer efficient bicistronic gene expression in cultured cells and rat substantia nigra neurons Gene Ther., 8, 864-873

Gorbatyuk, O.S., Li, S., Nash, K., Gorbatyuk, M., et al (2010) In vivo RNAi-mediated α-synuclein silencing induces nigrostriatal degeneration Mol. Ther., 18, 1450–1457

Gustafsson, E., Andsberg, G., Darsalia, V., Mohapel, P., et al (2003) Anterograde delivery of brain-derived neurotrophic factor to striatum via nigral transduction of recombinant adeno-associated virus increases neuronal death but promotes neurogenic response following stroke Eur. J. Neurosci., 17, 2667-2678

Humbert-Claude, M., Duc, D., Dwir, D., Thieren, L., Sandstrom von Tobel, J., Begka, C., Legueux, F. et al (2016) Tollip, an early regulator of the acute inflammatory response in the substantia nigra J. Neuroinflamm., 13: 303

Kang, S.S., Zhang, Z., Liu, X., Manfredsson, F.P., He, L., Iuvone, P.N., Cao, X., Sun, Y.E., Jin, L. and Ye, K. (2017) α-Synuclein binds and sequesters PIKE-L into Lewy bodies, triggering dopaminergic cell death via AMPK hyperactivation Proc. Natl. Acad. Sci. Usa, 114, 1183–1188

Khodr, C.E., Sapru, M.K., Pedapati, J., Han, Y., et al (2011) An alpha-synuclein AAV gene silencing vector ameliorates a behavioral deficit in a rat model of Parkinson’s disease, but displays toxicity in dopamine neurons Brain Res., 1395, 94-107

Khodr, C.E., Pedapati, J., Han, Y. and Bohn, M.C. (2012) Inclusion of a portion of the native SNCA 30UTR reduces toxicity of human S129A SNCA on striatal-projecting dopamine neurons in rat substantia nigra Develop. Neurobiol., 72, 906–917

Klein, R.L., King, M.A., Hamby, M.E. and Meyer, E.M. (2002) Dopaminergic cell loss induced by human A30P -synuclein gene transfer to the rat substantia nigra Hum. Gene Ther., 13, 605-612

Klein, R.L., Dayton, R.D., Lin, W-L. and Dickson, D.W. (2005) Tau gene transfer, but not alpha-synuclein, induces both progressive dopamine neuron degeneration and rotational behavior in the rat Neurobiol. Dis., 20, 64-73

Klein, R.L., Dayton, R.D., Terry, T.L., Vascoe, C., et al (2009) PET imaging in rats to discern temporal onset differences between 6-hydroxydopamine and tau gene vector neurodegeneration models Brain Res., 1259, 113-122

Klein, R.L., Dayton, R.D., Diaczynsky, C.G. and Wang, D.B. (2010) Pronounced microgliosis and neurodegeneration in aged rats after tau gene transfer Neurobiol. Aging, 31, 2091–2102

Koprich, J.B., Johnston, T.H., Reyes, M.G., Sun, X. and Brotchie, J.M. (2010) Expression of human A53T alpha-synuclein in the rat substantia nigra using a novel AAV1/2 vector produces a rapidly evolving pathology with protein aggregation, dystrophic neurite architecture and nigrostriatal degeneration with potential to model the pathology of Parkinson’s disease Mol. Neurodegener., 5 :43

Krumova, P., Meulmeester, E., Garrido, M., Tirard, M., et al (2011) Sumoylation inhibits -synuclein aggregation and toxicity J. Cell Biol., 194, 49–60

Landeck, N., Buck, K. and Kirik, D. (2017) Toxic effects of human and rodent variants of alpha-synuclein in vivo Eur. J. Neurosci., 45, 536–547

Lawlor, P.A., Bland, R.J., Mouravlev, A., Young, D. and During, M.J. (2009) Efficient gene delivery and selective transduction of glial cells in the mammalian brain by AAV serotypes isolated from nonhuman primates Mol. Ther., 17, 1692-1702

Löw, K., Aebischer, P. and Schneider, B.L. (2013) Direct and retrograde transduction of nigral neurons with AAV6, 8, and 9 and intraneuronal persistence of viral particles Hum. Gene Ther., 24, 613–629

McFarland, N.R., Fan, Z., Xu, K., Schwarzschild, M.A., et al (2009) -Synuclein S129 phosphorylation mutants do not alter nigrostriatal toxicity in a rat model of Parkinson disease J. Neuropathol. Exp. Neurol., 68, 515-524

McFarland, N.R., Dimant, H., Kibuuka, L., Ebrahimi-Fakhari, D., et al (2014) Chronic treatment with novel small molecule Hsp90 inhibitors rescues striatal dopamine levels but not -synuclein-induced neuronal cell loss PLoS One, 9: e86048

Manfredsson, F.P., Burger, C., Sullivan, L.F., Muzyczka, N., et al (2007) rAAV-meidated nigral human parkin over-expression partially ameliorates motor deficits via enhanced dopamine neurotransmission in a rat model of Parkinson’s disease Exp. Neurol., 207, 289-301

Manfredsson, F.P., Tumer, N., Erdos, B., Landa, T., et al (2009) Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity Mol. Ther., 17, 980-991

Mendez-Gomez, H.R., Singh, J., Meyers, C., Chen, W., Gorbatyuk, O.S. and Muzyczka, N. (2018) The lipase activity of phospholipase D2 is responsible for nigral neurodegeneration in a rat model of Parkinson’s disease Neuroscience, 377, 174–183

Mudannayake, J.M., Mouravlev, A., Fong, D.M. and Young, D. (2016) Transcriptional activity of novel ALDH1L1 promoters in the rat brain following AAV vector-mediated gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16075

Nihira, T., Yasuda, T., Hirai, Y., Shimada, T., Mizuno, Y. and Mochizuki, H. (2011) Adeno-associated viral vector-mediated gene transduction in mesencephalic slice culture J. Neurosci. Methods, 201, 55– 60

Paterna, J-C., Feldon, J. and Büeler, H. (2004) Transduction profiles of recombinant adeno-associated virus vectors derived from serotypes 2 and 5 in the nigrostriatal system of rats J. Virol., 78, 6808-6817

Polinski, N.K., Manfredsson, F.P., Benskey, M.J., Fischer, D.L., Kemp, C.J., Steece-Collier, K., Sandova, I.M., Paumier, K.L. and Sortwell, C.E. (2016) Impact of age and vector construct on striatal and nigral transgene expression Mol. Ther. Meth. Clin. Devel., 3: 16082

Sanchez-Guajardo, V., Febbraro, F., Kirik, D. and Romero-Ramos, M. (2010) Microglia acquire distinct activation profiles depending on the degree of -synuclein neuropathology in a rAAV based model of Parkinson’s disease PLoS One, 5: e8784

Sato, H., Arawaka, S., Hara, S., Fukushima, S., et al (2011) Authentically phosphorylated -synuclein at Ser129 accelerates neurodegeneration in a rat model of familial Parkinson’s disease J. Neurosci., 31, 16884 –16894

Seo, B.B., Nakamaru-Ogiso, E., Cruz, P., Flotte, T.R., et al (2004) Functional expression of the single subunit NADH dehydrogenase in mitochondria in vivo: a potential therapy for complex I deficiencies Hum. Gene Ther., 15, 887-895

Seo, B.B., Nakamura-Ogiso, E., Flotte, T.R., Matsuno-Yagi, A. and Yagi, T. (2006) In vivo complementation of complex I by the yeast Ndi enzyme J. Biol. Chem.,281, 14250-14255

Tang, F-L., Erion, J.R., Tian, Y., Liu, W., Yin, D-M., Ye, J., Tang, B., Mei, L. and Xiong, W-C. (2015) VPS35 in dopamine neurons is required for endosome-to-Golgi retrieval of Lamp2a, a receptor of chaperone-mediated autophagy that is critical for -synuclein degradation and prevention of pathogenesis of Parkinson’s disease J. Neurosci., 35, 10613–10628

Tatom, J.B., Wang, D.B., Dayton, R.D., Skalli, O., et al (2009) Mimicking aspects of frontotemporal lobar degeneration and Lou Gehrig’s disease in rats via TDP-43 overexpression Mol. Ther., 17, 607–613

Ulusoy, A., Sahin, G. and Kirik, D. (2010) Presynaptic dopaminergic compartment determines the susceptibility to L-DOPA–induced dyskinesia in rats Proc. Natl. Acad. Sci. USA, 107, 13159–13164

Ulusoy, A., Febbraro, F., Jensen, P.H., Kirik, D., et al (2010) Co-expression of C-terminal truncated alphasynuclein enhances full-length alpha-synuclein-induced pathology Eur. J. Neurosci., 32, 409–422

Ulusoy, A., Björklund, T., Buck, K. and Kirik, D. (2012) Dysregulated dopamine storage increases the vulnerability to α-synuclein in nigral neurons Neurobiol. Dis., 47, 367–377

Van der Perren, A., Toelen, J., Carlon, M., Van den Haute, C., et al (2011) Efficient and stable transduction of dopaminergic neurons in rat substantia nigra by rAAV 2/1, 2/2, 2/5, 2/6.2, 2/7, 2/8 and 2/9 Gene Ther., 18, 517–527

Van Rompuy, A-S., Lobbestael, E., Van der Perren, A., Van den Haute, C., et al (2014) Long-term overexpression of human wild-type and T240R mutant parkin in rat substantia nigra induces progressive dopaminergic neurodegeneration J. Neuropathol. Exp. Neurol., 73, 159-174

Van Rompuy, A-S., Oliveras-Salvá, M., Van der Perren, A., Corti, O., Van den Haute, C. and Baekelandt, V. (2015) Nigral overexpression of alpha-synuclein in the absence of parkin enhances alpha-synuclein phosphorylation but does not modulate dopaminergic neurodegeneration Mol. Neurodegen., 10, 23

Wang, D.B., Dayton, R.D., Zweig, R.M. and Klein, R.L. (2010) Transcriptome analysis of a tau overexpression model in rats implicates an early pro-inflammatory response Exp. Neurol., 224, 197–206

Yasuda, T., Hayakawa, H., Nihira, T., Ren, Y-R., et al (2011) Parkin-mediated protection of dopaminergic neurons in a chronic MPTP-minipump mouse model of Parkinson disease J. Neuropathol. Exp. Neurol., 70, 686-697

Subthalamic nucleus
Fischer, D.L., Manfredsson, F.P., Kemp, C.J., Cole-Strauss, A., Lipton, J.W., Duffy, M.F., Polinski, N.K., Steece-Collier, K. et al (2017) Subthalamic nucleus deep brain stimulation does not modify the functional deficits or axonopathy induced by nigrostriatal α-synuclein overexpression Sci. Rep., 7: 16356

Fitzsimons, H.L., Riban, V., Bland, R.J., Wendelken, J.L., et al (2010) Biodistribution and safety assessment of AAV2-GAD following intrasubthalamic injection in the rat J. Gene Med., 12, 385–398

Lee, B., Lee, H., Nam, Y.R., Oh, J.H., et al (2005) Enhanced expression of glutamate decarboxylase 65 improves symptoms of rat parkinsonian models Gene Ther.,12, 1215-1222

Suprachiasmic nucleus
Enokia, R., Ono, D., Hasan, M.T., Honma, S. and Honma, K-i., (2012) Single-cell resolution fluorescence imaging of circadian rhythms detected with a Nipkow spinning disk confocal system J. Neurosci. Methods, 207, 72– 79

Landgraf, D., Long, J.E., Proulx, C.D., Barandas, R., Malinow, R. and Welsh, D.K. (2016) Genetic disruption of circadian rhythms in the suprachiasmatic nucleus causes helplessness, behavioral despair, and anxiety-like behavior in mice Biol. Psych., 80, 827–835

Synaptic function/transmission
Elagabani, M.N., Brisevac, D., Kintscher, M., Pohle, J., Köhr, G., Schmitz, D. and Kornau, H-C. (2016) Subunit-selective N-methyl-D-aspartate (NMDA) receptor signaling through brefeldin A-resistant Arf guanine nucleotide exchange factors BRAG1 and BRAG2 during synapse maturation J. Biol. Chem., 291, 9105–9118

Gerstein, H., O’Riordan, K., Osting, S., Schwarz, M., Burger, C. (2012) Rescue of synaptic plasticity and spatial learning deficits in the hippocampus of Homer1 knockout mice by recombinant adeno-associated viral gene delivery of Homer1c Neurobiol. Learn. Mem., 97, 17–29

Hausrat, T.J., Muhia, M., Gerrow, K., Thomas, P., Hirdes, W., Tsukita, S., Heisler, F.F., Herich, L., Dubroqua, S. (2015) Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and shortterm memory Nat. Commun., 6: 6872

O’Riordan, K., Gerstein, H., Hullinger, R. and Burger, C. (2014) The role of Homer1c in metabotropic glutamate receptor-dependent long-term potentiation Hippocampus, 24, 1-6

Rost, B.R., Schneider, F., Grauel, M.K., Wozny, C., Bentz, C.G., Blessing, A., Rosenmund, T., Jentsch, T.J. et al (2015) Optogenetic acidification of synaptic vesicles and lysosomes Nat. Neurosci., 18, 1845-1852

Sim, S-E., Lim, C-S., Kim, J-I., Seo, D., Chun, H., Yu, N-K., Lee, J., Kang, S.J., Ko, H-G., Choi, J-H. et al (2016) The brain-enriched microRNA miR-9-3p regulates synaptic plasticity and memory J. Neurosci., 36, 8641– 8652

Valluy, J., Bicker, S., Aksoy-Aksel, A., Lackinger, M., Sumer, S., Fiore, R., Wüst, T., Seffer, D. et al (2015) A coding-independent function of an alternative Ube3a transcript during neuronal development Nat. Neurosci., 18, 666-673

Xu, W., Morishita, W., Buckmaster, P.S., Pang, Z.P., et al (2012) Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission Neuron, 73, 990-1001

Yu, N-K., Kim, H.F., Shim, J., Kim, S., Kim, D.W., Kwak, C., Sim, S-E., Choi, J-H., Ahn, S. et al (2016) A transducible nuclear/nucleolar protein, mLLP, regulates neuronal morphogenesis and synaptic transmission Sci. Rep., 6: 22892

Syndapin 1
Del Pino, I., Koch, D., Schemm, R., Qualmann, B., et al (2014) Proteomic analysis of glycine receptor ß Subunit (GlyRß)-interacting proteins – evidence for syndapin I regulating synaptic glycone receptors J. Biol. Chem., 289, 1396–11409

SynGAP1 signalling
Muhia, M., Willadt, S., Yee, B.K., Feldon, J., et al (2012) Molecular and behavioral changes associated with adult hippocampus-specific SynGAP1 knockout Learn. Mem., 19, 268-281

a-Synuclein expression (see also “Substantia nigra delivery”)
Aldrin-Kirk, P., Davidsson, M., Holmqvist, S., Li, J-Y. and Björklund, T. (2014) Novel AAV based rat model of forebrain synucleinopathy shows extensive pathologies and progressive loss of cholinergic interneurons PLoS One, 9: e100869

Arawaka, S., Fukushima, S., Sato, H., Sasaki, A., Koga, K., Koyama, S. and Kato, T. (2014) Zonisamide attenuates a-synuclein neurotoxicity by an aggregation-independent mechanism in a rat model of familial Parkinson’s disease PLoS One, 9: e89076

Danzer, K.M., Kranich, L.R., Ruf, W.P., Cagsal-Getkin, O., Winslow, A.R., Zhu, L., Vanderburg, C.R. and McLean, P.J. (2012) Exosomal cell-to-cell transmission of alpha synuclein oligomers Mol. Neurodegener., 7: 42

Delenclos, M., Faroqi, A.H., Yue, M., Kurti, A., Castanedes-Casey, M., Rousseau, L., Phillips, V., Dickson, D.W., Fryer, J.D. and McLean, P.J. (2017) Neonatal AAV delivery of alpha-synuclein induces pathology in the adult mouse brain Acta Neuropath. Comm., 5: 51

Febbraro, F., Sahin, G., Farran, A., Soares, S., et al (2013) Ser129D mutant alpha-synuclein induces earlier motor dysfunction while S129A results in distinctive pathology in a rat model of Parkinson’s disease Neurobiol. Dis., 56, 47–58

Febbraro, F., Andersen, K.J., Sanchez-Guajardo, V., Tentillier, A., et al (2013) Chronic intranasal
deferoxamine ameliorates motor defects and pathology in the α-synuclein rAAV Parkinson’s model Exp. Neurol., 247, 45–58

Fischer, D.L., Manfredsson, F.P., Kemp, C.J., Cole-Strauss, A., Lipton, J.W., Duffy, M.F., Polinski, N.K., Steece-Collier, K. et al (2017) Subthalamic nucleus deep brain stimulation does not modify the functional deficits or axonopathy induced by nigrostriatal α-synuclein overexpression Sci. Rep., 7: 16356

Hall, H., Jewett, M., Landeck, N., Nilsson, N., et al (2013) Characterization of cognitive deficits in rats overexpressing human alpha-synuclein in the ventral tegmental area and medial septum using recombinant adeno-associated viral vectors PLoS One 8: e64844

Klein, R.L., King, M.A., Hamby, M.E. and Meyer, E.M. (2002) Dopaminergic cell loss induced by human
A30P a-synuclein gene transfer to the rat substantia nigra Hum. Gene Ther., 13, 605-612
Koch, J.C., Bitow, F., Haack, J., d`Hedouville, Z., Zhang, J-N., Tönges, L., Michel, U. et al (2015) Alpha-Synuclein affects neurite morphology, autophagy, vesicle transport and axonal degeneration in CNS neurons Cell Death Dis., 6: e1811

Kunadt, M., Eckermann, K., Stuendl, A., Gong, J., Russo, B., Strauss, K., Rai, S., Kugler, S. et al (2015)

Extracellular vesicle sorting of α‑synuclein is regulated by sumoylation Acta Neuropathol., 129, 695-713

Manfredsson, F.P., Luk, K.C., Benskey, M.J., Gezer, A., Garcia, J., Kuhn, N.C., Sandoval, I.M., Patterson, J.R. et al (2018) Induction of alpha-synuclein pathology in the enteric nervous system of the rat and non-human primate results in gastrointestinal dysmotility and transient CNS pathology Neurobiol. Dis., 112, 106–118

Mandel, R.J., Marmikon, D.J., Kirik, D., Chu, Y., Heindel, C., McCown, T., Gray, S.J. and Kordower, J. H. (2017) Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodemts and nonhuman primates Acta Neuropath. Comm., 5: 47

Mendez-Gomez, H.R., Singh, J., Meyers, C., Chen, W., Gorbatyuk, O.S. and Muzyczka, N. (2018) The lipase activity of phospholipase D2 is responsible for nigral neurodegeneration in a rat model of Parkinson’s disease Neuroscience, 377, 174–183

Morabito, G., Giannelli, S.G., Ordazzo, G., Bido, S., Castoldi, V., Indrigo, M., Cabassi, T., Cattaneo, S. and Luoni, M. et al (2017) AAV-PHP.B-mediated global-scale expression in the mouse nervous system enables GBA1 gene therapy for wide protection from synucleinopathy Mol. Ther., 25, 2727-2742

Oksman, M., Wisman, L.A., Jiang, H., Miettinen, P.,.Kirik, D. and Tanila, H. (2013) Transduced wild-type but not P301S mutated human tau shows hyperphosphorylation in transgenic mice overexpressing A30P mutated human alpha-synuclein Neurodegenerative Dis., 12, 91–102

Ulusoy, A., Musgrove, R.E., Rusconi, R., Klinkenberg, M., Helwig, M., Schneider, A. and Di Monte, D.A. (2015) Neuron-to-neuron α-synuclein propagation in vivo is independent of neuronal injury Acta Neuropathol. Commun., 3: 13

Yasuda, T., Miyachi, S., Kitagawa, R., Wada, K., et al (2007) Neuronal specificity of α-synuclein toxicity and effect of Parkin co-expression in primates Neuroscience., 144, 743-753

Yasuda, T., Nihira, T., Ren, Y-R., Cao, X-Q., et al (2009) Effects of UCH-L1 on a-synuclein over-expression mouse model of Parkinson’s disease J. Neurochem., 108, 932–944

Tar DNA binding protein
Sasaguri, H., Chew, J., Xu, Y-F., Gendron, T.F., Garrett, A., Lee, C.W., Jansen-West, K., Bauer, P.O. et al (2016) The extreme N-terminus of TDP-43 mediates the cytoplasmic aggregation of TDP-43 and associated toxicity in vivo Brain Res., 1647, 57–64

Target area/tropism, serotype effect
Chakrabarty, P., Rosario, A., Cruz, P., Siemienski, Z., et al (2013) Capsid serotype and timing of injection determines AAV transduction in the neonatal mice brain PLoS One, 8: e67680

Holehonnur, R., Luong, J.A., Chaturvedi, D., Ho, A., Lella, S.K., Hosek, M.P. and Ploski, J.E. (2014) Adeno associated viral serotypes produce differing titers and differentially transduce neurons within the rat basal and lateral amygdala BMC Neurosci., 15: 28

Tau-related neurodegeneration
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S. and Ikezu, T. (2015) Depletion of microglia and inhibition of exosome synthesis halt tau propagation Nat. Neurosci., 18, 1584-1593

Cook, C., Kang, S.S., Carlomagno, Y., Lin, W-L., Yue, M., Kurti, A., Shinohara, M., Jansen-West, K., Perkerson, E. et al (2015) Tau deposition drives neuropathological, inflammatory and behavioral abnormalities independently of neuronal loss in a novel mouse model Hum. Mol. Genet., 24. 6198-6212

Klein, R.L., Lin, W-L., Dickson, D.W., Lewis, J., et al (2004) Rapid neurofibrillary tangle formation after localized gene transfer of mutated Tau Am. J. Pathol. 164, 347-353

Klein, R.L., Dayton, R.D., Diaczynsky, C.G. and Wang, D.B. (2010) Pronounced microgliosis and neurodegeneration in aged rats after tau gene transfer Neurobiol. Aging, 31, 2091–2102

Liu, X., Zeng, K., Li, M., Wang, Q., Liu, R., Zhang, B., Wang, J-Z., Shu, X. and Wang, X. (2017) Expression of P301L-hTau in mouse MEC induces hippocampus-dependent memory deficit Sci. Rep., 7: 3914

Ljungberg, M.C., Ali, Y.O., Zhu, J., Wu, C-S., et al (2012) CREB-activity and nmnat2 transcription are downregulated prior to neurodegeneration, while NMNAT2 over expression is neuroprotective, in a mouse model of human tauopathy Hum. Mol. Genet., 21, 251-267

Mustroph, M.L., King, M.A., Klein, R.L. and Ramirez, J.J. (2012) Adult-onset focal expression of mutated human tau in the hippocampus impairs spatial working memory of rats Behav. Brain Res., 233, 141-148

Oksman, M., Wisman, L.A., Jiang, H., Miettinen, P.,.et al (2013) Transduced wild-type but not P301S mutated human tau shows hyperphosphorylation in transgenic mice overexpressing A30P mutated human alphasynuclein Neurodegenerative Dis., 12, 91–102

Platt, T.L., Beckett, T.L., Kohleer, Niedowicz, K.D.M. and Murphy, M.P. (2016) Obesity, diabetes, and leptin resistance promote tau pathology in a mouse model of disease Neuroscience 315, 162–174

Ramirez, J.J., Poulton, W.E., Knelson, E., Barton, C., et al (2011) Focal expression of mutated tau in entorhinal cortex neurons of rats impairs spatial working memory Behav. Brain Res., 216, 332–340

Wang, P., Joberty, G., Buist, A., Vanoosthuyse, A., Stancu, I-C., Vasconcelos, P., Pierrot, N. et al (2017) Tau interactome mapping based idenitification of Otub1 as Tau deubiquitinase involved in accumulation of pathological Tau forms in vitro and in vivo Acta Neruopathol., 133, 731-749

Yang, S., Cacquevel, M., Saksida, L.M., Bussey, T.J., Schneider, B.L., Aebischer, P., Melani, R. et al (2015) Perineuronal net digestion with chondroitinase restores memory inmice with tau pathology Exp. Neurol., 265, 48–58

Thalamus/tectothalamic neurons
Auffenberg, E., Jurik, A., Mattusch, C., Stoffel, R., Genewsky, A., Namendorf, C., Schmid, R.M. Rammes, G. et al (2016) Remote and reversible inhibition of neurons and circuits by small molecule induced potassium channel stabilization Sci. Rep., 6: 19293

Gilkes, J.A., Bloom, M.D. and Heldermon, C.D. (2016) Preferred transduction with AAV8 and AAV9 via thalamic administration in the MPS IIIB model: A comparison of four rAAV serotypes Mol. Genet. Metab. Rep., 6, 48–54

Golebiowski, D., van der Bom, I.M.J., Kwon, C-S., Miller, A.D., Petrosky, K., Bradbury, A.M., Maitland, S., Kühn, A.L., Bishop, N. et al (2017) Direct intracranial injection of AAVrh8 encoding monkey β-Nacetylhexosaminidase causes neurotoxicity in the primate brain Hum. Gene Ther., 28, 510-522

Ito, T., Hioki, H., Sohn, J., Okamoto, S., Kaneko, T., Iino, S. and Oliver, D.L. (2015) Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons J. Comp. Neurol., 523, 2277–2296

Kwon, J-T., Nakajima, R., Kim, H-S., Jeong, Y., Augustine, G.J. and Han, J-H. (2014) Optogenetic activation of presynaptic inputs in lateral amygdala forms associative fear memory Learn. Mem., 21, 627-633

Neumann, P.A., Wang, Y., Yan, Y., Wang, Y., Ishikawa, M., Cui, R., Huang, Y.H. et al (2016) Cocaineinduced synaptic alterations in thalamus to nucleus accumbens projection Neuropsychopharmacology, 41, 2399–2410

Yoon, S.Y., Gay-Antaki, C., Ponde, D.E., Poptani, H., et al (2014) Quantitative, noninvasive, in vivo longitudinal monitoring of gene expression in the brain by co-AAV transduction with a PET reporter gene Mol. Ther. Methods Clin. Dev., 1, 14016

Transduction efficiency
Matsuzaki, Y., Konno, A., Mochizuki, R., Shinohara, Y., Nitta, K., Okada, Y. and Hirai, H. (2018) Intravenous administration of the adeno-associated virus-PHP.B capsid fails to upregulate transduction efficiency in the marmoset brain Neurosci. Lett., 665, 182–188

Mendoza, S.D., El-Shamayleh, Y. and Horwitz, G.D. (2017) AAV-mediated delivery of optogenetic constructs to the macaque brain triggers humoral immune responses J. Neurophysiol., 117, 2004–2013

Trigeminal ganglia delivery
Dang, C.H., Aubert, M., De Silva Feelixge, H.S., Diem, K., Loprieno, M.A., Roychoudhury, P., Stone, D. and Jerome, K.R. (2017) In vivo dynamics of AAV-mediated gene delivery to sensory neurons of the trigeminal ganglia Sci. Rep., 7: 927

Tuberous sclerosis complex
Prabhakar, S., Goto, J., Zuang, X., Sena-Esteves, M., et al (2013) Stochastic model of Tsc1 lesions in mouse brain PLoS One, 8: e64224
Prabhakar, S., Zhang, X., Goto, J., Han, S., Lai, C., Bronson, R., Sena-Esteves, M., Ramesh, V. et al (2015)

Survival benefit and phenotypic improvement by hamartin gene therapy in a tuberous sclerosis mouse brain model Neurobiol. Dis., 82, 22–31

Tumour necrosis factor
Klaus, F., Paterna, J-C., Marzorati, E., Sigrist, H., Götze, L., Schwendener, S., Bergamini, G., Jehli, E., Azzinnari, D. et al (2016) Differential effects of peripheral and brain tumor necrosis factor on inflammation, sickness, emotional behavior and memory in mice Brain Behav. Immun., 58, 310–326

Vagus nerve infusion
Ulusoy, A., Musgrove, R.E., Rusconi, R., Klinkenberg, M., Helwig, M., Schneider, A. and Di Monte, D.A. (2015) Neuron-to-neuron α-synuclein propagation in vivo is independent of neuronal injury Acta Neuropathol. Commun., 3: 13

Vector properties
Polinski, N.K., Manfredsson, F.P., Benskey, M.J., Fischer, D.L., Kemp, C.J., Steece-Collier, K., Sandova, I.M., Paumier, K.L. and Sortwell, C.E. (2016) Impact of age and vector construct on striatal and nigral transgene expression Mol. Ther. Meth. Clin. Devel., 3: 16082

Ventral mid-brain delivery
Eisch, A.J., Bolanos, C.A., de Wit, J., Simonak, R.D., Pudiak, C.M., Barrot, M., Verhagen, J. and Nestler, E.J. (2003) Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression Biol. Psychiatry, 54, 994-1005

Piguet, F., Sondhi, D., Piraud, M., Fouquet, F., et al (2012) Correction of brain oligodendrocytes by AAVrh.10 intracerebral gene therapy in metachromatic leukodystrophy mice Hum. Gene Ther., 23, 903–914

Tang, F-L., Liu, W., Hu, J-X., Erion, J.R., Ye, J., Mei, L. and Xiong, W-C. (2015) VPS35 deficiency or mutation causes dopaminergic neuronal loss by impairing mitochondrial fusion and function Cell Rep., 12, 1631–1643

Ventral pallidial neurons
Knowland, D., Lilascharoen, V., Pham Pacia, C., Shin, S., Wang, E.H-J. and Lim, B.K. (2017) Distinct ventral pallidal neural populations mediate separate symptoms of depression Cell, 170, 284-297

Ventral tegmental delivery
Grieder, T.E., Herman, M.A., Contet, C., Tan, L.A., Vargas-Perez, H., Cohen, A., Chwalek, M., Maal-Bared, G. et al (2014) VTA CRF neurons mediate the aversive effects of nicotine withdrawal and promote intake escalation Nat. Neurosci., 17, 1751-1758

Hall, H., Jewett, M., Landeck, N., Nilsson, N., et al (2013) Characterization of cognitive deficits in rats overexpressing human alpha-synuclein in the ventral tegmental area and medial septum using recombinant adeno-associated viral vectors PLoS One 8: e64844

Zona incerta
Liu, M., Blanco-Centurion, C., Konadhode, R., Begum, S., et al (2011) Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice J. Neurosci., 31, 6028–6040

Cholesterol metabolism (see also “Lipoprotein metabolism-related disorders”)

Jäger, J., Greiner, V., Strzoda, D., Seibert, O., et al (2014) Hepatic transforming growth factor-ß 1 stimulated clone-22 D1 controls systemic cholesterol metabolism Mol. Metab., 3, 155–166

Pasta, S., Akhile, O., Tabron, D., Ting, F., Shackleton, G. and Watson, G. (2015) Delivery of the 7- dehydrocholesterol reductase gene to the central nervous system using adeno-associated virus vector in a mouse model of Smith-Lemli-Opitz Syndrome Mol. Genet. Metab. Rep., 4, 92–98

Ying, L., Matabosch, X., Serra, M., Watson, B., et al (2014) Biochemical and physiological improvement in a mouse model of Smith–Lemli–Opitz syndrome (SLOS) following gene transfer with AAV vectors Mol. Genet. Metab. Rep., 1, 103–113

Coagulation factor VIII

Zolotukhin, I., Markusic, D.M., Palaschak, B., Hoffman, B.E., Srikanthan, M.A. and Herzog, R.W. (2016) Potential for cellular stress response to hepatic factor VIII expression from AAV vector Mol. Ther. Meth. Clin. Dev., 3: 16063

Cocaine

Geng, L., Gao, Y., Chen, X., Hou, S., et al (2013) Gene transfer of mutant mouse cholinesterase provides high lifetime expression and reduced cocaine responses with no evident toxicity PLoS One, 8: e67446

Murthy, V., Gao, Y., Geng, L., LeBrasseur, N., White, T. and Brimijoin, S. (2014) Preclinical studies on neurobehavioral and neuromuscular effects of cocaine hydrolase gene therapy in mice J. Mol. Neurosci., 53, 409–416

Murthy, V., Geng, L., Gao, Y., Zhang, B., Miller, J.D., Reyes, S. and Brimijoin, S. (2015) Reward and toxicity of cocaine metabolites generated by cocaine hydrolase Cell. Mol. Neurobiol., 35, 819–826

Murthy, V., Reyes, S., Geng, L., Gao, Y. and Brimijoin, S. (2016) Cocaine hydrolase gene transfer demonstrates cardiac safety and efficacy against cocaine-induced QT prolongation in mice J. Pharmacol. Exp. Ther., 356, 720–725

Rosenberg, J.B., Hicks, M.J., De, B.P., Pagovich, O., et al (2012) AAVrh.10-mediated expression of an anticocaine antibody mediates persistent passive immunization that suppresses cocaine-induced behavior Hum. Gene Ther., 23, 451–459

Cochlear delivery (see also “Inner ear delivery”)

Akil, O., Seal, R.P., Burke, K., Wang, C., et al (2012) Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy Neuron 75, 283–293

Chang, Q., Wang, J., Li, Q., Kim, Y., Zhou, B., Wang, Y., Li, H. and Lin, X. (2015) Virally mediated Kcnq1 gene replacement therapy in the immature scala media restores hearing in a mouse model of human Jervell and Lange-Nielsen deafness syndrome EMBO Mol. Med., 7, 1077–1086

Duarte, M.J., Kanumuri, V.V., Landegger, L.D., Tarabichi, O., Sinha, S., Meng, X., Hight, A.E., Kozin et al (2018) Ancestral adeno-associated virus vector delivery of opsins to spiral ganglion neurons: implications for optogenetic cochlear implants Mol. Ther. 26, 1931-1939

Schaechinger, T.J., Gorbunov, D., Halaszovich, C.R., Moser, T., et al (2011) A synthetic prestin reveals  protein domains and molecular operation of outer hair cell piezoelectricity EMBO J., 30, 2793–2804

Suzuki, J., Hashimoto, K., Xiao, R., Vandenberghe, L.H. and Liberman, M.C. (2017) Cochlear gene therapy with ancestral AAV in adult mice: complete transduction of inner hair cells without cochlear dysfunction Sci. Rep., 7: 45524

Yu, Q., Wang, Y., Chang, Q., Wang, J., et al (2014) Virally expressed connexin26 restores gap junction function in the cochlea of conditional Gjb2 knockout mice Gene Ther., 21, 71–80

Colitis (experimental)

Polyak, S., Mach, A., Porvasnik, S., Dixon, L., et al (2012) Identification of adeno-associated viral vectors suitable for intestinal gene delivery and modulation of experimental colitis Am. J. Physiol. Gastrointest. Liver Physiol., 302, G296–G308

Complement activated disorders

Leaderer, D., Cashman, S.M. and Kumar-Singh, R. (2015) Adeno-associated virus mediated delivery of an engineered protein that combines the complement inhibitory properties of CD46, CD55 and CD59 J. Gene Med., 17, 101-115

Congenital deafness

Akil, O., Seal, R.P., Burke, K., Wang, C., Alemi, A., During, M., Edwards, M.H. and Lustig, L.R. (2012) Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy Neuron 75, 283–293

Coxsackie virus/AdV receptor

Larochelle, N., Teng, Q., Gilbert, R., Deol, J.R., et al (2010) Modulation of coxsackie and adenovirus receptor expression for gene transfer to normal and dystrophic skeletal muscle J. Gene Med., 12, 266–275

Creatine kinase

Rodino-Klapac, L.R., Lee, J-S., Mulligan, R.C., Clark, K.R. and Mendell, J.R. (2008) Lack of toxicity of alpha-sarcoglycan overexpression supports clinical gene transfer trial in LGMD2D Neurology, 71, 240-247

CRISPR-Cas systems delivery

Bak, R.O. and Porteus, M.H. (2017) CRISPR-mediated integration of large gene cassettes using AAV donor
vectors Cell Rep., 20, 750–756

Gaj, T. and Schaffer, D.V. (2016) Adeno-associated virus–mediated delivery of CRISPR–Cas systems for genome engineering in mammalian cells Cold Spring Harb Protoc; doi:10.1101/pdb.prot086868 Gundry, M.C., Dever, D.P., Yudovich, D., Bauer, D.E., Haas, S., Wilkinson, A.C. and Singbrant, S. (2017) Technical considerations for the use of CRISPR/Cas9 in hematology research Exptl. Hematol., 54, 4-11

Gwiazda, K.S., Grier, A.E., Sahni, J., Burleigh, S.M., Martin, U., Yang, J.G., Popp, N.A., Krutein, M.C., Khan, I.F. et al (2016) High efficiency CRISPR/Cas9-mediated gene editing in primary human T-cells using mutant adenoviral E4orf6/E1b55k “helper” proteins Mol. Ther., 24, 1570–1580

Kim, E., Koo, T., Park, S.W., Kim, D., Kim, K., Cho, H-Y., Song, D.W., Lee, K.J., Jung, M.H. et al (2017) In vivo genome editing with a small Cas9 orthologue derived from Campylobacter jejuni Nat. Comm., 8: 14500

Yoon, Y., Wang, D., Tai, P.W.L., Riley, J., Gao, G. and Rivera-Pérez, J.A. (2018) Streamlined ex vivo and in vivo genome editing in mouse embryos using recombinant adeno-associated viruses Nat. Comm., 9: 412 Crystallographic studies

Mahon, B.P., Kurian, J.J., Lomelino, C.L., Smith, I.R., Socorro, L., Bennett, A., Hendon, A.M., Chipman, P., Savin, D.A., Agbandje-McKenna, M. and McKenna, R. (2016) Microbatch mixing: “Shaken not Stirred”, a method for macromolecular microcrystal production for serial crystallography Cryst. Growth Des., 16, 6214−6221

C-termical epitopes

Ashley, S.N., Somanathan, S., Hinderer, C., Arias, M., McMenamin, D., Draper, C. and Wilson, J.M. (2017) Alternative start sites downstream of non-sense mutations drive antigen presentation and tolerance induction to C-terminal epitopes J. Immunol., 198, 4581–4587

Cultured cell and tissue delivery

AAV variant delivery
Santiago-Ortiz, J., Ojala, D.S., Westesson, O., Weinstein, J.R., Wong, S.Y., Steinsapir, A., Kumar, S., Holmes, I and Schaffer, D.V. (2015) AAV ancestral reconstruction library enables selection of broadly infectious viral variants Gene Ther., 22, 934–946

Astrocytes
Gong, Y., Chen, S., Sonntag, C.F., Sumners, C., Klein, R.L., King, M.A., Hughes, J.A. and Meyer, E.M. (2004) Recombinant adeno-associated virus serotype 2 effectively transduces primary rat brain astrocytes and microglia Brain Res. Brain Res. Protoc., 14, 18-24

Cardiomyopathy/cardiomyocytes
Bénard, L., Oh, J.G., Cacheux, M., Lee, A., Nonnenmacher, M., Matasic, D.S., Kohlbrenner, E., Kho, C., Pavoine, C et al (2016) Cardiac Stim1 silencing impairs adaptive hypertrophy and promotes heart failure through inactivation of mTORC2/Akt signaling Circulation, 133, 1458-1471

Gedicke-Hornung, C., Behrens-Gawlik, V., Reischmann, S., Geertz, B., et al (2013) Rescue of cardiomyopathy through U7snRNA – mediated exon skipping in Mybpc3 – targeted knock – in mice EMBO Mol. Med., 5, 1060-1077

Gröbl, T., Hammer, E., Bien-Möller, S., Geisler, A., Pinkert, S., Röger, C., Poller, W., Kurreck, J., Völker, U., Vetter, R. and Fechner, H. (2014) A novel artificial microRNA expressing AAV vector for phospholamban silencing in cardiomyocytes improves Ca2+ uptake into the sarcoplasmic reticulum PLoS One, 9: e92188

Hertig, V., Matos-Nieves, A., Garg, V., Villeneuve, L., Mamarbachi, M., Caland, L. and Calderone, A. (2018) Nestin expression is dynamically regulated in cardiomyocytes during embryogenesis J. Cell Physiol., 233, 3218–3229

Jian, Z., Liang, B., Pan, X., Xu, G., Guo. S-S., Li, T., Zhou, T., Xiao, Y-B. and Li, A-L. (2016) CUEDC2 modulates cardiomyocyte oxidative capacity by regulating GPX1 stability EMBO Mol. Med., 8, 813-829

Karakikes, I., Stillitano, F., Nonnenmacher, M., Tzimas, C., Sanoudou, D., Termglinchan, V., Kong, C-W., Rushing, S. et al (2015) Correction of human phospholamban R14del mutation associated with cardiomyopathy using targeted nucleases and combination therapy Nat. Commun., 6: 6955

Mearini, G., Stimpel, D., Krämer, E., Geertz, B., et al (2013) Repair of Mybpc3 mRNA by 5′-trans-splicing in a mouse model of hypertrophic cardiomyopathy Mol. Ther. Nucleic Acids 2: e102

Karakikes, I., Stillitano, F., Nonnenmacher, M., Tzimas, C., Sanoudou, D., Termglinchan, V., Kong, C-W., Rushing, S. et al (2015) Correction of human phospholamban R14del mutation associated with cardiomyopathy using targeted nucleases and combination therapy Nat. Commun., 6: 6955

Prondzynski, M., Krämer, E., Laufer, S.D., Shibamiya, A., Pless, O., Flenner, F., Müller, O.J., Münch, J. et al (2017) Evaluation of MYBPC3 trans-splicing and gene replacement as therapeutic options in human iPSCderived cardiomyocytes Mol. Ther: Nucleic Acids, 7, 475-486

Rapti, K., Stillitano, F., Karakikes, I., Nonnenmacher, M., Weber, T., Hulot, J-S. and Hajjar, R.J. (2015) Effectiveness of gene delivery systems for pluripotent and differentiated cells Mol. Ther. Methods Clin, Dev., 2:14067

Rutschow, D., Bauer, R., Göhringer, C., Bekeredjian, R., Schinkel, S., Straub, V., Koenen, M., Weichenhan, D., Katus, H.A. and Müller, O.J. (2014) S151A -sarcoglycan mutation causes a mild phenotype of cardiomyopathy in mice Eur. J. Hum. Genet., 22, 119–125

Sun, F., Li, X., Duan, W-Q., Tian, W., Gao, M., Yang, J., Wu, X-Y., Huang, D. et al (2017) Transforming growth factor-β receptor III is a potential regulator of ichemia-induced cardiomyocyte apoptosis J. Am. Heart Assoc., 6: e005357

Trochet, D., Prudhon, B., Beuvin, M., Peccate, C., Lorain, S., Julien, L., Benkhelifa-Ziyyat, S., Rabai, A., Mamchaoui, K. et al (2018) Allele-specific silencing therapy for Dynamin 2-related dominant centronuclear myopathy EMBO Mol. Med., 10.15252/emmm.201707988

Chondrocytes
Goodrich, L.R., Phillips, J.N., McIlwraith, C.W., Foti, S.B., et al (2013) Optimization of scAAVIL-1ra in vitro and in vivo to deliver high levels of therapeutic protein for treatment of osteoarthritis Mol. Ther. Nucleic Acids, 2: e70

Corneal cells
Bosiack, A.P., Giuliano, E.A., Gupta, R. and Mohan, R.R. (2012) Canine corneal fibroblast and myofibroblast transduction with AAV5 Vet. Ophthalmol., 15, 291–298
COS cells

Najate, A., Fridlich, R., Millet-Pue, G., Clerin, E., Delalande, F., Jaillard, C., Blond, F., Perrocheau, L., Reichman, S. et al (2015) Rod-derived cone viability factor promotes cone survival by stimulating aerobic glycolysis Cell, 161, 817–832

Dendritic cells
Aslanidi, G.V., Rivers, A.E., Ortiz, L., Govindasamy, L., et al (2012) High-efficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors Vaccine, 30, 3908– 3917

Rogers, G.L., Shirley, J.L., Zolotukhin, I., Kumar, S.R.P., Sherman, A., Perrin, G.Q., Hoffman, B.E., Srivastava, A., Basner-Tschakarjan, E. et al (2017) Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD81 T cells Blood, 129, 3184-3195

Ussher, J.E. and Taylor, J.A. (2010) Optimized transduction of human monocyte-derived dendritic cells by recombinant adeno-associated virus serotype 6 Hum. Gene Ther., 21, 1675–1686

Embryonic stem cells (see “Stem cell delivery”)

Epithelial (polarized) cells
Sorcher, E.J., Harris, J., Alexander, M., Rottgers, A., Hardy, K., Ponnazhagen, S., Collawn, J.F., McClintock, J., Amsler, C.D., Webster, A., Maddry, J., Baker, B.J. and Hong, J.S. (2006) Activators of viral gene expression in polarized epithelial monolayers identified by rapid-throughput drug screening Gene Ther., 13, 781-788

Yan, Z., Lei-Butters, D.C.M., Liu, X., Zhang, L., Luo, M., Zak, R. and Engelhardt, J.F. (2006) Unique biologic properties of recombinant AAV1 transduction in polarized human airway epithelia J. Biol. Chem., 281, 29684-29692

White, A.F., Mazur, M., Sorscher, E.J., Zinn, K.R. and Ponnazhagan, S. (2008) Genetic modification of adenoassociated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells Hum. Gene Ther., 19, 1407–1414

Fibroblasts
Cataldi, M.P. and McCarty, D.M. (2010) Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes J. Virol., 84, 8673–8682

Glial/glioma/glioblastoma cells
Cataldi, M.P. and McCarty, D.M. (2010) Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes J. Virol., 84, 8673–8682

Gaj, T., Staahl, B.T., Rodrigues, G.M.C., Limsirichai, P., Ekman, F.K., Doudna, J.A. and Schaffer, D.V. (2017) Targeted gene knock-in by homology-directed genome editing using Cas9 ribonucleoprotein and AAV donor delivery Nucleic Acids Res., 45: e98

Maguire, C.A., Gianni, D., Meijer, D.H., Shaket, L.A., Wakimoto, H., Rabkin, S.D., Gao, G. and Sena-Esteves, M. (2010) Directed evolution of adeno-associated virus for glioma cell transduction J. Neurooncol., 96, 337–347

Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M.H.W., Ericsson, M., Mincheva-Nilsson, L., Baranov, V. et al (2012) Microvesicle-associated AAV vector as a novel gene delivery system Mol. Ther., 20, 960–971

Yao, K., Qiu, S., Wang, Y.V., Park, S.J.H., Mohns, E.J., Mehta, B., Liu, X., Chang, B., Zenisek, D. et al (2018) Restoration of vision after de novo genesis of rod photoreceptors in mammalian retinas Nature, 560, 484-488

Haematopoetic stem cells (see “Stem cell delivery”)

HEK cells
Benskey, M.J., Sandoval, I.M. and Manfredsson, F.P. (2016) Continuous collection of adeno-associated virus from producer cell medium significantly increases total viral yield Hum. Gene Ther. Meth., 27, 32-45

Gaj, T., Staahl, B.T., Rodrigues, G.M.C., Limsirichai, P., Ekman, F.K., Doudna, J.A. and Schaffer, D.V. (2017) Targeted gene knock-in by homology-directed genome editing using Cas9 ribonucleoprotein and AAV donor delivery Nucleic Acids Res., 45: e98

Gröbl, T., Hammer, E., Bien-Möller, S., Geisler, A., et al (2014) A novel artificial microRNA expressing AAV vector for phospholamban silencing in cardiomyocytes improves Ca2+ uptake into the sarcoplasmic reticulum PLoS One, 9: e92188

Ho, M.L., Judd, J., Kuypers, B.E., Yamagami, M., Wong, F.F. and Suh, J. (2014) Efficiency of proteaseactivatable virus nanonodes tuned through incorporation of wild type capsid subunits Cell. Mol. Bioeng., 7, 334–343

Jazwa, A., Tomczyk, M., Taha, H.M., Hytonen, E., et al (2013) Arteriogenic therapy based on simultaneous delivery of VEGF-A and FGF4 genes improves the recovery from acute limb ischemia Vasc. Cell, 5: 13

Ji, G., Zhang, W., Mahimainathan, L., Narasimhan, M., Kiritoshi, T., Fan, X., Wang, J., Green, T.A. and Neugebauer, V. (2017) 5-HT2C receptor knockdown in the amygdala inhibits neuropathic-pain-related plasticity and behaviors J. Neurosci., 37, 1378 –1393

Kodippili, K. and Duan, D, (2018) Expressing full-length dystrophin using adeno-associated virus In Gene Therapy in Neurological Disorders Elsevier Inc. pp 259-276

Li, B., Ma, W., Ling, C., Van Vliet, K., Huang, L-Y., Agbandje-McKenna, M., Srivastava, A. and Aslanidi, G.V. (2015) Site-directed mutagenesis of surface-exposed lysine residues leads to improved transduction by AAV2, but not AAV8, vectors in murine hepatocytes in vivo Hum. Gene Ther. Methods 26, 211-220

Ling, C., Wang, Y., Lu, Y., Wang, L., Jayandharan, G.R., Aslanidi, G.V., Li, B. et al (2015) Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo J. Virol., 89, 952-961

Neerincx, A., Jakobshagen, K., Utermöhlen, O., Büning, H., Steimle, V. and Kufer, T.A. (2014) The N-terminal domain of NLRC5 confers transcriptional activity for MHC class I and II gene expression J. Immunol., 193, 3090–3100

Nicolas, A., Jolinon, N., Alazard-Dany, N., Barateau, V., Epstein, A.L., Greco, A., Büning, H. and Salvetti, A. (2012) Factors influencing helper-independent adeno-associated virus replication Virology, 432, 1–9

Platt, T.L., Beckett, T.L., Kohleer, Niedowicz, K.D.M. and Murphy, M.P. (2016) Obesity, diabetes, and leptin resistance promote tau pathology in a mouse model of disease Neuroscience 315, 162–174

Schiller, L.T., Lemus-Diaz, N., Ferreira, R.R., Böker, K.O. and Gruber, J. (2018) Enhanced production of exosome-associated AAV by overexpression of the tetraspanin CD9 Mol. Ther. Meth. Clin. Dev., 9, 278-287

Schnödt, M., Schmeer, M., Kracher, B., Krüsemann, C., Escalona Espinosa, L., Grünert, A., Fuchsluger, T., Rischmüller, A., Schleef, M. and Büning, H. (2016) DNA minicircle technology improves purity of adenoassociated viral vector preparations Mol. Ther. Nucleic Acids, 5, e355

Truong, D-J.J., Kühner, K., Kühn, R., Werfel, S., Engelhardt, S., Wurst, W. and Ortiz, O. (2015) Development of an intein-mediated split–Cas9 system for gene therapy Nucleic Acids Res., 43, 6450–6458

Yu, H., Koilkonda, R.D., Chou, T-H., Porciatti, V., et al (2012) Gene delivery to mitochondria by targeting modified adenoassociated virus suppresses Leber’s hereditary optic neuropathy in a mouse model Proc. Natl. Acad. Sci. USA, 109, E1238–E1247

HeLa cells
Aydemir, F., Salganik, M., Resztak, J., Singh, J., Bennett, A., Agbandje-McKenna, M. and Muzyczka, N. (2016) Mutants at the 2-fold interface of adeno-associated virus type 2 (AAV2) structural proteins suggest a role in viral transcription for AAV capsids J. Virol. 90, 7196-7204

Franzoso, F.D., Seyffert, M., Vogel, R., Yakimovich, A., de Andrade Pereira, B., Meier, A.F., Sutter, S.O., Tobler, K. et al (2017) Cell cycle-dependent expression of adeno-associated virus 2 (AAV2) rep in coinfections with herpes simplex virus 1 (HSV-1) gives rise to a mosaic of cells replicating either AAV2 or HSV-1 J. Virol., 91: e00357-17

Hölscher, C., Sonntag, F., Henrich, K., Chen, Q., Beneke, J., Matula, P., Rohr, K.. Kaderali, L. et al (2015) The SUMOylation pathway restricts gene transduction by adeno-associated viruses PLoS Pathog., 11: e1005281

Li, B., Ma, W., Ling, C., Van Vliet, K., Huang, L-Y., Agbandje-McKenna, M., Srivastava, A. and Aslanidi, G.V. (2015) Site-directed mutagenesis of surface-exposed lysine residues leads to improved transduction by AAV2, but not AAV8, vectors in murine hepatocytes in vivo Hum. Gene Ther. Methods 26, 211-220

Nicolas, A., Jolinon, N., Alazard-Dany, N., Barateau, V., Epstein, A.L., Greco, A., Büning, H. and Salvetti, A. (2012) Factors influencing helper-independent adeno-associated virus replication Virology, 432, 1–9

Schnödt, M., Schmeer, M., Kracher, B., Krüsemann, C., Escalona Espinosa, L., Grünert, A., Fuchsluger, T., Rischmüller, A., Schleef, M. and Büning, H. (2016) DNA minicircle technology improves purity of adenoassociated viral vector preparations Mol. Ther. Nucleic Acids, 5, e355

Hepatocarcinoma cells/hepatocytes
Leaderer, D., Cashman, S.M. and Kumar-Singh, R. (2015) Adeno-associated virus mediated delivery of an engineered protein that combines the complement inhibitory properties of CD46, CD55 and CD59 J. Gene Med., 17, 101-115

Lee, D-H., Park, J.O., Kim, T-S., Kim, S-K., Kim, T-h., Kim, M-c., Park, G.S., Kim, J-H., Kuninaka, S., Olson, E.N. et al (2016) LATS-YAP/TAZ controls lineage specification by regulating TGFβ signaling and Hnf4a expression during liver development Nat. Comm., 7: 11961

Li, B., Ma, W., Ling, C., Van Vliet, K., Huang, L-Y., Agbandje-McKenna, M., Srivastava, A. and Aslanidi, G.V. (2015) Site-directed mutagenesis of surface-exposed lysine residues leads to improved transduction by AAV2, but not AAV8, vectors in murine hepatocytes in vivo Hum. Gene Ther. Methods 26, 211-220

Ling, C., Wang, Y., Lu, Y., Wang, L., Jayandharan, G.R., Aslanidi, G.V., Li, B. et al (2015) Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo J. Virol., 89, 952-961

Mockenhaupt, S., Grosse, S., Rupp, D., Bartenschlager, R., and Grimm, D. (2015) Alleviation of off-target effects from vector-encoded shRNAs via co-delivered RNA decoys Proc. Natl. Acad. Sci., 112, E4007-E4016

Mueller, S., Huard, J., Waldow, K., Huang, X., D’Alessandro, L.A., Bohl, S., Börner, K., Grimm, D., Klamt, S., Klingmüller, U. and Schilling, M. (2015) T160-phosphorylated CDK2 defines threshold for HGF-dependent proliferation in primary hepatocytes Mol. Syst. Biol., 11: 795

Vercauteren, K., Hoffman, B.E., Zolotukhin, I., Keeler, G.D., Xiao, J.W., Basner-Tschakarjan, E., High, K.A., Ertl, H.C.J. et al (2016) Superior in vivo transduction of human hepatocytes using engineered AAV3 capsid Mol. Ther., 24, 1042-1049

Human corneal endothelial cells
Gruenert, A.K., Czugala, M., Mueller, C., Schmeer, M., Schleef, M., Kruse, F.E. and Fuchsluger, T.A. (2016) Self-complementary adeno-associated virus vectors improve transduction efficiency of corneal endothelial cells PLoS One, 11: e0152589

Human fibroblasts
Franzoso, F.D., Seyffert, M., Vogel, R., Yakimovich, A., de Andrade Pereira, B., Meier, A.F., Sutter, S.O., Tobler, K. et al (2017) Cell cycle-dependent expression of adeno-associated virus 2 (AAV2) rep in coinfections with herpes simplex virus 1 (HSV-1) gives rise to a mosaic of cells replicating either AAV2 or HSV-1 J. Virol., 91: e00357-17

Lojewski, X., Staropoli, J.F., Biswas-Legrand, S., Simas, A.M., et al (2014) Human iPSC models of neuronal ceroid lipofuscinosis capture distinct effects of TPP1 and CLN3 mutations on the endocytic pathway Hum. Mol. Genet., 23, 2005–2022

Industrial scale culture
Chahal, P.S., Schulze, E., Tran, R., Montes, J. and Kamen, A.A. (2014) Production of adeno-associated virus (AAV) serotypes by transient transfection of HEK293 cell suspension cultures for gene delivery J. Virol. Methods, 196, 163– 173

Keratinocytes
Chamorro, C., Mencía, A., Almarza, D., Duarte, B., Büning, H., Sallach, J., Hausser, I., Del Río, M., Larcher, F. and Murillas, R. (2016) Gene editing for the efficient correction of a recurrent COL7A1 mutation in recessive dystrophic epidermolysis bullosa keratinocytes Mol. Ther. Nucleic Acids, 5: e307

Sallach, J., Di Pasquale, G., Larcher, F., Niehoff, N., et al (2014) Tropism-modified AAV vectors overcome barriers to successful cutaneous therapy Mol. Ther., 22, 929–939

Lung fibroblasts
Hüser, D., Gogol-Döring, A., Chen, W. and Heilbronn, R. (2014) Adeno-associated virus type 2 wild-type and vector-mediated genomic integration profiles of human diploid fibroblasts analyzed by third-generation PacBio DNA sequencing J. Virol., 88, 11253–11263

Melanocytes
Sheppard, H.M., Ussher, J.E., Verdon, D., Chen, J., et al (2013) Recombinant adeno-associated virus serotype 6 efficiently transduces primary human melanocytes PLoS One, 8: e62753

33-20. Neurons (see also “33-26”)
Ahn, J-H., Sung, J.Y., McAvoy, T., Nishi, A., Janssens, V., Goris, J., Greengard, P. and Nairn, A.C. (2007) The B’’/PR72 subunit mediates Ca2+-dependent dephosphorylation of DARPP-32 by protein phosphatase 2A Proc. Natl. Acad. Sci., 104, 9876-9881

Bender, J., Engeholm, M., Ederer, M.S., Breu, J., Møller, T.C., Michalakis, S., Rasko, T. 5, Wanker, E.E. et al (2015) Corticotropin-releasing hormone receptor type 1 (CRHR1) clustering with MAGUKs is mediated via its C-terminal PDZ binding motif PLoS One, 10: e0136768

Chtarto, A., Bockstael, O., Gebara, E., Vermoesen, K., Melas, C., Pythoud, C., Levivier, M., De Witte, O., Luthi-Carter, R., Clinkers, R. and Tenenbaum, L. (2013) An adeno-associated virus-based intracellular sensor of pathological nuclear factor-B activation for disease-inducible gene transfer PLoS One, 8: e53156

Dogra, S., Kumar, A., Umrao, D., Sahasrabuddhe, A.A. and Yadav, P.M. (2016) Chronic Kappa opioid receptor activation modulates NR2B: Implication in treatment resistant depression Sci. Rep., 6: 33401

Hasegawa, K., Yasuda, T., Shiraishi, C., Fujiwara, K., Przedborski, S., Mochizuki, H. and Yoshikawa, K. (2016) Promotion of mitochondrial biogenesis by necdin protects neurons against mitochondrial insults Nat. Comm., 7: 10943

Jin, L., Lange, W., Kempmann, A., Maybeck, V., Günther, A., Gruteser, N., Baumann, A. and Offenhäusser, A. (2016) High-efficiency transduction and specific expression of ChR2opt for optogenetic manipulation of primary cortical neurons mediated byrecombinant adeno-associated viruses J. Biotech., 233, 171–180

Kneynsberg A., Collier, T.J., Manfredsson, F.P. and Kanaan, N.M. (2016) Quantitative and semi-quantitative measurements of axonal degeneration in tissue and primary neuron cultures J. Neurosci. Meth., 266, 32–41

Koch, J.C., Bitow, F., Haack, J., d`Hedouville, Z., Zhang, J-N., Tönges, L., Michel, U. et al (2015) AlphaSynuclein affects neurite morphology, autophagy, vesicle transport and axonal degeneration in CNS neurons

Cell Death Dis., 6: e1811
Kunadt, M., Eckermann, K., Stuendl, A., Gong, J., Russo, B., Strauss, K., Rai, S., Kugler, S. et al (2015) Extracellular vesicle sorting of α synuclein is regulated by sumoylation Acta Neuropathol., 129, 695-713

Lutz, D., Loers, G., Kleene, R., Oezen, I., Kataria, H., Katagihallimath, N., Braren, I., Harauz, G. and Schachner, M. (2014) Myelin basic protein cleaves cell adhesion molecule L1 and promotes neuritogenesis and cell survival J. Biol. Chem., 289, 13503–13518

Maddalena, A., Tereshchenko, J., Bähr, M. and Kügler, S. (2013) Adeno-associated virus-mediated, vifepristone-regulated transgene expression in the brain Mol. Ther. Nucleic Acids 2: e106

Ortiz-Abalia, J., Sahún, I., Altafaj, X., Andreu, N., Estivill, X., Dierssen, M. and Fillat, C. (2008) Targeting Dyrk1A with AAVshRNA attenuates motor alterations in TgDyrk1A, a mouse model of Down syndrome Am. J. Hum. Genet., 83, 479-488

Pulizzi, R., Musumeci, G., Van den Haute, C., Van De Vijver, S., Baekelandt, V. and Giugliano, M. (2016) Brief wide-field photostimuli evoke and modulate oscillatory reverberating activity in cortical networks Sci. Rep., 6: 24701

Rosario, A.M., Cruz, P.E., Ceballos-Diaz, C., Strickland, M.R., Siemienski, Z., Pardo, M., Schob, K-L., Li, A., Aslanidi, G.V. et al (2016) Microglia-specific targeting by novel capsid-modified AAV6 vectors Mol. Ther. Meth. Clin. Dev., 3: 16026

Sasaguri, H., Chew, J., Xu, Y-F., Gendron, T.F., Garrett, A., Lee, C.W., Jansen-West, K., Bauer, P.O. et al (2016) The extreme N-terminus of TDP-43 mediates the cytoplasmic aggregation of TDP-43 and associated toxicity in vivo Brain Res., 1647, 57–64

Sohn, J., Takahashi, M., Okamoto, S., Ishida, Y., Furuta, T. and Hioki, H. (2017) A single vector platform for high-level gene transduction of central neurons: adeno-associated virus vector equipped with the Tet-off system PLoS One, 12: e0169611

Truong, D-J.J., Kühner, K., Kühn, R., Werfel, S., Engelhardt, S., Wurst, W. and Ortiz, O. (2015) Development of an intein-mediated split–Cas9 system for gene therapy Nucleic Acids Res., 43, 6450–6458

Vullhorst, D., Mitchell, R.M., Keating, C., Roychowdhury, S., Karavanova, I., Tao-Cheng, J-H. and Buonanno, A. (2015) A negative feedback loop controls NMDA receptor function in cortical interneurons via neuregulin 2/ErbB4 signalling Nat. Commun., 6: 7222

Xu, J., Ma, C., Bass, C. and Terwilliger, E.F. (2005) A combination of mutations enhances the neurotropism of AAV-2 Virology, 341, 203-214

Yu, Z., Liu, N., Li, Y., Xu, J. and Wang, X. (2013) Neuroglobin overexpression inhibits oxygen–glucose deprivation-induced mitochondrial permeability transition pore opening in primary cultured mouse cortical neurons Neurobiol. Dis., 56, 95–103

Zheng, D., Sabbagh, J.J., Blair, L.J., Darling, A.L., Wen, X. and Dickey, C.A. (2016) MicroRNA-511 binds to FKBP5 mRNA, which encodes a chaperone protein, and regulates neuronal differentiation J. Biol. Chem., 291, 17897–17906

Nucleus pulposus cells
Mern, D.S. and Thomé, C. (2015) Identification and characterization of human nucleus pulposus cell specific serotypes of adeno-associated virus for gene therapeutic approaches of intervertebral disc disorders BMC Musculoskelet. Disorders, 16: 341

Oligodendrocytes
Aggarwal, S., Snaidero, N., Pähler, G., Frey, S., Sánchez, P., Zweckstetter, M., Janshoff, A., Schneider, A., Weil, M-T., Schaap, I.A.T., Görlich, D. and Simons, M. (2013) Myelin membrane assembly is driven by a phase transition of myelin basic proteins into a cohesive protein meshwork PLoS Biol., 11: e1001577

Frühbeis, C., Fröhlich, D., Kuo, W.P., Amphornrat, J., Thilemann, S., Saab, A.S., Kirchhoff, F., Möbius, W., Goebbels, S., Nave, K-A., Schneider, A., Simons, M., Klugmann, M., Trotter, J., Krämer-Albers, E-M., (2013) Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte–neuron communication PLoS Biol., 11: e1001604

Osteosarcoma cells
Gaj, T., Staahl, B.T., Rodrigues, G.M.C., Limsirichai, P., Ekman, F.K., Doudna, J.A. and Schaffer, D.V. (2017) Targeted gene knock-in by homology-directed genome editing using Cas9 ribonucleoprotein and AAV donor delivery Nucleic Acids Res., 45: e98

Nicolas, A., Jolinon, N., Alazard-Dany, N., Barateau, V., Epstein, A.L., Greco, A., Büning, H. and Salvetti, A. (2012) Factors influencing helper-independent adeno-associated virus replication Virology, 432, 1–9

Ovarian carcinoma
Xie, Y., Hicks, M.J., Kaminsky, S.M., Moore, M.A.S., Crystal, R.G. and Rafii, A. (2014) AAV-mediated persistent bevacizumab therapy suppresses tumor growth of ovarian cancer Gynecol. Oncol., 135, 325–332

Primary human brain endothelial cells
Merkel, S.F., Andrews, A.M., Lutton, E.M., Mu, D., Hudry, E., Hyman, B.T., Maguire, C.A. and Ramirez, S.H. (2017) Trafficking of adeno-associated virus vectors across a model of the blood-brain barrier; a comparative study of transcytosis and transduction using primary human brain endothelial cells J. Neurochem., 140, 216-230

Primary midbrain neurons
Koch, J.C., Bitow, F., Haack, J., d`Hedouville, Z., Zhang, J-N., Tönges, L., Michel, U. et al (2015) AlphaSynuclein affects neurite morphology, autophagy, vesicle transport and axonal degeneration in CNS neurons Cell Death Dis., 6: e1811

Receptor-independent
Dudek, A.M., Pillay, S., Puschnik, A.S., Nagamine, C.M., Cheng, F., Qiu, J., Carette, J.E. and Vandenberghe, L.H. (2018) An alternate route for adeno-associated Virus (AAV) entry independent of AAV receptor J. Virol., 92: e02213-17

Smooth muscle progenitor cells
Chen, F., Zhang, ZD., and Zhu, XH. (2015) Inhibition of development of experimental abdominal aortica neurysm by c-junN-terminal protein kinase inhibitor combined with lysyl oxidase gene modified smooth muscle progenitor cells Eur. J. Pharmacol., 766, 114–121

SV40 tranformed human cell lines
Nicolas, A., Jolinon, N., Alazard-Dany, N., Barateau, V., Epstein, A.L., Greco, A., Büning, H. and Salvetti, A. (2012) Factors influencing helper-independent adeno-associated virus replication Virology, 432, 1–9

Synoviocytes
Goodrich, L.R., Phillips, J.N., McIlwraith, C.W., Foti, S.B., et al (2013) Optimization of scAAVIL-1ra in vitro and in vivo to deliver high levels of therapeutic protein for treatment of osteoarthritis Mol. Ther. Nucleic Acids, 2: e70

Kyostio-Moore, S., Bangari, D.S., Ewing, P., Nambiar, B., et al (2013) Local gene delivery of heme oxygenase1 by adeno-associated virus into osteoarthritic mouse joints exhibiting synovial oxidative stress Osteoarthritis Cartilage, 21, 358-367

T-cells
Paul, B., Romano Ibarra, G.S., Hubbard, N., Einhaus, T., Astrakhan, A., Rawlings, D.J., Kiem, H-P. and Peterson, C.W. (2018) Efficient enrichment of gene-modified primary T cells via CCR5-targeted integration of mutant dihydrofolate reductase Mol. Ther. Meth.Clin. Dev., 9, 347-357

Rogers, G.L., Shirley, J.L., Zolotukhin, I., Kumar, S.R.P., Sherman, A., Perrin, G.Q., Hoffman, B.E., Srivastava, A., Basner-Tschakarjan, E. et al (2017) Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD81 T cells Blood, 129, 3184-3195

Cutaneous therapy

Sallach, J., Di Pasquale, G., Larcher, F., Niehoff, N., et al (2014) Tropism-modified AAV vectors overcome barriers to successful cutaneous therapy Mol. Ther., 22, 929–939

Cystic fibrosis (see “Respiratory system delivery”)
Deafness (see “Cochlear delivery”)

Dental disorders

Kunze, M., Huber, A., Krajewski, A., Lowden, E., et al (2009) Efficient gene transfer to periodontal ligament cells and human gingival fibroblasts by adeno-associated virus vectors J. Dent., 37, 502-508

Designed ankyrin repeat proteins

Münch, R.C., Janicki, H., Völker, I., Rasbach, A., et al (2013) Displaying high-affinity ligands on adenoassociated viral vectors enables tumor cell-specific and safe gene transfer Mol. Ther., 21, 109–118

Diabetes and other pancreatic disorders

Diabetic neuropathy

Homs, J., Pagès, G., Ariza, L., Casas, C., et al (2014) Intrathecal administration of IGF-I by AAVrh10 improves sensory and motor deficits in a mouse model of diabetic neuropathy Mol. Ther. Methods Clin. Dev., 1: 7

Platt, T.L., Beckett, T.L., Kohleer, Niedowicz, K.D.M. and Murphy, M.P. (2016) Obesity, diabetes, and leptin resistance promote tau pathology in a mouse model of disease Neuroscience 315, 162–174

Glucotoxicity
Poungvarin, N., Lee, J.K., Yechoor, V.K., Li, M.V., et al (2012) Carbohydrate response element-binding protein (ChREBP) plays a pivotal role in beta cell glucotoxicity Diabetologia (2012) 55, 1783–1796

Hypothalamic regulation
Kim, J.D., Toda, C., D’Agostino, G., Zeiss, C.J., DiLeone, R.J., Elsworth, J.D., Kibbey, R.G., Chan, O., Harvey, B.K., Richie, C.T. et al (2014) Hypothalamic prolyl endopeptidase (PREP) regulates pancreatic insulin and glucagon secretion in mice Proc. Natl. Acad. Sci. USA, 111, 11876–11881

Insulin growth factor/insulin receptor
Chu, Q., Moreland, R., Yew, N.S., Foley, J., et al (2008) Systemic insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy Mol. Ther., 16, 1400-1408

Liu, X., Magee, D., Wang, C., McMurphy, T., et al (2014) Adipose tissue insulin receptor knockdown via a new primate-derived hybrid recombinant AAV serotype Mol. Ther. Methods Clin. Dev., 1: 8

Islet (pancreatic) delivery
Craig, A.T., Gavrilova, O., Dwyer. N.K., Jou, W., et al (2009) Transduction of rat pancreatic islets with pseudotyped adeno-associated virus vectors Virol. J. 6:61

Flotte, T., Agarwal, A., Wang, J., Song, S., et al (2001) Efficient ex vivo transduction of pancreatic islet cells with recombinant adeno-associated virus vectors Diabetes, 50, 515-520

Kapturczak, M., Zolotukhin, S., Cross, J., Pileggi, A., et al (2002) Transduction of human and mouse pancreatic islet cells using a bicistronic recombinant adeno-associated viral vector Mol. Ther., 5, 154-160

Loiler, S.A., Conlon, T.J., Tang, Q., Warrington, K.H., et al (2003) Targeting recombinant adeno-associated virus vectors to enhance gene transfer to pancreatic islets and liver Gene Ther., 10, 1551-1558

Loiler, S.A., Tang, Q., Clarke, T., Campbell-Thompson, M.L., et al (2005) Localized gene expression following administration of adeno-associated viral vectors via pancreatic ducts Mol. Ther., 12, 519-527

Lu, Y., Tang, M., Wasserfall, C., Kou, Z., et al (2006) α 1-Antitrypsin gene therapy modulates cellular immunity and efficiently prevents type 1 diabetes in nonobese diabetic mice Hum. Gene Ther., 17, 625-634

Vizzardelli, C., Molano, R.D., Pileggi, A., Berney, T., et al (2002) Neonatal porcine pancreatic cell clusters as a potential source for transplantation in humans: characterization of proliferation, apoptosis, xenoantigen expression and gene delivery with recombinant AAV Xenotransplantation, 9, 14-24

Pancreatic/Pancreatic cell delivery
Batchu, R.B., Gruzdyn, O.V., Kung, S.T., Weaver, D.W., et al (2014) Novel AAV-DJ capsid tyrosine mutants with enhanced transgene expression in a pancreatic cancer cell line J. Surg, Res., 186, 637-638

Chen, M., Maeng, K., Nawab, A., Francois, R.A., Bray, J.K., Reinhard, M.K., Boye, S.L., Hauswirth, W.W., Kaye, F.J., Aslanidi, G., Srivastava, A. and Zajac-Kaye, M. (2017) Efficient gene delivery and expression in pancreas and pancreatic tumors by capsid-optimized AAV8 vectors Human Gene Ther. Meth., 28, 49-59

Griffin, M.A., Restrepo, M.S., Abu-El-Haija, M., Wallen, T., et al (2014) A novel gene delivery method transduces porcine pancreatic duct epithelial cells Gene Ther., 21, 123–130

Poungvarin, N., Lee, J.K., Yechoor, V.K., Li, M.V., et al (2012) Carbohydrate response element-binding protein (ChREBP) plays a pivotal role in beta cell glucotoxicity Diabetologia (2012) 55, 1783–1796

Quirin, K.A., Kwon, J.J., Alioufi, A., Factora, T., Temm, C.J., Jacobsen, M., Sandusky, G.E., Shontz, K. et al (2018) Safety and efficacy of AAV retrograde pancreatic ductal gene delivery in normal and pancreatic cancer mice Mol. Ther.: Meth. Clin. Dev., 8, 8-20

Sheng, Q., Xiao. X., Prasadan, K., Chen, K., Ming, Y., Fusco, J., Gangopadhyay, N.N., Ricks, D. and Gittes, G.K. (2017) Autophagy protects pancreatic beta cell mass and function in the setting of a high-fat and highglucose diet Sci. Rep., 7: 16348

Tonne, J.M., Sakuma, T., Deeds, M.C., Munoz-Gomez, M., et al (2013) Global gene expression profiling of pancreatic islets in mice during streptozotocin-induced β-cell damage and pancreatic Glp-1 gene therapy Dis. Mod. Mech., 6, 1236-1245

DNA

DNA binding proteins
Satkunanathan, S., Thorpe, R. and Zhao, Y. (2017) The function of DNA binding protein nucleophosmin in AAV replication Virology, 510, 46–54

Xu, Y-F., Prudencio, M., Hubbard, J.M., Tong, J., et al (2013) The pathological phenotypes of human TDP-43 transgenic mouse models are independent of downregulation of mouse Tdp-43 PLoS One, 8: e69864

Clones
Schnepp, B.C., Jensen, R.L., Clark, K.R. and Johnson, P.R (2009) Infectious molecular clones of adenoassociated virus isolated directly from human tissues J. Virol., 83, 1456-1464

Inverted terminal repeats
Aurnhammer, C., Haase, M., Muether, N., Haus, M., et al (2012) Universal real-time PCR for the detection and quantification of adeno-associated virus serotype 2-derived inverted terminal repeat sequences Hum. Gene Ther. Methods, Part B 23, 18-28

Julien, L., Chassagne, J., Peccate, C., Lorain, S., Piétri-Rouxel, F., Danos, O. and Benkhelifa-Ziyyat, S. (2018) RFX1 and RFX3 transcription factors interact with the D sequence of adeno-associated virus inverted terminal repeat and regulate AAV transduction Sci. Rep., 8: 210

Manipulation/modification
Cataldi, M.P. and McCarty, D.M. (2010) Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes J. Virol., 84, 8673–8682

Choi, V.W., Samulski, R.J. and McCarty, D. (2005) Effects of adeno-associated virus DNA hairpin structure on recombination J. Virol., 79, 6801-6807

Choi, V.W., McCarty, D.M. and Samulski, R.J. (2006) Host cell DNA repair pathways in adeno-associated viral genome processing J. Virol., 80, 10346-10356

Fraefel, C., Bittermann, A.G., Bueler, H., Heid, I., et al (2004) Spatial and temporal organization of adenoassociated virus DNA replication in live cells J. Virol., 78, 389 398

Glauser, D.L., Strasser, R., Laimbacher, A.S., Saydam, O., et al (2007) Live covisualization of competing adeno-associated virus and herpes simplex virus type 1 DNA replication: Molecular mechanisms of interaction J. Virol., 81, 4723-4743

Hamilton, H., Gomos, J., Berns, K.I.and Falck-Pedersen, E. (2004) Adeno-associated virus site-specific integration and AAVS1 disruption J. Virol., 78, 7874-7882

Hirsch, M.L., Storici, F., Li, C., Choi, V.W., et al (2009) AAV recombineering with single strand  oligonucleotides PLoS One, 4: e7705

Hüser, D., Weger, S. and Heilbronn, R. (2003) Packaging of human chromosome 19-specific adeno-associated virus (AAV) integration sites in AAV virions during AAV wild-type and recombinant AAV vector production J. Virol., 77, 4881-4887

Katrekar, D., Moreno, A.M., Chen, G., Worlikar, A. and Mali, P. (2018) Oligonucleotide conjugated multifunctional adeno-associated viruses Sci. Rep., 8: 3589

Koerber, J.T., Jang, J-H., and Schaffer, D.V. (2008) DNA shuffling of adeno-associated virus yields functionally diverse viral progeny Mol. Ther., 16, 1703-1709

Miller, D.G., Petek, L.M. and Russell, D.W. (2003) Human gene targeting by adeno-associated virus vectors is enhanced by DVA double-strand breaks Mol. Cell. Biol., 23, 3550-3557

Miller, D.G., Petek, L.M. and Russell, D.W. (2004) Adeno-associated virus vectors integrate at chromosome breakage sites Nat. Genet., 36, 767-773

Miller, D.G., Trobridge, G.D., Petek, L.M., Jacobs, M.A., et al (2005) Large-scale analysis of adeno-associated virus vector integration sites in normal human cells J. Virol., 79, 11434-11442 Petek, L.M., Russell, D.W. and Miller, D.G. (2010) Frequent endonuclease cleavage at off-target locations in vivo Mol. Ther., 18, 983–986

Porteus, M.H., Cathomen, T., Weitsman, M.D. and Baltimore, D. (2003) Efficient gene targeting mediated by adeno-associated virus and DNA double-stranded breaks Mol. Cell. Biol., 23, 3558-3565

Stracker, T.H., Cassell, G.D., Ward, P., Loo, Y-M., et al (2004) The Rep protein of adeno-associated virus type 2 interacts with single-stranded DNA-binding proteins that enhance viral replication J. Virol., 78, 441-453

Polymorphisms
Deyle, D.R., Li, L.B., Ren, G. and Russell, D.W. (2014) The effects of polymorphisms on human gene targeting Nucleic Acids Res., 42, 3119–3124

Dogs, administration to

Hinderer, C., Bell, P., Louboutin, J-P., Zhu, Y., Yu, H., Lin, G., Choa, R., Gurda, B.L. et al (2015) Neonatal systemic AAV induces tolerance to CNS gene therapy in MPS I dogs and nonhuman primates Mol. Ther., 23, 1298-1307

Dopaminergic neurons

Tang, F-L., Liu, W., Hu, J-X., Erion, J.R., Ye, J., Mei, L. and Xiong, W-C. (2015) VPS35 deficiency or mutation causes dopaminergic neuronal loss by impairing mitochondrial fusion and function Cell Rep., 12, 1631–1643

Drug delivery/screening

Bouard, D., Alazard-Dany, N. and Cosset, F-L. (2009) Viral vectors: from virology to transgene expression Br. J: Pharmacol., 157, 153-165

Yan, Z., Lei-Butters, D., Engelhardt, J.F. and Leno, G.H. (2009) Indexing TNF-α gene expression using a genetargeted reporter cell line BMC Biol., 7:8

D-sequence substituted rAAV

Ling, C., Wang, Y., Lu, Y., Wang, L., Jayandharan, G.R., Aslanidi, G.V., Li, B. et al (2015) Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo J. Virol., 89, 952-961

Dystrophic epidermolysis bullosa

Chamorro, C., Mencía, A., Almarza, D., Duarte, B., Büning, H., Sallach, J., Hausser, I., Del Río, M., Larcher, F. and Murillas, R. (2016) Gene editing for the efficient correction of a recurrent COL7A1 mutation in recessive dystrophic epidermolysis bullosa keratinocytes Mol. Ther. Nucleic Acids, 5: e307

Eating disorders (see also “Leptin therapy”)

Ganella, D.E., Callander, G.E., Ma, S., Bye, C.R., et al (2013) Modulation of feeding by chronic rAAV expression of a relaxin-3 peptide agonist in rat hypothalamus Gene Ther., 20, 703–716

Ebola treatment

Robert, M.A., Nassouri, N., Chahal, P.S., Venne, M.H., Kamen, A., Kobinger, G., Gilbert, R. and Gaillet, B. (2016) Gene therapy for Ebola virus infections based on AAV vectors and Zmapp antibody cocktail Hum. Gene Ther., 27, A42

Robert, M-A., Kamen, A., Kobinger, G., Gilbert, R. and Gaillet, B. (2016) Development of a post-exposure treatment for Ebola virus infections based on AAV vectors and Zmapp antibody cocktail Mol. Ther., 24, Suppl. 1, S222

Robert, M-A., Nassoury, N., Chahal, P.S., Venne, M-H., Racine, T., Qiu, X., Kobinger, G., Kamen, A., Gilbert, R. and Gaillet, B. (2018) Gene transfer of ZMapp antibodies mediated by recombinant adeno-associated virus protects against Ebola infections Hum Gene Ther., 29, 452-466

Van Lieshout, L.P., Soule, G., Sorensen, D., Frost, K.L., He, S., Tierney, K., Safronetz, D., Booth, S.A. (2018) Intramuscular adeno-associated virus–mediated expression of monoclonal antibodies provides 100% protection against Ebola virus infection in mice J. Infect. Dis., 217, 917-925

Endonucleases

Agúndez, L., Zúrate-Pérez, F., Meier, A.F., Bardelli, M., Llosa, M., Escalante, C.R., Linden, M. and Henckaerts, E. (2018) Exchange of functional domains between a bacterial conjugative relaxase and the integrase of the human adeno-associated virus PLoS One, 13: e0200841

Petek, L.M., Russell, D.W. and Miller, D.G. (2010) Frequent endonuclease cleavage at off-target locations in vivo Mol. Ther., 18, 983–986

Endosomal trafficking

Aoto, J., Martinelli, D.C., Malenka, R.C., Tabuchi, K., et al (2013) Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking Cell, 154, 75–88

Dickey, D.D., Excoffon, K.J.D.A., Koerber, J.T., Bergen, J., et al (2011) Enhanced sialic acid-dependent endocytosis explains the increased efficiency of infection of airway epithelia by a novel adeno-associated virus J. Virol., 85, 9023–9030

Nam, H-J., Gurda, B.L., McKenna, R., Potter, M., et al (2011) Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking J. Virol., 85, 11791–11799

Endothelial cell targeting

Chen, S., Kapturczak, M., Loiler, S.A., Zolotukhin, S., et al (2005) Efficient transduction of vascular endothelial cells with recombinant adeno-associated virus serotype 1 and 5 vectors Hum. Gene Ther., 16, 235-247

Jeltsch, M., Jha, S.K., Tvorogov, D., Anisimov, A., et al (2014) CCBE1 enhances lymphangiogenesis via A disintegrin and metalloprotease with thrombospondin motifs-3–mediated vascular endothelial growth factor-C activation Circulation, 129, 1962-1971

Karkkainen, M. J., Saaristo, A., Jussila, L., Karila, K. A., et al (2001) A model for gene therapy of humanhereditary lymphedema Proc. Natl. Acad. Sci. USA, 98, 12677-12682

Kealy, B., Liew, A., McMahon, J.M., Ritter, T., et al (2009) Comparison of viral and nonviral vectors for gene transfer to human endothelial progenitor cells Tissue Eng. Part C, 15, 223-231

Lipinski, D.M., Reid, C.A., Boye, S.L., Peterson, J.J., Qi, X., Boye, S.E., Boulton, M.E. and Hauswirth, W.W. (2015) Systemic vascular transduction by capsid mutant adeno-associated virus after intravenous injection Hum. Gene Ther., 26, 767-776

Müller, O.J., Kaul, F., Weitzman, M.D., Pasqualini, R., et al (2003) Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors Nat. Biotechnol., 21, 1040-1046

Nykänen, A.I., Pajusola, K., Krebs, R., Keränen, M.A.I., et al (2006) Common protective and diverse smooth muscle cell effects of AAV-mediated angiopoietin-1 and -2 expression in rat cardiac allograft vasculopathy Circ. Res., 98, 1373-1380

Pajusola, K., Gruchala, M., Joch, H., Luscher, T. F., et al (2002) Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells J. Virol., 76, 11530-11540

Sen, S., Contoy, S., Hynes, S.O., McMahon, J., et al (2008) Gene delivery to the vasculature mediated by lowtitre adeno-associated virus serotypes 1 and 5 J. Gene Med., 10, 143-151

Stachler, M.D. and Bartlett, J.S. (2006) Mosaic vectors comprised of modified AAV1 capsid proteins for efficient vector purification and targeting to vascular endothelial cells Gene Ther., 13, 926-931

Work, L.M., Büning, H., Hunt, E., Nicklin, S.A., et al (2006) Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses Mol. Ther., 13, 683-693

Enveloped vector

György, B., Fitzpatrick, Z., Crommentuijn, M.H.W., Mu, D. and Maguire, C.A. (2014) Naturally enveloped AAV vectors for shielding neutralizing antibodies and robust gene delivery in vivo Biomaterials, 35, 7598-7609

Evolutionary lineage of

Zinn, E., Pacouret, S., Khaychuk, V., Turunen, H.T., Carvalho, L.S., Andres-Mateos, E., Shah, S. Shelke, R. et al (2015) In silico reconstruction of the viral evolutionary lineage yields a potent gene therapy vector Cell Rep., 12, 1056–1068

Exosome gene delivery (see Vexosome gene delivery)
External carotid artery injection

Foley, C.P., Rubin, D.G.., Santillan, A., Sondhi, D., Dyke, J.P., Gobin, Y.P., Crystal, R.G. and Ballon, D.J. (2014) Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption J. Control. Release, 196, 71–78

GABAA receptor

Lin, W-C., Davenport, C.M., Mourot, A., Vytla, D., Smith, C.M., Medeiros, K.A., Chambers, J.J. and Kramer, R.H. (2014) Engineering a light-regulated GABAA receptor for optical control of neural inhibition ACS Chem. Biol., 9, 1414−1419

Galectin interaction

Denard, J., Beley, C., Kotin, R., Lai-Kuen, R., et al (2012) Human galectin 3 binding protein interacts with recombinant adeno-associated virus type 6 J. Virol., 86, 6620-6631

Gene delivery using Cas9

Gaj, T., Staahl, B.T., Rodrigues, G.M.C., Limsirichai, P., Ekman, F.K., Doudna, J.A. and Schaffer, D.V. (2017) Targeted gene knock-in by homology-directed genome editing using Cas9 ribonucleoprotein and AAV donor delivery Nucleic Acids Res., 45: e98

Truong, D-J.J., Kühner, K., Kühn, R., Werfel, S., Engelhardt, S., Wurst, W. and Ortiz, O. (2015) Development of an intein-mediated split–Cas9 system for gene therapy Nucleic Acids Res., 43, 6450–6458

Gene expression inhibition

Lentz, T.B. and Samulski, J. (2015) Insight into the mechanism of inhibition of adeno-associated virus by the Mre11/Rad50/Nbs1 complex J. Virol., 89, 181-194

Genome packaging

Drouin, L.M., Lins, B., Janssen, M., Bennett, A., Chipman, P., McKenna, R., Chen, W., Muzyczka, N., Cardone, G., Baker, T.S. and Agbandje-McKenna, M. (2106) Cryo-electron microscopy reconstruction and stability studies of the wild type and the R432A variant of adeno-associated virus type 2 reveal that capsid structural stability is a major factor in genome packaging J. Virol., 90, 8542-8541

Genome release

Horowitz, E.D., Rahman, K.S., Bower, B,D., Dismuke, D.J., et al (2013) Biophysical and ultrastructural characterization of adeno-associated virus capsid uncoating and genome release J. Virol., 87, 2994–3002

Glucocorticoid receptor

De Guia, R.M., Rose, A.J., Sommerfeld, A., Seibert, O., Strzoda, D., Zota, A., Feuchter, Y., Krones-Herzig, A., Sijmonsma, T. et al (2015) microRNA-379 couples glucocorticoid hormones to dysfunctional lipid homeostasis EMBO J., 34, 344–360

Glycan binding

Huang, L-Y., Patel, A., Ng, R., Miller, E.B., Halder, S., McKenna, R., Asokan, A. and Agbandje-McKenna, M. (2016) Characterization of the adeno-associated virus 1 and 6 sialic acid binding site J. Virol., 90, 5219-6230

Glycogen metabolism (see “Lysosomal storage diseases”)
Growth factors

Braun-Falco, M., Eisenried, A., Büning, H. and Ring, J. (2005) Recombinant adeno-associated virus type 2- mediated gene transfer into human keratinocytes is influenced by both the ubiquitin/proteasome pathway and epidermal growth factor receptor tyrosine kinase Arch. Dermatol. Res., 296, 528-535

Chu, Q., Moreland, R., Yew, N.S., Foley, J., et al (2008) Systemic insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy Mol. Ther., 16, 1400-1408

Jäger, J., Greiner, V., Strzoda, D., Seibert, O., et al (2014) Hepatic transforming growth factor- 1 stimulated clone-22 D1 controls systemic cholesterol metabolism Mol. Metab., 3, 155–166

Jazwa, A., Kucharzewska, P., Leja, J., Zagorska, A., et al (2010) Combined vascular endothelial growth factorA and fibroblast growth factor 4 gene transfer improves wound healing in diabetic mice Genet. Vaccines Ther., 8: 6

Jazwa, A., Tomczyk, M., Taha, H.M., Hytonen, E., et al (2013) Arteriogenic therapy based on simultaneous delivery of VEGF-A and FGF4 genes improves the recovery from acute limb ischemia Vasc. Cell, 5: 13

Karvinen, H., Pasanen, E., Rissanen, T.T., Korpisalo, P., et al (2011) Long-term VEGF-A expression promotes aberrant angiogenesis and fibrosis in skeletal muscle Gene Ther., 18, 1166–1172

Kuo, C-H., Chen, P-K., Chang, B-I., Sung, M-C., et al (2012) The recombinant lectin-like domain of thrombomodulin inhibits angiogenesis through interaction with Lewis Y antigen Blood, 119, 1302-1313

Paradiso, B., Marconi, P., Zucchini, S., Berto, E., et al (2009) Localized delivery of fibroblast growth factor–2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model Proc. Natl. Acad. Sci. USA, 106, 7191–7196

Pinkenburg, O., Pfosser, A., Hinkel, R., Böttcher, M., et al (2009) Recombinant adeno-associated virus-based gene transfer of cathelicidin induces therapeutic neovascularization preferentially via potent collateral growth Hum Gene Ther., 20, 159–167

Reid, C.A., Nettesheim, E.R., Connor, T.B. and Lipinski, D.M. (2018) Development of an inducible anti-VEGF rAAV gene therapy strategy for the treatment of wet AMD Sci. Rep., 8: 11763

Schievenbusch, S., Strack, I., Scheffler, M., Nischt, R., et al (2010) Combined paracrine and endocrine AAV9- mediated expression of hepatocyte growth factor for the treatment of renal fibrosis Mol. Ther. 18, 1302–1309

Takei, Y., Mizukami, H., Saga, Y., Yoshimura, I., et al (2006) Suppression of ovarian cancer by musclemediated expression of soluble VEGFR-1/Flt-1 using adeno associated virus serotype 1-derived vector Int. J. Cancer, 120, 278-284

Tuuminen, R., Dashkevich, A., Keränen, M.A.I., Raissadati, A., Krebs, R., Jokinen, J.J., Arnaudova, R., Rouvinen, E., Ylä-Herttuala, S. et al (2016) Platelet-derived growth factor-B protects rat cardiac allografts from ischemia-reperfusion injury Transplantation, 100, 303–313

Watanabe, M., Boyer, J.L. and Crystal, R.G. (2010) AAVrh.10-mediated genetic delivery of bevacizumab to the pleura to provide local anti-VEGF to suppress growth of metastatic lung tumors Gene Ther., 17, 1042–1051

Haemophilia

Sen, D., Gadkari, R.A., Sudha, G., Gabriel, N., et al (2013) Targeted modifications in adeno-associated virus serotype 8 capsid improves its hepatic gene transfer efficiency in vivo Hum. Gene Ther. Methods, 24, 104–116

Rogers, G.L., Martino, A.T., Zolotukhin, I., Ertl, H.C.J., et al (2014) Role of the vector genome and underlying factor IX mutation in immune responses to AAV gene therapy for hemophilia B J. Translat. Med., 12: 25

Xu, L., Daly, T., Gao, C., Flotte, T.R., et al (2001) CMV – ß – actin promoter directs higher expression from an adeno-associated viral vector in the liver than the cytomegalovirus or elongation factor 1 promoter and results in therapeutic levels of human factor X in mice Hum. Gene Ther., 12, 563-573

Zolotukhin, I., Markusic, D.M., Palaschak, B., Hoffman, B.E., Srikanthan, M.A. and Herzog, R.W. (2016) Potential for cellular stress response to hepatic factor VIII expression from AAV vector Mol. Ther. Meth. Clin. Dev., 3: 16063

Haematopoietic cells

Bak, R.O., Dever, D.P. and Porteus, M.H. (2018) CRISPR/Cas9 genome editing in human hematopoietic stem cells Nat. Protocols, 13, 358-376

Charlesworth, C.T., Camarena, J., Cromer, M.K., Vaidyanathan, S., Bak, R.O., Carte, J.M., Potter, J., Dever, D.P. and Porteus, M.H. (2018) Priming human repopulating hematopoietic stem and progenitor cells for Cas9/sgRNA gene targeting Mol. Ther: Nucl. Acids, 12, 89-104

Dever, D.P.D., Bak, R.O., Reinisch, A., Camarena, J., Washington, G., Nicolas, C.E., Pavel-Dinu, M., Saxena, N., Wilkens, A.B. et al (2016) CRISPR/Cas9 β-globin gene targeting in human haematopoietic stem cells Nature, 539, 384-389

Gundry, M.C., Dever, D.P., Yudovich, D., Bauer, D.E., Haas, S., Wilkinson, A.C. and Singbrant, S. (2017) Technical considerations for the use of CRISPR/Cas9 in hematology research Exptl. Hematol., 54, 4-11

Han, Z., Zhong, L., Maina, N., Hu, Z., et al (2008) Stable integration of recombinant adeno-associated virus vector genomes after transduction of murine hematopoietic stem cells Hum. Gene Ther., 19, 267-278

Hiramoto, T., Li, L.B., Funk, S.E., Hirata, R.K. and Russell, D.W. (2018) Nuclease-free adeno-associated virus-mediated Il2rg gene editing in X-SCID mice Mol. Ther., 26, 1255-1265

McMahon, J.M., Conroy, S., Lyons, M., Greiser, U., et al (2006) Gene transfer into rat mesenchymal stem cells: a comparative study of viral and nonviral vectors Stem Cell. Dev., 15, 87-96

Nathwani, A.C., Hanwa, H., Vandergriff, J., Kely, P., et al (2000) Efficient gene transfer into human cord blood CD34+ cells and the CD34+ CD38- subset using highly purified recombinant adeno-associated viral vector preparations that are free of helper virus and wild-type AAV Gene Ther., 7, 183-195

Paiboonsukwong, K., Ohbayashi, F., Shiiba, H., Aizawa, E., et al (2009) Correction of mutant Fanconi anemia gene by homologous recombination in human hematopoietic cells using adeno-associated virus vector J. Gene Med., 11, 1012-1019

Ryu, B.Y., Evans-Galea, M.V., Gray, J.T., Bodine, D.M., et al (2008) An experimental system for the evaluation of retroviral vector design to diminish the risk for proto-oncogene activation Blood, 111, 1866-1875

Sather, B.D., Romano Ibarra, G.S., Sommer, K., Curinga, G., Hale, M., Khan, I.F., Singh, S., Song, Y. et al (2015) Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template Sci. Transl. Med., 7: 307ra156

Vakulskas, C.A, Dever, D.P., Rettig, G.R., Turk, R., Jacobi, A.M., Collingwood, M.A., Bode, N.M., McNeill, M.S., Yan, S. et al (2018) A high-fidelity Cas9 mutant delivered as a ribonucleoprotein complex enables efficient gene editing in human hematopoietic stem and progenitor cells Nat. Med., 24, 1216–1224

Haem oxygenase delivery

Kyostio-Moore, S., Bangari, D.S., Ewing, P., Nambiar, B., et al (2013) Local gene delivery of heme oxygenase1 by adeno-associated virus into osteoarthritic mouse joints exhibiting synovial oxidative stress Osteoarthritis Cartilage, 21, 358-367

Hearing disorders (see also “Cochlear delivery”)

Iizuka, T., Kanzaki, S., Mochizuki, H., Inoshita, A., et al (2008) Noninvasive in vivo delivery of transgene via adeno-associated virus into supporting cells of the neonatal mouse cochlea Human Gene Therapy, 19, 384-390

Kilpatrick, L.A., Li, Q., Yang, J., Goddard, J.C., et al (2011) Adeno-associated virus-mediated gene delivery into the scala media of the normal and deafened adult mouse ear Gene Ther., 18, 569–578

Luebke, A.E., Foster, P.K., Muller, C.D. and Peel, A.L. (2001) Cochlear function and transgene expression in the guinea pig cochlea, using adenovirus- and adeno-associated virus-directed gene transfer Hum. Gene Ther., 12, 773-781

György, B., Sage, C., Indzhykulian, A.A., Scheffer, D.I., Brisson, A.R., Tan, S., Wu, X., Volak, A., Mu, D. et al (2017) Rescue of hearing by gene delivery to inner-ear hair cells using exosome-associated AAV Mol. Ther., 25, 379-391

Stone, I.M., Lurie, D.I., Kelley, M.W. and Poulsen, D.J. (2005) Adeno-associated virus-mediated gene transfer to hair cells and support cells of the murine cochlea Mol. Ther., 11, 843-848

Suzuki, J., Hashimoto, K., Xiao, R., Vandenberghe, L.H. and Liberman, M.C. (2017) Cochlear gene therapy with ancestral AAV in adult mice: complete transduction of inner hair cells without cochlear dysfunction Sci. Rep., 7: 45524

Heart/heart failure (see “Vascular smooth muscle”)
Helper virus functions

Kang, W., Wang, L., Harrell, H., Liu, J., et al (2009) An efficient rHSV-based complementation system for the production of multiple rAAV vector serotypes Gene Ther., 16, 229-239

Mistry, A.R., De Alwis, M., Feudner, E., Ali, R.R. and Thrasher, A.J. (2002) High-titer stocks of adenoassociated virus from replicating amplicons and herpes vectors Methods Mol. Med., 69, 445-460

Pozzuto, T., von Kietzell, K., Bock, T., Schmidt-Lucke, C., et al (2011) Transactivation of human parvovirus B19 gene expression in endothelial cells by adenoviral helper functions Virology 411, 50–64

Seyffert, M., Glauser, D.L., Schraner, E.M., de Oliveira, A-P., Mansilla-Soto, J., Vogt, B., Büning, H., Linden, R.M., Ackermann, M. and Fraefel, C. (2017) Novel mutant AAV2 Rep proteins support AAV2 replication without blocking HSV-1 helper virus replication PLoS One, 12: e0170908

Toublanc, E., Benraiss, A., Bonnin, D., Blouin, V., et al (2004) Identification of a replication-defective herpes simplex virus for recombinant adeno-associated virus type 2 (rAAV2) particle assembly using stable producer cell lines J. Gene Med., 6, 555-564

Hepadnavirus infection

Berraondo, P., Di Scala, M., Korolowicz, K., Thampi, L.M., Otano, I., Suarez, L., Fioravanti, J., Aranda, F., Ardaiz, N. et al (2015) Liver-directed gene therapy of chronic hepadnavirus infection using interferon alpha tethered to apolipoprotein A-I J. Hepatol., 63, 329–336

Hepatic/hepatocyte delivery
Acyl-CoA dehydrogenase

Beattie, S.G., Goetzman, E., Conlon, T., Germain, S., Walter, G., et al (2008) Biochemical correction of shortchain acyl-coenzyme A dehydrogenase deficiency after portal vein injection of rAAV8-SCAD Hum. Gene Ther., 19, 579-588

Ancestral rAAVs, targeting of,
Zinn, E., Pacouret, S., Khaychuk, V., Turunen, H.T., Carvalho, L.S., Andres-Mateos, E., Shah, S. Shelke, R. et al (2015) In silico reconstruction of the viral evolutionary lineage yields a potent gene therapy vector Cell Rep., 12, 1056–1068

Anti-inflammatory agents
Gil-Fariña, I., Di Scala, M., Vanrell, L., Olagüe, C., et al (2013) IL12-mediated liver inflammation reduces the formation of AAV transcriptionally active forms but has no effect over preexisting AAV transgene expression PLoS One, 8: e67748

a-1Anti-trypsin
Conlon, T.J., Cossette, T., Erger, K., Choi, Y-K., et al (2005) Efficient hepatic delivery and expression from a recombinant adeno-associated virus 8 pseudotyped 1-antitrypsin vector Mol. Ther., 12, 867-875

Song, S., Embury, J., Laipis, P.J., Berns, K.I., et al (2001) Stable therapeutic serum levels of human alpha-1 antitrypsin (AAT) after portal vein injection of recombinant adeno-associated virus (rAAV) vectors Gene Ther., 8, 1299-1306

Capsid uncoating
Tenney, R.M., Bell, C.L. and Wilson, J.M. (2014) AAV8 capsid variable regions at the two-fold symmetry axis contribute to high liver transduction by mediating nuclear entry and capsid uncoating Virology 454-455 (2014) 227–236

Carcinogenesis/carcinoma
Gruber, S., Straub, B.K., Ackermann, J., Wunderlich, C.M., et al (2013) Obesity promotes liver carcinogenesis via Mcl-1 stabilization independent of IL-6Ra signaling Cell Rep., 4, 669–680

Logan, G.J., Dane, A.P., Hallwirth, C.V., Smyth, C.M., Wilkie, E.E., Amaya, A.K., Zhu, E., Khandekar, N. et al (2017) Identification of liver-specific enhancer–promoter activity in the 3′ untranslated region of the wildtype AAV2 genome Nat. Genet., 49, 1267-1273

Santamaria, M., Pardo–Saganta, A., Alvarez–Asiain, L., Di Scala, M., et al (2013) Nuclear a1-anti-chymotrypsin promotes chromatin condensation and inhibits proliferation of human hepatocellular carcinoma cells Gastroenterology, 144, 818-828

Vanrell, L., Di Scala, M., Blanco, L., Otano, I., et al (2011) Development of a liver-specific Tet-On inducible system for AAV vectors and its application in the treatment of liver cancer Mol. Ther., 19, 1245–1253

DNA demethylation
Gil-Fariña, I., Di Scala, M., Vanrell, L., Olagüe, C., et al (2013) IL12-mediated liver inflammation reduces the formation of AAV transcriptionally active forms but has no effect over preexisting AAV transgene expression PLoS One, 8: e67748

Fatty liver disease
Schultze, S.M., Dietrich, M., Hynx, D., Geier, A., Niessen, M., Spinas, G.A., Hemmings, B.A. and Tschopp, O. (2015) Reduced hepatic lipid content in Pten-haplodeficient mice because of enhanced AKT2/PKBb activation in skeletal muscle Liver Int., 35, 1354–1366

Fibrosis
Rezvani, M., Espanõl-Suner, R., Malato, Y., Dumont, L., Grimm, A.A., Kienle, E., Bindman, J.G., Wiedtke, E., Hsu, B.Y. et al (2016) In vivo hepatic reprogramming of myofibroblasts with AAV vectors as a therapeutic strategy for liver fibrosis Cell Stem Cell, 18, 809–816

Green fluorescent protein
Piras, B.A., O’Connor, D.M. and French, B.A. (2013) Systemic delivery of shRNA by AAV9 provides highly efficient knockdown of ubiquitously expressed GFP in mouse heart, but not liver PLoS One, 8: e75894

Hepatotoxicity
Liang, K.J., Woodard, K.T., Weaver, M.A., Gaylor, J.P., Weiss, E.R. and Samulski, R.J. (2017) AAV-Nrf2 promotes protection and recovery in animal models of oxidative stress Mol. Ther., 25, 765-779

Hypercholesterolaemia
Kassim, S.H., Li, H., Bell, P., Somanathan, S., et al (2013) Adeno-associated virus serotype 8 gene therapy leads to significant lowering of plasma cholesterol levels in humanized mouse models of homozygous and heterozygous familial hypercholesterolemia Hum. Gene Ther., 24, 19–26

Hyperoxaluria
Salido, E., Rodriguez-Pena, M., Santana, A., Beattie, S.G., et al (2011) Phenotypic correction of a mouse model for primary hyperoxaluria with adeno-associated virus gene transfer Mol. Ther., 19, 870–875

IFN-a
Vanrell, L., Olague, C., Vales, A., Pãneda, A., et al (2009) Evaluation of AAV-mediated IFNa-gene therapy efficacy in HBV transgenic mice: constitutive versus inducible expression J. Hepatol., 50 Supp. 1, S215-S215

Immunity/immune response
Faust, S.M., Bell, P., Zhu, Y., Sanmiguel, J. and Wilson, J.M. (2013) The role of apoptosis in immune hyporesponsiveness following AAV8 liver gene transfer Mol. Ther., 21, 2227–2235

Hurlbut, G.D., Ziegler, R.J., Nietupski, J.B., Foley, J.W., et al (2010) Preexisting immunity and low expression in primates highlight translational challenges for liver-directed AAV8-mediated gene therapy Mol. Ther., 18, 1983–1994

Martino, A.T., Suzuki, M., Markusic, D.M., Zolotukhin, I., et al (2011) The genome of self-complementary adeno-associated viral vectors increases Toll-like receptor 9–dependent innate immune responses in the liver Blood, 117, 6459-6468

Insulin, effect of
Carrig, S., Bijjiga, E., Wopat, M.J. and Martino, A.T. (2016) Insulin therapy improves adeno-associated virus transduction of liver and skeletal muscle in mice and cultured cells Hum. Gene Ther., 27, 892-905

Liver-draining lymph nodes
Perrin, G.Q., Zolotukhin, I., Sherman, A., Biswas, M., de Jong, Y.P., Terhorst, C., Davidoff, A.M. and Herzog, R.W. (2016) Dynamics of antigen presentation to transgene product-specific CD4+ T cells and of Treg induction upon hepatic AAV gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16083

Lysosome effects
Batista, A.R., Sena-Esteves, M. and Saraiva, M.J. (2013) Hepatic production of transthyretin L12P leads to intracellular lysosomal aggregates in a new somatic transgenic mouse model Biochim. Biophys. Acta, 1832, 1183–1193

Mesenchymal stromal cells
Gabriel, N., Samuel, R. and Jayandharan, G.R. (2017) Targeted delivery of AAV-transduced mesenchymal stromal cells to hepatic tissue for ex vivo gene therapy J, Tissue Eng, Regen, Med., 11, 1354–1364

Porphyria
Serrano-Mendioroz, I., Sampedro, A., Alegre, M., de Salamanca, R-E., Berraondo, P. and Fontanellas, A. (2018) An inducible promoter responsive to different porphyrinogenic stimuli improves gene therapy vectors for acute intermittent porphyria Hum, Gene Ther., 29, 480-491

Unzu, C., Sampedro, A., Mauleón, I., Alegre, M., et al (2011) Sustained enzymatic correction by rAAVmediated liver gene therapy protects against induced motor neuropathy in acute porphyria mice Mol. Ther., 19, 243–250

Proliferation of hepatocytes
Lin, S., Nascimento, E.M., Gajera, C.R., Chen, L., Neuhöfer, P., Garbuzov, A., Wang, S. and Artandi, S.E. (2018) Distributed hepatocytes expressing telomerase repopulate the liver in homeostasis and injury Nature, 556, 244-248

Mueller, S., Huard, J., Waldow, K., Huang, X., D’Alessandro, L.A., Bohl, S., Börner, K., Grimm, D., Klamt, S., Klingmüller, U. and Schilling, M. (2015) T160-phosphorylated CDK2 defines threshold for HGF-dependent proliferation in primary hepatocytes Mol. Syst. Biol., 11: 795

Propionic acidaemia
Guenzel, A.J., Hofherr, S.E., Hillestad, M., Barry, M., et al (2013) Generation of a hypomorphic model of propionic acidemia amenable to gene therapy testing Mol. Ther., 21, 1316-1323

Retroviruses
Herquel, B., Ouararhni, K., Martianov, I., Le Gras, S., et al (2013) Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA Nat. Struct. Mol. Biol., 20, 339-346

miRNA disregulation
Awazawa, M., Gabel, P., Tsaousidou, E., Nolte, H., Krüger, M., Schmitz, J., Ackermann, P.J., Brandt, C., Altmüller, J. et al (2017) A microRNA screen reveals that elevated hepatic ectodysplasin A expression contributes to obesity-induced insulin resistance in skeletal muscle Nat. Med., 23, 1466-1473

Transduction efficiency
Gabriel, N., Hareendran, S., Sen, D., Gadkari, R.A., et al (2013) Bioengineering of AAV2 capsid at specific serine, threonine, or lysine residues improves its transduction efficiency in vitro and in vivo Hum. Gene Ther. Methods, 24, 80–93

Kleven, M.D., Gomes, M.M., Wortham, A.M., Enns, C.A. and Kahl, C. (2018) Ultrafiltered recombinant AAV8 vector can be safely administered in vivo and efficiently transduces liver PLoS ONE 13: e0194728

Ling, C., Lu, Y., Cheng, B., McGoogan, K.E., et al (2011) High-efficiency transduction of liver cancer cells by recombinant adeno-associated virus serotype 3 vectors J. Vis. Exp., 49, 10.3791/2538

Ling, C., Wang, Y., Lu, Y., Wang, L., Jayandharan, G.R., Aslanidi, G.V., Li, B. et al (2015) Enhanced transgene expression from recombinant single-stranded D-sequence-substituted adeno-associated virus vectors in human cell lines in vitro and in murine hepatocytes in vivo J. Virol., 89, 952-961

Loiler, S.A., Conlon, T.J., Tang, Q., Warrington, K.H., et al (2003) Targeting recombinant adeno-associated virus vectors to enhance gene transfer to pancreatic islets and liver Gene Ther., 10, 1551-1558

Montenegro-Miranda, P.S., Pañeda, A., ten Bloemendaal, L., Duijst, S., et al (2013) Adeno-associated viral vector serotype 5 poorly transduces liver in rat models PLoS One, 8: e82597

Nathwani, A.C., Cochrane, M., McIntosh, J., Ng, C.Y.C., et al (2009) Enhancing transduction of the liver by adeno-associated viral vectors Gene Ther., 16, 60–69

Mayra, A., Tomimitsu, H., Kubodera, T., Kobayashi, M., et al (2011) Intraperitoneal AAV9-shRNA inhibits target expression in neonatal skeletal and cardiac muscles Biochem. Biophys. Res. Comm., 405, 204–209

Paneda, A., Vanrell, L., Mauleon, I., Crettaz, J.S., et al (2009) Effect of adeno-associated virus serotype and genomic structure on liver transduction and biodistribution in mice of both genders Hum. Gene Ther., 20, 908-917

Raupp, C., Naumer, M., Müller, O.J., Gurda, B.L., et al (2012) The threefold protrusions of adeno-associated virus type 8 are involved in cell surface targeting as well as post-attachment processing J. Virol., 86, 9396-9408

Sen, D., Gadkari, R.A., Sudha, G., Gabriel, N., et al (2013) Targeted modifications in adeno-associated virus serotype 8 capsid improves its hepatic gene transfer efficiency in vivo Hum. Gene Ther. Methods, 24, 104–116

Tenney, R.M., Bell, C.L. and Wilson, J.M. (2014) AAV8 capsid variable regions at the two-fold symmetry axis contribute to high liver transduction by mediating nuclear entry and capsid uncoating Virology 454-455 (2014) 227–236

Wang, L., Bell, P., Somanathan, S., Wang, Q., He, Z., Yu, H., McMenamin, D., Goode, T., Calcedo, R. and Wilson, J.M. (2015) Comparative study of liver gene transfer with AAV vectors based on natural and engineered AAV capsids Mol. Ther., 23, 1877–1887

Herpes simplex helper virus

Franzoso, F.D., Seyffert, M., Vogel, R., Yakimovich, A., de Andrade Pereira, B., Meier, A.F., Sutter, S.O., Tobler, K. et al (2017) Cell cycle-dependent expression of adeno-associated virus 2 (AAV2) rep in coinfections with herpes simplex virus 1 (HSV-1) gives rise to a mosaic of cells replicating either AAV2 or HSV-1 J. Virol., 91: e00357-17

Kang, W., Wang, L., Harrell, H., Liu, J., et al (2009) An efficient rHSV-based complementation system for the production of multiple rAAV vector serotypes Gene Ther., 16, 229-239

Millet, R., Jolinon, N., Nguyen, X-N., Berger, G., Cimarelli, A., Greco, A., Bertrand, P., Odenthal, M., Büning, H. and Salvetti, A. (2015) Impact of the MRN complex on adeno-associated virus integration and replication during coinfection with herpes simplex virus J. Virol., 89, 6824-6834

Mistry, A.R., De Alwis, M., Feudner, E., Ali, R.R. and Thrasher, A.J. (2002) High-titer stocks of adenoassociated virus from replicating amplicons and herpes vectors Methods Mol. Med., 69, 445-460

Toublanc, E., Benraiss, A., Bonnin, D., Blouin, V., et al (2004) Identification of a replication-defective herpes simplex virus for recombinant adeno-associated virus type 2 (rAAV2) particle assembly using stable producer cell lines J. Gene Med., 6, 555-564

High affinity ligands

Münch, R.C., Janicki, H., Völker, I., Rasbach, A., et al (2013) Displaying high-affinity ligands on adenoassociated viral vectors enables tumor cell-specific and safe gene transfer Mol. Ther., 21, 109–118

HIV therapy

Badamchi-Zadeh, A., Tartaglia, L.J., Abbink, P., Bricault, C.A., Liu, P-T., Boyd, M., Kirilova, M., Mercado, N.B., Nanayakkara, O.S. et al (2018) Therapeutic efficacy of vectored PGT121 gene delivery in HIV-1-infectedhumanized mice J. Virol., 92: e01925-17

De Silva Feelixge, H.S., Stone, D., Pietz, H.L., Roychoudhury, P., Greninger, A.L., Schiffer, J.T., Aubert, M. and Jerome, K.R. (2016) Detection of treatment-resistant infectious HIV after genome-directed antiviral endonuclease therapy Antiviral Res., 126, 90-98

Kunze, C., Börner, K., Kienle, E., Orschmann, T., Rusha, E., Schneider, M., Radivojkov-Blagojevic, M., Drukker, M. et al (2018) Synthetic AAV/CRISPR vectors for blocking HIV-1 expression in persistently infected astrocytes Glia. 66, 413–427

Roychoudhury, P., De Silva Feelixge, H.S., Pietz, H.L., Stone, D., Jerome, K.R. and Schiffer, J.T. (2016) Pharmacodynamics of anti-HIV gene therapy using viral vectors and targeted endonucleases J. Antimicrob. Chemother., 71, 2089–2099

Hypercholesterolaemia (see Lipoprotein metabolism-related disorders”)
Hyperoxaluria (see Hepatic/hepatocyte delivery”)

Hypertension

Cataliotti, A., Tonne, J.M., Bellavia, D., Martin, F.L., et al (2011) Long-term cardiac pro-B-type natriuretic peptide gene delivery prevents the development of hypertensive heart disease in spontaneously hypertensive rats Circulation, 123, 1297-1305

Chen, P, G-F. and Sun, Z. (2017) AAV delivery of endothelin-1 shRNA attenuates cold-induced hypertension Hum. Gene Ther., 28. 190-199

Immune response/ Immune neuropathy

Aubert, D., Pichard, V., Durand, S., Moullier, P. and Ferry, N. (2003) Cytotoxic immune response after retroviral-mediated hepatic gene transfer in rat does not preclude expression from adeno-associated virus 1 transducted muscles Hum. Gene Ther., 14, 473-481

Chen, S., Kapturczak, M.H., Wasserfall, C., Glushakova, O.Y., et al (2005) Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway Proc. Natl. Acad. Sci. USA, 102, 7251-7256

Chu, Q., Moreland, R.J., Gao, L., Taylor, K.M., et al (2010) Induction of immune tolerance to a therapeutic protein by intrathymic gene delivery Mol. Ther., 18, 2146–2154

Gao, T., Bogdanova, N., Ghauri, S., Zhang, G., Lin, J. and Sheikh, K. (2018) Systemic IGF-1 gene delivery by rAAV9 improves spontaneous autoimmune peripheral polyneuropathy (SAPP) Sci. Rep., 8: 5408

Lu, Y. and Song, S. (2009) Distinct immune responses to transgene products from rAAV1 and rAAV8 vectors Proc. Natl. Acad. Sci. USA, 106, 17158–17162

Huang, J., Li, X., Coelho-dos-Reis, J.G.A., Wilson, J.M., Tsuji, M. (2014) An AAV vector-mediated gene delivery approach facilitates reconstitution of functional human CD8+ T cells in mice PLoS One, 9: e88205

Madsen, D., Cantwell, E.R., O’Brien, T., Johnson, P.A. and Mahon, B.P. (2009) Adeno-associated virus serotype 2 induces cell-mediated immune responses directed against multiple epitopes of the capsid protein VP1 J. Gen. Virol., 90, 2622–2633

Maersch, S., Huber, A., Büning, H., Hallek, M. and Perabo, L. (2010) Optimization of stealth adeno-associated virus vectors by randomization of immunogenic epitopes Virology, 397, 167–175

Mendoza, S.D., El-Shamayleh, Y. and Horwitz, G.D. (2017) AAV-mediated delivery of optogenetic constructs to the macaque brain triggers humoral immune responses J. Neurophysiol., 117, 2004–2013

Peden, C.S., Manfredsson, F.P., Reimsnider, S.K., Poirier, A.E., et al (2009) Striatal readministration of rAAV vectors reveals an immune response against AAV2 capsids that can be circumvented Mol. Ther., 17, 524–537

Rogers, G.L., Suzuki, M., Zolotukhin, I., Markusic, D.M., Morel, L.M., Lee, B., Ertl, H.C.J. and Herzog, R.F.W. (2015) Unique roles of TLR9- and MyD88-dependent and -independent pathways in adaptive immune responses to AAV-mediated gene transfer J. Innate. Immun., 7, 302–314

Rogers, G.L., Shirley, J.L., Zolotukhin, I., Kumar, S.R.P., Sherman, A., Perrin, G.Q., Hoffman, B.E., Srivastava, A., Basner-Tschakarjan, E. et al (2017) Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD81 T cells Blood, 129, 3184-3195

Rybniker, J., Nowag, A., Janicki, H., Demant, K., et al (2012) Incorporation of antigens into viral capsids augments immunogenicity of adeno-associated virus vector-based vaccines J. Virol., 86, 13800-13804

Sun, J.Y., Anand-Jawa, V., Chatterjee, S. and Wong, K.K. (2003) Immune responses to adeno-associated virus and its recombinant vectors Gene Ther., 10, 964-976

Zhang, Y.C., Powers, M., Wasserfall, C., Brusko, T., et al (2004) Immunity to adeno-associated virus serotype 2 delivered transgenes impared by genetic predisposition to autoimmunity Gene Ther., 11, 233-240

Infectivity

Excoffon, K.J.D.A., Koerber, J.T., Dickey, D.D., Murtha, M., et al (2009) Directed evolution of adenoassociated virus to an infectious respiratory virus Proc. Natl. Acad. Sci., 106, 3865–3870

Kang, W., Wang, L., Harrell, H., Liu, J., et al (2009) An efficient rHSV-based complementation system for the production of multiple rAAV vector serotypes Gene Ther., 16, 229-239

Popa-Wagner, R., Porwal, M., Kann, M., Reuss, M., et al (2012) Impact of VP1-specific protein sequence motifs on adeno-associated virus type 2 intracellular trafficking and nuclear entry J. Virol., 86, 9163-9174

Salganik, M., Venkatakrishnan, B., Bennett, A., Lins, B., et al (2012) Evidence for pH-dependent protease activity in the adeno-associated virus capsid J. Virol., 86, 11877-11885

Zeltner, N., Kohlbrenner, E., Clément, N., Weber, T., and Linden, R.M. (2010) Near-perfect infectivity of wildtype AAV as benchmark for infectivity of recombinant AAV vectors Gene Ther., 17, 872–879

Influenza virus

Sipo, I., Knauf, M., Fechner, H., Poller, W. et al (2011) Vaccine protection against lethal homologous and heterologous challenge using recombinant AAV vectors expressing codon-optimized genes from pandemic swine origin influenza virus (SOIV) Vaccine 29, 1690–1699

Inner ear delivery (see also “Cochlear delivery”)

Landegger, L.D., Pan, B., Askew, C., Wassmer, S.J., Gluck, S.D., Galvin, A., Taylor, R., Forge, A., Stankovic, K.M. et al (2017) A synthetic AAV vector enables safe and efficient gene transfer to the mammalian inner ear Nat. Biotech., 35, 280-284

Okada, H., Iizuka, T., Mochizuki, H., Nihira, T., et al (2012) Gene transfer targeting mouse vestibule using adenovirus and adeno-associated virus vectors Otol. Neurotol., 33, 655-659

Insulin growth factor etc, see “Diabetes and other pancreatic disorders”
Intervertebral disc disorders

Mern, D.S. and Thomé, C. (2015) Identification and characterization of human nucleus pulposus cell specific serotypes of adeno-associated virus for gene therapeutic approaches of intervertebral disc disorders BMC Musculoskelet. Disorders, 16: 341

Shenegelegn Mern, D., Tschugg, A., Hartmann, S. and Thome, C. (2017) Self-complementary adenoassociated virus serotype 6 mediated knockdown of ADAMTS4 induces long-term and effective enhancement of aggrecan in degenerative human nucleus pulposus cells: A new therapeutic approach for intervertebral disc disorders PloS One, 12: e0172181

Intestinal delivery

Buckinx, R., Van Remoortel, S., Gijsbers, R., Waddington, S.N. and Timmermans, J-P. (2016) Proof-ofconcept: neonatal intravenous injection of adenoassociated virus vectors results in successful transduction of myenteric and submucosal neurons in the mouse small and large intestine Neurogastroenterol. Motil., 28, 299–305

Manfredsson, F.P., Luk, K.C., Benskey, M.J., Gezer, A., Garcia, J., Kuhn, N.C., Sandoval, I.M., Patterson, J.R. et al (2018) Induction of alpha-synuclein pathology in the enteric nervous system of the rat and non-human primate results in gastrointestinal dysmotility and transient CNS pathology Neurobiol. Dis., 112, 106–118

Polyak, S., Mach, A., Porvasnik, S., Dixon, L., et al (2012) Identification of adeno-associated viral vectors suitable for intestinal gene delivery and modulation of experimental colitis Am. J. Physiol. Gastrointest. Liver Physiol., 302, G296–G308

Intracellular interactions
Molecular interactions

Nash, K., Chen, W., Salganik, M. and Muzyczka, N. (2009) Identification of cellular proteins that interact withthe adeno-associated virus Rep protein J. Virol., 83, 454-469
Trafficking

Dickey, D.D., Excoffon, K.J.D.A., Koerber, J.T., Bergen, J., et al (2011) Enhanced sialic acid-dependent endocytosis explains the increased efficiency of infection of airway epithelia by a novel adeno-associated virus J. Virol., 85, 9023–9030

Gurda, B.L., Raupp, C., Popa-Wagner, R., Naumer, M., et al (2012) Mapping a neutralizing epitope onto the capsid of adeno-associated virus serotype 8 J. Virol., 86, 7739–7751

Johnson, J.S. and Samulski, R.J. (2009) Enhancement of adeno-associated virus infection by mobilizing capsids into and out of the nucleolus J. Virol., 83, 2632-2644

Lux, K., Goerlitz, N., Schlemminger, S., Perabo, L., et al (2005) Green fluorescent protein-tagged adenoassociated virus particles allow the study of cytosolic and nuclear trafficking J. Virol., 79, 11776-11787

Nam, H-J., Gurda, B.L., McKenna, R., Potter, M., et al (2011) Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking J. Virol., 85, 11791–11799

Nonnenmacher, M.E., Cintrat, J-C., Gillet, D. and Weber, T. (2015) Syntaxin 5-dependent retrograde transport to the trans-Golgi network is required for adeno-associated

Popa-Wagner, R., Porwal, M., Kann, M., Reuss, M., et al (2012) Impact of VP1-specific protein sequence motifs on adeno-associated virus type 2 intracellular trafficking and nuclear entry J. Virol., 86, 9163-9174

Sonntag, F., Bleker, S., Leuchs, B., Fischer, R. and Kleinschmidt, J.A. (2006) Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus J. Virol., 80, 11040-11054

Stahnke, S., Lux, K., Uhrig, S., Kreppel, F., et al (2011) Intrinsic phospholipase A2 activity of adenoassociated virus is involved in endosomal escape of incoming particles Virology, 409, 77–83

Xiao, W., Warrington, K.H., Hearing, P. Hughes, J. and Muzyczka, N. (2002) Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2 J. Virol., 76, 11505-11517

Intramuscular injection

Benkhelifa-Ziyyat, S., Besse, A., Roda, M., Duque, S., Astord, S., Carcenac, R., Marais, T. and Barkats, M. (2013) Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice Mol. Ther., 21, 282–290

Chew, W.L., Tabebordbar, M., Cheng, J.K.W., Mali, P., Wu, E.Y., Ng, A.H.M., Zhu, K., Wagers, A.J. and Church, G.M. (2016) A multifunctional AAV–CRISPR–cas9 and its host response Nat. Meth., 13, 868-874

Van Lieshout, L.P., Soule, G., Sorensen, D., Frost, K.L., He, S., Tierney, K., Safronetz, D., Booth, S.A. (2018) Intramuscular adeno-associated virus–mediated expression of monoclonal antibodies provides 100% protection against Ebola virus infection in mice J. Infect. Dis., 217, 917-925

Intraperitoneal injection

Akbar, M.A., Cao, J.J., Lu, Y., Nardo, D., Chen, M-J., Elshikha, A.S., Ahamed, R., Brantly, M., Holliday, L.S. and Song, S. (2016) Alpha-1 antitrypsin gene therapy ameliorates bone loss in ovariectomy-induced osteoporosis mouse model Hum. Gene Ther., 27, 679-686

Machida, A., Kuwahara, H., Mayra, A., Kubodera, T., et al (2013) Intraperitoneal administration of AAV9- shRNA inhibits target gene expression in the dorsal root ganglia of neonatal mice Mol. Pain, 9:36

Medina-Echeverz, J., Fioravanti, J., Díaz-Valdés, N., Frank, K., et al (2014) Harnessing high density lipoproteins to block transforming growth factor beta and to inhibit the growth of liver tumor metastases PLoS One, 9: e96799

Schultze, S.M., Dietrich, M., Hynx, D., Geier, A., Niessen, M., Spinas, G.A., Hemmings, B.A. and Tschopp, O. (2015) Reduced hepatic lipid content in Pten-haplodeficient mice because of enhanced AKT2/PKBβ activation in skeletal muscle Liver Int., 35, 1354–1366

Shettigar, V., Zhang, B., Little, S.C., Salhi, H.E., Hansen, B.J., Li, N., Zhang, J., Roof, S.R., Ho, H-T., Brunello, L. et al (2016) Rationally engineered Troponin C modulates in vivo cardiac function and performance in health and disease Nat. Comm., 7: 10794

Vrontou, S., Wong, A.M., Rau, K.K., Koerber, R. and Anderson, D.J. (2013) Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo Nature, 493, 669-673

Intramuscular injection

Davis, A.S., Federici, T., Ray, W.C., Boulis, N.M., O’Connor, D., Clark, K.R. and Bartlett, J.S. (2015) Rational design and engineering of a modified adeno-associated virus (AAV1)-based vector system for enhanced retrograde gene delivery Neurosurgery, 76, 216-225

Intrathecal injection

Huda, F., Konno, A., Matsuzaki, Y., Goenawan, H., Miyake, K., Shimada, T. and Hirai, H. (2014) Distinct transduction profiles in the CNS via three injection routes of AAV9 and the application to generation of a neurodegenerative mouse model Mol. Ther. Methods Clin. Dev., 1: 14032

Ramsingh, A.I., Gray, S.J., Reilly, A., Koday, M., Bratt, D., Koday, M.T., Murnane, R., Smedley, J., Hu, Y., Messer, A. and Fuller, D.H. (2018) Sustained AAV9-mediated expression of a non-self protein in the CNS of non-human primates after immunomodulation PLoS One, 13: e0198154

Intrathoracic injection

Huang, J., Li, X., Coelho-dos-Reis, J.G.A., Wilson, J.M., Tsuji, M. (2014) An AAV vector-mediated gene delivery approach facilitates reconstitution of functional human CD8+ T cells in mice PLoS One, 9: e88205

Intratracheal injection

Vidović, D., Gijsbers, R., Quiles-Jimenez, A., Dooley, J., Van den Haute, C., Van der Perren, A., Liston, A., Baekelandt, V., Debyser, Z. and Carlon, M.S. (2016) Noninvasive imaging reveals stable transgene expression in mouse airways after delivery of a nonintegrating recombinant adeno-associated viral vector Hum. Gene Ther., 27, 60-71

Intravenous injection

The vast number of papers reporting the use of intravenous injection in rAAV studies makes such a list unhelpful; these papers are therefore listed elsewhere according to target organ or cell and/or intracellular compartment, clinical condition and/or biological/biochemical/physiological studies.

In utero administration

Chansel-Debordeaux, L., Bourdenx, M., Dovero, S., Grouthier, V., Dutheil, N., Espana, A., Groc, L., Jimenez, C., Bezard, E. and Dehay, B. (2017) In utero delivery of rAAV2/9 induces neuronal expression of the transgene in the brain: towards new models of Parkinson’s disease Gene Ther., 24, 801–809

Picconi, J.L., Muff-Luett, M.A., Wu, D., Bunchman, E., Schaefer, F. et al (2014) Kidney-specific expression of GFP by in-utero delivery of pseudotyped adeno-associated virus 9 Mol. Ther. Meth. Clin. Dev., 1: 14014

Joint delivery (see “Arthritic joint delivery”)
Keratinocyte transduction

Roedl, D., Oji, V., Buters, J.T.M., Behrendt, H. and Braun-Falco, M. (2011) rAAV2-Mediated restoration of LEKTI in LEKTI-deficient cells from Netherton patients J. Dermatol. Sci., 61, 194–198

Kidney delivery (incl. Renal fibrosis)

Asico, L.D., Cuevas, S., Ma, X., Jose, P.A., Armando, I. and Konkalmatt, P.R. (2018) Nephron segment-specific gene expression using AAV vectors Biochem. Biophys. Res. Comm., 497, 19-24

Chen, S., Agarwal, A., Glushakova, O.Y., Jorgensen, M.A., et al (2003) Gene delivery in renal tubular epithelial cells using recombinant adeno-associated viral vectors J. Am. Soc. Nephrol., 14, 947-958

Clark, K.R. (2002) Recent advances in recombinant adeno-associated virus vector production Kidney Int., 61, Sympos. 1, S9-S15

Mu, W., Ouyang, X., Agarwal, A., Zhang, L., et al (2005) IL-10 suppresses chemokines, inflammation, and fibrosis in a model of chronic disease J. Am. Soc. Nephrol., 16, 3651-3660

Mu, W., Long, D.A., Ouyang, X., Agarwal, A., et al (2009) Angiostatin overexpression is associated with an improvement in chronic kidney injury by an anti-inflammatory mechanism Am. J. Physiol. Renal. Physiol., 296: F145–F152

Picconi, J.L., Muff-Luett, M.A., Wu, D., Bunchman, E., et al (2014) Kidney-specific expression of GFP by inutero delivery of pseudotyped adeno-associated virus 9 Mol. Ther. Methods and Clin. Dev., 1: 14014

Schievenbusch, S., Strack, I., Scheffler, M., Nischt, R., et al (2010) Combined paracrine and endocrine AAV9- mediated expression of hepatocyte growth factor for the treatment of renal fibrosis Mol. Ther. 18, 1302–1309

Xie, J., Li, X., Meng, D., Liang, Q., Wang, X., Wang, L., Wang, R., Xiang, M. and Chen, S. (2016) Transduction of interleukin-10 through renal artery attenuates vascular neointimal proliferation and infiltration of immune cells in rat renal allograft Immunol. Lett., 176, 105–113

Leptin therapy (see “Obesity”)
Leptomeningeal amyloidosis

Batista, A.R., Sena-Esteves, M. and Saraiva, M.J. (2013) Hepatic production of transthyretin L12P leads to intracellular lysosomal aggregates in a new somatic transgenic mouse model Biochim. Biophys. Acta, 1832, 1183–1193

Leukaemias

Han, T., Abdel-Motal, U.M., Chang, D-K., Sui, J., et al (2012) Human anti-CCR4 minibody gene transfer for the treatment of cutaneous T-cell lymphoma PLoS One, 7: e44455

Kofler, D.M., Büning, H., Mayr, C., Bund, D., et al (2004) Engagement of the B-cell antigen receptor (BCR) allows efficient transduction of ZAP-70-positive primary B-CLL cells by recombinant adeno-associated virus (rAAV) vectors Gene Ther., 11, 1415-1424

Michelfelder, S., Lee, M-K., deLima-Hahn, E., Wilmes, T., et al (2007) Vectors selected from adeno-associated viral display peptide libraries for leukemia cell-targeted cytotoxic gene therapy Exp. Heamatol., 35, 1766-1776

Stiefelhagen, M., Sellner, L., Kleinschmidt, J.A., Jauch, A., et al (2008) Application of a haematopoetic progenitor cell-targeted adeno-associated viral (AAV) vector established by selection of an AAV random peptide library on a leukaemia cell line Genet., Vaccines Ther., 6:12

Tamai, H., Miyake, K., Yamaguchi, H., Takatori, M., et al (2012) AAV8 vector expressing IL24 efficiently suppresses tumor growth mediated by specific mechanisms in LL/AF4-positiveALL model mice Blood, 119, 64-71

Theiss, H.D., Kofler, D.M., Buning, H., Aldenhoff, A-L., et al (2003) Enhancement of gene transfer with recombinant adeno-associated virus (rAAV) vectors into primary B-cell chronic lymphocytic leukemia cells by CpG-oligodeoxynucleotides Exp. Hematol., 31, 1223-1229

Wendtner, C-M., Kofler, D.M., Theiss, H.D., Kurzeder, C., et al (2002) Efficient gene transfer of CD40 ligand into primary B-CLL cells using recombinant adeno-associated virus (rAAV) vectors Blood, 100, 1655-1661

Wendtner, C-M., Kofler, D.M., Mayr, C., Bund, D. and Hallek, M. (2004) The potential of gene transfer into primary B-CLL cells using recombinant virus vectors Leuk. Lymphoma, 45, 897-904

Leukodystrophy (metachromatic), see also Lysosomal storage disease

Iwamoto, N., Watanabe, A., Yamamoto, M., Miyake, N., et al (2009) Global diffuse distribution in the brain and efficient gene delivery to the dorsal root ganglia by intrathecal injection of adeno-associated viral vector serotype 1 J. Gene Med., 11, 498-505

Kurai, T., Hisayasu, S., Kitagawa, R., Migita, M., et al (2007) AAV1 Mediated co-expression of formylglycinegenerating enzyme and arylsulfatase A efficiently corrects sulfatide storage in a mouse model of metachromatic leukodystrophy Mol. Ther., 15, 38-43

Matalon, R., Surendran S., Rady, P.L., Quast, M.J., et al (2003) Adeno-asociated virus-mediated aspartoacylase gene transfer to the brain of knockout mouse for canavan disease Mol. Ther., 7, 580-587

Miyake, N., Miyake, K., Asakawa, N., Yamamoto, M. and Shimada, T. (2014) Long-term correction of biochemical and neurological abnormalities in MLD mice model by neonatal systemic injection of an AAV serotype 9 vector Gene Ther., 21, 427–433

Piguet, F., Sondhi, D., Piraud, M., Fouquet, F., et al (2012) Correction of brain oligodendrocytes by AAVrh.10 intracerebral gene therapy in metachromatic leukodystrophy mice Hum. Gene Ther., 23, 903–914

Life cycle (rAAV)

Zarate-Perez, F., Mansilla-Soto, J., Bardelli, M., Burgner II, J.W., et al (2013) Oligomeric properties of adenoassociated virus Rep68 reflect its multifunctionality J. Virol., 87, 1232-1241

Ligand coupling

Muik, A., Reul, J., Friedel, T., Muth, A., Hartmann, K.P., Schneider, I.C., Münch, R.C. and Buchholz, C.J. (2017) Covalent coupling of high-affinity ligands to the surface of viral vector particles by protein transsplicing mediates cell type-specific gene transfer Biomaterials, 144, 84-94

Limb ischaemia

Jazwa, A., Tomczyk, M., Taha, H.M., Hytonen, E., et al (2013) Arteriogenic therapy based on simultaneous delivery of VEGF-A and FGF4 genes improves the recovery from acute limb ischemia Vasc. Cell, 5: 13

Limbic seizures

Weinberg, M.S., Blake, B.L. and McCown, T.J. (2013) Opposing actions of hippocampus TNFα receptors on limbic seizure susceptibility Exp. Neurol., 247, 429–437

Lipid metabolism disorders

Haug, S. and Braun-Falco, M. (2005) Adeno-associated virus vectors are able to restore fatty aldehyde dehydrogenase-deficiency, implications for gene therapy in Sjögre-Larsson syndrome Arch. Dermatol. Res., 296, 568-572

Haug, S. and Braun-Falco, M. (2006) Restoration of fatty aldehyde dehydrogenase deficiency in Sjögren– Larsson syndrome Gene Ther., 13, 1021-1026

Matabosch, X., Ying, L., Serra, M., Wassif, C.A., Porter, F.D., Shackleton, C., Watson, G. (2010) Increasing cholesterol synthesis in 7-dehydrosterol reductase (DHCR7) deficient mouse models through gene transfer J. Steroid Biochem. Mol. Biol., 122, 303–309

Lipoprotein metabolism-related disorders

Bissig-Choisat, B., Wang, L., Legras, X., Saha, P.K., Chen, L., Bell, P.K., Pankowicz, F.P., Hill, M.C., Barzi, M. etal (2015) Development and rescue of human familial hypercholesterolaemia in a xenograft mouse model Nat. Commun., 6: 7339

Boesjes, M., Bloks, V.W., Hageman, J., Bos, T., van Dijk, T.H., Havinga, R., Wolters, H., Jonker, J.W., Kuipers, F. and Groen, A.K. (2014) Hepatic farnesoid X-receptor isoforms a2 and a4 differentially modulate bile salt and lipoprotein metabolism in mice PLoS One, 9: e115028

Chen, S-J., Sanmiguel, J., Lock, M., McMenamin, D. et al (2013) Biodistribution of AAV8 vectors expressing human low-density lipoprotein receptor in a mouse model of homozygous familial hypercholesterolemia Hum. Gene Ther. Clin. Dev., 24, 154-160

Craig, A.T., Gavrilova, O., Dwyer. N.K., Jou, W., et al (2009) Transduction of rat pancreatic islets with pseudotyped adeno-associated virus vectors Virol. J. 6:61

Evans, V., Foster, H., Graham, I.R., Foster, K., et al (2008) Human apoliporotein E expression from mouse skeletal muscle by electrotransfer of nonviral DNA (plasmid) and pseudotyped recombinant adeno-associated virus (AAV2/7) Hum. Gene Ther., 19, 569-578

Evans, V.C., Graham, I.R., Athanasopoulos, T., Galley, et al (2011) Adeno-associated virus serotypes 7 and 8 outperform serotype 9 in expressing atheroprotective human apoE3 from mouse skeletal muscle Metab. Clin. Exp., 60, 491–498

Harris, J.D., Schepelmann, S., Athanasopoulos, T., Graham, I.R., et al (2002) Inhibition of atherosclerosis in apolipoprotein-E-deficient mice following muscle transduction with adeno-associated virus vectors encoding human apolipoprotein-E Gene Ther., 9, 21-29

Hu, J., Liu, C-C., Chen, X-F., Zhang, Y-w., Xu, H. and Bu, G. (2015) Opposing effects of viral mediated brain expression of apolipoprotein E2 (apoE2) and apoE4 on apoE lipidation and Aβ metabolism in apoE4-targeted replacement mice Mol. Neurodegen., 10:6

Huang, Y-W.A., Zhou, B., Wernig, M. and Südhof, T.C. (2017) ApoE2, ApoE3, and ApoE4 differentially stimulate APP transcription and Ab secretion Cell 168, 427–441

Jäger, J., Greiner, V., Strzoda, D., Seibert, O., et al (2014) Hepatic transforming growth factor- 1 stimulated clone-22 D1 controls systemic cholesterol metabolism Mol. Metab., 3, 155–166

Jalkanen, J., Leppanen, P., Pajusola, K., Mahonen, A., et al (2003) Adeno-associated virus-mediated gene transfer of a secreted decoy human macrophage scavenger receptor reduces atherosclerotic lesion formation in LDL receptor knockout mice Mol. Ther., 8, 903-910

Kassim, S.H., Li, H., Bell, P., Somanathan, S., et al (2013) Adeno-associated virus serotype 8 gene therapy leads to significant lowering of plasma cholesterol levels in humanized mouse models of homozygous and heterozygous familial hypercholesterolemia Hum. Gene Ther., 24, 19–26

Koornneef, A., Maczuga, P., van Logtenstein, R., Borel, F., et al (2011) Apolipoprotein B knockdown by AAVdelivered shRNA lowers plasma cholesterol in mice Mol. Ther., 19, 731–740

Kumar, S., Kang, D-W., Rezvan, A. and Jo, H. (2017) Accelerated atherosclerosis development in C57Bl6 mice by overexpressing AAV-mediated PCSK9 and partial carotid ligation Lab. Invest., 97, 935–945

Osman, E., Graham, I., Athanasopoulos, T., Nathwani, A.C., Owen, J.S. (2007) Liver-directed gene transfer of atheroprotective human Apo-Imilano Hum.Gene Ther., 18, 967

Osman, E., Evans, V., Graham, I.R., Athanasopoulos, T., et al (2009) Preliminary evaluation of a selfcomplementary AAV2/8 vector for hepatic gene transfer of human apoE3 to inhibit atherosclerotic lesion development in apoE-deficient mice Atherosclerosis 204, 121–126

Ross, C.J.D., Twisk, J., Meulenberg, J.M., Liu, G., van den Oever, K., Moraal, E., Hermens, W.T., Rip, J., Kastelein, J.J.P., Kuivenhoven, J.A. and Hayden, M.R. (2004) Long-term correction of murine lipoprotein lipase deficiency with AAV1-mediated gene transfer of the naturally occurring LPLS447X beneficial mutation Hum. Gene Ther., 15, 906-919

Ross, C.J.D., Twisk, J., Bakker, A.C., Miao, F., Verbart, D., Rip, J., Godbey, T., Dijkhuizen, P., Hermens, W.T.J.M.C., Kastelein, J.J.P., Kuivenhoven, J.A., Meulenberg, J.M. and Hayden, M.R. (2006) Correction of feline lipoprotein lipase deficiency with adeno-associated virus serotype 1-mediated gene transfer of the lipoprotein lipase S447X beneficial mutation Hum. Gene Ther., 17, 487-499

Sharifi, B.G., Wu, K., Wang, L., Ong, J.M., et al (2005) AAV serotype-dependent apolipoprotein A-IMilano gene expression Atherosclerosis, 181, 261-269

Sun, S., Ford, T., Davis, A and Teng, B-B. (2001) Recombinant adeno-associated virus-mediated gene delivery of apolipoprotein B mRNA site-specific ribozyme Am. Soc. Gene Ther., 4th Annual Meeting Abstr. 430

Tian, F., Wang, L., Arias, A., Yang, M., Sharifi, B.G. and Shah, P.K. (2015) Comparative antiatherogenic effects of intravenous AAV8- and AAV2-mediated ApoA-IMilano gene transfer in hypercholesterolemic mice J. Cardiovasc. Pharmacol. Therapeut., 20, 66-75

Vaessen, S.F., Veldman, R.J., Comijn, E.M., Snapper, J., et al (2009) AAV gene therapy as a means to increase apolipoprotein (Apo) A-I and high-density lipoprotein-cholesterol levels: correction of murine ApoA-I deficiency J. Gene Med., 11, 697-707

Wang, L., Tian, F., Arias, A., Yang, M., Sharifi, B,G. and Shah, P.K. (2016) Comparative effects of dietinduced lipid lowering versus lipid lowering along with Apo A-I Milano gene therapy on regression of atherosclerosis J. Cardiovasc. Pharmacol. Therapeut., 21 320-328

White, K., Buning, H., Kritz, A., Janicki, H., et al (2008) Engineering adeno-associated virus 2 vectors for targeted gene delivery to atherosclerotic lesions Gene Ther., 15, 443-451

Zhong, S., Sun, S. and Teng, B-B. (2004) The recombinant adeno-associated virus vector (rAAV2)-mediated apolipoprotein B mRNA-specific hammerhead ribozyme: a self-complementary AAV2 vector improves the gene expression Genet. Vaccines Ther., 2, 1-11

Liver (see “Hepatic/hepatocyte delivery”)
Lung (see “Respiratory system delivery”)
Locus coeruleus delivery

Zhang, L., Kibaly, C., Wang, Y-J., Xu, C., Song, K.Y., McGarrah, P.W., Loh, H.H., Liu, J-G. and Law, P-Y. (2017) Src-dependent phosphorylation of l-opioid receptor at Tyr336 modulates opiate withdrawal EMBO Mol. Med., 9, 1521-1536

Lymphocyte receptor/lymph nodes

Martínez-Florensa, M., Consuegra-Fernández, M., Aranda, F., Armiger-Borràs, N., Di Scala, M., Carrasco, E., Pachón, J., Vila, J., González-Aseguinolaza, G. and Lozanoa, F. (2017) Protective effects of human and mouse soluble scavenger-like CD6 lymphocyte receptor in a lethal model of polymicrobial sepsis Antimicrob. Agents Chemother., 61: e01391-16

Perrin, G.Q., Zolotukhin, I., Sherman, A., Biswas, M., de Jong, Y.P., Terhorst, C., Davidoff, A.M. and Herzog, R.W. (2016) Dynamics of antigen presentation to transgene product-specific CD4+T cells and of Treg induction upon hepatic AAV gene transfer Mol. Ther. Meth. Clin. Devel., 3: 16083

Lysine residues, surface

Li, B., Ma, W., Ling, C., Van Vliet, K., Huang, L-Y., Agbandje-McKenna, M., Srivastava, A. and Aslanidi, G.V. (2015) Site-directed mutagenesis of surface-exposed lysine residues leads to improved transduction by AAV2, but not AAV8, vectors in murine hepatocytes in vivo Hum. Gene Ther. Methods 26, 211-220

Lysosomal storage diseases

Alméciga-Díaz, C.J., Montanõ, A.M., Tomatsu, S. and Barrera, L.A. (2010) Adeno-associated virus gene transfer in Morquio A disease – effect of promoters and sulfatase-modifying factor 1 FEBS J., 277, 3608–3619

Cavalca E., Cesani, M., Gifford, J.C., Sena-Esteves, M., Terreni, M.R., Leoncini, G., Peviani, M. and Biffi, A. (2018) Metallothioneins are neuroprotective agents in lysosomal storage disorders Ann. Neruol., 83, 418–432

Cresawn, K.O., Fraites, T.J., Wasserfall, C., Atkinson, M., et al (2005) Impact of humoral immune response on distribution and efficacy of recombinant adeno-associated virus-derived -glucosidese in a model of glycogen storage disease type II Hum. Gene Ther., 16, 68-80

Cressant, A., Desmaris, N., Verot, L., Brejot, T., et al (2004) Improved behavior and neuropathology in the mouse model of Sanfilippo type IIIb disease after adeno-associated virus-mediated gene transfer in the striatum J. Neurosci., 24, 10229-10239

Daly, T.M., Ohlemiller, K.K., Roberts, M.S., Vogler, C.A. and Sands, M.S. (2001) Prevention of systemic clinical disease in MPS VII mice following AAV-mediated neonatal gene transfer Gene Ther., 8, 1291-1298

Desmaris, N., Verot, L., Puech, J.P., Caillaud, C., et al (2004) Prevention of neuropathology in the mouse model of Hurler syndrome Ann. Neurol., 56, 68-76

Ellinwood, N.M., Ausseil, J., Desmaris, N., Bigou, S., et al (2011) Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes Mol. Ther., 19, 251–259

Ferla, R., Alliegro, M., Marteau, J-B., Dell’Anno, M., Nusco, E., Pouillot, S., Galimberti, S., Valsecchi, M.G., Zuliani, V. and Auricchio, A. (2017) Non-clinical safety and efficacy of an AAV2/8 vector administered intravenously for treatment of mucopolysaccharidosis Type VI Mol. Ther. Meth. Clin. Dev., 6, 143-158

Foley, J.W., Bercury, S.D., Finn, P., Cheng, S.H., et al (2010) Evaluation of systemic follistatin as an adjuvant to stimulate muscle repair and improve motor function in Pompe mice Mol. Ther., 9, 1584–1591

Ghosh, A., Allamarvdasht, M., Pan, C-J., Sun, M-S., et al (2006) Long-term correction of murine glycogen storage disease type Ia by recombinant adeno-associated virus-1-mediated gene transfer Gene Ther., 13, 321-329

Gilkes, J.A., Bloom, M.D. and Heldermon, C.D. (2016) Preferred transduction with AAV8 and AAV9 via thalamic administration in the MPS IIIB model: A comparison of four rAAV serotypes Mol. Genet. Metab. Rep. 6, 48–54

Golebiowski, D., van der Bom, I.M.J., Kwon, C-S., Miller, A.D., Petrosky, K., Bradbury, A.M., Maitland, S., Kühn, A.L., Bishop, N. et al (2017) Direct intracranial injection of AAVrh8 encoding monkey β-Nacetylhexosaminidase causes neurotoxicity in the primate brain Hum. Gene Ther., 28, 510-522

Gray-Edwards, H.L., Gross, A.L., Randle, A.N., Taylor, A., Brunson, B.L., Murdock, B., Stoica, L., Todessa, S., Lata, J., Sena-Esteves, M. and Martin, D.R. (2016) Pre-clinical optimization of AAV gene therapy in a feline model of GM1 gangliosidosis Hum. Gene Ther., 27, A50

Hartung, S.D., Frandsen, J.L., Pan, D., Koniar, B.L., et al (2004) Correction of metabolic, craniofacial, and neurologic abnormalities in MPS I mice treated at birth with adeno-associated virus vector transducing the human a-L-iduronidase gene Mol. Ther., 9, 866-875

Hennig, A.K., Ogilivie, J.M., Ohlemiller, K.K., Timmers, A.M., et al (2004) AAV-mediated intravitreal gene therapy reduces lysosomal storage in the retinal pigmented epithelium and improves retinal function in adult MPS VII mice Mol. Ther., 10, 106-116

Hinderer, C., Bell, P., Gurda, B.L., Wang, Q., Louboutin, J-P., Zhu, Y., Bagel, J., O’Donnell, P., Sikorac, T., Ruane, T., Wang, P., Haskins, M.E. and Wilson, J.M. (2014) Liver-directed gene therapy corrects cardiovascular lesions in feline mucopolysaccharidosis type I Proc. Natl. Acad. Sci. USA, 111, 14894–14899

Hinderer, C., Bell, P., Louboutin, J-P., Zhu, Y., Yu, H., Lin, G., Choa, R., Gurda, B.L. et al (2015) Neonatal systemic AAV induces tolerance to CNS gene therapy in MPS I dogs and nonhuman primates Mol. Ther., 23, 1298-1307

Hinderer, C., Katz, N., Louboutin, J-P., Bell, P., Yu, H., Nayal, M., Kozarsky, K., O’Brien, W.T., Goode, T. and Wilson, J.M. (2016) Delivery of an adeno-associated virus vector into cerebrospinal fluid attenuates central nervous system disease in mucopolysaccharidosis Type II mice Hum. Gene Ther., 27, 906-915

Ho, T.T., Maguire, A.M., Aguirre, G.D., Surace, E.M., et al (2002) Phenotypic rescue after adeno-associated virus-mediated delivery of 4-sulfatase to the retinal pigment epithelium of feline mucopolysaccharidosis VI J. Gene Med., 4, 613-621

Hurlbut, G.D., Ziegler, R.J., Nietupski, J.B., Foley, J.W., et al (2010) Preexisting immunity and low expression in primates highlight translational challenges for liver-directed AAV8-mediated gene therapy Mol. Ther., 18, 1983–1994

Kurai, T., Hisayasu, S., Kitagawa, R., Migita, M., et al (2007) AAV1 Mediated co-expression of formylglycinegenerating enzyme and arylsulfatase A efficiently corrects sulfatide storage in a mouse model of metachromatic leukodystrophy Mol. Ther., 15, 38-43

Miller, D.G., Wang, P-R., Petek, L.M., Hirata, R.K., et al (2006) Gene targeting in vivo by adeno-associated virus vectors Nat. Biotechnol., 24, 1022-1026

Miyake, N., Miyake, K., Asakawa, N., Yamamoto, M. and Shimada, T. (2014) Long-term correction of biochemical and neurological abnormalities in MLD mice model by neonatal systemic injection of an AAV serotype 9 vector Gene Ther., 21, 427–433

Qiu, K., Falk, D.J., Reier, P.R., Byrne, B.J. and Fuller, D.D. (2012) Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice Mol. Ther., 20, 21–27

Sondhi, D., Scott, E.C., Chen, A., Hackett, N.R., et al (2014) Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adenoassociated virus serotype rh.10 vector expressing the human CLN3 gene Hum. Gene Ther., 25, 223–239

Sun, B., Chen, Y-T., Bird, A., Xu, F., et al (2003) Packaging of an AAV vector encoding human acid a– glucosidase for gene therapy in glycogen storage disease type II with a modified hybrid adenovirus-AAV vector Mol. Ther., 7, 467-477

Sun, B., Zhang, H., Franco, L.M., Young, S.P., et al (2005) Efficacy of an adeno-associated virus 8- pseudotyped vector in glycogen storage disease type II Mol. Ther., 11, 57-65

Sun, M-S., Pan, C-J., Shieh, J-J., Ghosh, A., et al (2002) Sustained hepatic and renal glucose-6-phosphatase expression corrects glycogen storage disease type Ia in mice Hum. Mol. Genet., 11, 2155-2164

Sun, T., Yi, H., Yang, C., Kishnani, P.S. and Sun, B. (2016) Starch binding domain containing protein 1 plays a dominant role in glycogen transport to lysosomes in liver J. Biol. Chem., 291, 16479–16484

Tardieu, M., Zérah, M., Husson, B., de Bournonville, S., Deiva, K., Adamsbaum, K., Vincent, F., Hocquemiller, M., Broissand, C., Furlan, V. et al (2014) Intracerebral administration of adeno-associated viral vector Serotype rh.10 carrying human SGSH and SUMF1 cDNAs in children with muco-polysaccharidosis type IIIA disease: results of a phase I/II trial Hum. Gene Ther., 25, 506–516

Winner, L.K., Beard, H., Hassiotis, S., Lau, A.A., Luck, A.J., Hopwood, J.J. and Hemsley, K.M. (2016) A preclinical study evaluating AAVrh10-based gene therapy for Sanfilippo syndrome Hum. Gene Ther., 27, 363-375

Wolf, D.A., Lenander, A.W., Nan, Z., Belur, L.R., et al (2011 Direct gene transfer to the CNS prevents emergence of neurologic disease in a murine model of mucopolysaccharidosis type I Neurobiol. Dis., 43, 123–133

Yi, H., Fredrickson, K.B., Das, S., Kishnani, P.S. and Sun, B. (2013) Stbd1 is highly elevated in skeletal muscle of Pompe disease mice but suppression of its expression does not affect lysosomal glycogen accumulation Mol. Genet. Metab., 109, 312–314

Yi, H., Zhang, Q., Brooks, E.D., Yang, C., Thurberg, B.L., Kishnani, P.S. and Sun, B. (2017) Systemic correction of murine glycogen storage disease type IV by an AAV-mediated gene therapy Hum. Gene Ther., 28, 286-294

Yoon, S.Y., Bagel, J.H., O’Donnell, P., Vite, C.H. and Wolfe, J.H. (2016) Clinical improvement of alphamannosidosis cat following a single cisterna magna infusion of AAV1 Mol. Ther., 24, 26-33

Zhu, Y., Jiang, J-L., Gumlaw, N.K., Zhang, J., et al (2009) Glycoengineered acid α-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of Pompe disease Mol. Ther., 17, 954-963

Lysosomal aggregation

Batista, A.R., Sena-Esteves, M. and Saraiva, M.J. (2013) Hepatic production of transthyretin L12P leads to intracellular lysosomal aggregates in a new somatic transgenic mouse model Biochim. Biophys. Acta, 1832, 1183–1193

Malaria immunity

Huang, J., Li, X., Coelho-dos-Reis, J.G.A., Zhang, M., Mitchell, R., Nogueira, R.T., Tsao, T. et al (2015) Human immune system mice immunized with Plasmodium falciparum circumsporozoite protein induce protective human humoral immunity against malaria J. Immunol. Methods, 427, 42–50

Mammary gland

Wagner, S., Thresher, R., Bland, R. and Laible, G. (2015) Adeno-associated-virus-mediated transduction of the mammary gland enables sustained production of recombinant proteins in milk Sci. Rep., 5: 15115

MagaTAL nuclease

Sather, B.D., Romano Ibarra, G.S., Sommer, K., Curinga, G., Hale, M., Khan, I.F., Singh, S., Song, Y. et al (2015) Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template Sci. Transl. Med., 7: 307ra156

Metabotropic glutamate receptor

O’Riordan, K., Gerstein, H., Hullinger, R. and Burger, C. (2014) The role of Homer1c in metabotropic glutamate receptor-dependent long-term potentiation Hippocampus, 24, 1-6

MHC gene regulation

Neerincx, A., Jakobshagen, K., Utermöhlen, O., Büning, H., Steimle, V. and Kufer, T.A. (2014) The N-terminal domain of NLRC5 confers transcriptional activity for MHC class I and II gene expression J. Immunol., 193, 3090–3100

Mitochondrial defects

Beattie, S.G., Goetzman, E., Tang, Q., Conlon, T., et al (2008) Recombinant adeno-associated virus-mediated gene delivery of long chain acyl coenzyme A dehydrogenase (LCAD) into LCAD-deficient mice J. Gene Med., 10, 1113-1123

Conlon, T.J., Walter, G., Owen, R., Cossette, T., et al (2006) Systemic correction of a fatty acid oxidation defect by intramuscular injection of a recombinant adeno-associated virus vector Hum. Gene Ther., 17, 71-80

Doucet-Beaupré, H., Gilbert, C., Profes, M.S., Chabrat, A., Pacelli, C., Giguère, N., Rioux, V., Charest, J., Deng, Q. et al (2016) Lmx1a and Lmx1b regulate mitochondrial functions and survival of adult midbrain dopaminergic neurons Proc. Natl. Acad. Sci. USA, 111, E4387-E4396

Erger, K.E., Conlon, T.J., Leal, N.A., Zori, R., et al (2007) In vivo expression of human ATP:cob(I)alamin adenosyltransferase (ATR) using recombinant adeno-associated virus (rAAV) serotypes 2 and 8 J. Gene Med., 9, 462-469

Han, Z., Berendzen, K., Zhong, L., Surolia, I., et al (2008) A combined therapeutic approach for pyruvate dehydrogenase deficiency using self-complementary adeno-associated virus serotype-specific vectors and dichloroacetate Mol. Gen. Metabol., 93, 381-387

Kubodera, T., Yamada, H., Anzai, M., Ohira, S., et al (2011) In vivo application of an RNAi strategy for the selective suppression of a mutant allele Hum. Gene. Ther., 22, 27-34

Qi, X., Lewin, A.S., Sun, L., Hauswirth, W.W. and Guy, J. (2004) SOD2 gene transfer protects against optic neuropathy induced by deficiency of complex I Ann. Neurol., 56, 182-191

Seo, B.B., Wang, J.M., Flotte, T.R., Yagi, T. and Matsuno-Yagi, A. (2000) Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex I defects in human cells J. Biol. Chem., 275, 37774-37778

Seo, B.B., Nakamaru-Ogiso, E., Cruz, P., Flotte, T.R., et al (2004) Functional expression of the single subunit NADH dehydrogenase in mitochondria in vivo: a potential therapy for complex I deficiencies Hum. Gene Ther., 15, 887-895

Tang, F-L., Liu, W., Hu, J-X., Erion, J.R., Ye, J., Mei, L. and Xiong, W-C. (2015) VPS35 deficiency or mutation causes dopaminergic neuronal loss by impairing mitochondrial fusion and function Cell Rep., 12, 1631–1643

Yu, H., Koilkonda, R.D., Chou, T-H., Porciatti, V., et al (2012) Gene delivery to mitochondria by targeting modified adenoassociated virus suppresses Leber’s hereditary optic neuropathy in a mouse model Proc. Natl. Acad. Sci. USA, 109, E1238–E1247

Multiple sclerosis

Keeler, G.D., Kumar, S., Palaschak, B., Silverberg, E.L., Markusic, D.M., Jones, N.T. and Hoffman, B.E. (2018) Gene therapy-induced antigen-specific Tregs inhibit neuro-inflammation and reverse disease in a mouse model of multiple sclerosis Mol. Ther., 26, 173-183

Muscular dystrophy (see “Skeletal muscle delivery”)
Mucopolysaccharidosis (see “Lysosomal storage diseases”)
Myelin basic proteins

Aggarwal1, S., Snaidero, N., Pähler, G., Frey, S., et al (2013) Myelin membrane assembly is driven by a phase transition of myelin basic proteins into a cohesive protein meshwork PLoS Biol., 11: e1001577

Myocardial infarction

Prasad, K-M.R., Smith, R.S., Xu, Y., French, B.A. (2011) A single direct injection into the left ventricular wall of an adeno-associated virus 9 (AAV9) vector expressing extracellular superoxide dismutase from the cardiac troponin-T promoter protects mice against myocardial infarction J. Gene Med., 13, 333–341

Sun, F., Li, X., Duan, W-Q., Tian, W., Gao, M., Yang, J., Wu, X-Y., Huang, D. et al (2017) Transforming growth factor-β receptor III is a potential regulator of ichemia-induced cardiomyocyte apoptosis J. Am. Heart Assoc., 6: e005357

Nanodes (virus)

Ho, M.L., Judd, J., Kuypers, B.E., Yamagami, M., Wong, F.F. and Suh, J. (2014) Efficiency of proteaseactivatable virus nanonodes tuned through incorporation of wild type capsid subunits Cell. Mol. Bioeng., 7, 334–343

Nanoparticle binding

Musick, M.A., McConnell, K.I., Lue, J.K., Wei, F., Chen, C. and Suh, J. (2011) Reprogramming virus nanoparticles to bind metal ions upon activation with heat Biomacromolecules, 12, 2153–2158

Wei, F., McConnell, K.I., Yu, T-K. and Suh, J. (2012) Conjugation of paclitaxel on adeno-associated virus (AAV) nanoparticles for co-delivery of genes and drugs Eur. J. Pharm. Sci., 46, 167–172

Neonatal cardiopathy

Mearini, G., Stimpel, D., Geertz, B., Weinberger, F., Krämer, E., Schlossarek, S., Mourot-Filiatre, J. et al (2014) Mybpc3 gene therapy for neonatal cardiomyopathy enables long-term disease prevention in mice Nature Comm., 5: 5515

Neovascularization

Igarashi, T., Miyake, K., Masuda, I., Takahashi, H. and Shimada, T. (2010) Adeno-associated vector (type 8)- mediated expression of soluble Flt-1 efficiently inhibits neovascularization in a murine choroidal neovascularization model Hum. Gene Ther., 21, 631-637

Pinkenburg, O., Pfosser, A., Hinkel, R., Böttcher, M., et al C. (2009) Recombinant adeno-associated virusbased gene transfer of cathelicidin induces therapeutic neovascularization preferentially via potent collateral growth Hum Gene Ther., 20,159–167

Nephron segment: see “Kidney delivery”
Neutralizing antibodies

Rapti, K., Louis-Jeune, V., Kohlbrenner, E., Ishikawa, K., et al (2012) Neutralizing antibodies against AAV serotypes 1, 2, 6, and 9 in sera of commonly used animal models Mol. Ther., 20, 73–83

Nicotine withdrawal

Grieder, T.E., Herman, M.A., Contet, C., Tan, L.A., Vargas-Perez, H., Cohen, A., Chwalek, M., Maal-Bared, G. et al (2014) VTA CRF neurons mediate the aversive effects of nicotine withdrawal and promote intake escalation Nat. Neurosci., 17, 1751-1758

Non-human primate administration

Gray, S.J., Kalburgi, S,N., McCown, T.J. and Samulski, R.J. (2013) Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates Gene Ther., 20, 450–459

Hinderer, C., Bell, P., Louboutin, J-P., Zhu, Y., Yu, H., Lin, G., Choa, R., Gurda, B.L. et al (2015) Neonatal systemic AAV induces tolerance to CNS gene therapy in MPS I dogs and nonhuman primates Mol. Ther., 23, 1298-1307

Ramsingh, A.I., Gray, S.J., Reilly, A., Koday, M., Bratt, D., Koday, M.T., Murnane, R., Smedley, J., Hu, Y., Messer, A. and Fuller, D.H. (2018) Sustained AAV9-mediated expression of a non-self protein in the CNS of non-human primates after immunomodulation PLoS One, 13: e0198154

Nuclear interactions/translocation

Gomez, E.J., Gerhardt, K., Judd, J., Tabor, J.J. and Suh, J. (2016) Light-activated nuclear translocation of adeno-associated virus nanoparticles using phytochrome B for enhanced, tunable, and spatially programmable gene delivery ACS Nano, 10, 225−237

Nicolson, S.C. and Samulski, R.J. (2014) Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus J. Virol., 88, 4132–4144

Santamaria, M., Pardo–Saganta, A., Alvarez–Asiain, L., Di Scala, M., et al (2013) Nuclear 1- antichymotrypsin promotes chromatin condensation and inhibits proliferation of human hepatocellular carcinoma cells Gastroenterology, 144, 818-828

Tenney, R.M., Bell, C.L. and Wilson, J.M. (2014) AAV8 capsid variable regions at the two-fold symmetry axis contribute to high liver transduction by mediating nuclear entry and capsid uncoating Virology 454-455 (2014) 227–236

Nucleus pulposus cells

Shenegelegn Mern, D., Tschugg, A., Hartmann, S. and Thome, C. (2017) Self-complementary adenoassociated virus serotype 6 mediated knockdown of ADAMTS4 induces long-term and effective enhancement of aggrecan in degenerative human nucleus pulposus cells: A new therapeutic approach for intervertebral disc disorders PloS One, 12: e0172181

Obesity (including leptin therapy)

Bagnasco, M., Dube, M.G., Kalra, P.S. and Kalra, S.P. (2002) Evidence for the existence of distinct central appetite, energy expenditure, and ghrelin stimulation pathways as revealed by hypothalamic site-specific leptin gene therapy Endocrinology, 143, 4409-4421

Boender, A.J., Koning, N.A., van den Heuvel, J.K., Luijendijk, M.C.M., et al (2014) AAV-mediated gene transfer of the obesity-associated gene Etv5 in rat midbrain does not affect energy balance or motivated behavior PLoS One, 9: e94159

Dhillon, H., Ge, Y-L., Minter, R.M., Prima, V., et al (2000) Long-term differential modulation of genes encoding orexigenic and anorexigenic peptides by leptin delivered by rAAV vector in ob/ob mice Regul. Pept., 92, 97-105

Dhillon, H., Kalra, S.P., Prima, V., Zolotukhin, S., et al (2001) Central leptin gene therapy suppresses body weight gain, adiposity and serum insulin without affecting food consumption in normal rats Regul. Pept., 99, 69-77

Dhillon, H., Kalra, S.P. and Kalra, P.S. (2001) Dose-dependent effects of central leptin gene therapy on genes that regulate body weight and appetite in the hypothalamus Mol. Ther., 4, 139-145

Dube, M.G., Beretta, E., Dhillon, H., Ueno, N., et al (2002) Central leptin gene therapy blocks high-fat dietinduced weight gain, hyperleptinemia, and hyperinsulinemia Diabetes, 51, 1729-1736

Fernandez-Cachona, M.L., Pedersen, S.L., Rigbolt, K.T., Zhang, C., Fabricius, K., Hansen, H.H., Elster, L. Fink, L.N., Schäfer, M. et al (2018) Guanylin and uroguanylin mRNA expression is increased following Rouxen-Y gastric bypass, but guanylins do not play a significant role in body weight regulation and glycemic control Peptides, 101, 32–43

Galon-Tilleman, H., Yang, H., Bednarek, M.A., Spurlock, S.M., Paavola, K.J., Ko, B., To, C., Luo, J. et al (2017) Apelin-36 modulates blood glucose and body weight independently of canonical APJ receptor signaling J. Biol. Chem., 292, 1925–1933

Gardiner, J.V., Kong, W.M., Ward, H., Murphy, K.G., et al (2005) AAV mediated expression of anti-sense neuropeptide Y cRNA in the arcuate of rats results in decreased weight gain and food intake Biochem. Biophys. Res. Commun., 327, 1088-1093

Ge, X., Yang, H., Bednarek, M.A., Galon-Tilleman, H., Chen, P., Chen, M., Lichtman, J.S., Wang, Y. et al (2018) LEAP2 is an endogenous antagonist of the ghrelin receptor Cell Metab., 27, 461–469

Gruber, S., Straub, B.K., Ackermann, J., Wunderlich, C.M., et al (2013) Obesity promotes liver carcinogenesis via Mcl-1 stabilization independent of IL-6Ra signaling Cell Rep., 4, 669–680

Hayes, M.R., Skibicka, K.P., Leichner, T.M., Guarnieri, D.J., et al (2010) Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation Cell Metab., 11, 77–83

He, W., Lam, T.K.T., Obici, S. and Rossetti, L. (2006) Molecular disruption of hypothalamic nutrient sensing induces obesity Nat. Neurosci., 9, 227-233

Hommel, J.D., Trinko, R., Sears, R.M., Georgescu, D., et al (2006) Leptin receptor signaling in midbrain dopamine neurons regulates feeding Neuron, 51, 801-810

Kanoski, S.E., Zhao, S., Guarnieri, D.J., DiLeone, R.J., Yan, J., De Jonghe, B.C., Bence, K.K., Hayes, M.R. and Grill, H.J. (2012) Endogenous leptin receptor signaling in the medial nucleus tractus solitarius affects meal size and potentiates intestinal satiation signals Am. J. Physiol. Endocrinol. Metab., 303, E496–E503

Kas, M.J.H., Tiesjema, B., van Dijk, G., Garner, K.M., et al (2004) Induction of brain region-specific forms of obesity by Agouti J. Neurosci., 24, 10176-10181

Lecklin, A., Dube, M.G., Torto, R.N., Kalra, P.S. and Kalra, S.P. (2005) Perigestational suppression of weight gain with central leptin gene therapy results in lower weight F1 generation Peptides, 26, 1176-1187

Manfredsson, F.P., Tumer, N., Erdos, B., Landa, T., et al (2009) Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity Mol. Ther., 17, 980-991

Platt, T.L., Beckett, T.L., Kohleer, Niedowicz, K.D.M. and Murphy, M.P. (2016) Obesity, diabetes, and leptin resistance promote tau pathology in a mouse model of disease Neuroscience 315, 162–174

Prima, V., Tennant, M., Gorbatyuk, O.S., Muzyczka, N., et al (2004) Differential modulation of energy balance by leptin, ciliary neurotrophic factor, and leukemia inhibitory factor gene delivery: microarray deoxyribonucleic acid-chip analysis of gene expression Endocrinology, 145, 2035-2045

Qi, Y., Purtell, L., Fu, M., Zhang, L., Zolotukhin, S., Campbell, L. and Herzog, H. (2017) Hypothalamus Specific re-introduction of SNORD116 into otherwise Snord116 deficient mice increased energy expenditure J. Neuroendocrinol., 29: 10.1111/jne.12457

Scarpace, P.J., Matheny, M., Zhang, Y., Tumer, N., et al (2002) Central leptin gene delivery evokes persistent leptin signal transduction in young and aged-obese rats but physiological responses become attenuated over time in aged-obese rats Neuropharmacology, 42, 548-561

Scarpace, P.J., Matheny, M., Zhang, Y., Shek, E.W., et al (2002) Leptin-induced leptin resistance reveals separate roles for the anorexic and thermogenic responses in weight maintenance Endocrinology, 143, 3026-3035

Siu, J.J., Queen, N.J., Liu, X., Huang, W., McMurphy, T. and Cao, L. (2017) Molecular therapy of melanocortin-4-receptor obesity by an autoregulatory BDNF vector Mol. Ther: Meth. Clin. Dev., 7, 83-95

Tümer, N., Scarpace, P.J., Dogan, M.D., Broxson, C.S., et al (2006) Hypothalamic rAAV-mediated GDNF gene delivery ameliorates age-related obesity Neurobiol. Aging, 27, 459-470

Van Gestel, M.A., Sanders, L.E., de Jong, J.W., Luijendijk, M.C.M. and Adan, J.A.H. (2014) FTO knockdown in rat ventromedial hypothalamus does not affect energy balance Physiol. Rep., 2: e12152

Wilsey, J., Zolotukhin, S., Prima, V. and Scarpace, P.J. (2003) Central leptin gene therapy fails to oversome leptin resistance associated with diet-induced obesity Am. J. Physiol. Regul. Interg. Comp. Physiol., 285, R1101-R1020

Optical dysfunction

Achromatopsia
Banin, E., Gootwine, E., Obolensky, A., Ezra-Elia, R., Ejzenberg, A., Zelinger, L., Honig, H., Rosov, A. et al (2015) Gene augmentation therapy restores retinal function and visual behavior in a sheep model of CNGA3 achromatopsia Mol. Ther., 23, 1423–1433

Gootwine, E., Ofri, R., Banin, E., Obolensky, A., Averbukh, E., Ezra-Elia, R., Ross, M., Honig, H., Rosov, A. et al (2017) Safety and efficacy evaluation of rAAV2tYF-PR1.7-hCNGA3 vector delivered by subretinal injection in CNGA3 mutant achromatopsia sheep Hum. Gene Ther. Clin. Dev. 28, 96-107

Michalakis, S., Mühlfriedel, R., Tanimoto, N., Krishnamoorthy, V., et al (2012) Gene therapy restores missing cone-mediated vision in the CNGA3 −/− mouse model of achromatopsia In Retinal degenerative diseases: Advances in experimental medicine and biology, vol. 723 (eds. LaVail, M.M. et al) Springer Science+Business Media, LLC, pp 183-189

Schön, C., Asteriti, S., Koch, S., Sothilingam, V., Garrido, N.G., Tanimoto, N., Herms, J., Seeliger, M.W., Cangiano, L., Biel, M. and Michalakis, S. (2016) Loss of HCN1 enhances disease progression in mouse models of CNG channel-linked retinitis pigmentosa and achromatopsia Hum. Mol. Genet., 25, 1165–1175

Schön, C., Becirovic, E., Biel, M. and Michalakis, S. (2018) Design and development of AAV-based gene supplementation therapies for achromatopsia and retinitis pigmentosa In Retinal Gene Therapy: Methods and Protocols, Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media, LLC New York 33-46

Ye, G-J., Budzynski, E., Sonnentag, P., Nork, T.M., Sheibani, N., Gurel, Z., Boye, S.L., Peterson, J.J., Boye, S.E., Hauswirth, W.W. and Chulay, J.D. (2016) Cone-specific promoters for gene therapy of achromatopsia and other retinal diseases Hum. Gene Ther., 27, 72-82

Ancestral rAAVs, targeting of
Zinn, E., Pacouret, S., Khaychuk, V., Turunen, H.T., Carvalho, L.S., Andres-Mateos, E., Shah, S. Shelke, R. et al (2015) In silico reconstruction of the viral evolutionary lineage yields a potent gene therapy vector Cell Rep., 12, 1056–1068

Angiogenesis
Joyal, J-S., Sun, Y., Gantner, M.L., Shao, Z., Evans, L.P., Saba, N., Fredrick, T., Burnim, S., Kim, J.S., Pate, G., Juan, A.M. et al (2016) Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1 Nat. Med., 22, 439-445

Sun, Y., Lin, Z., Liu, C-H., Gong, Y., Liegl, R., Fredrick, T.W., Meng, S.S., Burnim, S.B., Wang, Z. et al (2017) Inflammatory signals from photoreceptor modulate pathological retinal angiogenesis via c-Fos J. Exp. Med., 214, 1753–1767

AIPL1 mutations
Sun, X., Pawlyk, B., Xu, X., Liu, X., Bulgakov, O.V., Adamian, M., Sandberg, M.A., Khani, S.C., Tan, M-H., Smith, A.J., Ali, R.R. and Li, T. (2010) Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations Gene Ther., 17, 117–131

Axonal degeneration/growth/misguidance

Koch, J.C., Tönges, L., Barski, E., Michel, U., et al (2014) ROCK2 is a major regulator of axonal degeneration, neuronal death and axonal regeneration in the CNS Cell Death Dis., 5: e1225

Koch, J.C., Solis, G.P., Bodrikov, V., Michel, U., Haralampieva, D., Shypitsyna, A., Tönges, L., Bähr, M., Lingor, P. and Stuermer, C.A.O. (2013) Upregulation of reggie-1/flotillin-2 promotes axon regeneration in the rat optic nerve in vivo and neurite growth in vitro Neurobiol. Dis., 51, 168–176

Pernet, V., Joly, S., Dalkara, D., Jordi, N., et al (2013) Long-distance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve Neurobiol. Dis., 51, 202–213

Planchamp, V., Bermel, C., Tönges, L., Ostendorf, T., et al (2008) BAG1 promotes axonal outgrowth and regeneration in vivo via Raf-1 and reduction of ROCK activity Brain 131, 2606-2619

Bardet-Biedl syndrome
Seo, S., Mullins, R.F., Dumitrescu, A.V., Bhattarai, S., et al (2013) Subretinal gene therapy of mice with Bardet-Biedl syndrome type 1 Invest. Ophthalmol. Vis. Sci., 54, 6118–6132

Bipolar cells
Cronin, T., Vandenberghe, L.H., Hantz, P., Juttner, J., Reimann, A., Kacso, A.E., Huckfeldt, R.M., Busskamp. V., Kohler, H., Lagali, P.S. et al (2014) Efficient transduction and optogenetic stimulation of retinal bipolar cells by a synthetic adeno-associated virus capsid and promoter EMBO Mol. Med., 6, 1175-1190

De Silva, S.R., Charbel Issa, P., Singh, M.S., Lipinski, D.M., Barnea-Cramer, A.O., Walker, N.J. Barnard, A.R., Hankins, M.W. and MacLaren, R.E. (2016) Single residue AAV capsid mutation improves transduction of photoreceptors in the Abca4-/- mouse and bipolar cells in the rd1 mouse and human retina ex vivo Gene Ther., 23, 767–774

Ciliary neurotrophic factor
Pernet, V., Joly, S., Dalkara, D., Jordi, N., Schwarz, O., Christ, F., Schaffer, D.V., Flannery, J.G. and Schwab, M.E. (2013) Long-distance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve Neurobiol. Dis., 51, 202–213

Channel rhodopsin 2
Sengupta, A., Chaffiol, A., Macé, E., Caplette, R., Desrosiers, M., Lampič, M., Forster, V., Marre, O. Lin, J.Y. et al (2016) Red-shifted channel rhodopsin stimulation restores light responses in blind mice, macaque retina, and human retina EMBO Mol. Med., 8, 148-1264

Choroideremia
Patrício, M.I., Barnard, A.R., Cox, C.I., Blue, C. and MacLaren, R.E. (2018) The biological activity of AAV vectors for choroideremia gene therapy can be measured by in vitro prenylation of RAB6A Mol. Ther. Meth. Clin. Dev., 9, 288-295

Cone vision/opsins/promoters/viability factor
Li, Q., Timmers, A.M., Guy, J., Pang, J. and Hauswirth, W.W. (2008) Cone-specific expression using a human red opsin promoter in recombinant AAV Vision Res., 48, 332-338

Masseck, O.A., Spoida, K., Dalkara, D., Maejima, T., et al (2014) Vertebrate cone opsins enable sustained and highly sensitive rapid control of Gi/o signaling in anxiety circuitry Neuron 81, 1263–1273

Michalakis, S., Mühlfriedel, R., Tanimoto, N., Krishnamoorthy, V., et al (2010) Restoration of cone vision in the CNGA3−/− mouse model of congenital complete lack of cone photoreceptor function Mol. Ther., 18, 2057–2063

Michalakis, S., Mühlfriedel, R., Tanimoto, N., Krishnamoorthy, V., et al (2012) Gene therapy restores missing cone-mediated vision in the CNGA3 −/− mouse model of achromatopsia In Retinal degenerative diseases: Advances in experimental medicine and biology, vol. 723 (eds. LaVail, M.M. et al) Springer Science+Business Media, LLC, pp 183-189

Najate, A., Fridlich, R., Millet-Pue, G., Clerin, E., Delalande, F., Jaillard, C., Blond, F., Perrocheau, L., Reichman, S. et al (2015) Rod-derived cone viability factor promotes cone survival by stimulating aerobic glycolysis Cell, 161, 817–832

Szikra, T., Trenholm, S., Drinnenberg, A., Jüttner, J., Raics, Z., Farrow, K., Biel, M. et al (2014) Rods in daylight act as relay cells for cone-driven horizontal cell–mediated surround inhibition Nat. Neurosci., 17, 1728-1735

Ye, G-J., Budzynski, E., Sonnentag, P., Nork, T.M., Sheibani, N., Gurel, Z., Boye, S.L. et al (2016) Conespecific promoters for gene therapy of achromatopsia and other retinal diseases Hum. Gene Ther., 27, 72-82

Corneal disorders/transduction
Gruenert, A.K., Czugala, M., Mueller, C., Schmeer, M., Schleef, M., Kruse, F.E. and Fuchsluger, T.A. (2016) Self-complementary adeno-associated virus vectors improve transduction efficiency of corneal endothelial cells PLoS One, 11: e0152589

Hippert, C., Ibanes, S., Serratrice, N., Court, F., et al V. (2012) Corneal transduction by intra-stromal injection of AAV vectors in vivo in the mouse and ex vivo in human explants PLoS One 7: e35318

Mohan, R.R., Sinha, S., Tandon, A., Gupta, R., et al (2011) Efficacious and safe tissue-selective controlled gene therapy approaches for the cornea PloS One, 6: e18771

Mohan, R.R., Tandon, A., Sharma, A., Cowden, J.W. et al (2011) Significant inhibition of corneal scarring in vivo with tissue-selective, targeted AAV5 decorin gene therapy Invest. Ophthalmol. Vis. Sci., 52, 4833–4841

Mohan, R.R., Tovey, J.C.K., Sharma, A., Schultz, G.S., et al (2011) Targeted decorin gene therapy delivered with adeno-associated virus effectively retards corneal neovascularization in vivo PLoS One 6: e26432

Pinto, B.S., Saxena, T., Oliveira, R., Méndez-Gómez, H.R., Cleary, J.D., Denes, L.T., McConnell, O. et al (2017) Impeding transcription of expanded microsatellite repeats by deactivated Cas9 Mol. Cell 68, 479-490

Delivery procedures (cells, serotypes, tissues)
Boye, S.L., Bennett, A., Scalabrino, M.L., McCullough, K.T., Van Vliet, K., Choudhury, S., Ruan, Q., Peterson, J., Agbandje-McKenna, M. and Boye, S.E. (2016) Impact of heparan sulfate binding on transduction of retina by recombinant adeno-associated virus vectors J. Virol., 90, 4215-4231

Buck, T.M., Pellissier, L.P., Vos, R.M., van Dijk E.H.C., Boon, C.J.F. and Wijnholds, J. (2018) AAV serotype testing on cultured human donor retinal explants In Retinal Gene Therapy: Methods and Protocols, Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media, LLC New York 275-288

Buie, L.K., Rasmussen, C.A., Porterfield, E.C., Ramgolam, V.S., (2010) Self-complementary AAV virus (scAAV) safe and long-term gene transfer in the trabecular meshwork of living rats and monkeys Invest. Ophthalmol. Vis. Sci., 51, 236–248

Charbel Issa, P., De Silva, S.R., Lipinski, D.M., Singh, M.S., et al (2013) Assessment of tropism and effectiveness of new primate-derived hybrid recombinant AAV serotypes in the mouse and primate retina PLoS One, 8: e60361y

Dalkara, D., Byrne, L.C., Lee, T., Hoffmann, N.V., Schaffer, D.V. and Flannery, J.G. et al (2012) Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9 Gene Ther., 19, 176–181

Fischer, M.D., Hickey, D.G., Singh, M.S. and MacLaren, R.E. (2016) Evaluation of an optimized injection system for retinal gene therapy in human patients Hum. Gene Ther. Meth., 27, 150-148

Flannery, J.G. and Visel, M. (2013) Adeno-associated viral vectors for gene therapy of inherited retinal degenerations In Methods Mol. Biol., 935, Retinal Degeneration: Methods and Protocols (ed. Weber, B.H.F. and Langmann, T) Springer Science+Business Media, LLC pp 351-369

Hickey, D.G., Edwards, T.L., Barnard, A.R., Singh, M.S., de Silva, S.R., McClements, M.E., Flannery, J.G., Hankins, M.W. and MacLaren, R.E. (2017) Tropism of engineered and evolved recombinant AAV serotypes in the rd1 mouse and ex vivo primate retina Gene Ther., 24, 787–800

Jacobson, S.G., Acland, G.M., Aguirre, G.D., Aleman, T.S., et al (2006) Safety of recombinant adenoassociated virus type-2 RPE65 vector delivered by ocular subretinal injection Mol. Ther., 13, 1074-1084

Kolstad, K.D., Dalkara, D., Guerin, K., Visel, M., et al (2010) Changes in adeno-associated virus-mediated gene delivery in retinal degeneration Hum. Gene Ther., 21, 571-578

Reid, C.A. and Lipinski, D.M. (2018) Small and micro-scale recombinant adeno-associated virus production and purification for ocular gene therapy applications In Retinal Gene Therapy: Methods and Protocols, Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media LLC, New York 19-31

You, Q., Brown, L.A., McClements, M., Hankins, M.W., et al (2012) Tetradecanoyl-phorbol-13-acetate (TPA) significantly increases AAV2/5 transduction of human neuronal cells in vitro Exp. Eye Res., 97, 148-153

Diabetic retinopathy
Adhi, M., Cashman, S.M. and Kumar-Singh, R. (2013) Adeno-associated virus mediated delivery of a nonmembrane targeted human soluble CD59 attenuates some aspects of diabetic retinopathy in mice PLoS One, 8: e79661
Vacca, O., Charles-Messance, H., El Mathari, B., Sene, A., Barbe, P., Fouquet, S., Aragón, J., Darche, M. et al

(2016) AAV-mediated gene therapy in Dystrophin-Dp71 deficient mouse leads to blood-retinal barrier restoration and oedema reabsorption Hum. Mol. Genet., 25, 3070-3079

Experimental autoimmune encephalomyelitis
Talla, V., Koilkonda, R., Porciatti, V., Chiodo, V., Boye, S.L., Hauswirth, W.W. and Guy, J. (2015) Complex I subunit gene therapy with NDUFA6 ameliorates neurodegeneration in EAE Invest. Ophthalmol. Vis. Sci., 56, 1129–1140

Gated channel complexes
Doroudchi, M.M., Greenberg, K.P., Liu, J., Silka, K.A., et al (2011) Virally delivered channel rhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness Mol. Ther., 19, 1220–1229

Michalakis, S., Mühlfriedel, R., Tanimoto, N., Krishnamoorthy, V., et al (2010) Restoration of cone vision in the CNGA3−/− mouse model of congenital complete lack of cone photoreceptor function Mol. Ther., 18, 2057–2063

Glaucoma
Borras, T., Xue, W., Choi, V.W., Bartlett, J.S., et al (2006) Mechanisms of AAV transduction in glaucomaassociated human trabecular meshwork cells J. Gene Med., 8, 589-602

Dai, Y., Hu, X. and Sun, X. (2018) Overexpression of parkin protects retinal ganglion cells in experimental glaucoma Cell Death Dis., 9: 88

Folliot, S., Briot, D., Conrath, H., Provost, N., et al (2003) Sustained tetracycline-regulated transgene expression in vivo in rat retinal ganglion cells using a single type 2 adeno-associated viral vector J. Gene Med., 5, 493-501

Martin, K.R.G., Quigley, H.A., Zack, D.J., Levkovitch-Verbin, H., et al (2003) Gene therapy with brainderived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model Invest. Ophthalmol. Vis. Sci., 44 4357-4365

Pease, M.E., Zack, D.J., Berlinicke, C., Bloom, K., et al (2009) Effect of CNTF on retinal ganglion cell survival in experimental glaucoma Invest. Ophthalmol. Vis. Sci., 50, 2194–2200

Renwick, J., Narang, M.A., Coupland, S.G., Xuan, J.Y., et al (2006) XIAP-mediated neuroprotection in retinal ischemia Gene Ther., 13, 339-347

Growth factors
Mao, Y., Kiss, S., Boyer, J.L., Hackett, N.R., et al (2011) Persistent suppression of ocular neovascularization with intravitreal administration of AAVrh.10 coding for bevacizumab Hum. Gene Ther., 22, 1525–1535

Human corneal endothelial tissue
Gruenert, A.K., Czugala, M., Mueller, C., Schmeer, M., Schleef, M., Kruse, F.E. and Fuchsluger, T.A. (2016) Self-complementary adeno-associated virus vectors improve transduction efficiency of corneal endothelial cells PLoS One, 11: e0152589

Juvenile retinal dysfunction
Acland, G.M., Aguirre, G.D., Ray, J., Zhang, Q., et al (2001) Gene therapy restores vision in a canine model of childhood blindness Nat. Genet., 28, 92-95

Acland, G.M., Aguirre, G.D., Bennett, J., Aleman, T.S., et al (2005) Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness Mol. Ther., 12, 1072-1082

Griffey, M., Shannon, L., Macauley, J.M.O. and Sands, M.S. (2005) AAV2-mediated ocular gene therapy for infantile neuronal ceroid lipofuscinosis Mol. Ther., 12, 413-421

Min, S.H., Molday, L.L., Seeliger, M.W., Dinculescu, A., et al (2005) Prolonged recovery of retinal structure/function after gene therapy in an Rs1h-deficient mouse model of X-linked juvenile retinoschisis Mol. Ther., 12, 644-651

Lateral genicuate nucleus
Rompani, S.B., Müllner, F.E., Wanner, A., Zhang, C., Roth, C.N., Yonehara, K. and Roska, B. (2017) Different modes of visual integration in the lateral geniculate nucleus revealed by single-cell-initiated transsynaptic tracing Neuron, 93, 767–776

Leber congenital amaurosis/hereditary neuropathy
Pawlyk, B.S., Bulgakov, O.V., Liu, X., Xu, X., et al (2010) Replacement gene therapy with a human RPGRIP1 sequence slows photoreceptor degeneration in a murine model of Leber congenital amaurosis Human Gene Ther., 21, 993–1004

Sun, X., Pawlyk, B., Xu, X., Liu, X., et al (2010) Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations Gene Ther., 17, 117–131

Yu, H., Koilkonda, R.D., Chou, T-H., Porciatti, V., et al (2012) Gene delivery to mitochondria by targeting modified adenoassociated virus suppresses Leber’s hereditary optic neuropathy in a mouse model Proc. Natl. Acad. Sci. USA, 109, E1238–E1247

Lysosome-related diseases
Griffey, M., Shannon, L., Macauley, J.M.O. and Sands, M.S. (2005) AAV2-mediated ocular gene therapy for infantile neuronal ceroid lipofuscinosis Mol. Ther., 12, 413-421

Hennig, A.K., Ogilivie, J.M., Ohlemiller, K.K., Timmers, A.M., et al (2004) AAV-mediated intravitreal gene therapy reduces lysosomal storage in the retinal pigmented epithelium and improves retinal function in adult MPS VII mice Mol. Ther., 10, 106-116

Ho, T.T., Maguire, A.M., Aguirre, G.D., Surace, E.M., et al (2002) Phenotypic rescue after adeno-associated virus-mediated delivery of 4-sulfatase to the retinal pigment epithelium of feline mucopolysaccharidosis VI J. Gene Med., 4, 613-621

Macular degeneration
Ardeljan, D., Wang, Y., Park, S., Shen, D., et al (2014) Interleukin-17 retinotoxicity is prevented by gene transfer of a soluble interleukin-17 receptor acting as a cytokine blocker: implications for age-related macular degeneration PLoS One, 9: e95900

Joyal, J-S., Sun, Y., Gantner, M.L., Shao, Z., Evans, L.P., Saba, N., Fredrick, T., Burnim, S., Kim, J.S., Pate, G., Juan, A.M. et al (2016) Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1 Nat. Med., 22, 439-445

Kim, E., Koo, T., Park, S.W., Kim, D., Kim, K., Cho, H-Y., Song, D.W., Lee, K.J., Jung, M.H. et al (2017) In vivo genome editing with a small Cas9 orthologue derived from Campylobacter jejuni Nat. Comm., 8: 14500

Koo, T., Park, S.W., Jo, D.H., Kim, D., Kim, J.H., Cho, H-Y., Kim, J., Kim, J.H. and Kim, J-S, (2018) CRISPRLbCpf1 prevents choroidal neovascularization in a mouse model of age-related macular degeneration Nat. Comm., 9: 1855

Liang, K.J., Woodard, K.T., Weaver, M.A., Gaylor, J.P., Weiss, E.R. and Samulski, R.J. (2017) AAV-Nrf2 promotes protection and recovery in animal models of oxidative stress Mol. Ther., 25, 765-779

Reid, C.A., Nettesheim, E.R., Connor, T.B. and Lipinski, D.M. (2018) Development of an inducible anti-VEGF rAAV gene therapy strategy for the treatment of wet AMD Sci. Rep., 8: 11763

Sun, Y., Liegl, R., Gong, Y., Bühler, A., Cakir, B., Meng, S.S., Burnim, S.B., Liu, C-H., Reuer, T., Zhang, P. et al (2017) Sema3f protects against subretinal neovascularization in vivo EbioMed., 18, 281–287

Melanopsin
Rodgers, J., Hughes, S., Pothecary, C.A., Brown, L.A., Hickey, D.G., Peirson, S.N. and Hankins, M.W. (2018) Defining the impact of melanopsin missense polymorphisms using in vivo functional rescue Hum. Mol. Genet., 27, 2589–2603

Mitochondrial dysfunction
Koilkonda, R.D., Chou, T-H., Porciatti, V., Hauswirth, W.H. and Guy, J. (2010) Induction of rapid and highly efficient expression of the human ND4 complex I subunit in the mouse visual system by self-complementary adeno-associated virus Arch. Ophthalmol., 128, 876-883

Qi, X., Lewin, A., Hauswirth, W.W. and Guy, J. (2003) Optic neuropathy induced by reductions in mitochondrial superoxide dismutase Invest. Ophthal. Vis. Sci., 44, 1088-1096

Qi, X., Lewin, A.S., Hauswirth, W.W. and Guy, J. (2003) Suppression of complex I gene expression induces optic neuropathy Ann. Neurol., 53, 198-205

Qi, X., Lewin, A.S., Sun, L., Hauswirth, W.W. and Guy, J. (2004) SOD2 gene transfer protects against optic neuropathy induced by deficiency of complex I Ann. Neurol., 56, 182-191

Müller glial cells
Aartsen, W.M., van Cleef, K.W.R., Pellissier, L.P., Hoek, R.M., et al (2010) GFAP-driven GFP expression in activated mouse Müller glial cells aligning retinal blood vessels following intravitreal injection of AAV2/6 vectors PLoS One, 5: e12387

Alves, C.H., Pellissier, L.P., Vos, R.M., Garrido, M.G., et al (2014) Targeted ablation of Crb2 in photoreceptor cells induces retinitis pigmentosa Hum. Mol. Genet., 23, 3384–3401

Byrne, L.C., Khalid, F., Lee, T., Zin, E.A., et al (2013) AAV-mediated, optogenetic ablation of Müller glia leads to structural and functional changes in the mouse retina PLoS One, 8: e76075

Byrne, L.C., Öztürk, B.E., Lee, T., Fortuny, C., Visel, M., Dalkara, D., Schaffer, D.V. and Flannery, J.G. (2014) Retinoschisin gene therapy in photoreceptors, Müller glia or all retinal cells in the Rs1h−/−mouse Gene Ther., 21, 585–592

Klimczak, R.R., Koerber, J.T., Dalkara, D., Flannery, J.G. and Schaffer, D.V. (2009) A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells PLoS One 4: e7467

Pellissier, L.P., Hoek, R.M., Vos, R.M., Aartsen, et al (2014) Specific tools for targeting and expression in Müller glial cells Mol. Ther. Methods Clin. Dev., 1: 14009

Pellissier, L.P., Quinn, P.M., Alves, H., Vos, R.M., Klooster, J., Flannery, J.G., Heime, A. and Wijnholds, J. (2015) Gene therapy into photoreceptors and Müller glial cells restores retinal structure and function in CRB1

retinitis pigmentosa mouse models Hum.Mol. Genet., 24, 3104–3118 Vacca, O., Darche, M., Schaffer, D.V., Flannery, J.G., et al (2014) AAV-mediated gene delivery in Dp71-null mouse model with compromised barriers Glia, 62, 468–476

Vacca, O., Charles-Messance, H., El Mathari, B., Sene, A., Barbe, P., Fouquet, S., Aragón, J., Darche, M. et al (2016) AAV-mediated gene therapy in Dystrophin-Dp71 deficient mouse leads to blood-retinal barrier restoration and oedema reabsorption Hum. Mol. Genet., 25, 3070-3079

Wassmer, S.J., Carvalho, L.S., György, B., Vandenberghe, L.H., and Maguire, C.A. (2017) Exosomeassociated AAV2 vector mediates robust gene delivery into the murine retina upon intravitreal injection Sci. Rep., 7: 45329

Yao, K., Qiu, S., Tian, L., Snider, W.D., Flannery, J.G., Schaffer, D.V. and Chen, B. (2016) Wnt regulates proliferation and neurogenic potential of Müller glial cells via a Lin28/let-7 miRNA-dependent pathway in adult mammalian retinas Cell Rep., 17, 165–178

Yao, K., Qiu, S., Wang, Y.V., Park, S.J.H., Mohns, E.J., Mehta, B., Liu, X., Chang, B., Zenisek, D. et al (2018) Restoration of vision after de novo genesis of rod photoreceptors in mammalian retinas Nature, 560, 484-488

Neovascularization
Bainbridge, J.W.B., Mistry, A., De Alwis, M., Paleolog, E., et al (2002) Inhibition of retinal neovascularisation by gene transfer of soluble VEGF receptor sFlt-1 Gene Ther., 9, 320-326

Haurigot, V., Villacampa, P., Ribera, A., Bosch, A., et al (2012) Long-term retinal PEDF overexpression prevents neovascularization in a murine adult model of retinopathy PLoS One, 7: e41511

Mao, Y., Kiss, S., Boyer, J.L., Hackett, N.R., et al (2011) Persistent suppression of ocular neovascularization with intravitreal administration of AAVrh.10 coding for bevacizumab Hum. Gene Ther., 22, 1525–1535

Sun, Y., Liegl, R., Gong, Y., Bühler, A., Cakir, B., Meng, S.S., Burnim, S.B., Liu, C-H., Reuer, T., Zhang, P. et al (2017) Sema3f protects against subretinal neovascularization in vivo EbioMed., 18, 281–287

Neurotrophins/neurotrophic factor
Adamus, G., Sugden, B., Shiraga, S., Timmers, A.M. and Hauswirth, W.W. (2003) Anti-apoptotic effects of CNTF gene transfer on photoreceptor degeneration in experimental antibody-induced retinopathy J. Autoimmun., 21, 121-129

Cheng, L., Sapieha, P., Kittlerova, P., Hauswirth, W.W. and Di Polo, A. (2002) TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo J. Neurosci., 22, 3977-3986

Dalkara, D., Kolstad, K.D., Guerin, K.I., Hoffmann, N.V., et al (2011) AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa Mol. Ther., 19, 1602–1608

Leaver, S.G., Cui, Q., Plant, G.W., Arulpragasam, A., Hisheh, S., et al (2006) AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells Gene Ther., 13, 1328-1341

Pernet, V., Joly, S., Dalkara, D., Jordi, N., et al (2013) Long-distance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve Neurobiol. Dis., 51, 202–213

Shevtsova, Z., Malik, I., Garrido, M., Schöll, U., et al (2006) Potentiation of in vivo neuroprotection by BclXL and GDNF co-expression depends on post-lesion time in deafferentiated CNS neurons Gene Ther., 13, 1569-1578

Martin, K.R.G., Quigley, H.A., Zack, D.J., Levkovitch-Verbin, H., et al (2003) Gene therapy with brainderived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model Invest. Ophthalmol. Vis. Sci., 44 4357-4365

Pease, M.E., Zack, D.J., Berlinicke, C., Bloom, K., et al (2009) Effect of CNTF on retinal ganglion cell survival in experimental glaucoma Invest. Ophthalmol. Vis. Sci., 50, 2194–2200

Optic nerve function/injury/regeneration
Huang, Z-R., Hu, Z-Z, Xie, P. and Liu, Q-H. (2017) Tyrosine-mutated AAV2-mediated shRNA silencing of PTEN promotes axon regeneration of adult optic nerve PLoS One, 12: e0174096

Koch, J.C., Solis, G.P., Bodrikov, V., Michel, U., et al (2013) Upregulation of reggie-1/flotillin-2 promotes axon regeneration in the rat optic nerve in vivo and neurite growth in vitro Neurobiol. Dis., 51, 168–176

Koch, J.C., Bitow, F., Haack, J., d`Hedouville, Z., Zhang, J-N., Tönges, L., Michel, U. et al (2015) AlphaSynuclein affects neurite morphology, autophagy, vesicle transport and axonal degeneration in CNS neurons

Cell Death Dis., 6: e1811
Pernet, V., Joly, S., Dalkara, D., Schwarz, O., et al (2012) Neuronal Nogo-A upregulation does not contribute to ER stress-associated apoptosis but participates in the regenerative response in the axotomized adult retina Cell Death Differ., 19, 1096–1108

Pernet, V., Joly, S., Jordi, N., Dalkara, D., et al (2013) Misguidance and modulation of axonal regeneration by Stat3 and Rho/ROCK signaling in the transparent optic nerve Cell Death Dis., 4: e734

Pulizzi, R., Musumeci, G., Van den Haute, C., Van De Vijver, S., Baekelandt, V. and Giugliano, M. (2016) Brief wide-field photostimuli evoke and modulate oscillatory reverberating activity in cortical networks Sci. Rep., 6: 24701

Talla, V., Koilkonda, R., Porciatti, V., Chiodo, V., Boye, S.L., Hauswirth, W.W. and Guy, J. (2015) Complex I subunit gene therapy with NDUFA6 ameliorates neurodegeneration in EAE Invest. Ophthalmol. Vis. Sci., 56, 1129–1140

Optogenetic expression/inhibition
Burmeister, J.J., Pomerleau, F., Quintero, J.E., Huettl, P., Jakobsson, Y.A.J., Lundblad, M., Heuer, A., Slevin, J.T. and Gerhardt, G.A. (2018) In vivo electrochemical studies of optogenetic control of glutamate signaling measured using enzyme-based ceramic microelectrode arrays In Biochemical Approaches for Glutamatergic Neurotransmission, Neuromethods, vol. 130 (eds. Parrot, S. and Denoroy, L.) Springer Science+Business Media LLC, New York, pp 327-351

Lin, J.Y., Sann, S.B., Zhou, K., Nabavi, S., Proulx, C.D., Malinow, R., Jin, Y. and Tsien, R.Y. (2013) Optogenetic inhibition of synaptic release with chromophore-assisted light inactivation (CALI) Neuron, 79, 241–253

Lin, W-C., Davenport, C.M., Mourot, A., Vytla, D., Smith, C.M., Medeiros, K.A., Chambers, J.J. and Kramer, R.H. (2014) Engineering a light-regulated GABAA receptor for optical control of neural inhibition ACS Chem. Biol., 9, 1414−1419

Cronin, T., Vandenberghe, L.H., Hantz, P., Juttner, J., Reimann, A., Kacso, A.E., Huckfeldt, R.M., Busskamp. V., Kohler, H., Lagali, P.S. et al (2014) Efficient transduction and optogenetic stimulation of retinal bipolar cells by a synthetic adeno-associated virus capsid and promoter EMBO Mol. Med., 6, 1175-1190

Photoreceptor delivery/degeneration/function
De Silva, S.R., Charbel Issa, P., Singh, M.S., Lipinski, D.M., Barnea-Cramer, A.O., Walker, N.J. Barnard, A.R., Hankins, M.W. and MacLaren, R.E. (2016) Single residue AAV capsid mutation improves transduction of photoreceptors in the Abca4-/- mouse and bipolar cells in the rd1 mouse and human retina ex vivo Gene Ther., 23, 767–774

Fu, Z., Löfqvist, C.A., Liegl, Wang, Z., Sun, Y., Gong, Y., Liu, C-H., Meng, S.S., Burnim, S.B. et al (2018) Photoreceptor glucose metabolism determines normal retinal vascular growth EMBO Mol. Med., 10, 76-90

Pellissier, L.P., Quinn, P.M., Alves, H., Vos, R.M., Klooster, J., Flannery, J.G., Heime, A. and Wijnholds, J. (2015) Gene therapy into photoreceptors and Müller glial cells restores retinal structure and function in CRB1 retinitis pigmentosa mouse models Hum.Mol. Genet., 24, 3104–3118
Sun, Y., Lin, Z., Liu, C-H., Gong, Y., Liegl, R., Fredrick, T.W., Meng, S.S., Burnim, S.B., Wang, Z. et al

(2017) Inflammatory signals from photoreceptor modulate pathological retinal angiogenesis via c-Fos J. Exp. Med., 214, 1753–1767

Van Wyk, M., Pielecka-Fortuna, J., Löwel, S. and Kleinlogel, S. (2015) Restoring the ON switch in blind retinas: Opto-mGluR6, a next-generation, cell-tailored optogenetic tool PLoS Biol 13: e1002143

Presynaptic dysfunction
Zhou, L., McInnes, J., Wierda, K., Holt, M., Herrmann, A.G., Jackson, R.J., Wang, Y-C., Swerts, J., Beyens, J., Miskiewicz, K. et al (2017) Tau association with synaptic vesicles causes presynaptic dysfunction Nat. Comm., 8: 15295

Recombinant-AAV serotypes and variants in optical studies
Charbel Issa, P., De Silva, S.R., Lipinski, D.M., Singh, M.S., et al (2013) Assessment of tropism and effectiveness of new primate-derived hybrid recombinant AAV serotypes in the mouse and primate retina PLoS One, 8: e60361y

Dalkara, D., Kolstad, K.D., Caporale, N., Visel, M., et al (2009) Inner limiting membrane barriers to AAVmediated retinal transduction from the vitreous Mol. Ther., 17, 2096–2102

Giove, T.J., Sena-Esteves, M. and Eldred, W.D. (2010) Transduction of the inner mouse retina using AAVrh8 and AAVrh10 via intravitreal injection Exp. Eye Res., 91, 652-659

Hellström, M., Ruitenberg, M.J., Pollett, M.A., Ehlert, E.M.E., et al (2009) Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection Gene Ther., 16, 521–532

Klimczak, R.R., Koerber, J.T., Dalkara, D., Flannery, J.G., et al (2009) A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells PLoS One 4: e7467

Petrs-Silva. H., Dinculescu, A., Li, Q., Min, S-H., et al (2009) High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors Mol., Ther., 17, 463–471

Petrs-Silva, H., Dinculescu, A., Li, Q., Deng, W-T., et al (2011) Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina Mol. Ther., 19, 293–301

Thompson, K.R. and Towne, C. (2018) A hitchhiker’s guide to the selection of viral vectors for optogenetic studies In Optogenetics: A Roadmap, Neuromethods, vol. 133 (ed. Stroh, A.) Springer Science+Business Media, LLC New York, pp 1-23

Retinal angiogenesis
Sun, Y., Lin, Z., Liu, C-H., Gong, Y., Liegl, R., Fredrick, T.W., Meng, S.S., Burnim, S.B., Wang, Z. et al (2017) Inflammatory signals from photoreceptor modulate pathological retinal angiogenesis via c-Fos J. Exp. Med., 214, 1753–1767

Retinal bipolar cells
Cronin, T., Vandenberghe, L.H., Hantz, P., Juttner, J., Reimann, A., Kacso, A.E., Huckfeldt, R.M., Busskamp, V., Kohler, H., Lagali, P.S. et al (2014) Efficient transduction and optogenetic stimulation of retinal bipolar cells by a synthetic adeno-associated virus capsid and promoter EMBO Mol. Med., 6, 1175-1190

Retinal cell types, delivery and transduction efficiency
Hartl, D., Krebs, A.R., Jüttner, J., Roska, B. and Schübeler, D. (2017) Cis-regulatory landscapes of four cell types of the retina Nucleic Acids Res., 45, 11607–11621

Harvey, A.R., Kamphuis, W., Eggers, R., Symons, N.A., Blits, B., et al (2002) Intravitreal injection of adenoassociated viral vectors results in the transduction of different types of retinal neurons in neonatal and adult rats: A comparison with Lentivirus vectors Mol. Cell. Neurosci., 21, 141-157

Lai, C-M., Yu, M.J.T., Brankov, M., Barnett, N.L., Zhou, X., et al (2004) Recombinant adeno-associated virus type 2-mediated gene delivery into the Rpe65-/- knockout mouse eye results in limited rescue Genet. Vaccines Ther., 2:3

Malik, J.M.I., Shevtsova, Z., Bähr, M. and Kügler, S. (2005) Long-term in vivo inhibition of CNS neurodegradation by Bcl-XL gene transfer Mol. Ther., 11, 373-381

Shen, W-Y., Lai, C-M., Lai, Y.K.Y., Zhang, D., et al (2003) Practical considerations of recombinant adenoassociated virus-mediated gene transfer for treatment of retinal degenerations J. Gene Med., 5, 576-587

Retinal ganglion cells
Cruz-Martín, A., El-Danaf, R.N., Osakada, F., Sriram, B., et al (2014) A dedicated circuit links directionselective retinal ganglion cells to the primary visual cortex Nature, 507, 358-361

Dai, Y., Hu, X. and Sun, X. (2018) Overexpression of parkin protects retinal ganglion cells in experimental glaucoma Cell Death Dis., 9: 88

Koch, J.C., Solis, G.P., Bodrikov, V., Michel, U., et al (2013) Upregulation of reggie-1/flotillin-2 promotes axon regeneration in the rat optic nerve in vivo and neurite growth in vitro Neurobiol. Dis., 51, 168–176

Koch, J.C., Tönges, L., Barski, E., Michel, U., et al (2014) ROCK2 is a major regulator of axonal degeneration, neuronal death and axonal regeneration in the CNS Cell Death Dis., 5: e1225

Langouet-Astrie, C.J., Yang, Z., Polisetti, S.M., Welsbie, D.S., Hauswirth, W.W., Zack, D.J., Merbs, S.L. and Enke, R.A. (2016) Characterization of intravitreally delivered capsid mutant AAV2-Cre vector to induce tissuespecific mutations in murine retinal ganglion cells Exp. Eye Res., 151, 61-67

Pernet, V., Joly, S., Dalkara, D., Jordi, N., et al (2013) Long-distance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve Neurobiol. Dis., 51, 202–213

Pernet, V., Joly, S., Dalkara, D., Schwarz, O., Christ, F., Schaffer, D., Flannery, J.G. and Schwab, M.E. (2012) Neuronal Nogo-A upregulation does not contribute to ER stress-associated apoptosis but participates in the regenerative response in the axotomized adult retina Cell Death Differ., 19, 1096–1108

Zhang, C., Rompani, S.B., Roska, B. and McCall, M.A. (2014) Adeno-associated virus-RNAi of GlyR1 and characterization of its synapse-specific inhibition in OFF alpha transient retinal ganglion cells J. Neurophysiol., 112, 3125–3137

Retinal lipid/glucose metabolism
Joyal, J-S., Sun, Y., Gantner, M.L., Shao, Z., Evans, L.P., Saba, N., Fredrick, T., Burnim, S., Kim, J.S., Pate, G., Juan, A.M. et al (2016) Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1 Nat. Med., 22, 439-445

Retinal vascularization
Aartsen, W.M., van Cleef, K.W.R., Pellissier, L.P., Hoek, R.M., et al (2010) GFAP-driven GFP expression in activated mouse Müller glial cells aligning retinal blood vessels following intravitreal injection of AAV2/6 vectors PLoS One, 5: e12387

Bainbridge, J.W.B., Mistry, A., De Alwis, M., Paleolog, E., et al (2002) Inhibition of retinal neovascularisation by gene transfer of soluble VEGF receptor sFlt-1 Gene Ther., 9, 320-326

Fu, Z., Löfqvist, C.A., Liegl, Wang, Z., Sun, Y., Gong, Y., Liu, C-H., Meng, S.S., Burnim, S.B. et al (2018) Photoreceptor glucose metabolism determines normal retinal vascular growth EMBO Mol. Med., 10, 76-90

Igarashi, T., Miyake, K., Masuda, I., Takahashi, H. and Shimada, T. (2010) Adeno-associated vector (type 8)- mediated expression of soluble Flt-1 efficiently inhibits neovascularization in a murine choroidal neovascularization model Hum. Gene Ther., 21, 631-637

Pechan, P., Rubin, H., Lukason, M., Ardinger, J., et al (2009) Novel anti-VEGF chimeric molecules delivered by AAV vectors for inhibition of retinal neovascularization Gene Ther., 16, 10–16

Retinitis pigmentosa/retinal pigmented epithelium
Alves, C.H., Pellissier, L.P., Vos, R.M., Garrido, M.G., et al (2014) Targeted ablation of Crb2 in photoreceptor cells induces retinitis pigmentosa Hum. Mol. Genet., 23, 3384–3401

Beltran, W.A., Cideciyan, A.V., Boye, S.E., Ye, G-J., Iwabe, S., Dufour, V.L., Marinho, L.F., Swider, M. et al (2017) Optimization of retinal gene therapy for X-linked retinitis pigmentosa due to RPGR mutations Mol. Ther., 25, 1866-1880

Dalkara, D., Kolstad, K.D., Guerin, K.I., Hoffmann, N.V., et al (2011) AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa Mol. Ther., 19, 1602–1608

Fischer, M.D., McClements, M.E., Martinez-Fernandez de la Camara, C., Bellingrath, J-S., Dauletbekov, D., Ramsden, S.C., Hickey, D.G., Barnard, A.R. and MacLaren, R.E. (2017) Codon-optimized RPGR improves stability and efficacy of AAV8 gene therapy in two mouse models of X-linked retinitis pigmentosa Mol. Ther., 25, 1854-1865

Folliot, S., Briot, D., Conrath, H., Provost, N., et al (2003) Sustained tetracycline-regulated transgene expression in vivo in rat retinal ganglion cells using a single type 2 adeno-associated viral vector J. Gene Med., 5, 493-501

Giannelli, S.G., Luoni, M., Castoldi, V., Massimino, L., Cabassi, T., Angeloni, D., Demontis, G.C., Leocani, L., Andreazzoli, M. and Broccoli, V. (2018) Cas9/sgRNA selective targeting of the P23H Rhodopsin mutant allele for treating retinitis pigmentosa by intravitreal AAV9.PHP.B-based delivery Hum. Mol. Genet., 27, 761–779

Koch, S., Sothilingam, V., Garcia Garrido, M., Tanimoto, N., et al (2012) Gene therapy restores vision and delays degeneration in the CNGB12/2 mouse model of retinitis pigmentosa Hum. Mol. Genet., 21, 4486–4496

Kole, C., Berdugo, N., Da Silva, C., Aït-Ali, N., Millet-Puel, G., Pagan, D., Blond, F., Poidevin, L., Ripp, R., Fontaine, V. et al (2016) Identification of an alternative splicing product of the Otx2 gene expressed in the neural retina and retinal pigmented epithelial cells PLoS One, 11: e0150758

Kole, C., Klipfel, L., Yang, Y., Ferracane, V., Blond, F., Reichman, S., Millet-Puel, G., Clérin, E., Aït-Ali, N. et al (2018) Otx2-genetically modified retinal pigment epithelial cells rescue photoreceptors after transplantation Mol. Ther., 26, 219-237

Leonard, K.C., Petrin, D., Coupland, S.G., Baker, A.N., et al (2007) XIAP protection of photoreceptors in animal models of retinitis pigmentosa PLoS ONE, 3:e314

Lipinski, D.M., Barnard, A.R., Singh, M.S., Martin, C., Lee, E.J., Davies, W.I.L. and MacLaren, R.E. (2015) CNTF gene therapy confers lifelong neuroprotection in a mouse model of human retinitis pigmentosa Mol. Ther., 23, 1308–1319

Najate, A., Fridlich, R., Millet-Pue, G., Clerin, E., Delalande, F., Jaillard, C., Blond, F., Perrocheau, L., Reichman, S. et al (2015) Rod-derived cone viability factor promotes cone survival by stimulating aerobic glycolysis Cell, 161, 817–832

Pawlyk, B.S., Bulgakov, O.V., Liu, X., Xu, X., et al (2010) Replacement gene therapy with a human RPGRIP1 sequence slows photoreceptor degeneration in a murine model of Leber congenital amaurosis Human Gene Ther., 21, 993–1004

Pellissier, L.P., Quinn, P.M., Alves, H., Vos, R.M., Klooster, J., Flannery, J.G., Heime, A. and Wijnholds, J. (2015) Gene therapy into photoreceptors and Müller glial cells restores retinal structure and function in CRB1 retinitis pigmentosa mouse models Hum.Mol. Genet., 24, 3104–3118

Schön, C., Asteriti, S., Koch, S., Sothilingam, V., Garrido, N.G., Tanimoto, N., Herms, J., Seeliger, M.W., Cangiano, L., Biel, M. and Michalakis, S. (2016) Loss of HCN1 enhances disease progression in mouse models of CNG channel-linked retinitis pigmentosa and achromatopsia Hum. Mol. Genet., 25, 1165–1175

Schön, C., Becirovic, E., Biel, M. and Michalakis, S. (2018) Design and development of AAV-based gene supplementation therapies for achromatopsia and retinitis pigmentosa In Retinal Gene Therapy: Methods and Protocols, Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media, LLC New York 33-46

Sun, X., Pawlyk, B., Xu, X., Liu, X., et al (2010) Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations Gene Ther., 17, 117–131

Zou, J., Luo, L., Shen, Z., Chiodo, V.A., et al (2011) Whirlin replacement restores the formation of the USH2 protein complex in whirlin knockout photoreceptors Invest. Ophthalmol. Vis. Sci., 52, 2343–2351

Rhodopsin transport/expression
Chaffiol, A., Caplette, R., Jaillard, C, Brazhnikova, E., Desrosiers, M., Dubus, E., Duhamel, L., Macé, E. et al (2017) A new promoter allows optogenetic vision restoration with enhanced sensitivity in macaque retina 2546-2560

Dalkara, D., Byrne, L.C., Lee, T., Hoffmann, N.V., et al (2012) Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9 Gene Ther., 19, 176–181

Khani, S.C., Pawlyk, B.S., Bulgakov, O.V., Kasperek, E., et al (2007) AAV-mediated expression targeting of rod and cone photoreceptors with a human rhodopsin kinase promoter Invest. Ophthal. Vis. Sci., 48, 3954-3961

Ying, G., Gerstner, C.D., Frederick, J.M., Boye, S.L., Hauswirth, W.W. and Baehr, W. (2016) Small GTPases Rab8a and Rab11a are dispensable for rhodopsin transport in mouse photoreceptors PLoS One, 11: e0161236

119-40. Starburst amacrine cells
Grau, T., Michalakis, S. and Euler, T. (2013) Viral transfer of the genetically-encoded chloride indicator Clomeleon into ChAT/Cre retinae to study chloride dynamics in „starburst“ amacrine cells Invest. Ophthalmol. Vis. Sci., 54: e-Abstract 2504

Subretinal delivery
Gootwine, E., Ofri, R., Banin, E., Obolensky, A., Averbukh, E., Ezra-Elia, R., Ross, M., Honig, H., Rosov, A. et al (2017) Safety and efficacy evaluation of rAAV2tYF-PR1.7-hCNGA3 vector delivered by subretinal injection in CNGA3 mutant achromatopsia sheep Hum. Gene Ther. Clin. Dev. 28, 96-107

Seo, S., Mullins, R.F., Dumitrescu, A.V., Bhattarai, S., et al (2013) Subretinal gene therapy of mice with Bardet-Biedl syndrome type 1 Invest. Ophthalmol. Vis. Sci., 54, 6118–6132

Sun, Y., Liegl, R., Gong, Y., Bühler, A., Cakir, B., Meng, S.S., Burnim, S.B., Liu, C-H., Reuer, T., Zhang, P. et al (2017) Sema3f protects against subretinal neovascularization in vivo EbioMed., 18, 281–287

Ye, G-J., Budzynski, E., Sonnentag, P., Nork, T.M., Sheibani, N., Gurel, Z., Boye, S.L., Peterson, J.J., . Boye, S.E., Hauswirth, W.W. and Chulay, J.D. (2016) Cone-specific promoters for gene therapy of achromatopsia and other retinal retinaldiseases Hum. Gene Ther., 27, 72-82

Usher syndrome type IID
Zou, J., Luo, L., Shen, Z., Chiodo, V.A., et al (2011) Whirlin replacement restores the formation of the USH2 protein complex in whirlin knockout photoreceptors Invest. Ophthalmol. Vis. Sci., 52, 2343–2351

VIP+ interneurons
Lee, S-H., Kwan, A.C., Zhang, S., Phoumthipphavong, V., et al (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception Nature 488, 379-382

Park, S.J.H., Borghuis, B.G., Rahmani, P., Zeng, Q., Kim, I-J. and Demb, J.B. (2015) Function and circuitry of VIP+ interneurons in the mouse retina J. Neurosci., 35, 10685–10700

Visual cortex
Han, K-S., Cooke, S.F. and Xu, W. (2017) Experience-dependent equilibration of AMPAR-mediated synaptic transmission during the critical period Cell Rep., 18, 892–904

Huang, X., Stodieck, S.K., Goetze, B., Cui, L., Wong, M.H., Wenzel, C., Hosang, L. Dong, Y., Löwel, S. and Schlüter, O.M. (2015) Progressive maturation of silent synapses governs the duration of a critical period Proc. Natl. Acad. Sci. USA, E3131–E3140

Visual integration
Rompani, S.B., Müllner, F.E., Wanner, A., Zhang, C., Roth, C.N., Yonehara, K. and Roska, B. (2017) Different Modes of Visual integration in the lateral geniculate nucleus revealed by single-cell-initiated transsynaptic tracing Neuron, 93, 767–776

Vitreal delivery
Dalkara, D., Byrne, L.C., Klimczak, R.R., Visel, M., et al (2013) In vivo–directed evolution of a new adenoassociated virus for therapeutic outer retinal gene delivery from the vitreous.Sci. Translat. Med., 5: 189ra76

Langouet-Astrie, C.J., Yang, Z., Polisetti, S.M., Welsbie, D.S., Hauswirth, W.W., Zack, D.J., Merbs, S.L. and Enke, R.A. (2016) Characterization of intravitreally delivered capsid mutant AAV2-Cre vector to induce tissuespecific mutations in murine retinal ganglion cells Exp. Eye Res., 151, 61-67

De Silva, S.R., Charbel Issa, P., Singh, M.S., Lipinski, D.M., Barnea-Cramer, A.O., Walker, N.J. Barnard, A.R., Hankins, M.W. and MacLaren, R.E. (2016) Single residue AAV capsid mutation improves transduction of photoreceptors in the Abca4-/- mouse and bipolar cells in the rd1 mouse and human retina ex vivo Gene Ther., 23, 767–774

Wassmer, S.J., Carvalho, L.S., György, B., Vandenberghe, L.H., and Maguire, C.A. (2017) Exosomeassociated AAV2 vector mediates robust gene delivery into the murine retina upon intravitreal injection Sci. Rep., 7: 45329

XIAP-mediated gene therapy
Leonard, K.C., Petrin, D., Coupland, S.G., Baker, A.N., et al (2007) XIAP protection of photoreceptors in animal models of retinitis pigmentosa PLoS ONE, 3:e314

Renwick, J., Narang, M.A., Coupland, S.G., Xuan, J.Y., et al (2006) XIAP-mediated neuroprotection in retinal ischemia Gene Ther., 13, 339-347

X-linked retinoschisis
Byrne, L.C., Öztürk, B.E., Lee, T., Fortuny, C., Visel, M., Dalkara, D., Schaffer, D.V. and Flannery, J.G. (2014) Retinoschisin gene therapy in photoreceptors, Müller glia or all retinal cells in the Rs1h−/− mouse Gene Ther., 21, 585–592

Ornithine transcarbamylase deficiency
Wang, L., Morizono, H., Lin, J., Bell, P., et al (2012) Preclinical evaluation of a clinical candidate AAV8 vector for ornithine transcarbamylase (OTC) deficiency reveals functional enzyme from each persisting vector genome Mol. Genet. Metab., 105, 203–211

Osteoarthritis/osteoporosis
Akbar, M.A., Cao, J.J., Lu, Y., Nardo, D., Chen, M-J., Elshikha, A.S., Ahamed, R., Brantly, M., Holliday, L.S. and Song, S. (2016) Alpha-1 antitrypsin gene therapy ameliorates bone loss in ovariectomy-induced osteoporosis mouse model Hum. Gene Ther., 27, 679-686

Goodrich, L.R., Phillips, J.N., McIlwraith, C.W., Foti, S.B., et al (2013) Optimization of scAAVIL-1ra in vitro and in vivo to deliver high levels of therapeutic protein for treatment of osteoarthritis Mol. Ther. Nucleic Acids, 2: e70

Kyostio-Moore, S., Bangari, D.S., Ewing, P., Nambiar, B., et al (2013) Local gene delivery of heme oxygenase1 by adeno-associated virus into osteoarthritic mouse joints exhibiting synovial oxidative stress Osteoarthritis Cartilage, 21, 358-367

Watson, R.S., Broome, T.A., Levings, P.P., Rice, B.L., et al (2013) scAAV-mediated gene transfer of interleukin-1-receptor antagonist to synovium and articular cartilage in large mammalian joints Gene Ther., 20, 670–677

Pancreas see “Diabetes and other pancreatic disorders”
Pathological shear stress

Kang, L., Hillestad, M.L., Grande, J.P., Croatt, A.J., Barry, M.A., Farrugia, G., Katusic, Z.S. and Nath, K.A. (2015) Induction and functional significance of the heme oxygenase system in pathological shear stress in vivo. Am. J. Physiol. Heart Circ. Physiol., 308: H1402–H1413

Peritoneal delivery

Pagovich, O.E., Wang, B., Chiuchiolo, M.J., Kaminsky, S,M., Sondhi, D., Jose, C.L., Price, C.C., Brooks, S.F. et al (2016) Anti-hIgE gene therapy of peanut-induced anaphylaxis in a humanized murine model of peanut allergy J. Allergy Clin. Immunol., 138, 1652-1662

Phenotyping (organ and body)

Yang, B., Treweek, J.B., Kulkarni, R.P., Deverman, B.E., Chen, C-K., Lubeck, E., Shah, S., Cai, L. and Gradinaru, V. (2014) Single-cell phenotyping within transparent intact tissue through whole-body clearing Cell, 158, 945–958

Plasma cells

Hung, K.L., Meitlis, I., Hale, M., Chen, C-Y., Singh, S., Jackson, S.W., 1 Miao, C.H., Khan, I.F., Rawlings, D.J. and James, R.G. (2018) Engineering protein-secreting plasma cells by homology-directed repair in primary human B cells Mol. Ther., 26, 456-467

Polymicrobial sepsis

Martínez-Florensa, M., Consuegra-Fernández, M., Aranda, F., Armiger-Borràs, N., Di Scala, M., Carrasco, E., Pachón, J. et al (2017) Protective effects of human and mouse soluble scavenger-like CD6 lymphocyte receptor in a lethal model of polymicrobial sepsis Antimicrob. Agents Chemother., 61: e01391-16

Propionic acidemia

Guenzel, A.J., Hofherr, S.E., Hillestad, M., Barry, M., et al (2013) Generation of a hypomorphic model of propionic acidemia amenable to gene therapy testing Mol. Ther., 21, 1316-1323

Guenzel, A.J., Collard, R., Kraus, J.P., Matern, D. and Barry, M.A. (2015) Long-term sex-biased correction of circulating propionic acidemia disease markers by adeno-associated virus vectors Hum. Gene Ther., 26, 153–160

Protease-activated vectors

Robinson, T.M., Judd, J., Ho, M.L. and Suh, J. (2016) Role of tetra amino acid motif properties on the function of protease-activatable viral vectors ACS Biomater. Sci. Eng., 2, 2026−2033

Protein monoubiquitination

Bratena, O., Livneh, I., Ziv, T., Admon, A., Kehat, I., Caspi, L.H., Gonen, H., Bercovich, B., Godzik, A. (2016) Numerous proteins with unique characteristics are degraded by the 26S proteasome following monoubiquitination Proc. Natl. Acad. Sci. USA, 111, E4639-E4647

Protocols for production and quantitation of rAAV

AAV libraries
Körbelin, J., Hunger, A., Alawi, M., Sieber, T., Binder, M. and Trepel, M. (2017) Optimization of design and production strategies for novel adeno-associated viral display peptide libraries Gene Ther., 24, 470–481

Assay sytems (see also “129-14. Virus titre measurement and enhancement”)
Pacouret, S., Mevel, M., Bouzelha, M., Maurer, A., Shelke, R., Xiao, R., Penaud-Budloo, M., Turunen, H. et al (2016) Development and validation of identity and homogeneity assays for AAV preparations Mol. Ther., 24, Suppl. 1, S15

Clinical application considerations
Blits, B. and Bunge, M.B. (2006) Direct gene therapy for repair of the spinal cord J. Neurotrauma, 23, 508-520

De, B.P., Chen, A., Salami, C.O., Van de Graaf, B., Rosenberg, J.B., Pagovich, O.E., Sondhi, D., Crystal, R.G. and Kaminsky, S.M. (2018) In vivo potency assay for adeno-associated virus–based gene therapy vectors using AAVrh.10 as an example Hum. Gene Ther. Meth., 29, 146-155

Monahan, P.E. and Samulski, R.J. (2000) AAV vectors: is clinical success on the horizon? Gene Ther. 7, 24-30

Pfeifer, A. and Verma, I.M. (2001) Gene therapy: Promises and problems Annu. Rev. Genom. Hum. Genet., 2, 177-211

Empty capsid removal
Flotte, T.R. (2017) Empty adeno-associated virus capsids: contaminant or natural decoy? Hum. Gene Ther., 28, 147-148

Purification, scale-up, consistency and ancillary techniques of virus preparations Benskey, M.J., Sandoval, I.M. and Manfredsson, F.P. (2016) Continuous collection of adeno-associated virus from producer cell medium significantly increases total viral yield Hum. Gene Ther. Meth., 27, 32-45

Burova, E. and Ioffe, E. (2005) Chromatograpahic purification of recombinant adenoviral and adenoassociated viral vectors: methods and implications Gene Ther., 12, S5-S17

Chahal, P.S., Schulze, E., Tran, R., Montes, J., et al (2014) Production of adeno-associated virus (AAV) serotypes by transient transfection of HEK293 cell suspension cultures for gene delivery J. Virol. Methods, 196, 163– 173

Chahal, P., Schulze, E.A., Bernier, A., Lanthier, S., Coulombe, N., Kamen, A. and Gilbert, R. (2016) Towards large-scale manufacturing of adeno-associated virus by transient transfection of HEK293 suspension cells in a stirred tank bioreactor using serum-free medium Mol. Ther., 24, Suppl. 1, S118-S119

Chen, H., Merino, S. and Ho, C.Y. (2016) Large scale purification of adeno-associated virus (AAV) with continuous flow ultracentrifugation Hum. Gene Ther., 27, A160

Chen, H., Marino, S. and Ho, C.Y. (2016) Large scale purification of AAV with continuous flow ultracentrifugation Mol. Ther., 24, Suppl. 1, S42

Clément, N., Knop, D.R. and Byrne, B.J. (2009) Large-scale adeno-associated viral vector production using a herpesvirus-based system enables manufacturing for clinical studies Hum. Gene. Ther., 20, 796-806

Crosson, S.M., Dib, P., Smith, J.K. and Zolotukhin, S. (2018) Helper-free production of laboratory grade AAV and purification by iodixanol density gradient centrifugation Mol. Ther. Meth. Clin. Dev., 10: 1016

De Backer, M.W.A., Garner, K.M., Luijendijk, M.C.M. and Adan, R.A.H. (2011) Recombinant adenoassociated viral vectors In Methods Mol. Biol., 789, Neuropeptides: Methods and Protocols (ed. Merighi, A.), Springer Science+Business Media, pp 357-376

Dias-Florencio, G., Precigout, G., Beley, C., Buclez, P. ,Garcia, L. and Benchaouir, R. (2015) Simple downstream process based on detergent treatment improves yield and in vivo transduction efficacy of adenoassociated virus vectors Hum. Gene Ther., 26, A101

Doerfler, P.A., Byrne, B.J. and Clément, N. (2014) Co-packaging of multiple adeno-associated viral vectors in a single production step Hum. Gene Ther. Methods, 25, 269–276

Duffy, A.M., O’Doherty, A.M., O’Brien, T. and Strappe, P.M. (2005) Purification of adenovirus and adenoassociated virus: comparison of novel membrane-based technology to conventional techniques Gene Ther., 12, S62-S72

Faust, S.M., Bowles, D.E., Cunningham, S.E., Rabinowitz, J.E., et al (2004) Universal purification of AAV serotypes 1-5 modified to contain a heparin binding epitope Mol. Ther., 9 Suppl. 1 S36

Florencio, G.D., Precigout, G., Beley, C., Buclez, P-O., Garcia, L. and Benchaouir, R. (2015) Simple downstream process based on detergent treatment improves yield and in vivo transduction efficacy of adenoassociated virus vectors Mol. Ther. Methods Clin. Devel., 2: 15024

Grieger, J.C., Choi, V.W. and Samulski, R.J. (2006) Production and characterization of adeno-associated viral vectors Nat. Protoc., 1, 1412-1428

Grieger, J.C., Soltys, S.M. and Samulski, R.J. (2016) Production of recombinant adeno-associated virus vectors using suspension HEK293 cells and continuous harvest of vector from the culture media for GMP FIX and FLT1 clinical vector Mol. Ther., 24, 287–297

Hashimoto, H., Mizushima, T., Chijiwa, T., Nakamura, M. and Suemizu, H. (2017) Efficient production of recombinant adeno-associated viral vector, serotype DJ/8, carrying the GFP gene Virus Res., 238, 63–68

Heindorf, M. and Hasan, M.T. (2015) Fluorescent calcium indicator protein expression in the mouse brain using recombinant adeno-associated viruses Cold Spring Harb Protoc; doi: 10.1101/pdb.prot087635

Hermens, W.T.J.M.C., Ter Brake, O., Dijkhuizen, P.A., Sonnemans, M.A.F., et al (1999) Purification of recombinant adeno-associated virus by iodixanol gradient ultracentrifugation allows rapid and reproducible preparation of vector stocks for gene transfer in the nervous system Hum. Gene Ther., 10, 1885-1891

Huang, X., Hartley, A-V., Yin, Y., Herskowitz, J.H., et al (2013) AAV2 production with optimized N/P ratio and PEI-mediated transfection results in low toxicity and high titer for in vitro andin vivo applications J. Virol. Methods, 193, 270– 277

Jungmann, A., Leuchs, B., Rommelaere, J., Katus, H.A.and Müller, O.J. (2017) Protocol for efficient generation and characterization of Adeno-associated viral vectors Hum. Gene Ther. Meth., 28, 235-246

Khan, I.F., Hirata, R.K. and Russell, D.W. (2011) AAV-mediated gene targeting methods for human cells Nat. Protoc., 6, 482-501

Kleven, M.D., Gomes, M.M., Wortham, A.M., Enns, C.A. and Kahl, C. (2018) Ultrafiltered recombinant AAV8 vector can be safely administered in vivo and efficiently transduces liver PLoS ONE 13: e0194728

Koerber, J.T., Jang, J-Y., Yu, J.H., Kane, R.S., et al (2007) Engineering adeno-associated virus for one-step purification via immobilized metal affinity chromatography Hum. Gene Ther., 18, 367-378

Kohlbrenner, E., Aslanidi, G., Nash, K., Shklyaev, S., et al (2005) Successful production of pseudotyped rAAV vectors using a modified Baculovirus expression system Mol. Ther., 12, 1217-1225

Kohlbrenner, E. and Weber, T. (2017) Production and characterization of vectors based on the cardiotropic AAV serotype 9 In Cardiac Gene Therapy: Methods and Protocols, Meth. Mol. Biol., vol. 1521 (ed. Ishikawa, K.) Springer Science+Business Media New York 2017, pp 91-107

Kotin, R.M. (2011) Large-scale recombinant adeno-associated virus production Hum. Mol. Genet., 20, R2-R6 Leonard, J.N., Ferstl, P., Delgado, A. and Schaffer, D.V. (2007) Enhanced preparation of adeno-associated viral vectors by using high hydrostatic pressure to selectively inactivate helper adenovirus Biotechnol. Bioeng., 97, 1170-1179

Lock, M., Alvira, M., Vandenberghe, L.H., Samanta, A., et al (2010) Rapid, simple, and versatile manufacturing of recombinant adeno-associated viral vectors at scale Hum. Gene Ther., 21, 1259–1271

Merten, O-W., Geny-Fiamma, C. and Douar, A.M. (2005) Current issues in adeno-assocaited viral vector production Gene Ther., 12, S51-S61

Morenweiser, R. (2005) Downstream processing of viral vectors and vaccines Gene Ther., 12, S103-S110

Piedra, J., Ontiveros, M., Miravet, S., Penalva, C., Monfar, M. and Chillon, M. (2015) Development of a rapid, robust, and universal PicoGreen-based method to titer adeno-associated vectors Hum. Gene Ther. Methods, 26, 35–42

Pacouret, S., Bouzelha, M., Shelke, R., Andres-Mateos, E., Xiao, R., Maurer, A., Mevel, M., Turunen, H., Barungi, T. et al (2017) AAV-ID: A rapid and robust assay for batch-to-batch consistency evaluation of AAV preparations Mol. Ther., 25, 1375-1386

Penaud-Budloo, M., François, A., Clément, N. and Ayuso, E. (2018) Pharmacology of recombinant adenoassociated virus production Mol. Ther. Methods Clin. Dev., 8, 166-180

Potter, M., Lins, B., Mietzsch, M., Heilbronn, R., Van Vliet, K., Chipman, P., Agbandje-McKenna, M., Cleaver, B.D., Clement, N., Byrne, B.J. and Zolotukhin, S. (2014) A simplified purification protocol for recombinant adeno-associated virus vectors Mol. Ther. Methods Clin. Dev., 1: 14034

Qu, W., Wang, M., Wu, Y. and Xu, R. (2015) Scalable downstream strategies for purification of recombinant adeno-associated virus vectors in light of the properties Curr. Pharm. Biotechnol., 16, 684-695

Reid, C.A. and Lipinski, D.M. (2018) Small and micro-scale recombinant adeno-associated virus production and purification for ocular gene therapy applications In Retinal Gene Therapy: Methods and Protocols,Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media LLC, New York 19-31

Rohr, U-P., Wulf, M-A., Stahn, S., Steidl, U., et al (2002) Fast and reliable titration of recombinant adenoassociated virus type-2 using quantitative real-time PCR J. Virol. Methods, 106, 81-88

Schnödt, M., Schmeer, M., Kracher, B., Krüsemann, C., Escalona Espinosa, L., Grünert, A., Fuchsluger, T., Rischmüller, A., Schleef, M. and Büning, H. (2016) DNA minicircle technology improves purity of adenoassociated viral vector preparations Mol. Ther. Nucleic Acids, 5, e355

Schnödt, M. and Büning, H. (2017) Improving the quality of adeno-associated viral vector preparations: the challenge of product-related impurities Hum. Gene Ther. Meth., 28, 101-108

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

Sharon, D. and Kamen, A. (2018) Advancements in the design and scalable production of viral gene transfer vectors Biotech. Bioeng., 115, 25–40

Summerford, C. and Samulski, R.J. (1999) Viral receptors and vector purification: New approaches for generating clinical-grade reagents Nat. Med., 5, 587-588

Szarek, E. and Hung, J. (2017) Genet. Eng. Biotech. News 37, 22–23 Scalable production of AAV vectors: range of methods used in generating and purifying AAV vectors Toelen, J., Lock, M., Vandenberghe, L., Carlon, M., et al (2009) Novel and scalable approach to research grade AAV vector manufacturing and separation of distinct AAV serotypes Hum. Gene Ther., ESGCT, DGGT, GSZ, and ISCT 2009 Poster Presentations, # 52

Tomono, T., Hirai, Y., Okada, H., Adachi, K., Ishii, A., Shimada, T., Onodera, M., Tamaoka, A. and Okada, T. (2016) Ultracentrifugation-free chromatography-mediated large-scale purification of recombinant adenoassociated virus serotype 1 (rAAV1) Mol. Ther. Methods Clin. Dev., 3: 15058

Verhaagen, J., Hobo, B., Ehlert E.M.E., Eggers, R., Korecka, J.A., Hoyng, S.A., Attwell, C.L., Harvey, A.R. and Mason, M.R.J. (2018) Small scale production of recombinant adeno-associated viral vectors for gene delivery to the nervous system In Retinal Gene Therapy: Methods and Protocols, Methods in Molecular Biology, vol. 1715 (eds. Boon, C.J.F. and Wijnholds, J.) Springer Science+Business Media LLC New York 3-17

Wang, L., Blouin, V., Brument, N., Bello-Roufai, M. and Francois, A. (2011) Production and purification of recombinant adeno-associated vectors In Adeno-Associated Virus: Methods and Protocols, Methods Mol. Biol., 807 (ed. Snyder, R.O. and Moullier, P.), Springer Science+Business Media, pp 361-404

Wang, Q., Lock, M., Prongay, A.J., Alvira, M.R., Petkov, B. and Wilson, J.M. (2015) Identification of an adeno-associated virus binding epitope for AVB sepharose affinity resin Mol. Ther. Methods Clin. Dev., 2: 15040

Zolotukhin, S., Byrne, B.J., Mason, E., Zolotukhin, I., Potter, M., Chesnut, K., Summerford, C., Samulski, R.J. and Muzyczka, N. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield Gene Ther., 6, 973-985

Zolotukhin, S. (2005) Production of recombinant adeno-associated virus vectors Hum. Gene Ther., 16, 551- 557

Particle heterogeneity
Lock, M., Alvira, M.R. and Wilson, J.M. (2012) Analysis of particle content of recombinant adeno-associated virus serotype 8 vectors by ion-exchange chromatography Hum. Gene Ther. Methods, Part B 23, 56-64

Pierson, E.E., Keifer, D.Z., Asokan, A. and Jarrold, M.F. (2016) Resolving adeno-associated viral particle diversity with charge detection mass spectrometry Anal. Chem., 88, 6718−6725

Strobel, B., Miller, F.D., Rist, W. and Lamla, T. (2015) Comparative analysis of cesium chloride- and iodixanol-based purification of recombinant adeno-associated viral vectors for preclinical applications Hum. Gene Ther. Methods, 26, 147-157

rAAV-3
Ling, C., Yin, Z., Li, J., Zhang, D., Aslanidi, G. and Srivastava, A. (2016) Strategies to generate high-titer, high-potency recombinant AAV3 serotype vectors Mol. Ther. Meth. Clin. Dev., 3: 16029

Recombinant AAV libraries
Koerber, J.T., Maheshri, N., Kaspar, B.K. and Schaffer, D.V. (2006) Construction of diverse adeno-associated viral libraries for directed evolution of enhanced gene delivery vehicles Nat. Protoc., 1, 701-706

Waterkamp, D.A., Müller, O.J., Ying, Y., Trepel, M. and Kleinschmidt, J.A. (2006) Isolation of targeted AAV2 vectors from novel virus display libraries J. Gene Med., 8, 1307-1319

Receptor-targeted
Münch, R.C., Muth, A., Muik, A., Friedel, T., Schmatz, J., Dreier, B., Trkola, A., Plückthun, A., Büning, H. and Buchholz, C.J. (2015) Off-target-free gene delivery by affinity-purified receptor-targeted viral vectors Nat. Commun., 6: 6246

Small-scale production
Burger, C. and Nash, K.R. (2016) Small-scale recombinant adeno-associated virus purification In Gene Therapy for Neurological Disorders: Methods and Protocols: Methods in Molecular Biology, vol. 1382 (ed. Manfredsson, F.P.) Springer Science+Business Media New York, pp 95-106

Technological reviews
Ayuso, E. (2016) Manufacturing of recombinant adeno-associated viral vectors: new technologies are welcome Mol. Ther. Methods. Clin. Dev., 3, 15049

Hastie, E. and Samulski, R.J. (2015) Adeno-associated virus at 50: a golden anniversary of discovery, research, and gene therapy success – a personal perspective Hum. Gene Ther., 26, 257–265

Merten, O-W. and Gaillet, B. (2016) Viral vectors for gene therapy and gene modification approaches Biochem. Eng. J., 108, 98–115

Transduction efficiency
Grimm, D., Kay, M.A. and Kleinschmidt, J.A. (2003) Helper virus-free, optically controllable and twoplasmid-based production of adeno-associated virus vectors of serotypes 1 to 6 Mol. Ther., 7, 839-850

Julien, L., Chassagne, J., Peccate, C., Lorain, S., Piétri-Rouxel, F., Danos, O. and Benkhelifa-Ziyyat, S. (2018) RFX1 and RFX3 transcription factors interact with the D sequence of adeno-associated virus inverted terminal repeat and regulate AAV transduction Sci. Rep., 8: 210

Khan, I.F., Hirata, R.K. and Russell, D.W. (2011) AAV-mediated gene targeting methods for human cells Nat. Protoc., 6, 482-501

Kondratov, O., Marsic, D., Crosson, S.M., Mendez-Gomez, H.R., Moskalenko, O., Mietzsch, M., Heilbronn, R., Allison, J.R. et al (2017) Direct head-to-head evaluation of recombinant adeno-associated viral vectors manufactured in human versus insect cells Mol. Ther., 25, 2661-2675

Lane, M.D., Nam, H-J., Padron, E., Gurda-Whitaker, B., et al (2005) Production, purification, crystallization and preliminary X-ray analysis of adeno-associated virus serotype 8 Acta Cryst., F61, 558-561

Lee, K., Kim, Y-G., Jo, E-C. (2003) Shuttle PCR-based cloning of the infectious adeno-associated virus type 5 genome J. Virol. Methods, 111, 75-84

McConnell, K.I., Gomez, E.J. and Suh, J. (2012) The identity of the cell adhesive protein substrate affects the efficiency of adeno-associated virus reverse transduction Acta Biomater., 8, 4073–4079

Wright, J.F., Chunlin Tang, G.Q. and Sommer, J.M. (2003) Recombinant adeno.associated virus: formulation challenges and strategies for a gene therapy vector Curr. Opin. Drug Discov. Devel., 6, 174-178 Zolotukhin, S., Potter, M., Zolotukhin, I., Sakai, Y., et al (2002) Production and purification of serotype 1,2, and 5 recombinant adeno-associated viral vectors Methods, 28, 158-167

Transfection agents
Guo, P., Yu, C., Wang, Q., Zhang, R., Meng, X. and Feng, Y. (2108) Liposome lipid-based formulation has the least influence on rAAV transduction compared to other transfection agents Mol. Ther. Meth. Clin. Dev., 9, 367-375

Virion integrity and genome integration
Arnold, G.S., Sasser, A.K., Stachler, M.D. and Bartlett, J.S. (2006) Metabolic biotinylation provides a unique platform for the purification and targeting of multiple AAV vector serotypes Mol. Ther., 14, 97-106

Büning, H., Perabo, L., Coutelle, O., Quadt-Humme, S., et al (2008) Recent developments in adeno-associated virus vector technology J. Gene Med., 10, 717-733

Van Vliet, K.M., Blouin, V., Brument, N., Agbandje-McKenna, M., et al (2008) The role of the adenoassociated virus capsid in gene transfer Methods Mol Biol., 437, 51-91

Weitzman, M., Young Jr., S.M., Cathhomen, T. and Samulski, T.J. (2003) Targeted integration by adenoassociated virus Methods Mol. Med., 76, 201-219

Weitzman, M.D. and Linden, R.M. (2011) Adeno-associated virus biology In Adeno-Associated Virus: Methods and Protocols, Methods Mol. Biol., 807 (ed. Snyder, R.O. and Moullier, P.), Springer Science+Business Media, pp 1-23

Wu, Z., Asokan, A. and Samulski, R.J. (2006) Adeno-associated virus serotypes: vector toolkit for human gene therapy Mol. Ther., 14, 316-327

Virus titre measurement and enhancement
Clark, K.R. (2002) Recent advances in recombinant adeno-associated virus vector production Kidney Int., 61, Sympos. 1, S9-S15

De, B., Mendez, B., Hackett, N.R., Kaminsky, S.M. and Crystal, R.G. (2002) Adaptation of laboratory grade recombinant AAV production to manufacture of vector for human administration 5th. Annu. Meeting Am. Soc. Gene Ther., Abstr. 147

Harris, J.D., Beattie, S.G. and Dickson, J.G. (2003) Novel tools for production and purification of recombinant adeno-associated viral vectors Methods Mol. Med., 76, 255-267

Kohlbrenner, E., Henckaerts, E., Rapti, K., Gordon, R.E., et al (2012) Quantification of AAV particle titers by infrared fluorescence scanning of Coomassie-stained sodium dodecyl sulfate–polyacrylamide gels Hum. Gene Ther. Methods, 23, 198–203

Lock, M., Alvira, M.R., Chen, S-J. and Wilson, J.M. (2014) Absolute determination of single-stranded and selfcomplementary adeno-associated viral vector genome titers by droplet digital PCR Hum. Gene Ther. Methods 25, 115–125

Mistry, A.R., De Alwis, M., Feudner, E., Ali, R.R., et al (2002) High-titer stocks of adeno-associated virus from replicating amplicons and herpes vectors Methods Mol. Med., 69, 445-460

Rohr, U-P., Wulf, M-A., Stahn, S., Steidl, U., et al (2002) Fast and reliable titration of recombinant adenoassociated virus type-2 using quantitative real-time PCR J. Virol. Methods, 106, 81-88

Rohr, U-P., Heyd, F., Neukirchen, J., Wulf, M-A., et al (2005) Quantitative real-time PCR for titration of infectious recombinant AAV-2 particles J. Virol. Methods, 127, 40-45

Virus tracking
Kothari, P., De, B.P., He, B., Chen, A., Chiuchiolo, M.J., Kim, D., Nikolopoulou, A., Amor-Coarasa1, A., Dyke, J.P., Voss, H.U. et al (2017) Radioiodinated capsids facilitate in vivo non-invasive tracking of adenoassociated gene transfer vectors Sci. Rep., 7: 39594

Regulatory protein

Zarate-Perez, F., Mansilla-Soto, J., Bardelli, M., Burgner II, J.W., Villamil-Jarauta, M., Kekilli, D., Samso, M., Linden, R.M. and Escalante, C.R. (2013) Oligomeric properties of adeno-associated virus Rep68 reflect its multifunctionality J. Virol., 87, 1232-1241

Replication

Satkunanathan, S., Thorpe, R. and Zhao, Y. (2017) The function of DNA binding protein nucleophosmin in AAV replication Virology, 510, 46–54

Reporter proteins

Fluri, D.A., Kelm, J.M., Lesage, G., Daoud-El Baba, M., et al (2007) InXy and SeXy, compact heterologous
reporter proteins for mammalian cells Biotechnol. Bioeng., 98, 655-667

Respiratory system delivery

Acute lung injury
MacLoughlin, R.J., Higgins, B.D., Devaney, J., O’Toole, D., Laffey, J.G. and O’Brien, T. (2015) Aerosolmediated delivery of AAV2/6-IkjBa attenuates lipopolysaccharide-induced acute lung injury in rats Hum. Gene Ther., 26, 36–46

Anti-apoptosis
Petrache, I., Fijalkowska, I., Medler, T.R., Skirball, J., et al (2006) a-1 Antitrypsin inhibits caspase-3 activity, preventing lung endothelial cell apoptosis Am. J. Pathol., 169, 1155-1166

a-Anti-trypsin
De, B.P., Wasif, N., Hackett, N.R., Gao, G., et al (2004) Therapeutic levels for a1-antitrypsin following intrapleural administration of a non-human primate serotype rh10 AAV vector expressing a1-antitrypsin Mol. Ther., 9, Suppl. 1, S128

De, B., Heguy, A., Leopold, P.L., Wasif, N., et al (2004) Intrapleural administration of a serotype 5 adenoassociated virus coding for a1-antitrypsin mediates persistent, high lung and serum levels of a1-antitrypsin Mol. Ther., 10, 1003-1010

De, B.P., Heguy, A., Hackett, N.R., Ferris, B., et al (2006) High levels of persistent expression of a1antitrypsin mediated by the nonhuman primate serotype rh.10 adeno-associated virus despite preexisting immunity to common human adeno-associated viruses Mol. Ther., 13, 67-76

Cystic fibrosis

Schuster, B.S., Kim, A.J., Kays, J.C., Kanzawa, M.M., Guggino, W.B., Boyle, M.P., Rowe, S.M., Muzyczka, N. Suk, J.S. and Hanes, J. (2014) Overcoming the cystic fibrosis sputum barrier to leading adeno-associated virus gene therapy vectors Mol. Ther., 22, 1484–1493

Sirninger, J., Muller, C., Braag, S., Tang, Q., et al (2004) Functional characterization of a recombinant adenoassociated virus 5-pseudotyped cystic fibrosis transmembrane conductance regulator vector Hum. Gene Ther., 15, 832-841

Song, Y., Lou, H.H., Boyer, J.L., Limberis, M.P., et al (2009) Functional cystic fibrosis transmembrane conductance regulator expression in cystic fibrosis airway epithelial cells by AAV6.2-mediated segmental transsplicing Hum. Gene Ther., 20, 267–281

Delivery
Carlon, M., Toelen, J., Van der Perren, A., Vandenberghe, L.H., et al (2010) Efficient gene transfer into the mouse lung by fetal intratracheal injection of rAAV2/6.2 Mol. Ther., 18, 2130–2138

Dickey, D.D., Excoffon, K.J.D.A., Koerber, J.T., Bergen, J., et al (2011) Enhanced sialic acid-dependent endocytosis explains the increased efficiency of infection of airway epithelia by a novel adeno-associated virus J. Virol., 85, 9023–9030

Dickey, D.D., Excoffon, K.J.D.A., Young, K.R., Parekh, K.R., et al (2012) Hoechst increases adeno-associated virus-mediated transgene expression in airway epithelia by inducing the cytomegalovirus promoter J. Gene Med., 14, 366–373

Flotte, T.R., Fischer, A.C., Goetzmann, J., Mueller, C., et al (2010) Dual reporter comparative indexing of rAAV pseudotyped vectors in chimpanzee airway Mol. Ther., 18, 594–600

Körbelin, J., Sieber, T., Michelfelder, S., Lunding, L., Spies, E., Hunger, A., Alawi, M. Rapti, K., Indenbirken, D. et al (2016) Pulmonary targeting of adeno-associated viral vectors by next-generation sequencing-guided screening of random capsid displayed peptide libraries Mol. Ther., 24, 1050-1061

Lipinski, D.M., Reid, C.A., Boye, S.L., Peterson, J.J., Qi, X., Boye, S.E., Boulton, M.E. and Hauswirth, W.W. (2015) Systemic vascular transduction by capsid mutant adeno-associated virus after intravenous injection Hum. Gene Ther., 26, 767-776

Van Lieshout, L.P., Domm, J.M., Rindler, T.N., Frost, K.L., Sorensen, D.L., Medina, S.J., Booth, S.A., Bridges, J.P. and Wootton, S.K. (2018) A novel triple-mutant AAV6 capsid induces rapid and potent transgene expression in the muscle and respiratory tract of mice Mol. Ther. Meth.Clin. Dev., 9, 323-329

Vidović, D., Gijsbers, R., Quiles-Jimenez, A., Dooley, J., Van den Haute, C., Van der Perren, A., Liston, A., Baekelandt, V., Debyser, Z. and Carlon, M.S. (2016) Noninvasive imaging reveals stable transgene expression in mouse airways after delivery of a nonintegrating recombinant adeno-associated viral vector Hum. Gene Ther., 27, 60-71

Virella-Lowell, I., Zusman, B., Foust, K., Loiler, S., et al (2005) Enhancing rAAV vector expression in the lung J. Gene Med., 7, 842-850

White, A.F., Mazur, M., Sorscher, E.J., Zinn, K.R. et al (2008) Genetic modification of adeno-associated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells Hum. Gene Ther., 19, 1407–1414

Yan, Z., Lei-Butters, D.C.M., Liu, X., Zhang, L., et al (2006) Unique biologic properties of recombinant AAV1 transduction in polarized human airway epithelia J. Biol. Chem., 281, 29684-29692

Yan, Z., Sun, X., Evans, I.A., Tyler, S.R., Song, Y., et al (2013) Post-entry processing of recombinant adenoassociated virus type 1 and transduction of the ferret lung are altered by a factor in airway secretions Hum. Gene Ther., 24, 786–796

Lung tumours
Watanabe, M., Boyer, J.L. and Crystal, R.G. (2010) AAVrh.10-mediated genetic delivery of bevacizumab to the pleura to provide local anti-VEGF to suppress growth of metastatic lung tumors Gene Ther., 17, 1042–1051

Pompe disease
Doerfler, P.A., Todd, A.G., Clément, N., Falk, D.J., Nayak, S., Herzog, R.W. and Byrne, B.J. (2016) Copackaged AAV9 vectors promote simultaneous immune tolerance and phenotypic correction of Pompe disease Hum. Gene Ther., 27, 43-59

Qiu, K., Falk, D.J., Reier, P.R., Byrne, B.J., et al (2012) Spinal delivery of AAV vector restores enzyme activity and increases ventilation in Pompe mice Mol. Ther., 20, 21–27

Respiratory rhythm
Tan, W., Pagliardini, S., Yang, P., Janczewski, W.A., et al (2011) Projections of preBötzinger complex neurons in adult rats J. Comp. Neurol., 518, 1862–1878

Rheumatoid arthritis (see “Arthritic joint delivery”)
RNA

Interference applications
Wagner, A., Röhrs, V., Kedzierski, R., Fechner, H. and Kurreck, J. (2013) A novel method for the quantification of adeno-associated virus vectors for RNA interference applications using quantitative polymerase chain reaction and purified genomic adeno-associated virus DNA as a standard Hum. Gene Ther. Methods, 24, 355–363

miRNA/shRNA/siRNA/RNAi
Ahn, J-H., Kim, Y., Kim, H-S., Greengard, P., et al (2011) Protein kinase C-dependent dephosphorylation of tyrosine hydroxylase requires the B56d heterotrimeric form of protein phosphatase 2A PloS One, 6: e26292

Alves, C.H., Pellissier, L.P., Vos, R.M., Garrido, M.G., et al (2014) Targeted ablation of Crb2 in photoreceptor cells induces retinitis pigmentosa Hum. Mol. Genet., 23, 3384–3401

Boudreau, R.L., Spengler, R.M. and Davidson, B.L. (2011) Rational design of therapeutic siRNAs: minimizing off-targeting potential to improve the safety of RNAi therapy for Huntington’s disease Mol. Ther., 19, 2169–2177

Bourhill, T., Arbuthnot, P. and Ely, A. (2016) Successful disabling of the 5’UTR of HCV using adenoassociated viral vectors to deliver modular multimeric primary microRNA mimics J. Virol. Meth., 235, 26–33

Challagundla, M., Koch, J.C., Ribas, V.T., Michel, U., Kugler, S., Ostendorf, T., Bradke, F., Muller, H.W., Bahr, M. and Lingor, P. (2015) AAV-mediated expression of BAG1 and ROCK2shRNA promote neuronal survival and axonal sprouting in a rat model of rubrospinal tract injury J. Neurochem., 134, 261-275

Dardou, D., Monlezun, S., Foerch, P., Courade, J-P., et al (2013) A role for Sv2c in basal ganglia functions Brain Res., 1507, 61-73

De Backer, M.W.A., Brans, M.A.D., van Rozen, A.J., van der Zwaal, E.M., et al (2010) Suppressor of cytokine signaling 3 knockdown in the mediobasal hypothalamus: counterintuitive effects on energy balance J. Mol. Endocrinol., 45, 341–353

De Guia, R.M., Rose, A.J., Sommerfeld, A., Seibert, O., Strzoda, D., Zota, A., Feuchter, Y., Krones-Herzig, A., Sijmonsma, T. et al (2015) microRNA-379 couples glucocorticoid hormones to dysfunctional lipid homeostasis EMBO J., 34, 344–360

De Solis, C.A., Holehonnur, R., Banerjee, A., Luong, J.A., Lella, S.K., Ho, A., Pahlavan, B. and Ploski, J.E. (2015) Viral delivery of shRNA to amygdala neurons leads to neurotoxicity and deficits in Pavlovian fear conditioning Neurobiol. Learn. Mem., 124, 34–47

Elagabani, M.N., Brisevac, D., Kintscher, M., Pohle, J., Köhr, G., Schmitz, D. and Kornau, H-C. (2016) Subunit-selective N-methyl-D-aspartate (NMDA) receptor signaling through brefeldin A-resistant Arf guanine nucleotide exchange factors BRAG1 and BRAG2 during synapse maturation J. Biol. Chem., 291, 9105–9118

Enomoto, M., Hirai, T., Kaburagi, H. and Yokota, T. (2016) Efficient gene suppression in dorsal root ganglia and spinal cord using adeno-associated virus vectors encoding short-hairpin RNA In SiRNA Delivery Methods: Methods and Protocols, Methods in Molecular Biology, vol. 1364 (eds. Shum, K. and Rossi, J.) Springer Science+Business Media New York, pp 277-290

Fechner, H. and Kurreck, J. (2012) Viral vectors for RNA interference applications in cancer research and therapy In Drug delivery in oncology: From basic research to cancer therapy, (ed. Kratz, F., Senter, P. and Steinhagen, H.) 1st edition, Wiley-VCH Verlag GmbH & Co. KgaA, pp 1415-1442

Gröbl, T., Hammer, E., Bien-Möller, S., Geisler, A., et al (2014) A novel artificial microRNA expressing AAV vector for phospholamban silencing in cardiomyocytes improves Ca2+ uptake into the sarcoplasmic reticulum PLoS One, 9: e92188

Huang, Z-R., Hu, Z-Z, Xie, P. and Liu, Q-H. (2017) Tyrosine-mutated AAV2-mediated shRNA silencing of PTEN promotes axon regeneration of adult optic nerve PLoS One, 12: e0174096

Ito, N., Sakai, A., Miyake, N., Maruyama, M., Iwasaki, H., Miyake, K., Okada, T., Sakamoto, A. and Suzuki, H. (2017) miR-15b Mediates oxaliplatin-induced chronic neuropathic pain through BACE1 downregulation Br. J. Pharmacol., 174, 386–395

Kang, H.J., Voleti, B., Hajszan, T., Rajkowska, G., et al (2012) Decreased expression of synapse-related genes and loss of synapses in major depressive disorder Nat. Med., 18, 1413-1419

Kanoski, S.E., Zhao, S., Guarnieri, D.J., DiLeone, R.J., et al (2012) Endogenous leptin receptor signaling in the medial nucleus tractus solitarius affects meal size and potentiates intestinal satiation signals Am. J. Physiol. Endocrinol. Metab., 303, E496–E503

Koornneef, A., Maczuga, P., van Logtenstein, R., Borel, F., et al (2011) Apolipoprotein B knockdown by AAVdelivered shRNA lowers plasma cholesterol in mice Mol. Ther., 19, 731–740

Kubodera, T., Yamada, H., Anzai, M., Ohira, S., et al (2011) In vivo application of an RNAi strategy for the selective suppression of a mutant allele Hum. Gene. Ther., 22, 27-34

Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E., et al (2012) Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens Nature, 487, 183-189

Maczuga, P., Lubelski, J., van Logtenstein, R., Borel, F., et al (2013) Embedding siRNA sequences targeting Apolipoprotein B100 in shRNA and miRNA scaffolds results in differential processing and in vivo efficacy Mol. Ther., 21, 217–227

Malmevik, J., Petri, R., Klussendorf, T., Knauff, P., Åkerblom, M., Johansson, J., Soneji, S. and Jakobsson, J. (2015) Identification of the miRNA targetome in hippocampal neurons using RIP-seq Sci. Rep., 5:12609

Malmevik, J., Petri, R., Knauff, P., Brattås. P.L., Åkerblom, M. and Jakobsson, J. (2016) Distinct cognitive effects and underlying transcriptome changes upon inhibition of individual miRNAs in hippocampal neurons Sci. Rep., 6: 19879

Mayra, A., Tomimitsu, H., Kubodera, T., Kobayashi, M., et al (2011) Intraperitoneal AAV9-shRNA inhibits target expression in neonatal skeletal and cardiac muscles Biochem. Biophys. Res. Comm., 405, 204–209

McBride, J.L., Pitzer, M.R., Boudreau, R.L., Dufour, B., et al (2011) Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington’s disease Mol. Ther., 19, 2152–2162

Mockenhaupt, S., Grosse, S., Rupp, D., Bartenschlager, R., and Grimm, D. (2015) Alleviation of off-target effects from vector-encoded shRNAs via codelivered RNA decoys Proc. Natl. Acad. Sci., 112, E4007-E4016

Nicolson, S.C. and Samulski, R.J. (2014) Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus J. Virol., 88, 4132–4144

Pinto, B.S., Saxena, T., Oliveira, R., Méndez-Gómez, H.R., Cleary, J.D., Denes, L.T., McConnell, O. et al (2017) Impeding transcription of expanded microsatellite repeats by deactivated Cas9 Mol. Cell 68, 479-490

Piras, B.A., O’Connor, D.M. and French, B.A. (2013) Systemic delivery of shRNA by AAV9 provides highly efficient knockdown of ubiquitously expressed GFP in mouse heart, but not liver PLoS One, 8: e75894

Reid, C.A., Boye, S.L., Hauswirth, W.W. and Lipinski, D.M. (2017) miRNA-mediated post-transcriptional silencing of transgenes leads to increased adeno-associated viral vector yield and targeting specificity Gene Ther., 24, 462–469

Rothe, D., Gisela Wajant, G., Grunert, H-P., Zeichhardt, H., et al (2010) Rapid Construction of adenoassociated virus vectors expressing multiple short hairpin RNAs with high antiviral activity against echovirus 30 Oligonucleotides, 20, 191-198

Sakai, A., Saitow, F., Maruyama, M., Miyake, N., Miyake, K., Shimada, T., Okada, T. and Suzuki, H. (2017) MicroRNA cluster miR-17-92 regulates multiple functionally related voltage-gated potassium channels in chronic neuropathic pain Nat. Comm., 8: 16079

Schaar, K., Geisler, A., Kraus, M., Pinkert, S., Pryshliak, M., Spencer, J.F., Tollefson, A.E., Ying, B. et al (2017) Anti-adenoviral artificial microRNAs expressed from AAV9 vectors inhibit human adenovirus infection in immunosuppressed Syrian hamsters Mol. Ther. Nucleic Acids, 8, 300-316

Schreiber, C.A., Sakuma, T., Izumiya, Y., Holditch, S.J., Hickey, R.D., Bressin, R.K., Basu, U., Koide, K., Asokan, A. and Ikeda, Y. (2015) An siRNA screen identifies the U2 snRNP spliceosome as a host restriction factor for recombinant adeno-associated viruses PLoS Pathog., 11: e1005082

Stoica, L., Todeasa, S.H., Cabrera, G.T., Salameh, J.S., ElMallah, M.K., Mueller, C., Brown, Jr, R.H., and Sena-Esteves, M. (2016) Adeno-associated virus–delivered artificial microRNA extends survival and delays paralysis in an amyotrophic lateral sclerosis mouse model Ann. Neurol., 79, 687–700

Taschenberger, G., Tereshchenko, J. and Kügler, S. (2017) A microRNA124 target sequence restores astrocyte specificity of gfaABC1D-driven transgene expression in AAV-mediated gene transfer Mol. Ther. Nucl. Acids 8, 13-25

Theis, T., Yoo, M., Park, C.S., Chen, J., Kügler, S., Gibbs, K.M. and Schachner, M. (2017) Lentiviral delivery of miR-133b improves functional recovery after spinal cord injury in mice Mol. Neurobiol., 54, 4659–4671

Ulusoy, A., Sahin, G., Björklund, T., Aebischer, P., et al (2009) Dose optimization for long-term rAAVmediated RNA interference in the nigrostriatal projection neurons Mol. Ther., 17, 1574-1584

Van Gestel, M.A., van Erp, S., Sanders, L.E., Brans, M.A.D., et al (2014) shRNA-induced saturation of the microRNA pathway in the rat brain Gene Ther., 21, 205–211

Woldemichael, B.T., Jawaid, A., Kremer, E.A., Gaur, N., Krol, J., Marchais, A. and Mansuy, I.M. (2016) The microRNA cluster miR-183/96/182 contributes to long-term memory in a protein phosphatase 1-dependent manner Nat. Comm., 7: 12594

Yoo, J., Hajjar, R.J. and Jeong, D. (2017) Generation of efficient miRNA inhibitors using tough decoy constructs In Cardiac Gene Therapy: Methods and Protocols, Methods Mol. Biol., 1521, (ed. Ishikawa, K.)

Springer Science+Business Media, New York, pp 41-53

Zheng, D., Sabbagh, J.J., Blair, L.J., Darling, A.L., Wen, X. and Dickey, C.A. (2016) MicroRNA-511 binds to FKBP5 mRNA, which encodes a chaperone protein, and regulates neuronal differentiation J. Biol. Chem., 291, 17897–17906

Salivary gland tranduction

Srinivasan, P., Shanmugam, T., Dayton, R.D., Palaniyandi, S., et al (2013) Recombinant AAV9-TLK1B administration ameliorates fractionated radiation-induced xerostomia Hum. Gene Ther., 24, 604–612

Sarcoplasmic reticulum

Gröbl, T., Hammer, E., Bien-Möller, S., Geisler, A., et al (2014) A novel artificial microRNA expressing AAV vector for phospholamban silencing in cardiomyocytes improves Ca2+ uptake into the sarcoplasmic reticulum PLoS One, 9: e92188

Self-complimentary genomes (sc-AAV-Cre vectors)

Hillestad, M.L., Guenzel, A.J., Nath, K.A. and Barry, M.A. (2012) A vector–host system to fingerprint virus tropism Hum. Gene Ther., 23, 1116–1126
Langouet-Astrie, C.J., Yang, Z., Polisetti, S.M., Welsbie, D.S., Hauswirth, W.W., Zack, D.J., Merbs, S.L. and Enke, R.A. (2016) Characterization of intravitreally delivered capsid mutant AAV2-Cre vector to induce tissuespecific mutations in murine retinal ganglion cells Exp. Eye Res., 151, 61-67

Lee, D-H., Park, J.O., Kim, T-S., Kim, S-K., Kim, T-h., Kim, M-c., Park, G.S., Kim, J-H., Kuninaka, S., Olson, E.N. et al (2016) LATS-YAP/TAZ controls lineage specification by regulating TGFβ signaling and Hnf4a expression during liver development Nat. Comm., 7: 11961

Prabhakar, S., Goto, J., Zuang, X., Sena-Esteves, M., et al (2013) Stochastic model of Tsc1 lesions in mouse brain PLoS One, 8: e64224

Wang, Y., Ling, C., Song, L., Wang, L., et al (2012) Limitations of encapsidation of recombinant selfcomplementary adeno-associated viral genomes in different serotype capsids and their quantitation Hum. Gene Ther. Methods, 23, 225–233

138. Skeletal muscle

AAV variants, transduction efficiency of
Chew, W.L., Tabebordbar, M., Cheng, J.K.W., Mali, P., Wu, E.Y., Ng, A.H.M., Zhu, K., Wagers, A.J. and Church, G.M. (2016) A multifunctional AAV–CRISPR–cas9 and its host response Nat. Meth., 13, 868-874

Choudhury, S.R., Fitzpatrick, Z., Harris, A.F., Maitland, S.A., Ferreira, J.S., Zhang, Y., Ma, S., Sharma, R.B. et al (2016) In vivo selection yields AAV-B1 capsid for central nervous system and muscle gene therapy Mol. Ther., 24, 1247–1257

Santiago-Ortiz, J., Ojala, D.S., Westesson, O., Weinstein, J.R., Wong, S.Y., Steinsapir, A., Kumar, S., Holmes, I and Schaffer, D.V. (2015) AAV ancestral reconstruction library enables selection of broadly infectious viral variants Gene Ther., 22, 934–946

Van Lieshout, L.P., Domm, J.M., Rindler, T.N., Frost, K.L., Sorensen, D.L., Medina, S.J., Booth, S.A., Bridges, J.P. and Wootton, S.K. (2018) A novel triple-mutant AAV6 capsid induces rapid and potent transgene expression in the muscle and respiratory tract of mice Mol. Ther. Meth.Clin. Dev., 9, 323-329

Xu, R., Jia, Y., Zygmunt, D.A., Cramer, M.L., Crowe, K.E., Shao, G., Maki, A.E., Guggenheim, H.N., Hood, B.C. et al (2018) An isolated limb infusion method allows for broad distribution of rAAVrh74.MCK.GALGT2 to leg skeletal muscles in the rhesus macaque Mol. Ther: Meth. Clin. Dev., 10, 89-104

Yi, H., Zhang, Q., Brooks, E.D., Yang, C., Thurberg, B.L., Kishnani, P.S. and Sun, B. (2017) Systemic correction of murine glycogen storage disease type IV by an AAV-mediated gene therapy Hum. Gene Ther., 28, 286-294

Acidic oligopeptide effects
Lee, N-C., Falk, D.J., Byrne, B.J., Conlon, T.J., et al (2012) An acidic oligopeptide displayed on AAV2 improves axial muscle tropism after systemic delivery Genet. Vacc. Ther., 10: 3

Actin cytoskeleton
Vassilopoulos, S., Gentil, C., Lainé, J., Buclez, P-O., Franck, A., et al (2014) Actin scaffolding by clathrin heavy chain is required for skeletal muscle sarcomere organization J. Cell Biol., 205, 377–393

AKT2/PKBß
Schultze, S.M., Dietrich, M., Hynx, D., Geier, A., Niessen, M., Spinas, G.A., Hemmings, B.A. and Tschopp, O. (2015) Reduced hepatic lipid content in Pten-haplodeficient mice because of enhanced AKT2/PKBb activation in skeletal muscle Liver Int., 35, 1354–1366

Alpha-1-antitrypsin
Song, S., Morgan, M., Ellis, T., Poirier, A., et al (1998) Sustained secretion of human alpha-1-antitrypsin from murine muscle transduced with adeno-associated virus vectors Proc. Natl. Acad. Sci. USA, 95, 14384-14388

Song, S., Embury, J., Laipis, P.J., Berns, K.I., et al (2001) Stable therapeutic serum levels of human alpha-1 antitrypsin (AAT) after portal vein injection of recombinant adeno-associated virus (rAAV) vectors Gene Ther., 8, 1299-1306

Alpha-sarcoglycan
Mendell, J.R., Rodino-Klapac, L.R., Rosales-Quintero, X., Kota, J., et al (2009) Limb-girdle muscular dystrophy type 2D gene therapy restores a-sarcoglycan and associated proteins Ann. Neurol., 66, 290-297

Mendell, J.R., Rodino-Klapac, L.R., Rosales, X.Q., Coley, B.D., et al (2010) Sustained alpha-sarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D Ann. Neurol. 68, 629–638

Rodino-Klapac, L.R., Lee, J-S., Mulligan, R.C., Clark, K.R., et al (2008) Lack of toxicity of alpha-sarcoglycan overexpression supports clinical gene transfer trial in LGMD2D Neurology, 71, 240-247

ALS (see “Amyotrophic lateral sclerosis”)
Alzheimer’s disease
Yang, J., Pattanayak, A., Song, M., Kou, J., Taguchi, H., et al (2013) Muscle-directed anti-Aβ single-chain antibody delivery via AAV1 reduces cerebral Aβ load in an Alzheimer’s disease mouse model J. Mol. Neurosci., 49, 277–288

Ancestral rAAvs, targeting of
Zinn, E., Pacouret, S., Khaychuk, V., Turunen, H.T., Carvalho, L.S., Andres-Mateos, E., Shah, S. Shelke, R. et al (2015) In silico reconstruction of the viral evolutionary lineage yields a potent gene therapy vector Cell Rep., 12, 1056–1068

Apo-E expression
Evans, V., Foster, H., Graham, I.R., Foster, K., et al (2008) Human apoliporotein E expression from mouse skeletal muscle by electrotransfer of nonviral DNA (plasmid) and pseudotyped recombinant adeno-associated virus (AAV2/7) Hum. Gene Ther., 19, 569-578

Evans, V.C., Graham, I.R., Athanasopoulos, T., Galley, D.J., et al (2011) Adeno-associated virus serotypes 7 and 8 outperform serotype 9 in expressing atheroprotective human apoE3 from mouse skeletal muscle Metab. Clin. Exp., 60, 491–498

Harris, J.D., Schepelmann, S., Athanasopoulos, T., Graham, I.R., et al (2002) Inhibition of atherosclerosis in apolipoprotein-E-deficient mice following muscle transduction with adeno-associated virus vectors encoding human apolipoprotein-E Gene Ther., 9, 21-29 138-10.

Autophagy
Al-Qusairi, L., Prokic, I., Amoasii, L., Kretz, C., Messaddeq, N., Mandel, J-L. and Laporte, J. (2013) Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways FASEB J., 27, 3384–3394

Caveolae disfunction
Lo, H.P., Nixon, S.J., Hall, T.E., Cowling, B.S., Ferguson, C., Morgan, G.P., Schieber, N.L., Fernandez-Rojo, M.A., Bastiani, M. et al (2015) The caveolin–cavin system plays a conserved and critical role in mechanoprotection of skeletal muscle J. Cell Biol., 210, 833–849

Desmin
Joanne, P., Chourbagi, O., Hourdé, C., Ferry, A., et al (2013) Viral-mediated expression of desmin mutants to create mouse models of myofibrillar myopathy Skelet. Muscle 3: 4

DNA-dependent protein kinase
Song, S., Laipis, P.J., Berns, K.I. and Flotte, T.R. (2001) Effect of DNA-dependent protein kinase on the molecular fate of the rAAV2 genome in skeletal muscle Proc. Natl. Acad. Sci. USA, 98, 4084-4088

Dynamin
Cowling, B.S., Toussaint, A., Amoasii, L., Koebel, P., Ferry, A., et al (2011) Increased expression of wild-type or a centronuclear myopathy mutant of dynamin 2 in skeletal muscle of adult mice leads to structural defects and muscle weakness Am. J. Pathol., 178, 2224-2235

Trochet, D., Prudhon, B., Jollet, A., Lorain, S. and Bitoun, M. (2016) Reprogramming the dynamin 2 mRNA by spliceosome-mediated RNA trans-splicing Mol. Ther. Nucleic Acids, 5: e362

Dysferlinopathy
Grose, W.E., Clark, K.R., Griffin, D., Malik, V., et al (2012) Homologous recombination mediates functional recovery of dysferlin deficiency following AAV5 gene transfer PLoS One, 7: e39233

Dyslipidaemias
Ross, C.J.D., Twisk, J., Meulenberg, J.M., Liu, G., et al (2004) Long-term correction of murine lipoprotein lipase deficiency with AAV1-mediated gene transfer of the naturally occurring LPLS447X beneficial mutation Hum. Gene Ther., 15, 906-919

Wang, L.F., Fan, L.M., Chen, B.R., Wang, R.N., et al (2002) Expression of lecithin cholesterol acyltransferase and/or apoA-I mediated by recombinant adeno-associated virus in myogenic cells Acta Biochim. Biophys. Sinica, 34, 33-38

Fibrosis
Karvinen, H., Pasanen, E., Rissanen, T.T., Korpisalo, P., et al (2011) Long-term VEGF-A expression promotes aberrant angiogenesis and fibrosis in skeletal muscle Gene Ther., 18, 1166–1172

Schwarz, E. M. (2000) The adeno-associated virus vector for orthopaedic gene therapy Clin. Orthop. Relat. Res., 379S, S31-S39

Follistatin
Foley, J.W., Bercury, S.D., Finn, P., Cheng, S.H., et al (2010) Evaluation of systemic follistatin as an adjuvant to stimulate muscle repair and improve motor function in Pompe mice Mol. Ther., 9, 1584–1591

Kota, J., Handy, C.R., Haidet, A.M., Montgomery, C.L., et al (2009) Follistatin gene delivery enhances muscle growth and strength in nonhuman primates Sci. Transl. Med., 1: 6ra15

Histone deacetylases
Berdeaux, R., Goebel, N., Banaszynski, L., Takemori, H., et al (2007) SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes Nat. Med., 13, 597-603

Immune response
Aubert, D., Pichard, V., Durand, S., Moullier, P., et al (2003) Cytotoxic immune response after retroviralmediated hepatic gene transfer in rat does not precludenexpression from adeno-associated virus 1 transducted muscles Hum. Gene Ther., 14, 473-481

Insulin resistance/therapy
Awazawa, M., Gabel, P., Tsaousidou, E., Nolte, H., Krüger, M., Schmitz, J., Ackermann, P.J., Brandt, C., Altmüller, J. et al (2017) A microRNA screen reveals that elevated hepatic ectodysplasin A expression contributes to obesity-induced insulin resistance in skeletal muscle Nat. Med., 23, 1466-1473

Carrig, S., Bijjiga, E., Wopat, M.J. and Martino, A.T. (2016) Insulin therapy improves adeno-associated virus transduction of liver and skeletal muscle in mice and cultured cells Hum. Gene Ther., 27, 892-905

Ischaemia
Katwal, A.B., Konkalmatt, P.R., Piras, B.A., Hazarika, S., et al (2013) Adeno-associated virus serotype 9 efficiently targets ischemic skeletal muscle following systemic delivery Gene Ther., 20, 930–938

Saqib, A., Prasad, K-M.R., Katwal, A.B., Sanders, J.M., et al (2011) Adeno-associated virus serotype 9- mediated overexpression of extracellular superoxide dismutase improves recovery from surgical hind-limb ischemia in BALB/c mice J. Vasc. Surg., 54, 810-8

McArdle’s disease
Howell, J. McC., Walker, K.R., Davies, L., Dunton, E., et al (2008) Adenovirus and adeno-associated virusmediated delivery of human myophosphorylase cDNA and LacZ cDNA to muscle in the ovine model of McArdle’s disease: Expression and re-expression of glycogen phosphorylase Neuromusc. Disord., 18, 248-258

Metastatic cancers
Wang, G., Biswas, A.K., Ma, W., Kandpa, M., Coker, C., Grandgenett, P.M., Hollingsworth, M.A., Jain, R., Tanji, K., et al (2018) Metastatic cancers promote cachexia through ZIP14 upregulation in skeletal muscle Nat. Med., 770, 770–781

Muscular dystrophy (incl. y-sarcoglycanopathy)
Athanasopoulos, T., Graham, I.R., Foster, H. and Dickson, G. (2004) Recombinant adeno-associated viral (rAAv) vectors as therapeutic tools for duchenne muscular dystrophy (DMD) Gene Ther., 11, 109-121

Fabb, S.A., Wells, D.J., Serpente, P. and Dickson, G. (2002) Adeno-associated virus vector gene transfer and sarcolemmal expression of a 144 kDa micro-dystrophin effectively restores the dystrophin-associated protein complex and inhibits myofibre degeneration in nude/mdx mice Hum. Mol. Genet., 11, 733-741

Foster, H., Sharp, P.S., Athanasopoulos, T., Trollet, C., et al (2008) Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer Mol. Ther., 16, 1825-1832

Ghahramani Seno, M.M., Graham, I.R., Athanasopoulos, T. Trollet, C., et al (2008) RNAi-mediated knockdown of dystrophin expression in adult mice does not lead to overt muscular dystrophy pathology Hum. Mol. Genet., 17, 2622-2632

Goyenvalle, A., Babbs, A., Wright, J., Wilkins, V., et al (2012) Rescue of severely affected dystrophin/utrophin deficient mice through scAAV-U7snRNA-mediated exon skipping Hum. Mol, Genet., 21, 2559–2571

Goyenvalle, A., Wright, J., Babbs, A., Wilkins, V., et al (2012) Engineering multiple U7snRNA constructs to induce single and multiexon-skipping for Duchenne muscular dystrophy Mol. Ther., 20, 1212-1221

Grose, W.E., Clark, K.R., Griffin, D., Malik, V., et al (2012) Homologous recombination mediates functional recovery of dysferlin deficiency following AAV5 gene transfer PLoS One, 7: e39233

Heller, K.N., Montgomery, C.L., Janssen, P.M.L., Clark, K.R., et al (2013) AAV-mediated overexpression of human α7 integrin leads to histological and functional improvement in dystrophic mice Mol. Ther., 21, 520–525

Herson, S., Hentati, F., Rigolet, A., Behin, A., Romero, N.B., et al (2012) A phase I trial of adeno-associated virus serotype1--sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C Brain, 135, 483–492

Kemaladewi, D.U., Maino, E., Hyatt, E., Hou, H., Ding, M., Place, K.M., Zhu, X., Bassi, P. et al (2017) Correction of a splicing defect in a mouse model of congenital muscular dystrophy type 1A using a homologydirected-repair-independent mechanism Nat. Med., 23, 984-989

Kodippili, K. and Duan, D, (2018) Expressing full-length dystrophin using adeno-associated virus In Gene Therapy in Neurological Disorders Elsevier Inc. pp 259-276

Koo, T., Malerba, A., Athanasopoulos, T., Trollet, C., et al (2011) Delivery of AAV2/9-microdystrophin genes incorporating helix 1 of the coiled-coil motif in the C-terminal domain of dystrophin improves muscle pathology and restores the level of a1-syntrophin and a-dystrobrevin in skeletal muscles of mdx mice Hum. Gene Ther., 22, 1379–1388

Koo, T., Popplewell, L., Athanasopoulos, T., and Dickson, G. (2014) Triple trans-splicing adeno-associated virus vectors capable of transferring the coding sequence for full-length dystrophin protein into dystrophic mice Hum. Gene Ther., 25, 98–108

Koo, T., Lu-Nguyen, N.B., Malerba, A., Kim, E., Kim, D., Cappellari, O., Cho, H-Y., Dickson, G., Popplewell, L. and Kim, J-S. (2018) Functional rescue of dystrophin deficiency in mice caused by frameshift mutations using Campylobacter jejuni Cas9 Mol. Ther., 26, 1529-1538

Larochelle, N., Teng, Q., Gilbert, R., Deol, J.R., et al (2010) Modulation of coxsackie and adenovirus receptor expression for gene transfer to normal and dystrophic skeletal muscle J. Gene Med., 12, 266–275

Malerba, A., Klein, P., Bachtarzi, H., Jarmin, S.A., Cordova, G., Ferry, A., Strings, V., Espinoza, M.P., Mamchaoui, K. et al (2017) PABPN1 gene therapy for oculopharyngeal muscular dystrophy Nat Comm., 8:14848

Martin, P.T., Xu, R., Rodino-Klapac, L.R., Oglesbay, E., et al (2009) Overexpression of Galgt2 in skeletal muscle prevents injury resulting from eccentric contractions in both mdx and wild-type mice Am. J. Physiol. Cell Physiol., 296, C476–C488

Mendell, J.R., Rodino-Klapac, L.R., Rosales-Quintero, X., Kota, J., et al (2009) Limb-girdle muscular dystrophy type 2D gene therapy restores -sarcoglycan and associated proteins Ann. Neurol., 66, 290-297

Mendell, J.R., Rodino-Klapac, L.R., Rosales, X.Q., Coley, B.D., et al (2010) Sustained alpha-sarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D Ann. Neurol. 68, 629–638

Rodino-Klapac, L.R., Janssen, P.M.L., Montgomery, C.L., Coley, B.D., et al (2007) A translational approach for limb vascular delivery of the micro-dystrophin gene without volume or high pressure for treatment of Duchenne muscular dystrophy J. Translat. Med., 5:45

Voit, A., Patel, V., Pachon, R., Shah, V., Bakhutma, V., Kohlbrenner, E., McArdle, J.J., Dell’Italia, L.J., Mendell, J.R. et al (2017) Reducing sarcolipin expression mitigates Duchenne muscular dystrophy and associated cardiomyopathy in mice Nat. Comm., 8: 1068

Wein, N., Vulin, A., Falzarano, M.S., Al-Khalili Szigyarto, C., Maiti, B., Findlay, A., Heller, K.N., Uhlén, M., Bakthavachalu, B., Messina, S. et al (2014) Translation from a DMD exon 5 IRES results in a functional dystrophin isoform that attenuates dystrophinopathy in humans and mice Nat. Med., 9, 992-1000

Muscular hypotrophy
Al-Qusairi, L., Prokic, I., Amoasii, L., Kretz, C., et al (2013) Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways FASEB J., 27, 3384–3394

Tasfaout, H., Lionello, V.M., Kretz, C., Koebel, P., Messaddeq, N., Bitz, D., Laporte, J. and Cowling, B.S. (2018) Single intramuscular injection of AAV-shRNA reduces DNM2 and prevents myotubular myopathy in mice Mol. Ther., 26, 1082-1092

Myofibre transduction
Riaz, M., Raz, Y., Moloney, E.B., van Putten, M., Krom, Y.D., van der Maarel, S.M., Verhaagen, J. and Raz, V. (2015) Differential myofiber-type transduction preference of adeno-associated virus serotypes 6 and 9 Skelet. Muscle, 5: 37

Myostatin
Cleasby, M.E., Jarmin, S., Eilers, W., Elashry, M., et al (2014). Local overexpression of the myostatin propeptide increases glucose transporter expression and enhances skeletal muscle glucose disposal. Am. J. Physiol. Endocrinol. Metab., 306,:E814–E823

Myofibrillar myopathy
Joanne, P., Chourbagi, O., Hourdé, C., Ferry, A., et al (2013) Viral-mediated expression of desmin mutants to create mouse models of myofibrillar myopathy Skelet. Muscle 3: 4

Narcolepsy
Liu, M., Blanco-Centurion, C., Konadhode, R., Begum, S., et al (2011) Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice J. Neurosci., 31, 6028–6040

Neprilysin
Liu, Y., Studzinski, C., Beckett, T., Guan, H., et al (2009) Expression of neprilysin in skeletal muscle reduces amyloid burden in a transgenic mouse model of Alzheimer disease Mol. Ther., 17, 1381–1386

Liu, Y., Studzinski, C., Beckett, T., Murphy, M.P., et al (2010) Circulating neprilysin clears brain amyloid Mol. Cell. Neurosci., 45, 101–107

Pompe disease
Foley, J.W., Bercury, S.D., Finn, P., Cheng, S.H., et al (2010) Evaluation of systemic follistatin as an adjuvant to stimulate muscle repair and improve motor function in Pompe mice Mol. Ther., 9, 1584–1591

Yi, H., Fredrickson, K.B., Das, S., Kishnani, P.S. and Sun, B. (2013) Stbd1 is highly elevated in skeletal muscle of Pompe disease mice but suppression of its expression does not affect lysosomal glycogen accumulation Mol. Genet. Metab., 109, 312–314

Zhu, Y., Jiang, J-L., Gumlaw, N.K., Zhang, J., et al (2009) Glycoengineered acid α-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of Pompe disease Mol. Ther., 17, 954-963

Regeneration
Bryan, B.A., Mitchell, D.C., Zhao, L., Ma, W., et al (2005) Modulation of muscle regeneration, myogenesis, and adipogenesis by the Rho family nucleotide exchange factor GEFT Mol. Cell. Biol., 25, 11089-11101

RNA: shRNA-AAV
Mayra, A., Tomimitsu, H., Kubodera, T., Kobayashi, M., et al (2011) Intraperitoneal AAV9-shRNA inhibits target expression in neonatal skeletal and cardiac muscles Biochem. Biophys. Res. Comm., 405, 204–209

Sarcomere organization
Vassilopoulos, S., Gentil, C., Lainé, J., Buclez, P-O., Franck, A., et al (2014) Actin scaffolding by clathrin heavy chain is required for skeletal muscle sarcomere organization J. Cell Biol., 205, 377–393

Tibialis anterior injection
Beilschmidt, L.K., Ollagnier de Choudens, S., Fournier, M., Sanakis, I., Hograindleur, M-A., Clémancey, M., Blondin, G., Schmucker, S., Eisenmann, A. et al (2017) ISCA1 is essential for mitochondrial Fe4S4 biogenesis in vivo Nat Comm., 8: 15124

Transgene expression
Chenuaud, P., Larcher, T., Rabinowitz, J.E., Provost, N., et al (2004) Optimal design of a single recombinant adeno-associated virus derived from serotypes 1 and 2 to achieve more tightly regulated transgene expression from nonhuman primate muscle Mol. Ther., 9, 410-418

Ren, C., Kumar, S., Shaw, D.R. and Ponnazhagan, S. (2005) Genomic stability of self-complementary adenoassociated virus 2 during early stages of transduction in mouse muscle in vivo Hum. Gene Ther., 16, 1-11

Wnt/ß-catenin signalling
Aslanidi, G., Kroutov, V., Philipsberg, G., Lamb, K., et al (2007) Ectopic expression of Wnt10b decreases adiposity and improves glucose homeostasis in obese rats Am. J. Physiol. Endocrinol. Metab., 293, E726-E736

Skin targeting

Balaji, S., King, A., Dhamija, Y., Le, L.D., et al (2013) Pseudotyped adeno-associated viral vectors for gene transfer in dermal fibroblasts: implications for wound-healing applications J. Surg. Res., 184, 691-698

Braun-Falco, M., Eisenried, A., Büning, H. and Ring, J. (2005) Recombinant adeno-associated virus type 2- mediated gene transfer into human keratinocytes is influenced by both the ubiquitin/proteasome pathway and epidermal growth factor receptor tyrosine kinase Arch. Dermatol. Res., 296, 528-535

Büning, H., Braun-Falco, M. and Hallek, M. (2004) Progress in the use of adeno-associated viral vectors for gene therapy Cell. Tissue. Organ., 177, 139-150

Cross, K.J., Bomsztyk, E.D., Weinstein, A.L., Teo, E.H., et al (2009) A novel method for targeted gene therapy in ischemic tissues through viral transfection of an expression cassette containing multiple repetitions of hypoxia response element Plast. Reconstr. Surg. 123: Suppl 76S

Petek, L.M., Fleckman, P. and Miller, D.G. (2010) Efficient KRT14 targeting and functional characterization of transplanted human keratinocytes for the treatment of epidermolysis bullosa simplex Mol. Ther., 9, 1624–1632

Roedl, D., Oji, V., Buters, J.T.M., Behrendt, H. et al (2011) rAAV2-Mediated restoration of LEKTI in LEKTIdeficient cells from Netherton patients J. Dermatol. Sci., 61, 194–198

Smoking

Hicks, M.J., Rosenberg, J.B., De, B.P., Pagovich, O.E., Young, C.N., Qiu, J-P. et al (2012) AAV-directed persistent expression of a gene encoding anti-nicotine antibody for smoking cessation Sci. Transl. Med., 4: 140ra87

Spermatogenesis

Watanabe, S., Kanatsu-Shinohara, M., Ogonuki, N., Matoba, S., Ogura, A. and Shinohara, T. (2017) Adenoassociated virus-mediated delivery of genes to mouse spermatogonial stem cells Biol. Reprod., 96, 221–231

Spleen delivery

Miyake, N., Miyake, K., Yamamoto, M., Hirai, Y., et al (2011) Global gene transfer into the CNS across the BBB after neonatal systemic delivery of single-stranded AAV vectors Brain Res., 1389, 19-26

Stem cell delivery

Bartel, M.A. and Schaffer, M.A. (2014) Enhanced gene targeting of adult and pluripotent stem cells using evolved adeno-associated virus In Methods Mol. Biol., 1114, Gene Correction: Methods and Protocols, (ed. Storici, F.) Springer Science+Business Media, LLC pp 169-179

Brown, N., Song, L., Kollu, N.R. and Hirsch, M.L. (2017) Adeno-associated virus vectors and stem cells: friends or foes? Hum. Gene Ther., 28, 450-463

Chen, K.A., Cruz. P.E., Lanuto, D.J., Flotte, T.R., et al (2011) Cellular fusion for gene delivery to SCA1 affected Purkinje neurons Mol. Cell. Neurosci., 47, 61–70

Han, Z., Zhong, L., Maina, N., Hu, Z., et al (2008) Stable integration of recombinant adeno-associated virus vector genomes after transduction of murine hematopoietic stem cells Hum. Gene Ther., 19, 267-278

Jang, J-H., Koerber, J.T., Kim, J-S., Asuri, P., et al (2011) An evolved adeno-associated viral variant enhances gene delivery and gene targeting in neural stem cells Mol. Ther., 19, 667–675

Kumar, S., Nagy, T.R. and Ponnazhagan, S. (2010) Therapeutic potential of genetically modified adult stem cells for osteopenia Gene Ther., 17, 105–116

Kumar, S., Wan, C., Ramaswamy, G., Clemens, T.L., et al (2010) Mesenchymal stem cells expressing osteogenic and angiogenic factors synergistically enhance bone formation in a mouse model of segmental bone defect Mol. Ther., 18, 1026–1034

Ling, C., Bhukhai, K., Yin, Z., Tan, M., Yoder, M.C., Leboulch, P., Payen, E. and Srivastava, A. (2016) Highefficiency transduction of primary human hematopoietic stem/progenitor cells by AAV6 vectors: strategies for overcoming donor-variation and implications in genome editing Sci. Rep., 6: 35495

Locke, M., Ussher, J.E., Mistry, R., Taylor, J.A., et al (2011) Transduction of human adipose-derived mesenchymal stem cells by recombinant adeno-associated virus vectors Tissue Eng., 17, 949-959

McMahon, J.M., Conroy, S., Lyons, M., Greiser, U., et al (2006) Gene transfer into rat mesenchymal stem cells: a comparative study of viral and nonviral vectors Stem Cell. Dev., 15, 87-96

Mitsui, K., Suzuki, K., Aizawa, E., Kawase, E., et al (2009) Gene targeting in human pluripotent stem cells with adeno-associated virus vectors Biochem. Biophys. Res. Commun., 388, 711–717

Ojala, D.S., Sun, S., Santiago-Ortiz, J.L., Shapiro, M.G., Romero, P.A. and Schaffer, D.V. (2018) In vivo selection of a computationally designed SCHEMA AAV library yields a novel variant for infection of adult neural stem cells in the SVZ Mol. Ther., 26, 304-319

Rapti, K., Stillitano, F., Karakikes, I., Nonnenmacher, M., Weber, T., Hulot, J-S. and Hajjar, R.J. (2015) Effectiveness of gene delivery systems for pluripotent and differentiated cells Mol. Ther. Methods Clin, Dev., 2: 14067

Ren, C., Kumar, S., Chanda, D., Chen, J., et al (2008) Therapeutic potential of mesenchymal stem cells producing interferon- in a mouse melanoma lung metastasis model Stem Cells, 26, 2332-2338

Ryu, B.Y., Evans-Galea, M.V., Gray, J.T., Bodine, D.M., et al (2008) An experimental system for the evaluation of retroviral vector design to diminish the risk for proto-oncogene activation Blood, 111, 1866-1875

Sather, B.D., Romano Ibarra, G.S., Sommer, K., Curinga, G., Hale, M., Khan, I.F., Singh, S., Song, Y. et al (2015) Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template Sci. Transl. Med., 7: 307ra156

Schuhmann, N.K., Pozzoli, O., Sallach, J., Huber, A., Avitabile, D., Perabo, L., Rappl, G., Capogrossi, M.C., Hallek, M., Pesce, M. and Büning, H. (2010) Gene transfer into human cord blood-derived CD34+ cells by adeno-associated viral vectors Exp. Hematol., 38, 707–717

Sellner, L., Stiefelhagen, M., Kleinschmidt, J.A., Laufs, S., et al (2008) Generation of efficient human blood progenitor- targeted recombinant adeno-associated viral vectors (AAV) by applying an AAV random peptide library on primary human hematopoietic progenitor cells Exp. Hematol., 957, 957-964

Senís, E., Mosteiro, L., Wilkening, S., Wiedtke, E., Nowrouzi, A., Afzal, S., Fronza, R., Landerer, H., Abad, M. et al (2018) AAVvector-mediated in vivo reprogramming into pluripotency Nat. Comm., 9: 2651

Song, L., Li, X., Jayandharan, G.R., Wang, Y., Aslanidi, G.V., et al (2013) High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineage-restricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo PLoS One, 8: e58757

Song, L., Kauss, M.A., Kopin, E., Chandra, M., et al (2013) Optimizing the transduction efficiency of capsidmodified AAV6 serotype vectors in primary human hematopoietic stem cells in vitro and in a xenograft mouse model in vivo Cytotherapy, 15, 986-998

Stiefelhagen, M., Sellner, L., Kleinschmidt, J.A., Jauch, A., et al (2008) Application of a haematopoetic progenitor cell-targeted adeno-associated viral (AAV) vector established by selection of an AAV random peptide library on a leukaemia cell line Genet., Vaccines Ther., 6:12

Vakulskas, C.A., Dever, D.P., Rettig, G.R., Turk, R., Jacobi, A.M., Collingwood, M.A., Bode, N.M., McNeill, M.S., Yan, S. et al (2018) A high-fidelity Cas9 mutant delivered as a ribonucleoprotein complex enables efficient gene editing in human hematopoietic stem and progenitor cells Nat. Med., 24, 1216–1224

Watanabe, S., Kanatsu-Shinohara, M., Ogonuki, N., Matoba, S., Ogura, A. and Shinohara, T. (2017) Adenoassociated virus-mediated delivery of genes to mouse spermatogonial stem cells Biol. Reprod., 96, 221–231

Weltner, J., Anisimov, A., Alitalo, K., Otonkoski, T., et al (2012) Induced pluripotent stem cell clones reprogrammed via recombinant adeno-associated virus-mediated transduction contain integrated vector sequences J. Virol., 86, 4463–4467

Targeting/delivery mechanisms

Bennett, A.D., Wong, K., Lewis, J., Tseng, Y-S., Smith, J.K., Chipman, P., McKenna, R., Samulski, R.J., Kleinschmidt, J. and Agbandje-McKenna, M. (2018) AAV6 K531 serves a dual function in selective receptor and antibody ADK6 recognition Virology, 518, 369–376

Büning, H., Ried, M.U., Perabo, L., Gerner, N.A., et al (2003) Receptor targeting of adeno-associated virus vectors Gene Ther. 10, 1142-1151

Chtarto, A., Bender, H.U., Hanemann, C.O., Kemp, T., et al (2003) Tetracycline-inducible transgeneexpression mediated by a single AAV vector Gene Ther., 10, 84-94

Fenno, L.E., Mattis, J., Ramakrishnan, C., Hyun, M., Lee, S.Y., He, M., Tucciarone, J., Selimbeyoglu, A., Berndt, A., Grosenick, L. et al (2014) Targeting cells with single vectors using multiple-feature Boolean logic Nature Meth., 11, 762-772

Henckaerts, E., Dutheil, N., Zeltner, N., Kattman, S., et al (2009) Site-specific integration of adeno-associated virus involves partial duplication of the target locus Proc. Natl. Acad. Sci. USA, 106, 7571–7576

Hirata, R.K., Xu, C., Dong, R., Miller, D., et al (2004) Efficient PRNP gene targeting in bovine fibroblasts by adeno-associated virus vectors Cloning Stem Cells, 6, 31-36

Hirata, R., Chamberlain, J., Dong, R. and Russell, D.W. (2002) Targeted transgene insertion into human chromosomes by adeno-associated virus vectors Nat. Biotechnol., 20, 735-738

Judd, J., Ho, M.L., Tiwari, A., Gomez, E.J., et al (2014) Tunable protease-activatable virus nanonodes ACS Nano, 8, 4740–4746

Lu, Y. (2004) Recombinant adeno-associated virus as delivery vector for gene therapy – a review Stem Cells Dev., 13, 133-145

Müller, O.J., Kaul, F., Weitzman, M.D., Pasqualini, R., et al (2003) Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors Nat. Biotechnol., 21, 1040-1046

Maheshri, N., Koerber, J.T., Kaspar, B.K. and Schaffer, D.V. (2006) Directed evolution of adeno-associated virus yields enhanced gene delivery vectors Nat. Biotechnol., 24, 198-204

Michelfelder, S., Kohlschütter, J., Skorupa, A., Pfennings, S, et al (2009) Successful expansion but not complete restriction of tropism of adeno-associated virus by in vivo biopanning of random virus display peptide libraries PLoS One 4:e5122

Mitchell, A.M., Li, C. and Samulski, R.J. (2013) Arsenic trioxide stabilizes accumulations of adeno-associated virus virions at the perinuclear region, increasing transduction in vitro and in vivo J. Virol., 87, 4571–4583

Negishi, A., Chen, J., McCarty, D.M., Samulski, R.J., et al (2004) Analysis of the interaction between adenoassociated virus and heparan sulfate using atomic force microscopy Glycobiology, 14, 969-977

Reid, C.A., Boye, S.L., Hauswirth, W.W. and Lipinski, D.M. (2017) miRNA-mediated post-transcriptional silencing of transgenes leads to increased adeno-associated viral vector yield and targeting specificity Gene Ther., 24, 462–469

Ried, M.U., Girod, A., Leike., K., Büning, H. et al (2002) Adeno-associated virus capsids displaying immunoglobulin-binding domains permit antibody-mediated vector retargeting to specific cell surface receptors J. Virol., 76, 4559-4566

Raupp, C., Naumer, M., Müller, O.J., Gurda, B.L., et al (2012) The threefold protrusions of adeno-associated virus type 8 are involved in cell surface targeting as well as post-attachment processing J. Virol., 86, 9396-9408

Shi, W., Arnold, G.S. and Bartlett, J.S. (2001) Insertional mutagenesis of the adeno-associated virus type 2 (AAV2) capsid gene and generation of AAV2 vectors targeted to alternative cell-surface receptors Hum. Gene Ther., 12, 1697-1711

Shi, W. and Bartlett, J.S. (2003) RGD inclusion in VP3 provides adeno-associated virus type 2 (AAV2)-based vectors with a heparan sulfate-independent cell entry mechanism Mol. Ther., 7, 515-525

Stachler, M.D., Chen, I., Ting, A.Y. and Bartlett, J.S. (2008) Site-specific modification of AAV vector particles with biophysical probes and targeting ligands using biotin ligase Mol. Ther., 16, 1467-1473

Vasileva, A., Linden, R.M. and Jessberger, R. (2006) Homologous recombination is required for AAV-mediated gene targeting Nucleic Acids Res., 34, 3345-3360

Ying, Y., Müller, O.J., Goehringer, C., Leuchs, B., et al (2010) Heart-targeted adeno-associated viral vectors selected by in vivo biopanning of a random viral display peptide library Gene Ther., 17, 980–990

T-cell activation

Huang, J., Li, X., Coelho-dos-Reis, J.G.A., Wilson, J.M., Tsuji, M. (2014) An AAV vector-mediated gene delivery approach facilitates reconstitution of functional human CD8+ T cells in mice PLoS One, 9: e88205

Mays, L.E., Wang, L., Tenney, R., Bell, P., et al (2013) Cell activation to the immunogenic adeno-associated virus capsid from isolate rhesus 32.33 J. Virol., 87, 9473–9485

Transforming growth factor ß (TGF-ß) signalling

Jäger, J., Greiner, V., Strzoda, D., Seibert, O., Niopek, K., Sijmonsma, D.P., Schäfer, M. et al (2014) Hepatic transforming growth factor- 1 stimulated clone-22 D1 controls systemic cholesterol metabolism Mol. Metab., 3, 155–166

Lee, D-H., Park, J.O., Kim, T-S., Kim, S-K., Kim, T-h., Kim, M-c., Park, G.S., Kim, J-H., Kuninaka, S., Olson, E.N. et al (2016) LATS-YAP/TAZ controls lineage specification by regulating TGFβ signaling and Hnf4a expression during liver development Nat. Comm., 7: 11961

Sun, F., Li, X., Duan, W-Q., Tian, W., Gao, M., Yang, J., Wu, X-Y., Huang, D. et al (2017) Transforming growth factor-β receptor III is a potential regulator of ichemia-induced cardiomyocyte apoptosis J. Am. Heart Assoc., 6: e005357

Thymic delivery

Chu, Q., Moreland, R.J., Gao, L., Taylor, K.M., Meyers. E., Cheng, S.H. and Scheule, R.K. (2010) Induction of immune tolerance to a therapeutic protein by intrathymic gene delivery Mol. Ther., 18, 2146–2154

Tissue specificity

Chen, S-J., Johnston, J., Sandhu, A., Bish, L.T., et al (2013) Enhancing the utility of adeno-associated virus gene transfer through inducible tissue-specific expression Hum. Gene Ther. Methods, 24, 270–278

TNF-a

Alto, L.T., Chen, X., Ruhn, K.A., Trevino. I. and Tansey, M.G. (2014) AAV-dominant negative tumor necrosis factor (DN-TNF) gene transfer to the striatum does not rescue medium spiny neurons in the YAC128 mouse model of Huntington’s disease PLoS One, 9: e96544

Yan, Z., Lei-Butters, D., Engelhardt, J.F. and Leno, G.H. (2009) Indexing TNF-α gene expression using a genetargeted reporter cell line BMC Biol., 7:8 Weinberg, M.S., Blake, B.L. and McCown, T.J. (2013) Opposing actions of hippocampus TNFα receptors on limbic seizure susceptibility Exp. Neurol., 247, 429–437

Transduction efficiency/inhibition

Arap, M.A., Lahdenranta, J., Hajitou, A., Marini, F.C., et al (2004) Model of unidirectional transluminal gene transfer Mol. Ther., 9, 305-310

Aslanidi, G.V., Rivers, A.E., Ortiz, L., Govindasamy, L., et al (2012) High-efficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors Vaccine, 30, 3908– 3917

Fan, S., Maguire, C.A., Ramirez, S.H., Bradel-Tretheway, B., (2005) Valproic acid enhances gene expression from viral gene transfer vectors J. Virol. Methods, 125, 23-33

Fluri, D.A., Daoud-el baba, M. and Fussenegger, M.T (2007) Adeno-associated viral vectors engineered for macrolide-adjustable transgene expression in mammalian cells and mice BMC Biotech., 7:75

Gurda, B.L., Raupp, C., Popa-Wagner, R., Naumer, M., et al (2012) Mapping a neutralizing epitope onto the capsid of adeno-associated virus serotype 8 J. Virol., 86, 7739–7751

Hölscher, C., Sonntag, F., Henrich, K., Chen, Q., Beneke, J., Matula, P., Rohr, K.. Kaderali, L. et al (2015) The SUMOylation pathway restricts gene transduction by adeno-associated viruses PLoS Pathog., 11: e1005281

Huang, L-Y., Patel, A., Ng, R., Miller, E.B., Halder, S., McKenna, R., Asokan, A. and Agbandje-McKenna, M. (2016) Characterization of the adeno-associated virus 1 and 6 sialic acid binding site J. Virol., 90, 5219-6230

Kanaan, N.M., Sellnow, R.C., Boye, S.L., Coberly, B., Bennett, A., Agbandje-McKenna, M., Sortwell, C.E. et al (2017) Rationally engineered AAV capsids improve transduction and volumetric spread in the CNS Mol. Ther. Nucleic Acids, 8, 184-197

Lee, N-C., Falk, D.J., Byrne, B.J., Conlon, T.J., et al (2012) An acidic oligopeptide displayed on AAV2 improves axial muscle tropism after systemic delivery Genet. Vacc. Ther., 10: 3

McCarty, D.M., Fu, H., Monahan, P.E., Toulson, C.E., et al (2003) Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo Gene Ther., 10, 2112-2118

McFarland, N.R., Lee, J-S., Hyman, B.T. and McLean, P.J. (2009) Comparison of transduction efficiency of  recombinant AAV serotypes 1, 2, 5 and 8 in the rat nigrostriatal system J. Neurochem., 109, 838–845

Mitchell, A.M., Li, C. and Samulski, R.J. (2013) Arsenic trioxide stabilizes accumulations of adeno-associated virus virions at the perinuclear region, increasing transduction in vitro and in vivo J. Virol., 87, 4571–4583

Nathwani, A.C., Cochrane, M., McIntosh, J., Ng, C.Y.C., et al (2009) Enhancing transduction of the liver by adeno-associated viral vectors Gene Ther., 16, 60–69

Paneda, A., Vanrell, L., Mauleon, I., Crettaz, J.S., et al (2009) Effect of adeno-associated virus serotype and genomic structure on liver transduction and biodistribution in mice of both genders Hum. Gene Ther., 20, 908-917

Perabo, L., Büning, H., Kofler, D.M., Ried, M.U., et al (2003) In vitro selection of viral vectors with modified tropism: the adeno-associated virus display Mol. Ther., 8, 151-157

Petrs-Silva. H., Dinculescu, A., Li, Q., Min, S-H., et al (2009) High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors Mol., Ther., 17, 463–471

Popp, L., Gomez, E., Orji, W., Ho, M., Suh, J. and Segatori, L. (2017) TFEB-mediated activation of the lysosome-autophagy system affects the transduction efficiency of adeno-associated virus 2 Virology, 510, 1–8

Prudencio, M., Jansen-West, K.R., Lee, W.C., Gendron, T.F., et al (2012) Misregulation of human sortilin splicing leads to the generation of a nonfunctional progranulin receptor Proc. Natl. Acad. Sci. USA, 109, 21510–21515

Rabinowitz, J.E., Rolling, F., Li, C., Conrath, H., et al (2002) Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity J. Virol., 76, 791-801

Ren, C., Kumar, S., Shaw, D.R. and Ponnazhagan, S. (2005) Genomic stability of self-complementary adenoassociated virus 2 during early stages of transduction in mouse muscle in vivo Hum. Gene Ther., 16, 1-11

Seppen, J., Bakker, C., de Jong, B., Kunne, C., et al (2006) Adeno-associated virus vector serotypes mediate sustained correction of bilirubin UDP glucuronosyltransferase deficiency in rats Mol. Ther., 13, 1085-1092

Shen, W-Y., Lai, Y.K.Y., Lai, C-M. and Rakoczy, P.E. (2003) Impurity of recombinant adeno-associated virus type 2 affects the transduction characteristics following subretinal injection in the rat Vision Res., 44, 339-348

Shi, X., Fang, G. and Shi, W. (2006) Insertional mutagenesis at position 520 and 584 of adeno-associated virus type 2 (AAV2) capsid gene and generation of AAV2 vectors with eliminated heparin-binding ability and introduced novel tropism Hum. Gene Ther., 17, 353-361

Steel, M., Woodburn, K., Kniffin, T., Gebretsadik, K., Chan, J., Vijay, S., Chen, H., Chalberg, T.W. and Gasmi, N. (2015) In vitro and in vivo comparability assessment of an AAV vector manufactured by triple transfection in HEK293 cells or in the baculovirus expression system Hum. Gene Ther., 26, A70

Virella-Lowell, I., Poirier, A., Chesnut, K.A., Brantly, M. et al (2000) Inhibition of recombinant adenoassociated virus (rAAV) transduction by bronchial secretions from cystic fibrosis patients Gene Ther., 7, 1783-1789

Yan, Z., Lei-Butters, D.C.M., Zhang, Y., Zak, R. et al (2007) Hybrid adeno-associated virus bearing nonhomologous inverted terminal repeats enhances dual-vector reconstruction of minigenes in vivo Hum. Gene Ther., 18, 81-87

Zeltner, N., Kohlbrenner, E., Clément, N., Weber, T., et al (2010) Near-perfect infectivity of wild-type AAV as benchmark for infectivity of recombinant AAV vectors Gene Ther., 17, 872–879

Zhou, X., Zeng, X., Fan, Z., Li, C., et al (2008) Adeno-associated virus of a single-polarity DNA genome is capable of transduction in vivo Mol. Ther., 16, 494-499

Tropism

Alves, S., Bode, J., Bemelmans, A-P., von Kalle, C., Cartier, N. and Tews, B. (2016) Ultramicroscopy as a novel tool to unravel the tropism of AAV gene therapy vectors in the brain Sci. Rep., 6: 28272

Tumour cells, effect on

Batchu, R.B., Gruzdyn, O.V., M. Moreno-Bost, A.M., Szmania, S., et al (2014) Efficient lysis of epithelial ovarian cancer cells by MAGE-A3-inducedcytotoxic T lymphocytes using rAAV-6 capsid mutant vector Vaccine, 32, 938– 943

Berlinghoff, S., Veldwijk, M.R., Laufs, S., Maser, H-P., et al (2004) Susceptibility of mesothelioma cell lines to adeno-associated virus 2 vector-based suicide gene therapy Lung Cancer, 46, 179-186

George, J., Gondi, C.S., Dinh, D.H., Gujrati, M. et al (2007) Restoration of tissue factor pathway inhibitor-2 in a human glioblastoma cell line triggers caspase-mediated pathway and apoptosis Clin. Cancer Res., 13, 3507- 3517

Hacker, U.T., Wingenfeld, L., Kofler, D. M., Schuhmann, N.K., et al (2005) Adeno-associated virus serotypes 1 to 5 mediated tumor cell directed gene transfer and improvement of transduction efficiency J. Gene Med., 7, 1429-1438

Klaus, F., Paterna, J-C., Marzorati, E., Sigrist, H., Götze, L., Schwendener, S., Bergamini, G., Jehli, E., Azzinnari, D. et al (2016) Differential effects of peripheral and brain tumor necrosis factor on inflammation, sickness, emotional behavior and memory in mice Brain Behav. Immun., 58, 310–326

Medina-Echeverz, J., Fioravanti, J., Díaz-Valdés, N., Frank, K., et al (2014) Harnessing high density lipoproteins to block transforming growth factor beta and to inhibit the growth of liver tumor metastases PLoS One, 9: e96799

Münch, R.C., Janicki, H., Völker, I., Rasbach, A., et al (2013) Displaying high-affinity ligands on adenoassociated viral vectors enables tumor cell-specific and safe gene transfer Mol. Ther., 21, 109–118

Neukirchen, J., Meier, A., Rohrbeck, A., Garcia-Pardillos, G., et al (2007) The proteasome inhibitor bortezomib acts differently in combination with p53 gene transfer or cytotoxic chemotherapy on NSCLC cells Cancer Gene Ther., 14, 431-439

Pandya, M., Britt, K., Hoffman, B., Ling, C. and Aslanidi, G.V. (2015) Reprogramming immune response with capsid-optimized AAV6 vectors for immunotherapy of cancer J. Immunother., 38, 292–298

Ponnazhagan, S., Mahendra, G., Lima, J., Aldrich, W.A., et al (2004) Augmentation of antitumor activity of a recombinant adeno-associated virus carcinoembryonic antigen vaccine with plasmid adjuvant Hum. Gene Ther., 15, 856-864

Rohr, U-P., Wulf, M-A., Stahn, S., Heyd, F., et al (2003) Non-small lung cancer cells are prime targets for p53 gene transfer mediated by a recombinant adeno-associated virus type-2 vector Cancer Gene Ther., 10, 898-906

Santamaria, M., Pardo–Saganta, A., Alvarez–Asiain, L., Di Scala, M., et al (2013) Nuclear a1- antichymotrypsin promotes chromatin condensation and inhibits proliferation of human hepatocellular carcinoma cells Gastroenterology, 144, 818-828

Tamai, H., Miyake, K., Yamaguchi, H., Takatori, M., et al (2012) AAV8 vector expressing IL24 efficiently suppresses tumor growth mediated by specific mechanisms in LL/AF4-positiveALL model mice Blood, 119, 64-71

Teschendorf, C., Emons, B., Muzyczka, N., Graeven, U. et al (2010) Efficacy of recombinant adeno-associated viral vectors serotypes 1, 2, and 5 for the transduction of pancreatic and colon carcinoma cells Anticancer Res., 30, 1931-1936

Triozzi, P.L., Aldrich, W. and Ponnazhagan, S. (2010) Regulation of the activity of an adeno-associated virus vector cancer vaccine administered with synthetic Toll-like receptor agonists Vaccine, 28, 7837–7843

Veldwijk, M.R., Herskind, C., Laufs, S., Zeller, W.J., et al (2004) Recombinant adeno-associated virus 2- mediated transfer of the human superoxide-dismutase gene does not confer radioresistance on HeLa cervical carcinoma cells Radiother. Oncol., 72, 341-350

Xie, Y., Hicks, M.J., Kaminsky, S.M., Moore, M.A.S., Crystal, R.G. and Rafii, A. (2014) AAV-mediated persistent bevacizumab therapy suppresses tumor growth of ovarian cancer Gynecol. Oncol., 135, 325–332

Yanamandra, N., Kondraganti, S., Gondi, C.S., Gujrati, M., et al (2005) Recombinant adeno-associated virus (rAAV) expressing TFPI-2 inhibits invasion, angiogenesis and tumor growth in a human glioblastoma cell line Int. J. Cancer, 115, 998-1005

Yoo, J., Choi, S., Hwang, K-S., Cho, W-K., et al (2006) Adeno-associated virus-mediated gene transfer of a secreted form of TRAIL inhibits tumor growth and occurrence in an experimental tumor model J. Gene Med., 8, 163-174

Unfolded protein response

Balakrishnan, B., Sen, D., Hareendran, S., Roshini, V., et al (2013) Activation of the cellular unfolded protein response by recombinant adeno-associated virus vectors PLoS One, 8: e53845

Vascular smooth muscle delivery

Abdominal aortic aneurysm
Chen, F., Zhang, ZD., and Zhu, XH. (2015) Inhibition of development of experimental abdominal aortica neurysm by c-junN-terminal protein kinase inhibitor combined with lysyl oxidase gene modified smooth muscle progenitor cells Eur. J. Pharmacol., 766, 114–121

Actin filaments
Pappas, C.T., Mayfield, R.M., Henderson, C., Jamilpour, N., Cover, C., Hernandez, Z., Hutchinson, K.R., Chu, M. et al (2015) Knockout of Lmod2 results in shorter thin filaments followed by dilated cardiomyopathy and,juvenile lethality Proc. Natl. Acad. Sci. USA, 112, 13573–13578

Autoimmune myocarditis
Kaya, Z., Leib, C., Werfel, S., Göser, S., et al (2011) Comparison of IL-10 and MCP-1-7ND gene transfer with AAV9 vectors for protection from murine autoimmune myocarditis Cardiovasc. Res., 91, 116–123

Bioartificial pacemakers
Chan, P.K.W. and Li, R.A. (2017) Gene delivery for the generation of bioartificial pacemaker In Cardiac Gene Therapy: Methods and Protocols, Methods Mol. Biol., 1521, (ed. Ishikawa, K.) Springer Science+Business Media, New York, pp 293-306

Ca2+ cycling
Park, C.S., Cha, H., Kwon, E.J., Jeong, D., et al (2012) AAV-mediated knock-down of HRC exacerbates transverse aorta constriction-induced heart failure PLoS One, 7: e43282

Cardiac contractility
Gröbl, T., Hammer, E., Bien-Möller, S., Geisler, A., et al (2014) A novel artificial microRNA expressing AAV vector for phospholamban silencing in cardiomyocytes improves Ca2+ uptake into the sarcoplasmic reticulum PLoS One, 9: e92188

Oh, J.G., Jeong, D., Cha, H., Kim, J.M., et al (2012) PICOT increases cardiac contractility by inhibiting PKCζ activity J. Mol. Cell. Cardiol., 53, 53–63

Schwab, D.M., Tilemann, L., Bauer, R., Heckmann, M., Jungmann, A., Wagner, M., Burgis, J., Vettel, C., Katus, H.A., El-Armouche, A. and Müller, O.J. (2018) AAV-9 mediated phosphatase-1 inhibitor-1 overexpression improves cardiac contractility in unchallenged mice but is deleterious in pressure-overload Gene Ther., 25, 13–19

Wahlquist, C., Jeong, D., Rojas-Munõz, A., Kho, C., et al (2014) Inhibition of miR-25 improves cardiac contractility in the failing heart Nature, 508, 531-535

Cardiac fibrosis
Kim, J., Kim, J., Lee, S.H., Kepreotis, S.V., Yoo, J., Chun, J-S., Hajjar, R.J., Jeong, D. and Park, W.J. (2016) Cytokine-like 1 regulates cardiac fibrosis via modulation of TGF-β signaling PLoS One, 11: e0166480

Sassil, Y., Avramopoulos, P., Ramanujam, D., Grüter, L., Werfel, S., Giosele, S., Brunner, A-D., Esfandyari, D., Papadopoulou, A.S. et al (2017) Cardiac myocyte miR-29 promotes pathological remodeling of the heart by activating Wnt signaling Nat. Comm., 8: 1614

Cardiac gene knock-out
Werfel, S., Jungmann, A., Lehmann, L.., Ksienzyk, J., Bekeredjian, R., Kaya, Z., Leuchs, B., Nordheim, A., Backs, J., Engelhardt, S. et al (2014) Rapid and highly efficient inducible cardiac gene knockout in adultmicem using AAV-mediated expression of Cre recombinase Cardiovasc. Res., 104, 15–23

Cardic hypertrophy
González-Terán, B., López, J.A., Rodríguez, E., Leiva, L., Martínez-Martinez, S., Bernal, J.A. et al (2016) p38g and d promote heart hypertrophy by targeting the mTOR-inhibitory protein DEPTOR for degradation Nat. Comm., 7: 10477

Li, Y., Zhang, D., Kong, L., Shi, H., Tian, X., Gao, L., Liu, Y., Wu, L. et al (2018) Aldolase promotes the development of cardiac hypertrophy by targeting AMPK signalling Exp. Cell Res., 370, 78-86

Völkers, M., Toko, H., Doroudgar, S., Din, S., et al (2013) Pathological hypertrophy amelioration by PRAS40- mediated inhibition of mTORC1 Proc. Natl. Acad. Sci. USA, 110, 12661–12666

Cardiac remodelling (see also “153-16. Left ventricular remodelling”)
Moulay, G., Ohtani, T., Ogut, O., Guenzel, A., Behfar, A., Zakeri, R., Haines, P., Storlie, J. et al (2015) Cardiac AAV9 gene delivery strategies in adult canines: assessment by long-term serial SPECT imaging of sodium iodide symporter expression Mol. Ther., 23, 1211–1221

Ramanujam, D., Sassi, Y., Laggerbauer, B. and Engelhardt, S. (2016) Viral vector-based targeting of miR-21 in cardiac nonmyocyte cells reduces pathologic remodeling of the heart Mol. Ther., 24, 1939–1948

Viereck, J., Kumarswamy, R., Foinquinos, A., Xiao, K., Avramopoulos, P., Kunz, M., Dittrich, M., Maetzig, T., Zimmer, K., et al (2016) Long noncoding RNA Chast promotes cardiac remodeling Sci. Transl. Med., 8, 326ra22

Wong, F.F., Ho, M.L., Yamagami, M., Lam, M.T., Grande-Allen, K.J. and Suh, J. (2015) Effective gene delivery to valvular interstitial cells using adeno-associated virus serotypes 2 and 3 Tissue Eng. Part C, 21, 808-815

Cardiomyopathy
Fechner, F., Sipo, I., Westermann, D., Pinkert, S., et al (2008) Cardiac-targeted RNA interference mediated by an AAV9 vector improves cardiac function in coxsackievirus B3 cardiomyopathy J. Mol. Med., 86, 987-997

Gedicke-Hornung, C., Behrens-Gawlik, V., Reischmann, S., Geertz, B., et al (2013) Rescue of cardiomyopathy through U7snRNA – mediated exon skipping in Mybpc3 – targeted knock – in mice EMBO Mol. Med., 5, 1060-1077

Karakikes, I., Stillitano, F., Nonnenmacher, M., Tzimas, C., Sanoudou, D., Termglinchan, V., Kong, C-W., Rushing, S. et al (2015) Correction of human phospholamban R14del mutation associated with cardiomyopathy using targeted nucleases and combination therapy Nat. Commun., 6: 6955

Mearini, G., Stimpel, D., Krämer, E., Geertz, B., et al (2013) Repair of Mybpc3 mRNA by 5′-trans-splicing in a mouse model of hypertrophic cardiomyopathy Mol. Ther. Nucleic Acids, 2: e102

Prondzynski, M., Krämer, E., Laufer, S.D., Shibamiya, A., Pless, O., Flenner, F., Müller, O.J., Münch, J. et al (2017) Evaluation of MYBPC3 trans-splicing and gene replacement as therapeutic options in human iPSCderived cardiomyocytes Mol. Ther: Nucleic Acids, 7, 475-486

Rutschow, D., Bauer, R., Göhringer, C., Bekeredjian, R., et al (2014) S151A -sarcoglycan mutation causes a mild phenotype of cardiomyopathy in mice Eur. J. Hum. Genet., 2, 119–125

Catecholaminergic polymorphic ventricular tachycardia
Liu, B., Walton, S.D., Ho, H-T., Belevych, A.E., Tikunova, S.B., Bonilla, I., Shettigar, V., Knollmann, B.C., Priori, S.G. et al (2018) Gene transfer of engineered calmodulin alleviates ventricular arrhythmias in a calsequestrin-associated mouse model of catecholaminergic polymorphic ventricular tachycardia J. Am. Heart Assoc., 7: e008155

Extracelluar SOD
Prasad, K-M.R., Smith, R.S., Xu, Y., French, B.A. (2011) A single direct injection into the left ventricular wall of an adeno-associated virus 9 (AAV9) vector expressing extracellular superoxide dismutase from the cardiac troponin-T promoter protects mice against myocardial infarction J. Gene Med., 13, 333–341

Heart transplants
Raissadati, A., Jokinen, J.J., Syrjälä, S.O., Keränen, M.A.I., et al (2013) Ex vivo intracoronary gene transfer of adeno-associated virus 2 leads to superior transduction over serotypes 8 and 9 in rat heart transplants Transplant Int., 26, 1126–1137

Inflammatory responses/interleukins
Chen, S., Kapturczak, M.H., Wasserfall, C., Glushakova, O.Y., et al (2005) Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway Proc. Natl. Acad. Sci. USA, 102, 7251-7256

Kaya, Z., Leib, C., Werfel, S., Göser, S., et al (2011) Comparison of IL-10 and MCP-1-7ND gene transfer with AAV9 vectors for protection from murine autoimmune myocarditis Cardiovasc. Res., 91, 116–123

Intracardiac administration (scAAV2/9 and scAAV2/rh10 variants)
Chansel-Debordeaux, L., Bourdenx, M., Dutheil, N., Dovero, S., Canron, M-H., Jimenez, C., Bezard, E. and Dehay, B. (2018) Systemic gene delivery by single-dose intracardiac administration of scAAV2/9 and scAAV2/rh10 variants in newborn rats Hum. Gene Ther., 29, 189-199

Ischaemia
Tuuminen, R., Dashkevich, A., Keränen, M.A.I., Raissadati, A., Krebs, R., Jokinen, J.J., Arnaudova, R., Rouvinen, E., Ylä-Herttuala, S. et al (2016) Platelet-derived growth factor-B protects rat cardiac allografts from ischemia-reperfusion injury Transplantation, 100, 303–313

Left ventricular remodelling
Konkalmatt, P.R., Wang, F., Piras, B.A., Xu, Y., et al (2012) Adeno-associated virus serotype 9 administered systemically after reperfusion preferentially targets cardiomyocytes in the infarct border zone with pharmacodynamics suitable for the attenuation of left ventricular remodeling J. Gene Med., 14, 609–620

Konkalmatt, P.R., Beyers, R.J., O’Connor, D.M., Xu, Y., Seaman, M.E. and French, B.A. (2013) Cardiacselective expression of extracellular superoxide dismutase after systemic injection of adeno-associated virus 9 protects the heart against post–myocardial infarction left ventricular remodeling Circ. Cardiovasc. Imaging, 6, 478-456

Myocardial dysfunction (incl. fibrosis/heart failure/hypertension/infarction etc) Bénard, L., Oh, J.G., Cacheux, M., Lee, A., Nonnenmacher, M., Matasic, D.S., Kohlbrenner, E., Kho, C., Pavoine, C et al (2016) Cardiac Stim1 silencing impairs adaptive hypertrophy and promotes heart failure through inactivation of mTORC2/Akt signaling Circulation, 133, 1458-1471

Cataliotti, A., Tonne, J.M., Bellavia, D., Martin, F.L., et al (2011) Long-term cardiac pro-B-type natriuretic peptide gene delivery prevents the development of hypertensivc heart disease in spontaneously hypertensiverats Circulation, 123, 1297-1305

Chaanine, A.H., Nonnenmacher, M., Kohlbrenner, E., Jin, D., Kovacic, J.C., Akar, F.G., Hajjar, R.J. and Weber, T. (2014) Effect of bortezomib on the efficacy of AAV9.SERCA2a treatment to preserve cardiac function in a rat pressure-overload model of heart failure Gene Ther., 21, 379–386

Chaanine, A.H., Kohlbrenner, E., Gamb, S.I., Guenzel, A.J., Klaus, K., Fayyaz, A.U., Nair, K.S., Hajjar, R.J. and Redfield, M.M. (2016) FOXO3a regulates BNIP3 and modulates mitochondrial calcium, dynamics, and function in cardiac stress Am. J. Physiol. Heart. Circ. Physiol., 311, H1540–H1559

Chemaly, E.R., Hadri, L., Zhang, S., Kim, M., et al (2011) Long-term in vivo resistin overexpression induces myocardial dysfunction and remodeling in rats J. Mol. Cell. Cardiol., 51, 144–155

Fish, K.M., Ladage, D., Kawase, Y., Karakikes, I., et al (2013) AAV9.I-1c delivered via direct coronary infusion in a porcine model of heart failure improves contractility and mitigates adverse remodeling Circ. Heart Fail., 6, 310-317

Kho, C., Lee, A., Jeong, D., Oh, J.G., et al (2011) SUMO1-dependent modulation of SERCA2a in heart failure Nature, 477, 601-606

LaRocca, T.J., Jeong, D., Kohlbrenner, E., Lee, A., et al (2012) CXCR4 gene transfer prevents pressure overload induced heart failure J. Mol. Cell. Cardiol., 53, 223–232
Meier, S., Gilad, A.A., Brandon, J.A., Qian, C., Gao, E., Abisambra, J.F. and Vandsburger, M. (2018) Noninvasive detection of adeno-associated viral gene transfer using a genetically encoded CEST-MRI reporter gene in the murine heart Sci. Rep., 8: 4638

Meyer, I.S., Jungmann, A., Dieterich, C., Zhang, M., Lasitschka, F., Werkmeister, S., Haas, J., Müller, A.J., Boutros, M. et al (2017) The cardiac microenvironment uses non-canonical WNT signaling to activate monocytes after myocardial infarction EMBO Mol. Med., 9, 1279-1293

Moilanen, A-M., Rysä, J., Serpi, R., Mustonen, E., et al (2012) (Pro)renin receptor triggers distinct angiotensin II-independent extracellular matrix remodeling and deterioration of cardiac function PLoS One, 7(7): e41404

Moulay, G., Ohtani, T., Ogut, O., Guenzel, A., Behfar, A., Zakeri, R., Haines, P., Storlie, J. et al (2015) Cardiac AAV9 gene delivery strategies in adult canines: assessment by long-term serial SPECT imaging of sodium iodide symporter expression Mol. Ther., 23, 1211–1221

Park, C.S., Cha, H., Kwon, E.J., Jeong, D., et al (2012) AAV-mediated knock-down of HRC exacerbates transverse aorta constriction-induced heart failure PLoS One, 7: e43282

Pleger, S.T., Shan, C., Ksienzyk, J., Bekeredjian, R., et al (2011) Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model Sci. Transl. Med., 3: 92ra64

Prasad, K-M.R., Smith, R.S., Xu, Y., French, B.A. (2011) A single direct injection into the left ventricular wall of an adeno-associated virus 9 (AAV9) vector expressing extracellular superoxide dismutase from the cardiac troponin-T promoter protects mice against myocardial infarction J. Gene Med., 13, 333–341

Schmid, E., Neef, S., Berlin, C., Tomasovic, A., Kahlert, K., Nordbeck, P., Deiss, K., Denzinger, S., Herrmann, S. et al (2015) Cardiac RKIP induces a beneficial β-adrenoceptor–dependent positive inotropy Nat. Med., 21, 1298-1306

Shettigar, V., Zhang, B., Little, S.C., Salhi, H.E., Hansen, B.J., Li, N., Zhang, J., Roof, S.R., Ho, H-T., Brunello, L. et al (2016) Rationally engineered Troponin C modulates in vivo cardiac function and performance in health and disease Nat. Comm., 7: 10794

Wahlquist, C., Jeong, D., Rojas-Munõz, A., Kho, C., et al (2014) Inhibition of miR-25 improves cardiac contractility in the failing heart Nature, 508, 531-535

Myocardial gene delivery
White, J.D., Thesier, D.M., Swain, J.B.D., Katz, M.G., et al (2011) Myocardial gene delivery using molecular cardiac surgery with recombinant adeno-associated virus vectors in vivo Gene Ther., 18, 546–552

Myocyte cytokinesis
Jiang, J., Burgon, P.G., Wakimoto, H., Onoue, K., Gorham, J.M., O’Meara, C.C., Fomovsky, G., McConnell, B.K, Lee, R.T., Seidman, J.G. and Seidman, C.E. (2015) Cardiac myosin binding protein C regulates postnatal myocyte cytokinesis Proc. Natl. Acad. Sci. USA, 112, 9046-9051

153-20. Myotonic dystrophy
Freyermuth, F., Rau, F., Kokunai, Y., Linke, T., Sellier, C., Nakamori, M., Kino, Y., Arandel, L., Jollet, A., Thibault, C. et al (2016) Splicing misregulation of SCN5A contributes to cardiac-conduction delay and heart arrhythmia in myotonic dystrophy Nat. Comm., 7: 11067

Pinto, B.S., Saxena, T., Oliveira, R., Méndez-Gómez, H.R., Cleary, J.D., Denes, L.T., McConnell, O. et al (2017) Impeding transcription of expanded microsatellite repeats by deactivated Cas9 Mol. Cell 68, 479-490

Natriuretic peptide (B type) gene delivery
Cataliotti, A., Tonne, J.M., Bellavia, D., Martin, F.L., et al (2011) Long-term cardiac pro-B-type natriuretic peptide gene delivery prevents the development of hypertensivc heart disease in spontaneously hypertensive rats Circulation, 123, 1297-1305

Pericardial cavity delivery (see “Actin filaments”)
Phospholamban suppression

Andino, L.M., Takeda, M., Kashara, H., Jakymiw, A., et al (2008) AAV-mediated knockdown of phospholamban leads to improved contractility and calcium handling in cardiomyocytes J. Gene Med., 10, 132-142

Resistin overexpression
Chemaly, E.R., Hadri, L., Zhang, S., Kim, M., et al (2011) Long-term in vivo resistin overexpression induces myocardial dysfunction and remodeling in rats J. Mol. Cell. Cardiol., 51, 144–155

RNA interactions
Dastor, M., Schreiber, J., Prochazka, L., Angelici, B., Kleinert, J., Klebba, I., Doshi, J., Shen, L. and Benenson, Y. (2018) A workflow for in vivo evaluation of candidate inputs and outputs for cell classifier gene circuits ACS Synth. Biol., 7, 474−489

Fechner, H., Vetter, R., Kurreck, J. and Poller, W. (2017) Silencing genes in the heart In Cardiac Gene Therapy: Methods and Protocols, Meth. Mol. Biol., vol. 1521 (ed. Ishikawa, K.) Springer Science+Business Media New York 2017, pp 17-39

Jeong, D., Yoo, J., Lee, P., Kepreotis, S.V., Lee, A., Wahlquist, C., Brown, B.D., Kho, C., Mercola, M, and Hajjar, R.J. (2018) miR-25 Tough Decoy enhances cardiac function in heart failure Mol. Ther., 26, 718-729

Mayra, A., Tomimitsu, H., Kubodera, T., Kobayashi, M., et al (2011) Intraperitoneal AAV9-shRNA inhibits target expression in neonatal skeletal and cardiac muscles Biochem. Biophys. Res. Comm., 405, 204–209

Suckau, L., Fechner, H., Chemaly, E., Krohn, S., et al (2009) Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy Circulation, 119 1241-1252

Wahlquist, C., Jeong, D., Rojas-Munõz, A., Kho, C., Lee, A., Mitsuyama, S., van Mil, A., Park, W.J., Sluijter, J.P.G., Doevendans, P.A.F., Hajjar, R.J. and Mercola, M. (2014) Inhibition of miR-25 improves cardiac contractility in the failing heart Nature, 508, 531-535

§-Sarcoglycan

Ying, Y., Müller, O.J., Goehringer, C., Leuchs, B., et al (2010) Heart-targeted adeno-associated viral vectors selected by in vivo biopanning of a random viral display peptide library Gene Ther., 17, 980–990

Vector specificity and transduction efficiency
Bish, L.T., Sweeney, H.L., Müller, O.J. and Bekeredjian, R. (2011) Adeno-associated virus vector delivery to the heart In Adeno-Associated Virus: Methods and Protocols, Methods Mol. Biol., 807 (ed. Snyder, R.O. and Moullier, P., Springer Science+Business Media, pp 219-237

Chen, S-J., Johnston, J., Sandhu, A., Bish, L.T., Hovhannisyan, R., Jno-Charles, O., Sweeney, H.L. and Wilson, J.M. (2013) Enhancing the utility of adeno-associated virus gene transfer through inducible tissuespecific expression Hum. Gene Ther. Methods, 24, 270–278

Du, L., Kido, M., Lee, D.V., Rabinowitz, J.E., et al (2004) Differential myocardial gene delivery by recombinant serotype-specific adeno-associated viral vectors Mol. Ther., 10, 604-608

Fineta, J.E., Wan, X. and Donahue, J.K. (2018) Fusion of Anthopleurin-B to AAV2 increases specificity of cardiac gene transfer Virology 513, 43–51

Gruchala, M., Bhardwaj, S., Pajusola, K., Roy, H., et al (2004) Gene transfer into rabbit arteries with adenoassociated virus and adenovirus vectors J. Gene Med., 6, 545-554

Merentie, M., Lottonen-Raikaslehto, L., Parviainen, V., Huusko, J., Pikkarainen, S., Mendel, M., LahamKaram, N., Kärjä, V. et al (2016) Efficacy and safety of myocardial gene transfer of adenovirus, adeno associated virus and lentivirus vectors in the mouse heart Gene Ther., 23, 296–305

Müller, O.J., Leuchs, B., Pleger, S.T., Grimm, D., et al (2006) Improved cardiac gene transfer by transcriptional and transductional targeting of adeno-associated viral vectors Cardiovasc. Res., 70, 70-78

Müller, O.J., Schinkel, S., Kleinschmidt, J.A., Katus, H.A., et al (2008) Augmentation of AAV-mediated cardiac gene transfer after systemic administration in adult rats Gene Ther. 15, 1558–1565

Pleger, S.T., Shan, C., Ksienzyk, J., Bekeredjian, R., et al (2011) Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model Sci. Transl. Med., 3: 92ra64

Piras, B.A., O’Connor, D.M. and French, B.A. (2013) Systemic delivery of shRNA by AAV9 provides highly efficient knockdown of ubiquitously expressed GFP in mouse heart, but not liver PLoS One, 8: e75894

Prasad, K-M.R., Xu, Y., Yang, Z., Acton, S.T. and French, B.A. (2011) Robust cardiomyocyte-specific gene expression following systemic injection of AAV: in vivo gene delivery follows a Poisson distribution Gene Ther.,18, 43–52

Raake, P.W., Hinkel, R., Müller, S., Delker, S., et al (2008) Cardio-specific long term gene expression in a porcine model after selective pressure-regulated retroinfusion of adeno-associated viral (AAV) vectors Gene Ther., 15, 12-17

Rapti, K., Hajjar, R.J. and Weber, T. (2012) Novel approaches to deliver molecular therapeutics in cardiac disease using adeno-associated virus vectors In Translational Cardiology, Molecular and Translational Medicine (ed. Patterson, C. and Willis, M.S) (eds.), Springer Science+Business Media, pp 391-458

Rapti, K., Stillitano, F., Karakikes, I., Nonnenmacher, M., Weber, T., Hulot, J-S. and Hajjar, R.J. (2015) Effectiveness of gene delivery systems for pluripotent and differentiated cells Mol. Ther. Methods Clin, Dev., 2:14067

Sasano, T., Kikuchi, K., McDonald, A., Lai, S., et al (2007) Targeted high-efficiency, homogenous myocardial gene transfer J. Mol. Cell. Cardiol., 42, 954-961

Sen, S., Contoy, S., Hynes, S.O., McMahon, J., et al (2008) Gene delivery to the vasculature mediated by lowtitre adeno-associated virus serotypes 1 and 5 J. Gene Med., 10, 143-151

Sharif, F., Hynes, S.O., McMahon, J., Cooney, R., et al (2006) Gene-eluting stents: Comparison of adenoviral and adeno- associated viral gene delivery to the blood vessel wall in vivo Hum.Gene Ther., 17, 741-750

Shin, M., Lee, H-A., Lee, M., Shin, Y., Song, J-J., Kang, S-W., Nam, D-H., Jeon. E.J., Cho, M. et al (2018) Targeting protein and peptide therapeutics to the heart via tannic acid modification Nat. Biomed. Engineer., 2, 304–317

Sipo, I., Fechner, H., Pinkert, S., Suckau, L., et al (2007) Differential internalization and nuclear uncoating of self-complementary adeno-associated virus pseudotype vectors as determinants of cardiac cell transduction Gene Ther., 14, 1319-1329

Work, L.M., Nicklin, S.A., Brain, N.J.R., Dishart, K.L., et al (2004) Development of efficient viral vectors selective for vascular smooth muscle cells Mol. Ther., 9 198-208

Vestibular hair cells (see “Inner ear delivery” and “Cochlear delivery”)
Vexosome (exosome) gene delivery

György, B., Fitzpatrick, Z., Crommentuijn, M.H.W., Mu, D. and Maguire, C.A. (2014) Naturally enveloped AAV vectors for shielding neutralizing antibodies and robust gene delivery in vivo Biomaterials, 35, 7598-7609

Hudry, E., Martin, C., Gandhi, S., György, B., Scheffer, D.I., Mu, D., Merkel, S.F., Mingozzi, F., Fitzpatrick,
Z. et al (2016) Exosome-associated AAV vector as a robust and convenient neuroscience tool Gene Ther., 23, 380–392

Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M.H.W., et al (2012) Microvesicle-associated AAV vector as a novel gene delivery system Mol. Ther., 20, 960–971

Schiller, L.T., Lemus-Diaz, N., Ferreira, R.R., Böker, K.O. and Gruber, J. (2018) Enhanced production of exosome-associated AAV by overexpression of the tetraspanin CD9 Mol. Ther. Meth. Clin. Dev., 9, 278-287

PART B

Anneloviridae
Torque teno virus

Bzhalava, D., Ekströmb, J., Lysholm, F., Hultin, E., Faust, H., Persson, B., Lehtinen, M., Villiers, E-M. and Dillner, J. (2012) Phylogenetically diverse TT virus viremia among pregnant women Virology, 432, 427–434

Dependovirus
Avian adeno-associated virus

Aoki, N., Yamaguchi, S., Kitajima, T., Takehara, A., Katagari-Nakagawa, S., Matsui, R., Watanabe, D., Matsushima, T. and Homma, K.J. (2015) Critical role of the neural pathway from the intermediate medial mesopallium to the intermediate hyperpallium apicale in filial imprinting of domestic chicks (Gallus gallus domesticus) Neuroscience, 308, 115–124

Matsui, R., Tanabe, Y. and Watanabe, D. (2012) Avian adeno-associated virus vector efficiently transduces neurons in the embryonic and post-embryonic chicken brain PLoS One 7: e48730

Parvoviridae
Densovirinae (Penaeus stylirostris)

Kaufmann, B., Bowman, V.D., Li, Y., Szelei, J., Waddell, P.J., Tijssen, P. and Rossmann, M.G. (2010) Structure of Penaeus stylirostris densovirus, a shrimp pathogen J. Virol., 84, 11289-11296

Parvovirinae
Bocavirus

Fakhiri, J., Schneider, M., Kailasan, S., Meister, M., McKenna, M.A., Yan, Z., Qiu, J. and Grimm, D. (2016) New chimeric gene therapy vectors based on four different mammalian bocaviruses Mol. Ther., 24, Suppl. 1, S100

Hao, S., Zhang, J., Chen, Z., Xu, H., Wang, H. and Guana, W. (2017) Alternative polyadenylation of human bocavirus at its 3’ end is regulated by multiple elements and affects capsid expression J. Virol., 91: e02026-16

Minute virus (of mice)

Cotmore, S.F. and Tattersall, P. (2005) Encapsidation of minute virus of mice DNA: Aspects of the translocation mechanism revelaed by the structure of partially packaged genomes Virology, 336, 100-112

Cotmore, S.F., Hafenstein, S. and Tattersall, P. (2010) Depletion of virion-associated divalent cations induces parvovirus minute virus of mice to eject its genome in a 3’-to-5’ direction from an otherwise intact viral particle J. Virol., 84, 1945-1956

Cotmore, S.F. and Tattersall, P. (2012) Mutations at the base of the icosahedral five-fold cylinders of minute virus of mice induce 3’-to-5’ genome uncoating and critically impair entry functions J. Virol., 86, 69-80

D’Abramo Jr., A.M., Ali, A.A., Wang, F., Cotmore, S.F. and Tattersall, P. (2005) Host range mutants of minute virus of mice with a single VP2 amino acid change require additional silent mutations that regulate NS2 accumulation Virology, 340, 143-154

Farr, G.A., Cotmore, S.F. and Tattersall, P. (2006) VP2 cleavage and the leucine ring at the base of the fivefold cylinder control pH-dependent externalization of both the VP1 N terminus and the genome of minute virus of mice J. Virol., 80, 161-171

Grekova, S., Zawatzky, R., Hörlein, R., Cziepluch, C., Mincberg, M., Davis, C., Rommelaere, J. and Daeffler, L. (2010) Activation of an antiviral response in normal but not transformed mouse cells: a new determinant of minute virus of mice oncotropism J. Virol., 84, 516-531

Grekova, S.P., Raykov, Z., Zawatzky, R., Rommelaere, J. and Koch, U. (2012) Activation of a glioma-specific immune response by oncolytic parvovirus Minute Virus of Mice infection Cancer Gene Ther., 19, 468-475

Halder, S., Cotmore, S., Heimburg-Molinaro, J., Smith, D.F., Cummings, R.D., Chen, X. et al (2014) Profiling of glycan receptors for minute virus of mice in permissive cell lines towards understanding the mechanism of cell recognition PLoS One, 9: e86909

Lang, S.I., Boelz, S., Stroh-Dege, A.Y., Rommelaere, J., Dinsart, C. and Cornelis, J.J. (2005) The infectivity and lytic activity of minute virus of mice wild-type and derived vector particles are strikingly different J. Virol., 79, 289-298

Lang, S.I., Giese, N.A., Rommelaere, J., Dinsart, C. and Cornelis, J.J. (2006) Humoral immune responses against minute virus of mice vectors J. Gene Med., 8, 1141-1150

Li, L., Cotmore, S.F. and Tattersall, P. (2012) Maintenance of the flip sequence orientation of the ears in the parvoviral left-end hairpin is a nonessential consequence of the critical asymmetry in the hairpin stem J. Virol., 86, 12187-12197

Li, L., Cotmore, S.F. and Tattersall, P. (2013) Parvoviral left-end hairpin ears are essential during infection for establishing a functional intranuclear transcription template and for efficient progeny genome encapsidation J. Virol., 87, 10501–10514

Meira, C., Mincberga, M., Rostovskya, I., Tala, S., Vollmers, E.M., Levia, A., Tattersall, P. and Davis, C (2017) The MVMp P4 promoter is a host cell-type range determinant in vivo Virology, 506, 141–151

Paglino, J., Burnett, E. and Tattershall, P. (2007) Exploring the contribution of disgtal P4 promoter elements to the oncoselectivity of minute virus of mice Virology, 361, 174-184

Plevka, P., Hafenstein, S., Li, L., D’Abramo, A., Cotmore, S.F., Rossmann, M.G. and Tattersall, P. (2011) Structure of a packaging-defective mutant of minute virus of mice indicates that the genome is packaged via a pore at a 5-Fold axis J. Virol., 85, 4822–4827

Rostovsky, I. and Davis, C. (2015) Induction of an embryonic mouse innate immune response following inoculation in utero with minute virus of mice J. Virol., 89, 2182-2191

Ruiz, Z., Mihaylov, I.S., Cotmore, S.F. and Tattersall, P. (2011) Recruitment of DNA replication and damage response proteins to viral replication centers during infection with NS2 mutants of Minute Virus of Mice (MVM) Virology 410, 375–384

Subramanian, S., Organtini, L.J., Grossman, A., Domeier, P.P., Cifuente, J.O., Makhov, A.M., Conway, J.F., D’Abramo, A., Cotmore, S.F., Tattersall, P. and Hafenstein, S. (2017) Cryo-EM maps reveal five-fold channel structures and their modification by gatekeeper mutations in the parvovirus minute virus of mice (MVM) capsid Virology, 510, 216–223

Vollmers, E.M. and Tattersall, P. (2013) Distinct host cell fates for human malignant melanoma targeted by oncolytic rodent parvoviruses Virology, 446, 37–48

Parvovirinae

Adenvovirus-parvovirus chimeras
El-Andaloussi, N., Bonifati, S., Kaufmann, J.K., Mailly, L., Daeffler, L., Deryckère, F., Nettelbeck, D.M., Rommelaere, J. and Marchini, A. (2012) Generation of an adenovirus-parvovirus chimera with enhanced oncolytic potential J. Virol., 86, 10418-10431

Capsid genes and proteins
Allaume, X., El-Andaloussi, N., Leuchs, B., Bonifati, S., Kulkarni, A., Marttila, T., Kaufmann, J.K., Nettelbeck, D.M., Kleinschmidt, J., Rommelaere, J. and Marchinia, A. (2012) Retargeting of rat parvovirus H1PV to cancer cells through genetic engineering of the viral capsid J. Virol., 86, 3452–3465

Bloom, M.E., Best, S.M., Hayes, S.F., Wells, R.D., Wolfinbarger, J.B., McKenna, R. and Agbandje-McKenna, M. (2001) Identification of Aleutian mink disease parvovirus capsid sequences mediating antibody-dependent enhancement of infection, virus neutralization, and immune complex formation J. Virol., 75, 11116-11127 Farr, G.A. and Tattersall, P.A (2004) A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection Virology, 323, 243-256

Farr, G.A., Zhang, L-G. and Tattersall, P. (2005) Parvoviral virions deploy a capsid-tetrered lipolytic enzyme to breach the endosomal membrane during cell entry Proc. Natl. Acad. Sci. USA, 102, 17148-17153

Krüger, L., Eskerski, H., Dinsart, C., Cornelis, J., Rommelaere, J., Haberkorn, H. and Kleinschmidt, J.A. (2008) Augmented transgene expression in transformed cells using a parvoviral hybrid vector Cancer Gene Ther., 15, 252-267

Maxwell, I.H., Terrell, K.L. and Maxwell, F. (2002) Autonomous parvovirus vectors Methods, 28, 168-181 Nelson, C.D.S., Minkkinen, E., Bergkvist, M., Hoelzer, K., Fisher, M., Bothner, B. and Parrish, C.R. (2008) Detecting small changes and additional peptides in the canine parvovirus capsid structure J. Virol., 82, 10397-10407

Wrzesinski, C., Tesfay, L., Salome, N., Jauniaux, J-C., Rommeleare, J., Cornelis, J. and Dinsart, C. (2003) Chimeric and pseudotyped parvoviruses minimize the contamination of recombinant stocks with replicationcompetent viruses and identify a DNA sequence that restricts parvovirus H-1 in mouse cells J. Virol., 77, 3851-3858

Carcinoma cell killing
Angelova, A.L., Grekova, S.P., Heller, A., Kuhlmann, O., Soyka, E., Giese, T., Aprahamian, M., Bour, G., Rüffer, S., Cziepluch, C. et al (2014) Complementary induction of immunogenic cell death by oncolytic parvovirus H-1PV and gemcitabine in pancreatic cancer J. Virol., 88, 5263–5276

Bhat, R. and Rommelaere, J. (2013) NK-cell-dependent killing of colon carcinoma cells is mediated by natural cytotoxicity receptors (NCRs) and stimulated by parvovirus infection of target cells BMC Cancer, 13: 367

Cell, export from
Li, J. and Murtaugh, M.P. (2015) Functional analysis of porcine reproductive and respiratory syndrome virus N-glycans in infection of permissive cells Virology, 477, 82–88

Weiss, N., Stroh-Dege, A., Rommelaere, J., Dinsart, C. and Salomé, N. (2012) Infectivity of progeny virions H-1PV efficiently stimulates export and protein-coding sequence of parvovirus J. Virol., 86, 7554-7564

Cytokine/chemokine delivery
Dempe, S., Lavie, M., Struyf, S., Bhat, R., Verbeke, H., Paschek, S., Berghmans, N., Geibig, R., Rommelaere, J., Van Damme, J. and Dinsart, C. (2012) Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: implication of leucocyte recruitment Cancer Immunol. Immunother., 61, 2113–2123

Cytotoxicity
Hristov, G., Krämer, M., Li, J., El-Andaloussi, N., Mora, R., Daeffler, L., Zentgraf, H., Rommelaere, J. and Marchini, A. (2010) Through its nonstructural protein NS1, parvovirus H-1 induces apoptosis via accumulation of reactive oxygen species J. Virol., 84, 5909-5922

Lacroix, J., Leuchs, B., Li, J., Hristov, G., Deubzer, H.E., Kulozik, A.E., Rommelaere, J., Schlehofer, J.R. and Witt, O. (2010) Parvovirus H1 selectively induces cytotoxic effects on human neuroblastoma cells Int. J. Cancer, 127, 1230–1239

Drug delivery
Kiprianova, I., Thomas, N., Ayache, A., Fischer, M., Leuchs, B., Klein, M., Rommelaere, J. and Schlehofer, J.R. (2011) Regression of glioma in rat models by intranasal application of parvovirus H-1 Clin. Cancer Res., 17, 5333–5342

Gene therapy
Abschuetz, A., Kehl, T., Geibig, R., Leuchs, B., Rommelacre, J. and Régnier-Vigouroux, A. (2006) Oncolytic murine autonomous parvovirus, a candidate vector for glioma gene therapy, is innocuous to normal and immunocompetent mouse glial cells Cell Tissue Res., 325, 423-436

Allaume, X., El-Andaloussi, N., Leuchs, B., Bonifati, S., Kulkarni, A., Marttila, T., Kaufmann, J.K. et al (2012) Retargeting of rat parvovirus H-1PV to cancer cells through genetic engineering of the viral capsid J. Virol., 86, 3452–3465

Angelova, A.L., Aprahamian, M., Grekova, S.P., Hajri, A., Leuchs, B., Giese, N.A., Dinsart, C., Herrmann, A., Balboni, G., Rommelaere, J. and Raykov, Z. (2009) Improvement of gemcitabine-based therapy of pancreatic carcinoma by means of oncolytic parvovirus H-1PV Clin.Cancer Res., 2009; 15, 511-519

Angelova, A.L., Aprahamian, M., Balboni, G., Delecluse, H-J., Feederle, R., Kiprianova, I. et al (2009) Oncolytic rat parvovirus H-1PV, a candidate for the treatment of human lymphoma: in vitro and in vivo studies Mol. Ther., 17, 1164-1172

Bhat, R., Dempe, S., Dinsart, C. and Rommelaere, J. (2011) Enhancement of NK cell antitumor responses using an oncolytic parvovirus Int. J. Cancer, 128, 908–919

Brandenburger, A. and Velu, T. (2004) Autonomous parvovirus vectors: preventing the generation of wild-type or replication-competent virus J. Gene Med., 6, S203 S211

Dempe, S., Stroh-Dege, A.Y., Schwarz, E., Rommelaere, J. and Dinsart, C. (2010) SMAD4: a predictive marker of PDAC cell permissiveness for oncolytic infection with parvovirus H-1PV Int. J. Cancer, 126, 2914–2927

Enderlin, M., Kleinmann, E.V., Struyf, S., Buracchi, C., Vecchi, A., Kinscherf, R., Kiessling, F., Paschek, S. et al (2009) TNF-a and the IFN-c-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma Cancer Gene Ther., 16, 149–160

Hendrie, P.C. and Russell, D.W. (2001) Homologous gene targeting using an autonomous parvovirus vector Am. Soc. Gene Ther., 4th Annu. Meeting Abstr. 515

Hendrie, P.C., Hirata, R.K. and Russell, D.W. (2003) Chromsomal integration and homologous gene targeting by replication-incompetent vectors based on the autonomous parvovirus minute virus mice J. Virol., 77, 13136-13145

Krüger, L., Eskerski, H., Dinsart, C., Cornelis, J., Rommelaere, J., Haberkorn, H. and Kleinschmidt, J.A. (2008) Augmented transgene expression in transformed cells using a parvoviral hybrid vector Cancer Gene Ther., 15, 252-267

Li, J., Werner, E., Hergenhahn, M., Poirey, R., Luo, Z., Rommelaere, J. and Jauniaux, J-C. (2005) Expression profiling of human hepatoma cells reveals global repression of genes involved in cell proliferation, growth, and apotosis upon infection with parvovirus H-1 J. Virol., 79, 2274-2286

Pozzuto, T., von Kietzell, K., Bock, T., Schmidt-Lucke, C., Poller, W., Zobel, T., Lassner, D., Zeichhardt, H. Weger, S. and Fechner, H. (2011) Transactivation of human parvovirus B19 gene expression in endothelial cells by adenoviral helper functions Virology 411, 50–64

Ruitenberg, M.J., Eggers, R., Boer, G.J. and Verhaagen, J. (2002) Adeno-associated viral vectors as agents for gene delivery: application in disorders and trauma of the central nervous system Methods, 28, 182-194

Wetzel, K., Struyf, S., Van Damme, J., Kayser, T., Vecchi, A., Sozzani, S., Rommelaere, J., Cornelius, J.J. and Dinsart, C. (2007) MCP-3 (CCL7) delivered by parvovirus MVMp reduces tumorigenicity of mouse melanoma cells through activation of T lymphocytes and NK cells Int. J. Cancer, 120, 1364-1371

Glioma/glioblastoma/medulloblastoma
Enderlin, M., Kleinmann, E.V., Struyf, S., Buracchi, C., Vecchi, A., Kinscherf, R., Kiessling, F., Paschek, S. et al (2009) TNF- and the IFN-c-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma Cancer Gene Ther., 16, 149–160

Kiprianova, I., Thomas, N., Ayache, A., Fischer, M., Leuchs, B., Klein, M., Rommelaere, J. and Schlehofer, J.R. (2011) Regression of glioma in rat models by intranasal application of parvovirus H-1 Clin. Cancer Res., 17, 5333–5342

Lacroix, J., Schlund, F., Leuchs, B., Adolph, K., Sturm, D., Bender, S., Hielscher, T., Pfister, S.M., Witt, O., Rommelaere, J., Schlehofer, J.R. and Witt, H. (2014) Oncolytic effects of parvovirus H-1 in medulloblastoma are associated with repression of master regulators of early neurogenesis Int. J. Cancer, 134, 703–716

Paglino, J.C., Ozduman, K. and van den Pol, A.N. (2012) LuIII parvovirus selectively and efficiently targets, replicates in, and kills human glioma cells J. Virol. 2012, 86(13):7280-7291

H-PV, large-scale production
Leuchs, B., Roscher, M., Müller, M., Kürschner, K. and Rommelaere, J. (2016) Standardized large-scale H1PV production process with efficient quality and quantity monitoring J. Virol. Methods, 229, 48–59

Immune system activation
Moehler, M., Sieben, M., Roth, S., Springsguth, F., Leuchs, B., Zeidler, M., Dinsart, C., Rommelaere, J. and Galle, P.R. (2011) Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1 BMC Cancer, 11: 464

Moralès, O., Richard, A., Martin, N., Mrizak, D., Sénéchal, M., Miroux, C., Pancré, V., Rommelaere, J., Caillet-Fauquet, P., de Launoit, Y. and Delhem, N. (2012) Activation of a helper and not regulatory human CD4+ T cell response by oncolytic H-1 parvovirus PLoS One, 7: e32197

Raykov, Z., Grekova, S.P., Hörlein, R., Leuchs, B., Giese, T., Giese, N.A., Rommelaere, J., Zawatzky, R. and Daeffler, L. (2013) TLR-9 contributes to the antiviral innate immune sensing of rodent parvoviruses MVMp and H-1PV by normal human immune cells PLoS One, 8: e55086

Infection/infectivity
Bhat, R. and Rommelaere, J. (2013) NK-cell-dependent killing of colon carcinoma cells is mediated by natural cytotoxicity receptors (NCRs) and stimulated by parvovirus infection of target cells BMC Cancer, 13: 367

Weiss, N., Stroh-Dege, A., Rommelaere, J., Dinsart, C. and Salomé, N. (2012) Infectivity of progeny virions H1PV efficiently stimulates export and protein-coding sequence of parvovirus J. Virol., 86, 7554-7564

Interferon-dependent control
Mattei, L.M., Cotmore, S.F., Tattersall, P. and Iwasaki, A. (2013) Parvovirus evades interferon-dependent viral control in primary mouse embryonic fibroblasts Virology, 442, 20–27

Malignant melanoma
Vollmers, E.M. and Tattersall, P. (2013) Distinct host cell fates for human malignant melanoma targeted by oncolytic rodent parvoviruses Virology, 446, 37–48

Multiple myeloma
Ge, F., Zhang, L., Tao, S-C., Kitazato, K., Zhang, Z-P., Zhang, X-E. and Bi, L-J. (2011) Quantitative proteomic analysis of tumor reversion in multiple myeloma cells J. Proteome Res., 10, 845-855

Neo-angiogenesis inhibition
Lavie, M., Struyf, S., Stroh-Dege, A., Rommelaere, J., Van Damme, J. and Dinsart, C. (2013) Capacity of wildtype and chemokine-armed parvovirus H-1PV for inhibiting neo-angiogenesis Virology, 447, 221–232

Non-structural proteins
Weiss, N., Stroh-Dege, A., Rommelaere, J., Dinsart, C. and Salomé, N. (2012) Infectivity of progeny virions H1PV efficiently stimulates export and protein-coding sequence of parvovirus J. Virol., 86, 7554-7564

Mihaylov, I.S., Cotmore, S.F. and Tattersall, P. (2014) Complementation for an essential ancillary nonstructural protein function across parvovirus genera Virology, 468 470, 226–237

Oncolytic capacity
Alkassar, M., Gärtner, B., Roemer, K., Graesser, F., Rommelaere, J., Kaestner, L., Haeckel, I. and Graf, N. (2011) The combined effects of oncolytic reovirus plus Newcastle disease virus and reovirus plus parvovirus on U87 and U373 cells in vitro and in vivo J Neurooncol., 104, 715–727

El-Andaloussi, N., Bonifati, S., Kaufmann, J.K., Mailly, L., Daeffler, L., Deryckère, F., Nettelbeck, D.M., Rommelaere, J. and Marchini, A. (2012) Generation of an adenovirus-parvovirus chimera with enhanced oncolytic potential J. Virol., 86, 10418-10431

Lacroix, J., Schlund, F., Leuchs, B., Adolph, K., Sturm, D., Bender, S., Hielscher, T., Pfister, S.M., Witt, O., Rommelaere, J., Schlehofer, J.R. and Witt, H. (2014) Oncolytic effects of parvovirus H-1 in medulloblastoma are associated with repression of master regulators of early neurogenesis Int. J. Cancer, 134, 703–716

Moehler, M., Sieben, M., Roth, S., Springsguth, F., Leuchs, B., Zeidler, M., Dinsart, C., Rommelaere, J. and Galle, P.R. (2011) Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1 BMC Cancer, 11: 464

Moralès, O., Richard, A., Martin, N., Mrizak, D., Sénéchal, M., Miroux, C., Pancré, V., Rommelaere, J., Caillet-Fauquet, P., de Launoit, Y. and Delhem, N. (2012) Activation of a helper and not regulatory human CD4+ T cell response by oncolytic H-1 parvovirus PLoS One, 7: e32197

Sieben, M., Schafer, P., Dinsart, C., Galle, P.R. and Moehler, M. (2013) Activation of the human immune system via toll-like receptors by the oncolytic parvovirus H-1 Int. J. Cancer, 132, 2548–2556

Titze, M.I., Frank, J., Ehrhardt, M., Smola, S., Graf, N. and Lehr, T. (2017) A generic viral dynamic model to systematically characterize the interaction between oncolytic virus kinetics and tumor growth Eur. J. Pharmaceut. Sci., 97, 38–46

Pancreatic cancer
Angelova, A.L., Grekova, S.P., Heller, A., Kuhlmann, O., Soyka, E., Giese, T., Aprahamian, M. et al (2014) Complementary induction of immunogenic cell death by oncolytic parvovirus H-1PV and gemcitabine in pancreatic cancer J. Virol., 88, 5263–5276

Dempe, S., Lavie, M., Struyf, S., Bhat, R., Verbeke, H., Paschek, S., Berghmans, N., Geibig, R., Rommelaere, J., Van Damme, J. and Dinsart, C. (2012) Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: implication of leucocyte recruitment Cancer Immunol. Immunother., 61, 2113–2123

Réjiba, S., Bigand, C., Parmentier, C., Masmoudi, A. and Hajri, A. (2013) Oncosuppressive suicide gene virotherapy “PVH1-yCD/5-FC” for pancreatic peritoneal carcinomatosis treatment: NFB and Akt/PI3K involvement PLoS One, 8: e70594

Recombinant production
Brown, C.S., DiSumma, F.M., Rommelaere, J., Dege, A.Y., Cornelis, J.J., Dinsart, C. and Spaan, W.J.M. (2002) Production of recombinant H1 parvovirus stocks devoid of replication-competent viruses Hum. Gene Ther., 13, 2135-2145

Tumour reversion/therapy
Ge, F., Zhang, L., Tao, S-C., Kitazato, K., Zhang, Z-P., Zhang, X-E. and Bi, L-J. (2011) Quantitative proteomic analysis of tumor reversion in multiple myeloma cells J. Proteome Res., 10, 845-855

Sieben, M., Schafer, P., Dinsart, C., Galle, P.R. and Moehler, M. (2013) Activation of the human immune system via toll-like receptors by the oncolytic parvovirus H-1 Int. J. Cancer, 132, 2548–2556

Reference List RV02-1: 3rd edition, January 2020

OptiPrep™ Reference List RV02-2

GROUP II VIRUSES – rAAV

• IMPORTANT NOTE: RV02-2 LISTS rAAV PAPERS PUBLISHED AFTER SEPT. 2018. THE COMPANION LIST (RV02-1) LISTS rAAV PAPERS PUBLISHED
  BEFORE SEPT. 2018.
• RV02-1 also lists publications on Group II viruses other than rAAV.
• References are divided alphabetically into “Site of delivery” and/or “Research topic” sections. References in each section are listed alphabetically according to first author; multiple references by the same first author are presented chronologically.
• To aid selection, key words are highlighted in blue.
• For detailed methodologies of Group II virus purifications see OptiPrep™ Application Sheets V14-V16. V06 is a methodological review of OptiPrep™
  technology.

AAV properties

AAV2 capsid structure
Tan, Y.Z., Aiyer, S., Mietzsch, M., Hull, J.A., McKenna, R., Grieger, J., Samulski, R.J., Baker, T.S., AgbandjeMcKenna, M. and Lyumkis, D. (2018) Sub-2 Å Ewald curvature corrected structure of an AAV2 capsid variant Nat. Comm., 9: 3628

AAVr3.45
Cho, M., Jung, K., Kim, S-H., Kim, I-S., Kim, M., Shin, M., Lee, H., Park, K.I. and Jang, J-H. (2019) Safety and efficacy evaluations of an adeno-associated virus variant for preparing IL10-secreting human neural stem cell-based therapeutics Gene Ther., 26, 135–150

AAV biology
Wang, D., Tai, P.W.L. and Gao, G. (2019) Adeno-associated virus vector as a platform for gene therapy delivery Nat. Rev., 18, 358-378

AAV libraries
Schmit, P.F., Pacouret, S., Zinn, E., Telford, E., Nicolaou, F., Broucque, F., Andres-Mateos, E., Xiao, R. et al (2020) Cross-packaging and capsid mosaic formation in multiplexed AAV libraries Mol. Ther: Meth. Clin. Devel., 17, 107-121

AAV receptors
Zhang, R., Xu, G., Cao, L., Sun, Z., He, Y., Cui, M., Sun, Y., Li, S., Li, H., Qin, L. et al (2019) Divergent engagements between adeno-associated viruses with their cellular receptor AAVR Nat. Comm., 10: 3760

Adipose tissue (incl. brown fat tissue)

Huang, W., Queen, N.J. and Cao, L. (2019) rAAV-mediated gene delivery to adipose tissue In AdenoAssociated Virus Vectors: Design and Delivery, Methods in Mol. Biol., vol. 1950 (ed. Castle, M.J.), Springer Science+Business Media LLC New York, pp 389-405

Mouchiroud, M., Camiré, E., Aldow, M., Caron, A., Jubinville, E., Turcotte, L., Kaci, I., Beaulieu, M-J., Roy, C. et al (2019) The Hepatokine TSK does not affect brown fat thermogenic capacity, body weight gain, and glucose homeostasis Mol. Metab., 30, 184-191

Age-related diseases

Davidsohn, N., Pezzone, M., Vernet, A., Graveline, A., Oliver, D., Slomovic, S., Punthambaker, S., Sun, X., Liao, R., Bonventre, J.V., and Church, G.M. (2019) A single combination gene therapy treats multiple agerelated diseases Proc. Nat. Acad. Sci. USA, 116, 23505–23511

Aldehyde dehydrogenase

Matsumura, Y., Stiles, K.M., Reid, J., Frenk, E.Z., Cronin, S., Pagovich, O.E. and Crystal, R.G. (2019) Gene therapy correction of aldehyde dehydrogenase 2 deficiency Mol. Ther: Meth. Clin. Devel., 15 72-82

Amyloidosis

Colon-Perez, L.M., Ibanez, K.R., Suarez, M., Torroella, K., Acuna, K., Ofori, E., Levites, Y., Vaillancourt, D.E., Golde, T.E. et al (2019) Neurite orientation dispersion and density imaging reveals white matter and hippocampal microstructure changes produced by Interleukin-6 in the TgCRND8 mouse model of amyloidosis NeuroImage, 202: 116138

Anaesthesia

Zhou, B., Chen, L., Liao, P., Huang, L., Chen, Z., Liao, D., Yang, L., Wang, J. et al (2019) Astroglial dysfunctions drive aberrant synaptogenesis and social behavioral deficits in mice with neonatal exposure to lengthy general anesthesia PLoS Biol., 17: e3000086

Angiogenesis

Lee, S., Ahad, A., Luu, M., Moon, S., Caesar, JA., Cardoso, W.V., Grant, M.B. and Chaqoura, B. (2019) CCN1–Yes-associated protein feedback loop regulates physiological and pathological angiogenesis Mol. Cell. Biol., 39: e00107-19

Atherosclerosis

Zhou, M., Learned, R.M., Rossi, S.J., Tian, H., DePaoli, A.M. and Ling, L. (2019) Therapeutic FGF19 promotes HDL biogenesis and trans-hepatic cholesterol efflux to prevent atherosclerosis J. Lipid Res., 60, 550–565

Auditory function

Al-Moyed, H., Cepeda, A.P., Jung, SY., Moser, T., Kügler, S. and Reisinger, E. (2019) A dual-AAV approach restores fast exocytosis and partially rescues auditory function in deaf otoferlin knock-out mice EMBO Mol. Med., 11: e9396

Autoimmune disorders

Vasquez, M., Consuegra-Fernández, M., Aranda, F., Jimenez, A., Tenesaca, S., Fernandez-Sendin, M., Gomar, C., Ardaiz, N., Di Trani, C.A. (2019) Treatment of experimental autoimmune encephalomyelitis by sustained delivery of low-dose IFN-α J. mmunol., 203, 696–704

Autophagy

Wu, H., Chen, H., Zheng, Z., Li, J., Ding, J., Huang, Z., Jia, C., Shen, Z., Bao, G., Wu, L., Al Mamun, A. et al (2019) Trehalose promotes the survival of random-pattern skin flaps by TFEB mediated autophagy enhancement Cell Death Dis., 10: 483

Baculovirus expression vector

Sandro, Q., Relizani, K. and Benchaouir, R. (2019) AAV production using baculovirus expression vector system In Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Mol. Biol., 1937 (ed. Manfredsson F.P. and Benskey, M.J.), Springer Science+Business Media LLC New York, pp 91-99

Basolateral amygdalae

Huang, T-N., Hsu, T-T., Lin, M-H., Chuang, H-C., Hu, H-T., Sun, C-P., Tao, M-H., Lin, J.Y. and Hsueh, Y-P. (2019) Interhemispheric connectivity potentiates the basolateral amygdalae and regulates social interaction and memory Cell Reports 29, 34–48

Biomaterial-based delivery

Kim, S-H., Lee, S., Lee, H., Cho, M., Schaffer, D.V. and Jang, J-H. (2019) AAVR-displaying interfaces: serotype-independent adeno-associated virus capture and local delivery systems Mol. Ther: Meth. Clin. Devel., 15, 432-443

Bocaviruses

Fakhiri, J., Schneider, M.A., Puschhof, J., Stanifer, M., Schildgen, V., Holderbach, S., Voss, Y., El Andari, J., Schildgen, O. et al (2019) Novel chimeric gene therapy vectors based on adeno-associated virus and four different mammalian bocaviruses Mol. Ther. Meth. Clin. Devel., 12, 202-222

Bone targeting

Alméciga-Díaz, C.J., Montaño, A.M., Barrera, L.A. and Tomatsu, S. (2018) Tailoring the AAV2 capsid vector for bone-targeting Pediatr. Res., 84, 545–551

Bronchial epithelial cells – Cystic fibrosis Lopes-Pacheco, M., Kitoko, J.Z., Morales, M.M., Petrs-Silva, H. and Rocco, P.R.M. (2018) Selfcomplementary and tyrosine-mutant rAAV vectors enhance transduction in cystic fibrosis bronchial epithelial cells Exp. Cell Res., 372, 99–107

Capsid structure/capsid variants/libraries

Cabanes-Creus, M., Ginn, S.L., Amaya, A.K., Liao, S.H.Y., Westhaus, A., Hallwirth, C.V., Wilmott, P., Ward, J., Dilworth, K.L. (2019) Codon-optimization of wild-type adeno-associated virus capsid sequences enhances DNA family shuffling while conserving functionality Mol. Ther. Meth. Clin. Devel., 12, 71-84

Challis, R.C., Kumar, S.R., Chan, K.Y., Challis, C., Beadle, K., Jang, M.J., Kim, H.M., Rajendran, P.S., Tompkins, J.D et al (2019) Systemic AAV vectors for widespread and targeted gene delivery in rodents Nat. Protoc., 14, 379–414

Hanlon, K.S., Meltzer, J.C., Buzhdygan, T., Cheng, M.J., Sena-Esteves, M., Bennett, R.E., Sullivan, T.P., Razmpour, R. et al (2019) Selection of an efficient AAV vector for robust CNS transgene expression Mol. Ther. Meth. Clin, Devel. 15, 320-332

Mary, B., Maurya, S., Arumugam, S., Kumar, V. and Jayandharan, G.R. (2019) Post-translational modifications in capsid proteins of recombinant adeno-associated virus (AAV) 1-rh10 serotypes FEBS J., 286, 4964–4981

Shinohara, Y., Konno, A., Nitta, K., Matsuzaki, Y., Yasui, H., Suwa, J., Hiromura, K. and Hirai, H. (2019) Effects of neutralizing antibody production on AAV-PHP.B-mediated transduction of the mouse central nervous system Mol. Neurobiol., 56, 4203–4214

Thadani, N.N., Dempsey, C., Zhao, J., Vasquez, S.M. and Suh, J. (2018) Reprogramming the activatable peptide display function of adeno-associated virus nanoparticles ACS Nano, 12, 1445−1454

Cardiac disorders

Cardiac gene delivery
Adamiak, M., Liang, Y., Mathiyalagan, P., Agarwal, M., Jha, D., Kohlbrenner, E., Chepurko, E., Jeong, D. et al (2018) Robust cardiac gene delivery and evasion of neutralizing antibodies by extracellular vesicle-associated AAV vectors Circulation, 138, Suppl.1, abstr. 16378

Guenther, C.M., Brun, M.J., Bennett, A.D., Ho, M.L., Chen, W., Zhu, B., Lam, M., Yamagami, M., Kwon, S., Bhattacharya, N. et a. (2019) Protease-activatable adeno-associated virus vector for gene delivery to damaged heart tissue Mol. Ther., 27, 611-622

Lopez-Gordo, E., Kohlbrenner, E., Katz, M.G. and Weber, T. (2019) AAV vectors for efficient gene delivery to rodent hearts In Adeno-Associated Virus Vectors: Design and Delivery, Methods in Mol. Biol., vol. 1950 (ed. Castle, M.J.), Springer Science+Business Media LLC New York, pp 311-332

Yoo, J., Kohlbrenner, E., Kim, O., Hajjar, R.J. and Jeong, D. (2018) Enhancing atrial‐specific gene expression using a calsequestrin cis‐regulatory module 4 with a sarcolipin promoter J. Gene Med., 20: e3060

Cardiac failure/hypertrophy/functional protection
Gao, J., Guo, Y., Chen, Y., Zhou, J., Liu, Y. and Su, P. (2019) Adeno-associated virus 9-mediated RNA interference targeting SOCS3 alleviates diastolic heart failure in rats Gene, 697, 11–18

Jebessa, Z.H., Shanmukha, K.D., Dewenter, M., Lehmann, L.H., Xu, C., Schreiter, F., Siede, D., Gong, X-M., Worst, B.C., Federico, G. (2019) The lipid-droplet-associated protein ABHD5 protects the heart through proteolysis of HDAC4 Nat. Metab. (2019) 1, 1157–1167

Lee, D.P., Tan, W.L.W., Anene-Nzelu, C.G., Lee, C.J.M., Li, P.Y., Luu, T.D.A., Chan, C.X., Tiang, Z., Ng, S.L. et al (2019) Response robust CTCF-based chromatin architecture underpins epigenetic changes in the heart failure stress–gene response Circulation, 139, 1937–1956

Mi-Mi, L., Farman, G.P., Mayfield, R.M., Strom, J., Chu, M., Pappas, C.T. and Gregorio, C.C. (2020) In vivo elongation of thin filaments results in heart failure PLoS One, 15: e0226138

Müller, O.J., Heckmann, M.B., Ding, L., Rapti, K., Rangrez, A.Y., Gerken, T., Christiansen, N., Rennefahrt, U.E.E., Witt, H., González Maldonado, S. et al (2019) Comprehensive plasma and tissue profiling reveals systemicmetabolic alterations in cardiac hypertrophy and failure Cardiovasc. Res., 115, 1296–1305

Oh, J.G., Jang, S.P., Yoo, J., Lee, M-A., Lee, S.H., Lim, T., Jeong, E., Kho, C. et al (2019) Role of the PRC2- Six1-miR-25 signaling axis in heart failure J. Mol. Cell. Cardiol., 129, 58–68

Stroik, D.R., Ceholski, D.K., Bidwell, P.A., Mleczko, J., Thanel, P.F., Kamdar, F., Autry, J.M., Cornea, R.L. and Thomas, D.D. (2020) Viral expression of a SERCA2a-activating PLB mutant improves calcium cycling and synchronicity in dilated cardiomyopathic hiPSC-CMs J. Mol. Cell. Cardiol., 138, 59–65

Wang, X., Chen, L., Zhao, X., Xiao, L., Yi, S., Kong, Y., Jiang, Y. and Zhang, J. (2020) A cathelicidin-related antimicrobial peptide suppresses cardiac hypertrophy induced by pressure overload by regulating IGFR1/PI3K/AKT and TLR9/AMPKα Cell Death Dis., 11: 96

Cardiomyocyte proliferation
Haginiwa, S., Sadahiro, T., Kojima, H., Isomi, M., Tamura, F., Kurotsu, S., Tani, H., Muraoka, N. et al (2019) Tbx6 induces cardiomyocyte proliferation in postnatal and adult mouse hearts Biochem. Biophys. Res. Comm., 513, 1041-1047

Cardiomyopathy
Chatzifrangkeskou, M., Yadin, D., Marais, T., Chardonnet, S., Cohen-Tannoudji, M., Mougenot, N., Schmitt, A., Crasto, S., Di Pasquale, E. et al (2018) Cofilin-1 phosphorylation catalyzed by ERK1/2 alters cardiac actin dynamics in dilated cardiomyopathy caused by lamin A/C gene mutation Hum. Mol. Genet., 27, 3060-3078

Liao, D., Chen, W., Tan, C.Y., Wong, J.X., Chan, P.S., Tan, L.W., Foo, R. and Jiang, J. (2019) Upregulation of Yy1 suppresses dilated cardiomyopathy caused by Ttn insufficiency Sci. Rep., 9: 16330

Nakamura, M., Liu, T., Husain, S., Zhai, P., Warren, J.S., Hsu, C-P., Matsuda, T., Phiel, C.J. et al (2019) Glycogen synthase kinase-3a promotes fatty acid uptake and lipotoxic cardiomyopathy Cell Metab., 29, 1119–1134

Xu, R., Jia, Y., Zygmunt, D.A. and Martin, P.T. (2019) rAAVrh74.MCK.GALGT2 protects against loss of hemodynamic function in the aging mdx mouse heart Mol. Ther., 27, 636-649

Yadav, S., Yuan, C-C., Kazmierczak, K., Liang, J., Huang, W., Takeuchi, L.M., Kanashiro-Takeuchi, R.M. and Szczesna-Cordary, D. (2019) Therapeutic potential of AAV9-S15D-RLC gene delivery in humanized MYL2 mouse model of HCM J. Mol. Med., 97, 1033–1047

Heart rate control
Rajendran, P.S., Challis, R.C., Fowlkes, C.C., Hanna, P., Tompkins, J.D., Jordan, M.C., Hiyari, S., GabrisWeber, B.A., Greenbaum, A. et al (2019) Identification of peripheral neural circuits that regulate heart rate using optogenetic and viral vector strategies Nature Comm., 10: 1944

Myocardial infarction
Garikipati,V.N.S., Verma, S.K., Cheng, Z., Liang, D., Truongcao, M.M., Cimini, M., Yue, Y., Huang, G., Wang, C. et al (2019) Circular RNA CircFndc3b modulates cardiac repair after myocardial infarction via FUS/VEGF-A axis Nat. Comm., 10: 4317

Lee, S., Lee, D.H., Park, B-W., Kim, R., Hoang, A.D., Woo, S-K., Xiong, W., Lee, Y.J., Ban, K. and Park, H.J. (2019) In vivo transduction of ETV2 improves cardiac function and induces vascular regeneration following myocardial infarction Exp. Mol. Med., 51: 13

Motloch, L.J., Cacheux, M., Ishikawa, K., Xie, C., Hu, J., Aguero, J., Fish, K.M., Hajjar, R.J. and Akar, F.G. (2018) Primary effect of SERCA2a gene transfer on conduction reserve in chronic myocardial infarction J. Am. Heart Assoc., 7: e009598

Tian, S., Lei, I., Gao, W., Liu, L., Guo, Y., Creech, J., Herron, T.J., Xian, S., Ma, P.X., Chen, Y.E., Li, Y., Alam, H.B. and Wang, Z. (2019) HDAC inhibitor valproic acid protects heart function through Foxm1 pathway after acute myocardial infarction Ebio Med., 39, 83–94

Transcription factors
Akerberg, B.N., Gu, F., VanDusen, N.J., Zhang, X., Dong, R., Li, K., Zhang, B., Zhou, B., Sethi, I., Ma, Q. et al (2019) A reference map of murine cardiac transcription factor chromatin occupancy identifies dynamic and conserved enhancers Nat. Comm., 10: 4907

Cell-specific gene transfer

Reul, J., Muik, A. and Buchholz, C.J. (2019) Ligand coupling to the AAV capsid for cell-specific gene transfer In Adeno-Associated Virus Vectors: Design and Delivery, Methods in Mol. Biol., vol. 1950 (ed. Castle, M.J.), Springer Science+Business Media LLC New York, pp 35-50

Cellular communication network factor 1 (CCN1)

Lee, S., Ahad, A., Luu, M., Moon, S., Caesar, JA., Cardoso, W.V., Grant, M.B. and Chaqoura, B. (2019) CCN1–Yes-associated protein feedback loop regulates physiological and pathological angiogenesis Mol. Cell. Biol., 39: e00107-19

Cholestasis

Aronson, S.J., Bakker, R.S., Shi, X., Duijst, S., ten Bloemendaal, L., de Waart, D.R., Verheij, J., Ronzitti, G. et al (2019) Liver-directed gene therapy results in long-term correction of progressive familial intrahepatic cholestasis type 3 in mice J. Hepatol., 71, 153–162

Circular RNAs

Meganck, R.M., Borchardt, E.K., Castellanos Rivera, R.M., Scalabrino, M.L., Wilusz, J.E., Marzluff, W.F. and Asokan, A. (2018) Tissue-dependent expression and translation of circular RNAs with recombinant AAV vectors in vivo Mol. Ther. Nucleic Acids, 13, 89-98

Clinical application (AAV vector choice)

He, T., Itano, M.S., Earley, L.F., Hall, N.E., Riddick, N., Samulski, R.J.and Li, C. (2019) The influence of murine genetic background in adeno-associated virus transduction of the mouse brain Human Gene Ther. Clin. Devel., 30, 169-181

Cre recombinase gene

Meador, K., Wysoczynski, C.L., Norris, A.J., Aoto, J., Bruchas, M.R. and Tucker, C.L. (2019) Achieving tight control of a photoactivatable Cre recombinase gene switch: new design strategies and functional characterization in mammalian cells and rodent Nucl. Acids Res., 47: e97

CRISPR/Cas9

Chen, S., Sun, S., Moonen, D., Lee, C., Lee, A.Y-F., Schaffer, D.V. and He, L. (2019) CRISPR-READI: efficient generation of knockin mice by CRISPR RNP electroporation and AAV donor infection Cell Rep., 27, 3780–3789

D’Amico, D., Mottis, A., Potenza, F., Sorrentino, V., Li, H., Romani, M., Lemos, V., Schoonjans, K. et al (2019) The RNA-binding protein PUM2 impairs mitochondrial dynamics and mitophagy during aging Mol. Cell 73, 775–787

Ekman, F.K., Ojala, D.S., Adil, M.M., Lopez, P.A., Schaffer, D.V. and Gaj, T. (2019) CRISPR-Cas9-mediated genome editing increases lifespan and improves motor deficits in a Huntington’s disease mouse model Mol. Ther: Nucleic Acids, 17, 829-839

Fakhiri, J., Nickl, M. and Grimm, D. (2019) Rapid and simple screening of CRISPR guide RNAs (gRNAs) in cultured cells using adeno-associated viral (AAV) vectors In CRISPR Gene Editing: Methods and Protocols, Methods in Mol. Biol., vol. 1961 (ed. Luo, Y.), Springer Science+Business Media LLC New York, pp 111-126

Gao, Y., Hisey, E., Bradshaw, T.W.A., Erata, E., Brown, W.E., Courtland, J.L., Uezu, A., Xiang, Y., Diao, Y. and Soderling, S.H. (2019) Plug-and-play protein modification using homology-independent universal genome engineering Neuron,103, 583–597

Ideno, N., Yamaguchi, H., Okumura, T., Huang, J., Brun, M.J., Ho, M.L., Suh, J., Gupta, S., Maitra, A. and Ghosh, B. (2019) A pipeline for rapidly generating genetically engineered mouse models of pancreatic cancer using in vivo CRISPR-Cas9-mediated somatic recombination Lab. Invest., 99, 1233–1244

Jayavaradhan, R., Pillis, D.M., Goodman, M., Zhang, F., Zhang, Y., Andreassen, P.R. and Malik, P. (2019) CRISPR-Cas9 fusion to dominant-negative 53BP1 enhances HDR and inhibits NHEJ specifically at Cas9 target sites Nat. Comm., 10: 2866

Krooss, S.A., Dai, Z., Schmidt, F., Rovai, A., Fakhiri, J., Dhingra, A., Yuan, Q., Yang, T. et al (2020) Ex vivo/in vivo gene editing in hepatocytes using ‘‘All-in-One’’ CRISPR-adeno-associated virus vectors with a selflinearizing repair template iScience, 23: 100764

McCullough, K.T., Boye, S.L., Fajardo, D., Calabro, K., Peterson, J.J., Strang, C.E., Chakraborty, D., Gloskowski, S., Haskett, S. et al (2019) Somatic gene editing of GUCY2D by AAV-CRISPR/Cas9 alters retinal structure and function in mouse and macaque Hum. Gene Ther., 30, 571-589

Pavel-Dinu, M., Wiebking, V., Dejene, B.T., Srifa, W., Mantri, S., Nicolas, C.E., Lee, C., Bao, G. and Kildebeck, E.J. (2019) Gene correction for SCID-X1 in long-term hematopoietic stem cells Nat. Comm., 10:1634

Santiago-Fernández, O., Osorio, F.G., Quesada, V., Rodríguez, F., Basso, S., Maeso, D., Rolas, L., Barkaway, A. et al (2019) Development of a CRISPR/Cas9-based therapy for Hutchinson–Gilford progeria syndrome Nat. Med., 25, 423–426

Spence, E.F., Dube, S., Uezu, A., Locke, M., Soderblom, E.J. and Soderling, S.H. (2019) In vivo proximity proteomics of nascent synapses reveals a novel regulator of cytoskeleton-mediated synaptic maturation Nat. Comm., 10: 386

Tran, N.T., Sommermann, T., Graf, R., Trombke, J., Pempe, J., Petsch, K., K€uhn, R., Rajewsky, K. and Chu, V.T. (2019) Efficient CRISPR/Cas9-mediated gene knockin in mouse hematopoietic stem and progenitor cells Cell Reports 28, 3510- 3522

Yang, S., Li, S. and Li, X-J. (2018) Shortening the half-life of Cas9 maintains its gene editing ability and reduces neuronal toxicity Cell Rep., 25, 2653–2659

Zabaleta, N., Barberia, M., Martin-Higueras, C., Zapata-Linares, N., Betancor, I., Rodrigue, S., MartinezTurrillas, R., Torella, L. et al (2018) CRISPR/Cas9-mediated glycolate oxidase disruption is an efficacious and safe treatment for primary hyperoxaluria type I Nat. Comm., 9: 5454

Cytosine/adenine base editing

Levy, J.M., Yeh, W-H., Pendse, N., Davis, J.R., Hennessey, E., Butcher, R., Koblan, L.W., Comander, J., Liu, Q. and Liu, D.R. (2020) Cytosine and adenine base editing of the brain, liver, retina, heart and skeletal muscle of mice via adeno-associated viruses Nat. Biomed. Engineer., 4, 97–110

Dendritic cell targeting

Krotova, K., Day, A. and Aslanidi, G. (2019) An engineered AAV6-based vaccine induces high cytolytic antitumor activity by directly targeting DCs and improves Ag presentation Mol. Ther. Oncolytics, 15, 166-177

Rossi, A., Dupaty, L, Aillot, L, Zhang, L, Gallien, C., Hallek, M., Odenthal, M., Adriouch, S et al (2019) Vector uncoating limits adenoassociated viral vector-mediated transduction of human dendritic cells and vector immunogenicity Sci. Rep., 9: 3631

Diabetic disorders

Gan, S.U., Fu, Z., Sia, K.C., Kon, O.L., Calne, R. and Lee, K.O. (2019) Development of a liver-specific Tet-off AAV8 vector for improved safety of insulin gene therapy for diabetes J. Gene Med. 21: 3067

Guay, C., Kruit, J.K., Rome, S., Menoud, V., Mulder, N.L., Jurdzinski, A., Mancarella, F., Sebastiani, G., Donda, A. and Gonzalez, B.J. (2019) Lymphocyte-derived exosomal microRNAs promote pancreatic β cell death and may contribute to type 1 diabetes development Cell Metab., 28, 348-361

He, W-y., Zhang, B., Zhao, W-c., He, J., Zhang, L., Xiong, Q-m., Wang, J. and Wang, H-b. (2019) Contributions of mTOR activation-mediated upregulation of synapsin II and neurite outgrowth to hyperalgesia in STZ-induced diabetic rats ACS Chem. Neurosci., 10, 2385−2396

Li, T., Li, H., Li, W., Chen, S., Feng, T., Jiao, W., Wu, C., Dong, J. et al (2019) Interleukin-37 sensitize the elderly type 2 diabetic patients to insulin therapy through suppressing the gut microbiota dysbiosis Mol. Immunol., 112, 322–329

DNA shuffling

Herrmann, A-K., Bender, C., Kienle, E., Gross, S., El Andari, J., Botta, J., Schürmann, N., Wiedtke, E., Niopek, D. and Grimm, D. (2019) A robust and all-inclusive pipeline for shuffling of adeno-associated viruses ACS Synth. Biol., 8, 194−206

Endothelial cells

Zhang, L., Rossi, A., Lange, L., Meumann, N., Koitzsch, U., Christie, K., Nesbit, M.A., Moore, C.B.T., Hacker, U.T. et al (2019) Capsid engineering overcomes barriers toward adeno-associated virus vectormediated transduction of endothelial cells Hum. Gene Ther., 30. 1284-1296

Enteric nervous system

Boesmans, W., Hao, M.M., Fung, C., Li, Z., Van den Haute, C., Tack, J., Pachnis, V. and Vanden Berghe, P. (2019) Structurally defined signaling in neuro-glia units in the enteric nervous system Glia, 67, 1167–1178

Epidermal growth factor

Cramer, M.L., Xu, R. and Martin, P.T. (2019) Soluble heparin binding epidermal growth factor-like growth factor is a regulator of GALGT2 epression and GALGT2-dependent muscle and neuromuscular phenotypes Mol. Cell. Biol., 39: e00140-19

Epilepsy

Snowball, A., Chabrol, E., Wykes, R.C., Shekh-Ahmad, T., Cornford, J.H., Lieb, A., Hughes, M.P., Massaro, G., Rahim, A.A. (2019) Epilepsy gene therapy using an engineered potassium channel J. Neurosci., 39, 3159 – 3169

Food-seeking behaviour

Duraffourd, C., Huckstepp, R.T.R., Braren, I., Fernandes, C., Brock, O., Delogu, A., Prysyazhna, O., Burgoyne, J. and Eaton, P. (2019) PKG1α oxidation negatively regulates food seeking behaviour and reward Redox Biol., 21, 101077

Haemophilia

Maurya, S., Mary, B. and Jayandharan, G.R. (2019) Rational engineering and preclinical evaluation of Neddylation and SUMOylation site modified adeno-associated virus vectors in murine models of hemophilia B and Leber congenital amaurosis Hum. Gene Ther., 30, 1461-1476

Zhang, J-P., Cheng, X-X., Zhao, M., Li, G-H., Xu, J., Zhang, F., Yin, M-D., Meng, F-Y., Dai, X-Y. et al (2019) Curing hemophilia A by NHEJ-mediated ectopic F8 insertion in the mouse Genome Biol., 20: 276

Hearing

György, B., Meijer, E.J., Ivanchenko, M.V., Tenneson, K., Emond, F., Hanlon, K.S., Indzhykulian, A.A., Volak, A. et al (2019) Gene transfer with AAV9-PHP.B rescues hearing in a mouse model of Usher syndrome 3A and transduces hair cells in a non-human primate Mol. Ther. Meth. Clin. Devel., 13, 1-13

Hematopoietic stem cells

Cromer, M.K., Vaidyanathan, S., Ryan, D.E., Curry, B., Lucas, A.B., Camarena, J., Kaushik, M., Hay, S.R., et al (2018) Global transcriptional response to CRISPR/Cas9-AAV6-based genome editing in CD34+ hematopoietic stem and progenitor cells Mol. Ther., 26, 2431-2442

Gomez-Ospina, N., Scharenberg, S.G., Mostrel, N., Bak, R.O., Mantri, S., Quadros, R.M., Gurumurthy, C.B., Lee, C., Bao, G. et al (2019) Human genome-edited hematopoietic stem cells phenotypically correct mucopolysaccharidosis type I Nat. Comm., 10: 4045

Pavel-Dinu, M., Wiebking, V., Dejene, B.T., Srifa, W., Mantri, S., Nicolas, C.E., Lee, C., Bao, G. and Kildebeck, E.J. (2019) Gene correction for SCID-X1 in long-term hematopoietic stem cells Nat. Comm., 10:1634

Tran, N.T., Sommermann, T., Graf, R., Trombke, J., Pempe, J., Petsch, K., K€uhn, R., Rajewsky, K. and Chu, V.T. (2019) Efficient CRISPR/Cas9-mediated gene knockin in mouse hematopoietic stem and progenitor cells Cell Reports 28, 3510- 3522

Heparan sulphate binding

Gorbatyuk, O.S., Warrington JR, K.H., Gorbatyuk, M.S., Zolotukhin, I., Lewin, A.S. and Muzyczka, N. (2019) Biodistribution of adeno-associated virus type 2 with mutations in the capsid that contribute to heparan sulfate proteoglycan binding Virus Res., 274: 97771

Hepatic glucose metabolism

Pradas-Juni, M., Hansmeier, N.R., Link, J.C., Schmidt, E., Larsen, B.D., Klemm, P., Meola, N. et al (2020) A MAFG-lncRNA axis links systemic nutrient abundance to hepatic glucose metabolism Nat. Comm., 11: 644 Hepatocellular carcinoma (see also “Liver gene delivery”)

Khan, N., Bammidi, S., Chattopadhyay, S. and Jayandharan, G.R. (2019) Vector encoding inducible caspase‑9 and a chemical inducer of dimerization is effective in a xenotransplantation model of hepatocellular carcinoma Bioconjugate Chem., 30, 1754−1762

Hepatocytes (human)

Michailidis, E., Vercauteren, K., Mancio-Silva, L., Andrus, L., Jahan, C., Ricardo-Lax, I., Zou, C., Kabbani, M., Park, P. (2020) Expansion, in vivo–ex vivo cycling, and genetic manipulation of primary human hepatocytes Proc. Natl. Acad. Sci. USA 117, 1678–1688

Heriditary angioedema

Qiu, T., Chiuchiolo, M.J., Whaley, A.S., Russo, A.R., Sondhi, D., Kaminsky, S.M., Crystal, R.G. and Pagovich, O.E. (2109) Gene therapy for C1 esterase inhibitor deficiency in a murine model of hereditary angioedema Allergy, 74, 1081–1089

Hutchinson–Gilford progeria syndrome

Santiago-Fernández, O., Osorio, F.G., Quesada, V., Rodríguez, F., Basso, S., Maeso, D., Rolas, L., Barkaway, A. et al (2019) Development of a CRISPR/Cas9-based therapy for Hutchinson–Gilford progeria syndrome Nat. Med., 25, 423–426

Hyperlipidaemia

Yang, N., Song, Y., Dong, B., Li, Y., Kou, L., Yang, J. and Qin, Q. (2018) Elevated interleukin-38 level associates with clinical response to Atorvastatin in patients with hyperlipidemia Cell Physiol Biochem 2018, 49, 653-661

Immune responses

Ashley, S.N., Somanathan, S., Giles, A.R. amd Wilson, J.M. (2019) TLR9 signaling mediates adaptive immunity following systemic AAV gene therapy Cell. Immunol., 346: 103997

Infectivity

Rajasekaran, S., Thatte, J., Periasamy, J., Javali, A., Jayaram, M., Sen, D., Krishnagopal, A., Jayandharan, G.R. and Sambasivan, R. (2018) Infectivity of adeno-associated virus serotypes in mouse testis BMC Biotech., 18: 70

Inflammatory pain

Sondermann. J.R., Barry, A.M., Jahn, O., Michel, N., Abdelaziz, R., Kügler, S., Gomez-Varela, D. and Schmidt, M. (2019) Vti1b promotes TRPV1 sensitization during inflammatory pain Pain, 160, 508–527

Insulin signaling

Li, Q., Zhao, Q., Zhang, J., Zhou, L., Zhang, W., Chua, B.T., Chen, Y., Xu, L. and Li, P. (2019) The protein phosphatase 1 complex is a direct target of AKT that links insulin signaling to hepatic glycogen deposition Cell Reports 28, 3406–3422

Intrathecal delivery

Gong, Y., Berenson, A., Laheji, F., Gao, G., Wang, D., Ng, C., Volak, A., Kok, R., Kreouzis, V. et al (2019) Intrathecal adeno-associated viral vector-mediated gene delivery for adrenomyeloneuropathy Hum. Gene Ther., 30, 544-555

Intravenous injection

Challis, R.C., Kumar, S.R., Chan, K.Y., Challis, C., Beadle, K., Jang, M.J., Kim, H.M., Rajendran, P.S., Tompkins, J.D et al (2019) Systemic AAV vectors for widespread and targeted gene delivery in rodents Nat. Protoc., 14, 379–414

Leber congenital amaurosis

Maurya, S., Mary, B. and Jayandharan, G.R. (2019) Rational engineering and preclinical evaluation of Neddylation and SUMOylation site modified adeno-associated virus vectors in murine models of hemophilia B and Leber congenital amaurosis Hum. Gene Ther., 30, 1461-1476

Lipid homeostasis

Su, L., Zhou, L., Chen, F-J., Wang, H., Qian, H., Sheng, Y., Zhu, Y., Yu, H., Gong, X. et al (2019) Cideb controls sterol-regulated ER export of SREBP/SCAP by promoting cargo loading at ER exit sites EMBO J., 38: e100156

Lipoprotein metabolism

Hytönen, E., Laurema, A., Kankkonen, H., Miyanohara, A. Kärjä, V., Hujo, M., Laham-Karam, N., and YläHerttuala, S. (2019) Bile-duct proliferation as an unexpected side-effect after AAV2-LDLR gene transfer to rabbit liver Sci. Rep., 9:6934

Liver gene delivery

Cunningham, S.C. and Alexander, I.E. (2019) AAV-mediated gene delivery to the mouse liver In Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Mol. Biol., 1937 (ed. Manfredsson F.P. and Benskey, M.J.), Springer Science+Business Media LLC New York, pp 213-219

Gao, H., Lv, Y., Liu, Y., Li, J., Wang, X., Zhou, Z., Tipoe, G.L., Ouyang, S., Guo, Y. et al (2019) Wolfberryderived zeaxanthin dipalmitate attenuates ethanol-induced hepatic damage Mol. Nutr. Food Res., 63: 1801339

Wei, J., Ran, G., Wang, X., Jiang, N., Liang, J., Lin, X., Ling, C. and Zhao, B. (2019) Gene manipulation in liver ductal organoids by optimized recombinant adeno-associated virus vectors J. Biol. Chem., 294, 14096–14104

Lysosomal disorders

Doyle, B.M., Turner, S.M.F., Sunshine, M.D., Doerfler, P.A., Poirier, A.E., Vaught, L.A., Jorgensen, M.L., Falk, D.J., Byrne, B.J. and Fuller, D.D. (2019) AAV gene therapy utilizing glycosylation-independent lysosomal targeting tagged GAA in the hypoglossal motor system of Pompe mice Mol. Ther: Meth. Clin. Devel., 15, 194-203

Du, S., Ou, H., Cui, R., Jiang, N., Zhang, M., Li, X., Ma, J., Zhang, J. and Ma, D. (2019) Delivery of glucosylceramidase beta gene using AAV9 vector therapy as a treatment strategy in mouse models of gaucher disease Human Gene Ther., 30, 155-167

Gomez-Ospina, N., Scharenberg, S.G., Mostrel, N., Bak, R.O., Mantri, S., Quadros, R.M., Gurumurthy, C.B., Lee, C., Bao, G. et al (2019) Human genome-edited hematopoietic stem cells phenotypically correct Mucopolysaccharidosis type I Nat. Comm., 10: 4045

Metagenomic analysis of food

Dugat-Bony, E., Lossouarn, J., De Paepe, M., Sarthou, A-S., Fedala, Y., Petit, M.A. and Chaillou, S. (2020) Viral metagenomic analysis of the cheese surface: a comparative study of rapid procedures for extracting viral particles Food Microbiology 85 (2020) 103278

MicroRNA

Guay, C., Kruit, J.K., Rome, S., Menoud, V., Mulder, N.L., Jurdzinski, A., Mancarella, F., Sebastiani, G., Donda, A. and Gonzalez, B.J. (2019) Lymphocyte-derived exosomal microRNAs promote pancreatic β cell death and may contribute to type 1 diabetes development Cell Metab., 28, 348-361

Kozuka, T., Omori, Y., Watanabe, S., Tarusawa, E., Yamamoto, H., Chaya, T., Furuhashi, M., Morita, M., Sato, T. (2019) miR-124 dosage regulates prefrontal cortex function by dopaminergic modulation Sci. Rep., 9:3445

Mitochondrial function

Cabrera-Perez, R., Vila-Julia, F., Hirano, M., Mingozzi, F., Torres-Torronteras, J. and Martı, R. (2019) Alpha1-antitrypsin promoter improves the efficacy of an adeno associated virus vector for the treatment of mitochondrial neurogastrointestinal encephalomyopathy Hum. Gene Ther., 30. 985-998

D’Amico, D., Mottis, A., Potenza, F., Sorrentino, V., Li, H., Romani, M., Lemos, V., Schoonjans, K. et al (2019) The RNA-binding protein PUM2 impairs mitochondrial dynamics and mitophagy during aging Mol. Cell 73, 775–787

Muscle function/gene transfer

Butterfield, J.S.S., Biswas, M., Shirley, J.L., Kumar, S.R.P., Sherman, A., Terhorst, C., Ling, C. and Herzog, R.W. (2019) TLR9-Activating CpG-B ODN but not TLR7 agonists triggers antibody formation to factor IX in muscle gene transfer Hum. Gene Ther. Meth., 30, 81-92

Cramer, M.L., Xu, R. and Martin, P.T. (2019) Soluble heparin binding epidermal growth factor-like growth factor is a regulator of GALGT2 epression and GALGT2-dependent muscle and neuromuscular phenotypes Mol. Cell. Biol., 39: e00140-19

Li, M., Zhang, C-S., Zong, Y., Feng, J-W., Ma, T., Hu, M., Lin, Z., Li, X., Xie, C. et al (2019) Transient receptor potential V channels are essential for glucose sensing by aldolase and AMPK Cell Metab., 30, 508–524

Lornage, X., Romero, N.B., Grosgogeat, C.A., Malfatti, E., Donkervoort, S., Marchetti, M.M., Neuhaus, S.B., Foley, A.R., Labasse, C. et al (2019) ACTN2 mutations cause “Multiple structured core disease” (MsCD) Acta Neuropathol., 137, 501–519

Malerba, A., Klein, P., Lu-Nguyen, N., Cappellari, O., Strings-Ufombah, V., Harbaran, S., Roelvink, P., Suhy, D., Trollet, C. and Dickson, G. (2019) Established PABPN1 intranuclear inclusions in OPMD muscle can be efficiently reversed by AAV-mediated knockdown and replacement of mutant expanded PABPN1 Hum. Mol. Genet., 28, 3301–3308

Niranjan, N., Mareedu, S., Tian, Y., Kodippili, K., Fefelova, N., Voit, A., Xie, L.H., Duan, D., and Babu, G.J. (2019) Sarcolipin overexpression impairs myogenic differentiation in Duchenne muscular dystrophy Am. J. Physiol. Cell. Physiol., 317, C813–C824

Myeloid leukaemia

Khan, N., Bammidi, S. and Jayandharan, G.R. (2019) A CD33 antigen-targeted AAV6 vector expressing an inducible caspase‑9 suicide gene is therapeutic in a xenotransplantation model of acute myeloid leukemia Bioconjug. Chem., 30, 2404−2416

Neural system delivery

Adrenomyeloneuropathy
Gong, Y., Berenson, A., Laheji, F., Gao, G., Wang, D., Ng, C., Volak, A., Kok, R., Kreouzis, V. et al (2019) Intrathecal adeno-associated viral vector-mediated gene delivery for adrenomyeloneuropathy Hum. Gene Ther., 30, 544-555

Aging process
Jawaid, A., Woldemichael, B.T., Kremer, E.A., Laferriere, F., Gaur, N., Afroz, T., Polymenidou, M. and Mansuy, I.M. (2019) Memory decline and its reversal in aging and neurodegeneration involve miR-183/96/182 biogenesis Mol. Neurobiol., 56, 3451–3462

McMurphy, T., Huang, W., Liu, X., Siu, J.J., Queen, N.J., Xiao, R. and Cao, L. (2019) Hypothalamic gene transfer of BDNF promotes healthy aging in mice Aging Cell, 18: e12846

Alzheimer’s disease
Carlomagno, Y., Chung, D-e.C., Yue, M., Kurti, A., Avendano, N.M., Castanedes-Casey, M., Hinkle, K.M., Jansen-West, K., Daughrity, L.M., et al (2019) Enhanced phosphorylation of T153 in soluble tau is a defining biochemical feature of the A152T tau risk variant Acta Neuropathol. Comm., 7: 10

Luengo, E., Buendia, I., Fernández-Mendívil, C., Trigo-Alonso, P., Negredo, P., Michalska, P., HernándezGarcía, B., Sánchez-Ramos, C. et al (2019) Pharmacological doses of melatonin impede cognitive decline in tau-related Alzheimer models, once tauopathy is initiated, by restoring the autophagic flux J. Pineal Res., 67:e12578

Forner, S., Martini, A.C., Prieto, G.A., Dang, C.T., Rodriguez-Ortiz, C.J., Reyes-Ruiz, J.M., Trujillo-Estrada, L., da Cunha, C., Andrews, E.J. et al (2019) Intra- and extracellular β-amyloid overexpression via adenoassociated virus-mediated gene transfer impairs memoryand synaptic plasticity in the hippocampus Sci. Rep., 9: 15936

Rosenberg, J.B., Kaplitt, M.G., De, B.P., Chen, A., Flagiello, T., Salami, C., Pey, E., Zhao, L., Ricart, R.J. et al (2018) AAVrh.10-mediated APOE2 central nervous system gene therapy for APOE4-associated Alzheimer’s disease Hum. Gener Ther. Clin. Dev. 29, 24-47

Wang, Z-H., Xiang, J., Liu, X., Yu, S.P., Manfredsson, F.P., Sandoval, I.M., Wu, S., Wang, J-Z. and Ye, K. (2019) Deficiency in BDNF/TrkB neurotrophic activity stimulates δ-secretase by upregulating C/EBPb in Alzheimer’s disease Cell Reports 28, 655–669

Amygdal delivery
Babaev, O., Cruces-Solis, H., Chatain, C.P., Hammer, M., Wenger, S., Ali, H., Karalis, N., de Hoz, L. et al (2018) IgSF9b regulates anxiety behaviors through effects on centromedial amygdala inhibitory synapses Nat. Comm., 9: 5400

Guo, Z., Zhao, F., Wang, Y., Wang, Y., Geng, M., Zhang, Y., Ma, Q. and Xu, X. (2019) Sevoflurane exerts an anti-depressive action by blocking the HMGB1/TLR4 pathway in unpredictable chronic mild stress rats J. Mol. Neurosci., 69, 546–556

Mineur, Y.S., Cahuzac, E.L., Mose, T.N., Bentham, M.P., Plantenga, M.E., Thompson, D.C. and Picciotto, M.R. (2018) Interaction between noradrenergic and cholinergic signaling in amygdala regulates anxiety- and depression-related behaviors in mice Neuropsychopharmacology, 43, 2118–2125

Zhou, M., Liu, Z., Melin, M.D., Ng, Y.H., Xu, W. and Südhof, T.C. (2018) A central amygdala to zona incerta projection is required for acquisition and remote recall of conditioned fear memory Nat. Neurosci., 21, 1515–1519

Amyotrophic lateral sclerosis
Chew, J., Cook, C., Gendron, T.F., Jansen-West, K., del Rosso, G., Daughrity, L.M., Castanedes-Casey, M., Kurti, A. Stankowski, J.N. (2019) Aberrant deposition of stress granule resident proteins linked to C9orf72-associated TDP-43 proteinopathy Mol. Neurodegen., 14: 9

Lopez-Font, I., Sogorb-Esteve, A., Javier-Torrent, M., Brinkmalm, G., Herrando-Grabulosa, M., García-Lareu, B., Turon-Sans, J. Rojas-García, R. (2019) Decreased circulating ErbB4 ectodomain fragments as a read-out of impaired signaling function in amyotrophic lateral sclerosis Neurobiol. Disease, 124, 428–438

Zhang, Y-J., Guo, L., Gonzales, P.K., Gendron, T.F., Wu, Y., Jansen-West, K., O’Raw, A.D., Pickles, S.R., Prudencio, M., Carlomagno, Y. et al (2019) Heterochromatin anomalies and double-stranded RNA accumulation underlie C9orf72 poly(PR) toxicity Science 363, eaav2606

Anxiety-like behaviour
Günther, A., Luczak, V., Gruteser, N., Abel, T. and Baumann, A. (2019) HCN4 knockdown in dorsal hippocampus promotes anxiety-like behavior in mice Genes Brain Behav., 18: e12550

Astrocyte delivery/astrocyte-to-neuron conversion
Chen, Y-C., Ma, N-X., Pei, Z-F., Wu, Z., Do-Monte, F.H., Keefe, S., Yellin, E. Chen, M.S., Yin, J-C. et al (2020) A NeuroD1 AAV-based gene therapy for functional brain repair after ischemic injury through in vivo astrocyte-to-neuron conversion Mol. Ther., 28, 217-234

Mattugini, N., Bocchi, R., Scheuss, V., Russo, G.L., Torper, O., Lao, C.L.L. and Götz, M. (2019) Inducing different neuronal subtypes from astrocytes in the injured mouse vertebral cortex neuron 103, 1086–1095

Slezak, M., Kandler, S., Van Veldhoven, P.P., Van den Haute, C., Bonin, V. and Holt, M.G. (2019) Distinct mechanisms for visual and motor-related astrocyte responses in mouse visual cortex Curr. Biol., 29, 3120–3127

Zhao, B., Pan, Y., Xu, H. and Song, X. (2018) Kindlin-1 regulates astrocyte activation and pain sensitivity in rats with neuropathic pain Reg. Anesth. Pain Med., 43, 547–553

Autism spectrum disorder
Skelton. P.D., Frazel, P.W., Lee, D., Suh, H. and Luikart, B.W. (2019) Pten loss results in inappropriate excitatory connectivity Mol. Psych., 24, 1627–1640

Axon degeneratoin
Geisler, S., Huang, S.X., Strickland, A., Doan, R.A., Summers, D.W., Mao, X., Park, J., DiAntonio, A. and Milbrandt, J. (2019) Gene therapy targeting SARM1 blocks pathological axon degeneration in mice J. Exp. Med., 216, 294–303

Blood-brain barrier
Albright, B.H., Simon, K.E., Pillai, M., Devlin, G.W. and Asokan, A. (2019) Modulation of sialic acid dependence influences the central nervous system transduction profile of adeno-associated viruses J. Virol., 93, e00332-19

Hordeaux, J., Yuan, Y., Clark, P.M., Wang, Q., Martino, R.A., Sims, J.J., Bell, P., Raymond, A., Stanford, W.L. and Wilson, J.M. (2019) The GPI-linked protein LY6A drives AAV-PHP.B transport across the bloodbrain barrier Mol. Ther., 27, 912-921

Huang, Q., Chan, K.Y., Tobey, I.G., Chan, Y.A., Poterba, T., Boutros, C.L., Balazs, A.B., Daneman, R. et al (2019) Delivering genes across the blood-brain barrier: LY6A, a novel cellular receptor for AAV-PHP.B capsids PLoS One, 14: e0225206

Brain inflammation
Kano, S-i., Choi, E.Y., Dohi, E., Agarwal, S., Chang, D.J., Wilson, A.M., Lo, B.D., Rose, I.V.L., Gonzalez, S., Imai, T. and Sawa, A. (2019) Glutathione S-transferases promote proinflammatory astrocyte-microglia communication during brain inflammation Sci. Signal. 12, eaar2124

Calcium channel
Van Loo, K.M.J., Rummel, C.K., Pitsch, J., Müller, J.A., Bikbaev, A.F., Martinez-Chavez, E., Blaess, S., Dietrich, D., Heine, M., Becker, A.J. and Schoch, S. (2019) Calcium channel subunit α2δ4 is regulated by early growth response 1 and facilitates epileptogenesis J. Neurosci., 39, 3175–3187

Capsids
Herrmann, A-K., Große, S., Börner, K., Krämer, C., Wiedtke, E., Gunkel, M. and Grimm, D. (2019) Impact of the assembly-activating protein on molecular evolution of synthetic adeno-associated virus capsids Hum. Gene Ther., 30, 21-35

Cerebellar Purkinje cells
Hosio, N., Shibasaki, K., Hosono, M., Konno, A., Shinoda, Y., Kiyonari, H., Inoue, K., Muramatsu, S-I, Ishizaki, Y. et al (2019) Deletion of class II ADP-ribosylation factors in mice causes tremor by the Nav1.6 loss in cerebellar Purkinje cell axon initial segments J. Neurosci., 39, 6339–6353

Schlegel, J., Hoffmann, J., Röll, D., Müller, B., Günther, S., Zhang, W., Janise, A., Vössing, C., Fühler, B. et al (2019) Toward genome editing in X-linked RP- development of a mouse model with specific treatment relevant features Translat. Res., 203, 57-72

CNS distribution/expression (species comparison)
Hordeaux, J., Hinderer, C., Buza, E.L., Louboutin, J-P., Jahan, T., Bell, P., Chichester, J.A., Tarantal, A.F. and Wilson, J.M. (2019) Safe and sustained expression of human iduronidase after intrathecal administration of adeno-associated virus serotype 9 in infant rhesus monkeys Hum. Gene Ther., 30. 957-966

Liguore, W.A., Domire, J.S., Button, D., Wang, Y., Dufour, B,D., Srinivasan, S. and McBride, J.L. (2019) AAV-PHP.B administration results in a differential pattern of CNS biodistribution in non-human primates compared with mice Mol. Ther., 27, 2018-2037

Cochlea delivery/optogenetics
Dieter, A., Duque-Afonso, C-J., Rankovic, V., Jeschke, M. and Moser, T. (2019) Near physiological spectral selectivity of cochlear optogenetics Nature Comm., 10: 1962
Tan, F., Chu, C., Qi, J., Li, W., You, D., Li, K., Chen. X., Zhao, W., Chen, C., Liu, X. et al (2019) AAV-ie enables safe and efficient gene transfer to inner ear cells Nat. Comm., 10: 3733

Corticostriatal flow
Hwang, E.J., Link, T.D., Hu, Y.Y., Lu, S., Wang, E. H-J., Lilascharoen, V., Aronson, S., O’Neil, K., Lim, B.K. and Komiyama, T. (2019) Corticostriatal flow of action selection bias Neuron 104, 1126–1140

Dopaminergic neurons
Mahajani, S., Raina, A., Fokken, C., Kügler, S. and Bähr, M. (2019) Homogenous generation of dopaminergic neurons from multiple hiPSC lines by transient expression of transcription factors Cell Death Dis., 10: 898

Dorsal root ganglia
Bloom, D.C., Watson, Z.L. and Neumann, D.M. (2019) Peripheral AAV injection for retrograde transduction of dorsal root and trigeminal ganglia In Adeno-Associated Virus Vectors: Design and Delivery, Methods in Mol. Biol., vol. 1950 (ed. Castle, M.J.), Springer Science+Business Media LLC New York, pp 237-247

Epileptic encephalopathy
Colasante, G., Lignani, G., Brusco, S., Di Berardino, C., Carpenter, J., Giannelli, S., Valassina, N., Bido, S., Ricci, R. et al (2020) dCas9-based Scn1a gene activation restores inhibitory interneuron excitability and attenuates seizures in Dravet syndrome mice Mol. Ther., 28, 235-253

Frontotemporal dementia
Chew, J., Cook, C., Gendron, T.F., Jansen-West, K., del Rosso, G., Daughrity, L.M., Castanedes-Casey, M., Kurti, A. Stankowski, J.N. (2019) Aberrant deposition of stress granule resident proteins linked to C9orf72-associated TDP-43 proteinopathy Mol. Neurodegen., 14: 9

Zhang, Y-J., Guo, L., Gonzales, P.K., Gendron, T.F., Wu, Y., Jansen-West, K., O’Raw, A.D., Pickles, S.R., Prudencio, M., Carlomagno, Y. et al (2019) Heterochromatin anomalies and double-stranded RNA accumulation underlie C9orf72 poly(PR) toxicity Science 363, eaav2606

Genome editing
Rogers, G.L., Chen, H-Y., Morales, H. and Cannon, P.M. (2019) Homologous recombination-based genome editing by Clade F AAVs is inefficient in the absence of a targeted DNA break Mol. Ther., 27, 1726-1736

Glial cell targeting
Jüttner, J., Szabo, A., Gross-Scherf, B., Morikawa, R.K., Rompani, S.B., Hantz, P., Szikra, T., Esposti, F., Cowan, C.S. et al (2019) Targeting neuronal and glial cell types with synthetic promoter AAVs in mice, nonhuman primates and humans Nat. Neurosci., 22, 1345–1356

Glial tauopathy
Chung, D-e.Chloe, Carlomagno, Y., Cook, C.N., Jansen-West, K., Daughrity, L., Lewis-Tuffin, L.J., Castanedes-Casey, M., DeTure, M., Dickson, D.W. and Petrucelli, L. (2019) Tau exhibits unique seeding properties in globular glial tauopathy Acta Neuropathol. Comm., 7: 36

Hippocampus/hippocampal neurons
Colon-Perez, L.M., Ibanez, K.R., Suarez, M., Torroella, K., Acuna, K., Ofori, E., Levites, Y., Vaillancourt, D.E., Golde, T.E. et al (2019) Neurite orientation dispersion and density imaging reveals white matter and hippocampal microstructure changes produced by Interleukin-6 in the TgCRND8 mouse model of amyloidosis NeuroImage, 202: 116138

Forner, S., Martini, A.C., Prieto, G.A., Dang, C.T., Rodriguez-Ortiz, C.J., Reyes-Ruiz, J.M., Trujillo-Estrada, L., da Cunha, C., Andrews, E.J. et al (2019) Intra- and extracellular β-amyloid overexpression via adenoassociated virus-mediated gene transfer impairs memoryand synaptic plasticity in the hippocampus Sci. Rep., 9: 15936

Günther, A., Luczak, V., Gruteser, N., Abel, T. and Baumann, A. (2019) HCN4 knockdown in dorsal hippocampus promotes anxiety-like behavior in mice Genes Brain Behav., 18: e12550

Vullhorst, D. and Buonanno, A. (2019) NMDA receptors regulate neuregulin 2 binding to ER-PM junctions and ectodomain release Mol. Neurobiol., 56, 8345–8363

Wang, J., Cui, Y., Yu, Z., Wang, W., Cheng, X., Ji, W., Guo, S., Zhou, Q., Wu, N., Chen, Y. et al (2019) Brain endothelial cells maintain lactate homeostasis and control adult hippocampal neurogenesis Cell Stem Cell, 25, 754–767

Huntington’s disease
Ekman, F.K., Ojala, D.S., Adil, M.M., Lopez, P.A., Schaffer, D.V. and Gaj, T. (2019) CRISPR-Cas9-mediated genome editing increases lifespan and improves motor deficits in a Huntington’s disease mouse model Mol. Ther: Nucleic Acids, 17, 829-839

Hypothalamus
McMurphy, T., Huang, W., Liu, X., Siu, J.J., Queen, N.J., Xiao, R. and Cao, L. (2019) Hypothalamic gene transfer of BDNF promotes healthy aging in mice Aging Cell, 18: e12846

Quarta, C., Fisette, A., Xu, Y., Colldén, G., Legutko, B., Tseng, Y-T., Reim, A., Wierer, M., De Rosa, M.C. et al (2019) Functional identity of hypothalamic melanocortin neurons depends on Tbx3 Nat. Metab., 1, 222–235

Interneuronal delivery
Hartmann, J., Thalheimer, F.B., Höpfner, F., Kerzel, T., Khodosevich, K., García-González, D., Monyer, H., Diester, I. et al (2019) GluA4-targeted AAV vectors deliver genes selectively to interneurons while relying on the AAV receptor for entry Mol. Ther. Meth. Clin. Dev., 14, 252-260

Levodopa-induced dyskinesias
Sellnow, R.C., Newman, J.H., Chambers, N., West, A.R., Steece-Collier, K., Sandoval, I.M., Benskey, M.J., Bishop, C. and Manfredsson, F.P. (2019) Regulation of dopamine neurotransmission from serotonergic neurons by ectopic expression of the dopamine D2 autoreceptor blocks levodopa-induced dyskinesia Acta Neuropathol. Comm., 7: 8

Lower motor neuron transduction
Chen, Z., Fan, G., Li, A., Yuan, J. and Xu, T. (2020) rAAV2-Retro enables extensive and high-efficient transduction of lower motor neurons following intramuscular injection Mol. Ther: Meth. Clin, Devel., 17, 21-33

Memory
Awasthi, A., Ramachandran, B., Ahmed, S., Benito, E., Shinoda, Y., Nitzan, N., Heukamp, A., Rannio, S. et al (2019) Synaptotagmin-3 drives AMPA receptor endocytosis, depression of synapse strength, and forgetting Science 363, eaav:1483

Huang, T-N., Hsu, T-T., Lin, M-H., Chuang, H-C., Hu, H-T., Sun, C-P., Tao, M-H., Lin, J.Y. and Hsueh, Y-P. (2019) Interhemispheric connectivity potentiates the basolateral amygdalae and regulates social interaction and memory Cell Reports 29, 34–48

Lee, J., Leeb, H-R., Kim, J-I., Baek, J., Jang, E-H., Lee, J., Kim, M., Lee, R.U. et al (2020) Transient cAMP elevation during systems consolidation enhances remote contextual fear memory Neurobiol. Learn. Mem., 169:107171

Zhou, M., Liu, Z., Melin, M.D., Ng, Y.H., Xu, W. and Südhof, T.C. (2018) A central amygdala to zona incerta projection is required for acquisition and remote recall of conditioned fear memory Nat. Neurosci., 21, 1515–1519

Neurodegenerative diseases
Aguareles, J., Paraíso-Luna, J., Palomares, B., Bajo-Grañeras, R., Navarrete, C., Ruiz-Calvo, A., GarcíaRincón, D., García-Taboada, E., Guzmán, M. et al (2019) Oral administration of the cannabigerol derivative VCE-003.2 promotes subventricular zone neurogenesis and protects against mutant huntingtin-induced neurodegeneration Translat, Neurodegen., 8: 9

Neuronal cell targeting
Jüttner, J., Szabo, A., Gross-Scherf, B., Morikawa, R.K., Rompani, S.B., Hantz, P., Szikra, T., Esposti, F., Cowan, C.S. et al (2019) Targeting neuronal and glial cell types with synthetic promoter AAVs in mice, nonhuman primates and humans Nat. Neurosci., 22, 1345–1356

Neuronal ceroid lipofuscinoses
Mitchell, N.L., Russell, K.N., Wellby, M.P., Wicky, H.E., Schoderboeck, L., Barrell, G.K., Melzer, T.R., Gray, S.J., Hughes, S.M. and Palmer, D.N. (2018) Longitudinal in vivo monitoring of the CNS demonstrates the efficacy of gene therapy in a sheep model of CLN5 batten disease Mol. Ther., 26, 2366-2378

Neuronal homeostasis
Brekk, O.R., Makridakis, M., Mavroeidi, P., Vlahou, A. Xilouri, M. and Stefanis, L. (2019) Impairment of chaperone-mediated autophagy affects neuronal homeostasis through altered expression of DJ-1 and CRMP-2 proteins Mol. Cell. Neurosci., 95, 1–12

Neuronal toxicity
Yang, S., Li, S. and Li, X-J. (2018) Shortening the half-life of Cas9 maintains its gene editing ability and reduces neuronal toxicity Cell Rep., 25, 2653–2659

Neuropathic pain
Yu, H., Shin, S.M., Xiang, H., Chao, D., Cai, Y., Xu, H., Khanna, R., Pan, B. and Hogan, Q.H. (2019) AAVencoded CaV2.2 peptide aptamer CBD3A6K for primary sensory neuron-targeted treatment of established neuropathic pain Gene Ther., 26, 308–323

Neurotransmission
Liu, Q., Sinnen, B.L., Boxer, E.E., Schneider, M.W., Grybko, M.J., Buchta, W.C., Gibson, E.S., Wysoczynski, C.L., Ford, C.P. et al (2019) A photoactivatable botulinum neurotoxin for inducible control of neurotransmission Neuron 101, 863–875

Neurotrophic factor
Osborne, A., Khatib, T.Z., Songra, L., Barber, A.C., Hall, K., Kong, G.Y.X., Widdowson, P.S. and Martin, K.R. (2018) Neuroprotection of retinal ganglion cells by a novel gene therapy construct that achieves sustained enhancement of brain-derived neurotrophic factor/tropomyosinrelated kinase receptor-B signaling Cell Death Dis., 9: 1007

Niemann–Pick type C1 disease
Hughes, M.P., Smith, D.A., Morris, L., Fletcher, C., Colaco, A., Huebecker, M., Tordo, J., Palomar, N., Massaro, G. (2018) AAV9 intracerebroventricular gene therapy improves lifespan, locomotor function and pathology in a mouse model of Niemann–Pick type C1 disease Hum. Mol. Genet., 27, 3079–3098

Nucleus accumbens
Zhang, T., Deyama, S., Domoto, M., Wada, S., Yanagida, J., Sasase, H., Hinoi, E., Nishitani, N., Nagayasu, K., Kaneko, S. and Kaneda, K. (2018) Activation of GABAergic neurons in the nucleus accumbens mediates the expression of cocaine-associated memory Biol. Pharm. Bull., 41, 1084–1088

Nucleus incertus (relaxin-3 neurons)
Wykes, A., Ma, S., Bathgate, R.A.D., and Gundlach, A.L. (2020) Targeted viral vector transduction of relaxin3 neurons in the rat nucleus incertus using a novel cell-type specific promoter IBRO Rep., 8, 1–10

Parkinson’s disease
Carballo-Carbajal, I., Laguna, A., Romero-Giménez, J., Cuadros, T., Bové, J., Martinez-Vicente, M., Parent, A., Gonzalez-Sepulveda, M. et al (2019) Brain tyrosinase overexpression implicates age-dependent neuromelanin production in Parkinson’s disease pathogenesis Nat. Comm., 10: 973

George, S., Rey, N.L., Tyson, T., Esquibel, C., Meyerdirk, L., Schulz, E., Pierce, S., Burmeister, A.R. et al (2019) Microglia affect α-synuclein cell-to-cell transfer in a mouse model of Parkinson’s disease Mol. Neurodegen., 14: 34

Li, M., Xu, H., Chen, G., Sun, S., Wang, Q., Liu, B., Wu, X., Zhou, L., Chai, Z., Sun, X. et al (2019) Impaired D2 receptor-dependent dopaminergic transmission in prefrontal cortex of awake mouse model of Parkinson’s disease Brain, 142, 3099–3115

Lillethorup, T.P., Glud, A.N., Landeck, N., Olsen Alstrup, A.K., Jakobsen, S., Vang, K., Doudet, D.J., Brooks, D.J., Kirik, D. et al (2018) In vivo quantification of glial activation in minipigs overexpressing human αsynuclein Synapse, 72: e22060

Mahajani, S., Raina, A., Fokken, C., Kügler, S. and Bähr, M. (2019) Homogenous generation of dopaminergic neurons from multiple hiPSC lines by transient expression of transcription factors Cell Death Dis., 10: 898

Park, J-H., Burgess, J.D., Faroqi, A.H., DeMeo, N.N., Fiesel, F.C., Springer, W., Delenclos, M., and McLean, P.J. (2020) Alpha-synuclein-induced mitochondrial dysfunction is mediated via a sirtuin 3-dependent pathway Mol. Neurodegen., 15: 5

Sargent, D., Bétemps, D., Drouyer, M., Verchere, J., Gaillard, D., Arsac, J-N., Lakhdar, L., Salvetti, A. and Baron, T. (2018) Investigating the neuroprotective effect of AAV-mediated β-synuclein overexpression in a transgenic model of synucleinopathy Sci. Rep., 8: 17563

Sellnow, R.C., Newman, J.H., Chambers, N., West, A.R., Steece-Collier, K., Sandoval, I.M., Benskey, M.J., Bishop, C. and Manfredsson, F.P. (2019) Regulation of dopamine neurotransmission from serotonergic neurons by ectopic expression of the dopamine D2 autoreceptor blocks levodopa-induced dyskinesia Acta Neuropathol. Comm., 7: 8

Steece-Collier, K., Stancati, J.A., Collier, N.J., Sandoval, I.M., Mercado, N.M., Sortwell, C.E., Collier, T.J. and Manfredsson, F.P. (2019) Genetic silencing of striatal CaV1.3 prevents and ameliorates levodopa dyskinesia Mov. Disord., 34, 697-707

Von Hövel, F.F., Rumpel, R., Ratzka, A., Schreiner, D. and Grothe, C. (2019) AAV2/DJ-mediated alphasynuclein overexpression in the rat substantia nigra as early stage model of Parkinson’s disease Cell Tissue Res., 378, 1–14

Phenylketonuria
Richards, D.Y., Winn, S.R., Dudley, S., Nygaard, S., Mighell, T.L., Grompe, M. and Harding, C.O. (2020) AAV-Mediated CRISPR/Cas9 gene editing in murine phenylketonuria Mol. Ther: Meth. Clin, Devel., 17, 234-245

SHP2-ERK signaling network
Ryu, H-H., Kim, TH., Kim, J-W., Kang, M., Park, P., Kim, Y.G., Kim, H., Ha, J. et al (2019) Excitatory neuron–specific SHP2-ERK signaling network regulates synaptic plasticity and memory Sci. Signal. 12, eaau5755

Somatosensory neurons
Sharma, N., Flaherty, K., Lezgiyeva, K., Wagner, D.E., Klein, A.M. and Ginty, D.D. (2020) The emergence of transcriptional identity in somatosensory neurons Nature, 392, 392-398

Spinal cord injury
Nakanishi, T., Fujita, Y. and Yamashita, T. (2019) Neuropilin-1-mediated pruning of corticospinal tract fibers is required for motor recovery after spinal cord injury Cell Death Dis., 10: 67

Spinocerebellar ataxia
Watanave, M., Hoshino, C., Konno, A., Fukuzaki, Y., Matsuzaki, Y., Ishitani, T. and Hirai, H. (2019) Pharmacological enhancement of retinoid-related orphan receptor α function mitigates spinocerebellar ataxia type 3 pathology Neurobiol. Dis., 121, 263–273

Stria terminalis
Harris, N.A., Isaac, A.T., Günther, A., Merkel, K., Melchior, J., Xu, M., Eguakun, E., Perez, R., Nabit, B.P. et al (2018) Dorsal BNST α2A-adrenergic receptors produce HCN-dependent excitatory actions that initiate anxiogenic behaviors J. Neurosci., 38, 8922–8942

Synaptic function maturation/synaptic proteins
Favaro, P.D., Huang, X., Hosang, L., Stodieck, S., Cui, L., Liu, Y., Engelhardt, K.A., Schmitz, F., Dong, Y. Löwel, S. and Schlüter, O.M. (2018) An opposing function of paralogs in balancing developmental synapse maturation PLoS Biol 16: e2006838

Patzke, C., Brockmann, M.M., Dai, J., Acuna, C., Rosenmund, C. and Südhof, T.C. (2019) Neuromodulator signaling bidirectionally controls vesicle numbers in human synapses Cell, 179, 498–513

Spence, E.F., Dube, S., Uezu, A., Locke, M., Soderblom, E.J. and Soderling, S.H. (2019) In vivo proximity proteomics of nascent synapses reveals a novel regulator of cytoskeleton-mediated synaptic maturation Nat. Comm., 10: 386

Uezu, A. and Soderling, S. (2019) Identifying synaptic proteins by in vivo BioID from mouse brain In Proximity Labeling: Methods and Protocols, Methods in Mol. Biol., vol. 2008 (ed. Sunbul, M. and Jäschke, A.) Springer Science+Business Media, LLC, New York, pp 111-126

Taste receptors
Crosson, S.M., Marques, A., Dib, P., Dotson, C.D., Munger, S.D. and Zolotukhin, S. (2019) Taste receptor cells in mice express receptors for the hormone adiponectin Chem. Senses, 44, 409–422

Trigeminl ganglia
Bloom, D.C., Watson, Z.L. and Neumann, D.M. (2019) Peripheral AAV injection for retrograde transduction of dorsal root and trigeminal ganglia In Adeno-Associated Virus Vectors: Design and Delivery, Methods in Mol. Biol., vol. 1950 (ed. Castle, M.J.), Springer Science+Business Media LLC New York, pp 237-247

Neutralizing epitopes

Giles, A.R., Govindasamy, L., Somanathan, S. and Wilson, J.M. (2018) Mapping an adeno-associated virus 9- specific neutralizing epitope to develop next-generation gene delivery vectors J. Virol. 92: e01011-18

Nuclear targeting of viral capsids

Wang, H., Zhang, K., Lin, C., Zhou, J., Jin, Y., Dong, W., Gu, J., Zhou, J. (2019) Conformational changes and nuclear entry of porcine circovirus without disassembly J. Virol., 93: e00824-19

Obesity

Pradas-Juni, M., Hansmeier, N.R., Link, J.C., Schmidt, E., Larsen, B.D., Klemm, P., Meola, N. et al (2020) A MAFG-lncRNA axis links systemic nutrient abundance to hepatic glucose metabolism Nat. Comm., 11: 644

Wolff, G., Taranko, A.E., Meln, I., Weinmann, J., Sijmonsma, T., Lerch, S., Heide, D., Billeter, A.T., Tews, D., Krunic, D. et al (2019) Diet-dependent function of the extracellular matrix proteoglycan Lumican in obesity and glucose homeostasis Mol. Metab., 19, 97-106

Optical

Hughes, C.P., O’Flynn, N.M.J., Gatherer, M., McClements, M.E., Scott, J.A., MacLaren, R.E., Goverdhan, S., Glennie, M.J. and Lotery, A.J. (2019) AAV2/8 anti-angiogenic gene therapy using single-chain antibodies inhibits murine choroidal neovascularization Mol. Ther: Meth. Clin. Devel., 13 86-98

Xiong, W., Wu, D.M., Xu, Y., Wang, S.K., Chung, M.J., Ji. X., Rana, P., Zhao, S.R., Mai, S. and Cepkoc, C.L. (2019) AAV cis-regulatory sequences are correlated with ocular toxicity Proc. Natl. Acad. Sci. USA 116, 5785–5794

Optogenetics

Bedbrook, C.N., Yang, K.K., Robinson, J.E., Mackey, E.D., Gradinaru, V. and Arnold, F.H. (2019) Machine learning-guided channelrhodopsin engineering enables minimally invasive optogenetics Nat. Meth., 16, 1176–1184

Bernal Sierra, Y.A., Rost, B.R., Pofahl, M., Fernandes, A.M., Kopton, R.A., Moser, S., Holtkamp, D., Masala, N. et al (2018) Potassium channel-based optogenetic silencing Nat. Comm., 9: 4611

Garita-Hernandez, M., Lampič, M., Chaffiol, A., Guibbal, L., Routet, F., Santos-Ferreira, T., Gasparini, S., Borsch, O., Gagliardi, G. et al (2019) Restoration of visual function by transplantation of optogenetically engineered photoreceptors Nat. Comm., 10: 4524

Jung, H., Kim, S-W., Kim, M., Hong, J., Yu, D., Kim, J.H., Lee, Y., Kim, S., Woo, D. et al (2109) Noninvasive optical activation of Flp recombinase for genetic manipulation in deep mouse brain regions Nat. Comm., 10:314

Keppeler, D., Merino, R.M., Lopez de la Morena, D., Bali, B., Huet, A.T., Gehrt, A., Wrobel, C., Subramanian, S., Dombrowski, T. et al (2018) Ultrafast optogenetic stimulation of the auditory pathway by targeting-optimized Chronos EMBO J., 37: e99649

Yamada, M., Suzuki, Y., Nagasaki, S.C., Okuno, H. and Imayoshi, I. (2018) Light control of the Tet gene expression system in mammalian cells Cell Rep., 25, 487–500

Ovarian cancer (see also “Tumour activity”)

Tonga, J.G., Evans, A.C., Ho, M.L., Guenther, C.M., Brun, M.J., Judd, J., Wu, E. and Suh, J. (2019) Reducing off target viral delivery in ovarian cancer gene therapy using a protease-activated AAV2 vector platform J.

Control. Release, 307, 292–301
Pancreatic cancer (see also “Tumour activity”)

Ideno, N., Yamaguchi, H., Okumura, T., Huang, J., Brun, M.J., Ho, M.L., Suh, J., Gupta, S., Maitra, A. and Ghosh, B. (2019) A pipeline for rapidly generating genetically engineered mouse models of pancreatic cancer using in vivo CRISPR-Cas9-mediated somatic recombination Lab. Invest., 99, 1233–1244

Liu, S-H., Hong, Y., Markowiak, S., Sanchez, R., Creeden, J., Nemunaitis, J., Kalinoski, A., Willey, J., Erhardt, P. et al (2019) BIRC5 is a target for molecular imaging and detection of human pancreatic cancer Cancer Lett., 457, 10–19

Pompe disease

Keeler, A.M., Zieger, M., Todeasa, S.H., McCall, A.L., Gifford, J.C., Birsak, S., Choudhury, S.R., Byrne, B.J., Sena-Esteves, M. and ElMallah, M.K. (2019) Systemic delivery of AAVB1-GAA clears glycogen and prolongs survival in a mouse model of Pompe disease Hum. Gene Ther., 30, 57-68

Lim, J-A., Yi, H., Gao, F., Raben, N., Kishnani, P.S. and Sun, B. (2019) Intravenous injection of an AAVPHP.B vector encoding human acid a-glucosidase rescues both muscle and CNS defects in murine Pompe disease Mol. Ther: Meth. Clin. Devel., 12, 233-245

Progenitor cells

Cromer, M.K., Vaidyanathan, S., Ryan, D.E., Curry, B., Lucas, A.B., Camarena, J., Kaushik, M., Hay, S.R., et al (2018) Global transcriptional response to CRISPR/Cas9-AAV6-based genome editing in CD34+ hematopoietic stem and progenitor cells Mol. Ther., 26, 2431-2442

Tran, N.T., Sommermann, T., Graf, R., Trombke, J., Pempe, J., Petsch, K., K€uhn, R., Rajewsky, K. and Chu, V.T. (2019) Efficient CRISPR/Cas9-mediated gene knockin in mouse hematopoietic stem and progenitor cells Cell Reports 28, 3510- 3522

Provector locking

Chen, M.Y., Robinson, T.M. and Suh, J. (2019) Longer inactivating sequence in peptide lock improves performance of synthetic protease-activatable adeno-associated virus ACS Synth. Biol., 8, 91−98

Retinal cell interactions/retinal disorders/visual cortex etc

Boggio, E.M., Ehlert, E.M., Lupori, L., Moloney, E.B., De Winter, F., Vander Kooi, C.W., Baroncelli, L. Mecollari, V. et al (2019) Inhibition of semaphorin3A promotes ocular dominance plasticity in the adult rat visual cortex Mol. Neurobiol., 56, 5987–5997

Deng, S. and Oka, K. (2020) Adeno-associated virus as gene delivery vehicle into the retina In Retinal Development: Methods and Protocols, in Methods in Mol. Biol., vol. 2092 (Mao, C-A. ed), Springer Science+Business Media LLC New York, pp 77-90

Dias, M.S., Araujo, V.G., Vasconcelos, T., Li, Q., Hauswirth, W.W., Linden, R. and Petrs-Silva, H. (2019) Retina transduction by rAAV2 after intravitreal injection: comparison between mouse and rat Gene Ther., 26, 479–490

Falk, N., Kessler, K., Schramm, S-F., Boldt, K., Becirovic, E., Michalakis, S., Regus-Leidig, H., Noegel, A.A. et al (2018) Functional analyses of Pericentrin and Syne-2 interaction in ciliogenesis J. Cell Sci., 131: jcs218487

Hamon, A., García-García, D., Ail, D., Bitard, J., Chesneau, A., Dalkara, D., Locker, M., Roger, J.E. and Perron, M. (2019) Linking YAP to Müller glia quiescence exit in the degenerative retina Cell Rep., 27, 1712–1725

Jo, D.H., Koo, T., Cho, C.S., Kim, J.H., Kim, J-S. and Kim, J.H. (2019) Long-term effects of in vivo genome editing in the mouse retina using Campylobacter jejuni Cas9 expressed via adeno-associated virus Mol. Ther., 27, 130-136

Khabou, H., Cordeau, C., Pacot, L., Fisson, S. and Dalkara, D. (2018) Dosage thresholds and influence of transgene cassette in adeno-associated virus–related toxicity Human Gene Ther., 29, 1235-1241

Maeder, M.L., Stefanidakis, M., Wilson, C,J., Baral, R., Barrera, L.A., Bounoutas, G.S., Bumcrot, D., Chao, H., Ciulla, D.M. et al (2019) Development of a gene-editing approach to restore vision loss in Leber congenital amaurosis type 10 Nat. Med., 25, 229–233

McClements, M.E., Barnard, A.R., Singh, M.S., Issa, P.C., Jiang, Z., Radu, R.A. and MacLaren, R.E. (2019) An AAV dual vector strategy ameliorates the Stargardt phenotype in adult Abca4-/- mice Hum. Gene Ther. Meth., 30, 590-600

McCullough, K.T., Boye, S.L., Fajardo, D., Calabro, K., Peterson, J.J., Strang, C.E., Chakraborty, D., Gloskowski, S., Haskett, S. et al (2019) Somatic gene editing of GUCY2D by AAV-CRISPR/Cas9 alters retinal structure and function in mouse and macaque Hum. Gene Ther., 30, 571-589

Osborne, A., Khatib, T.Z., Songra, L., Barber, A.C., Hall, K., Kong, G.Y.X., Widdowson, P.S. and Martin, K.R. (2018) Neuroprotection of retinal ganglion cells by a novel gene therapy construct that achieves sustained enhancement of brain-derived neurotrophic factor/tropomyosinrelated kinase receptor-B signaling Cell Death Dis., 9: 1007

Ribic, A., Crair, M.C. and Biederer, T. (2019) Synapse-selective control of cortical maturation and plasticity by parvalbumin-autonomous action of SynCAM 1 Cell Reports 26, 381–393

Schlegel, J., Hoffmann, J., Röll, D., Müller, B., Günther, S., Zhang, W., Janise, A., Vössing, C., Fühler, B. et al (2019) Toward genome editing in X-linked RP- development of a mouse model with specific treatment relevant features Translat. Res., 203, 57-72

Shen, J., Xiao, R., Bair, J., Wang, F., Vandenberghe, L.H., Dartt, D. Baranov, P. and Ng, Y.S.E. (2018) Novel engineered, membrane-localized variants of vascular endothelial growth factor (VEGF) protect retinal ganglion cells: a proof-of-concept study Cell Death Dis., 9: 1018

Song, L., Llanga, T., Conatser, L.M., Zaric, V., Gilger, B.C., Hirsch, M.L. (2018) Serotype survey of AAV gene delivery via subconjunctival injection in mice Gene Ther., 25, 402–414

Wang, S-B., Xu, T., Peng, S., Singh, D., Ghiassi-Nejad, M., Adelman, R.A., and Rizzolo, L.J. (2019) Diseaseassociated mutations of claudin-19 disrupt retinal neurogenesis and visual function Commun. Biol., 2: 113

Wood, S.R., McClements, M.E., Martinez-Fernandez de la Camara, C., Patrıcio, M.I., Uggenti, C., Sekaran, S., Barnard, A.R., Manson, F.D. and MacLaren, R.E. (2019) A quantitative chloride channel conductance assay for efficacy testing of AAV.BEST1 (2019) Human Gene Therapy Meth., 30, 44-52

gRNAs

Fakhiri, J., Nickl, M. and Grimm, D. (2019) Rapid and simple screening of CRISPR guide RNAs (gRNAs) in cultured cells using adeno-associated viral (AAV) vectors In CRISPR Gene Editing: Methods and Protocols, Methods in Mol. Biol., vol. 1961 (ed. Luo, Y.), Springer Science+Business Media LLC New York, pp 111-126

RNA guided adenosine deaminases

Katrekar, D., Chen, G., Meluzzi, D., Ganesh, A., Worlikar, A., Shih, Y-R., Varghese, S. and Mali, P. (2019) In vivo RNA editing of point mutations via RNA guided adenosine deaminases Nat. Meth., 16, 239–242

Serotype identification

Rieser, R., Penaud-Budloo, M., Bouzelha, M., Rossi, A., Menzen, T., Biel, M., Büning, H. Ayuso, E., Winter, G. and Michalakis, S. (2020) Intrinsic differential scanning fluorimetry for fast and easy identification of adenoassociated virus serotypes J. Pharma. Sci., 109, 854-862

Sickle cell disease

Pattabhi, S., Lotti, S.N., Berger, M.P., Singh, S., Lux, C.T., Jacoby, K., Lee, C., Negre, O., Scharenberg, A.M. and Rawlings, D.J. (2019) In vivo outcome of homology-directed repair at the HBB gene in HSC using alternative donor template delivery methods Mol. Ther. Nucl. Acids, 17, 277-288

Skeletal/skeletal muscle

Ferrán Pérez, B., Kimura, T., Tsukahara, Y., Ido, Y., Pimentel. D., Adachi, T., Bachschmid, M. and Matsui, R. (2018) Use of adeno-associated viruses to inhibit Glutaredoxin-1 in mouse skeletal muscle Free Radical Biol. Med., 128, S21–S46

Franck, A., Lainéa, J., Moulay, G., Lemerle, E., Trichet, M., Gentil, C., Benkhelifa-Ziyyat, S., Lacène, E., Bui, M.T., Brochier, G. et al (2019) Clathrin plaques and associated actin anchor intermediate filaments in skeletal muscle Mol. Biol. Cell, 30, 579-590

Lee, L.R., Peacock, L., Lisowski, L., Little, D.G., Munns, C.F. and Schindeler, A. (2019) Targeting adenoassociated airus aectors for local delivery to fractures and systemic delivery to the skeleton Mol. Ther: Meth. Clin. Devel., 15, 101-111

Zhu, H., Wang, T., Lye, R.J., French, B.A. and Annex, B.H. (2018) Neuraminidase‐mediated desialylation augments AAV9‐mediated gene expression in skeletal muscle J. Gene. Med., 20: e3049

Zygmunt, D.A., Xu, R., Jia, Y., Ashbrook, A., Menke, C., Shao, G., Yoon, J.H., Hamilton, S. et al (2019) rAAVrh74.MCK.GALGT2 demonstrates safety and widespread muscle glycosylation after intravenous delivery in C57BL/6J mice Mol. Ther. Meth. Clin, Devel., 15, 305-319

α-Synuclein aggregates

Elfarrash, S., Jensen, N.M., Ferreira, N., Betzer, C., Thevathasan, J.V., Diekmann, R., Adel, M., Omar, N.M., Boraie, M.Z. et al (2019) Organotypic slice culture model demonstrates inter-neuronal spreading of alphasynuclein aggregates Acta Neuropathologica Comm., 7: 213

Target spcificity

Eichhoff, A. M., Börner, K., Albrecht, B., Schäfer, W., Baum, N., Haag, F., Körbelin, J., Trepel, M., Braren, I. et al (2019) Nanobody-enhanced targeting of AAV gene therapy vectors Mol. Ther: Meth. Clin. Devel., 15, 211-220

Tissue reconstruction

Zhou, K., Chen, H., Lin, J., Xu, H., Wu, H., Bao, G., Li, J., Deng, X. et al (2019) FGF21 augments autophagy in random-pattern skin flaps via AMPK signaling pathways and improves tissue survival Cell Death Dis., 10:872

Transplant vasculopathy

Remes, A., Franz, M., Mohr, F., Weber, A., Rapti, K., Jungmann, A., Karck, M., Hecker, M., Kallenbach, K. et al (2019) AAV-mediated expression of AP-1-neutralizing RNA decoy oligonucleotides attenuates transplant vasculopathy in mouse aortic allografts Mol. Ther: Meth. Clin. Devel., 15 246-256

Tuberous sclerosis

Prabhakar, S., Cheah, P.S., Zhang, X., Zinter, M., Gianatasio, M., Hudry, E., Bronson, R.T., Kwiatkowski, D.J. and Stemmer-Rachamimov, A. et al (2019) Long-term therapeutic efficacy of intravenous AAV-mediated hamartin replacement in mouse model of tuberous sclerosis type 1 Mol. Ther: Meth Clin. Dev., 15, 18-26

Tumour activity

Ballesteros-Briones, M.C., Martisova, E., Casales, E., Silva-Pilipich, N., Buñuales, M., Galindo, J., Mancheño, U., Gorraiz, M. et al (2019) Short-term local expression of a PD-L1 blocking antibody from a self-replicating RNA vector induces potent antitumor responses Mol. Ther., 27. 1892-1905

Bhere, D., Arghiani, N., Lechtich, E.R., Yao, Y., Alsaab, S., Bei, F., Matin, M.M. and Shah, K. (2020) Simultaneous downregulation of miR-21 and upregulation of miR-7 has anti-tumor efficacy Sci. Rep., 10: 1779

Krotova, K., Day, A. and Aslanidi, G. (2019) An engineered AAV6-based vaccine induces high cytolytic antitumor activity by directly targeting DCs and improves Ag presentation Mol. Ther. Oncolytics, 15, 166-177

Sun, M., Zheng, X., Meng, Q., Dong, Y., Zhang, G., Rao, D., An, X., Yang, Z., Pan, L. and Zhang, S. (2018) Interleukin-35 expression in non-small cell lung cancer is associated with tumor progression Cell Physiol. Biochem., 51, 1839-1851

Vaccine manufacture

Zhao, M., Vandersluis, M., Stout, J., Haupts, U., Sanders, M. and Jacquemart, R. (2019) Affinity chromatography for vaccines manufacturing: Finally ready for prime time? Vaccine, 37, 5491–5503

Vector production/purification/transduction efficiency

Chandler, L.C., Barnard, A.R., Caddy, S.L., Patrício, M.I., McClements, M.E., Fu, H., Rada, C., MacLaren, R.E. and Xue, K. (2019) Enhancement of adeno-associated virus-mediated gene therapy using hydroxychloroquine in murine and human tissues Mol. Ther. Meth. Clin. Devel., 14, 77-89

Chen, Y.H., Keiser, M.S. and Davidson, B.L. (2018) Adeno-associated virus production, purification, and titering In Current protocols in mouse biology, 8: e56

Wiley Online Library Fripont, S., Marneffe, C., Marino, M., Rincon, M.Y. and Holt, M.G. (2019) Production, purification, and quality control for adeno-associated virus based vectors J. Vis. Exp., 143: e58960

Kimura, T., Ferran, B., Tsukahara, Y., Shang, Q., Desai, S., Fedoce, A., Pimente, D.R., Luptak, I., Adachi, T., Ido, Y., Matsui, R. and Bachschmid, M.M. (2019) Production of adeno-associated virus vectors for in vitro and in vivo applications Sci. Rep., 9: 13601

Kondratova, L.L., Kondratov, O., Ragheb, R. and Zolotukhin, S. (2019) Removal of endotoxin from rAAV samples using a simple detergent-based protocol Mol. Ther: Meth. Clin. Devel., 15, 112-119

Lang, J.F., Toulmin, S.A., Brida, K.L., Eisenlohr, L.C. and Davidson, B.L. (2019) Standard screening methods underreport AAV-mediated transduction and gene editing Nat. Comm., 10: 3415

Lee, E.J., Robinson, T.M., Tabor, J.J., Mikos, A.G. and Suh, J. (2018) Reverse transduction can improve efficiency of AAV vectors in transduction‐resistant cells Biotech. Bioeng., 115, 3042–3049

Sandoval, I.M., Kuhn, N.M. and Manfredsson, F.P. (2019) Multimodal production of adeno-associated virus In Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Mol. Biol., 1937 (ed. Manfredsson F.P. and Benskey, M.J.), Springer Science+Business Media LLC New York, pp 101-124

Strobel, B., Zuckschwerdt, K., Zimmermann, G., Mayer, C., Eytner, R., Rechtsteiner, P., Kreuz, S. and Laml, T. (2019) Standardized, scalable, and timely flexible adeno-associated virus vector production using frozen high-density HEK-293 cell stocks and CELLdiscs Hum. Gene Ther. Meth., 30, 23-33

Wang, C., Mulagapati, S.H.R., Chen, Z., Du, J., Zhao, X., Xi, G., Chen, L., Linke, T., Gao, C. et al (2019) Developing an anion exchange chromatography assay for determining empty and full capsid contents in AAV6.2 Mol. Ther: Meth. Clin. Devel., 15 257-263

Wu, Y., Mei, T., Jiang, L., Han, Z., Dong, R., Yang, T. and Xu, F. (2019) Development of versatile and flexible  Sf9 packaging cell line-dependent OneBac system for large-scale recombinant adeno-associated virus production Hum. Gene Ther., 30. 172-183

Viral (virus-like) nanoparticles

Dashti, N.H. and Sainsbury, F. (2020) Virus-derived Nanoparticles In Protein Nanotechnology: Protocols, Instrumentation and Applications, in Methods in Mol. Biol., vol. 2073 (Gerrard , J.A. and Domigan, L.J. eds), Springer Science+Business Media LLC New York, pp 149-162

Váňová, J., Hejtmánková, A., Suchanová, J.Z., Sauerová, P., Forstová, J., Kalbáčová, M.H. and Španielová, H. (2020) Influence of cell-penetrating peptides on the activity and stability of virus-based nanoparticles Int. J. Pharmaceut., 576: 119008

OptiPrep™ Reference List RV02-2: 2nd edition, February 2020

OptiPrep™ Reference List RV03

GROUP III VIRUSES

• Viruses are listed alphabetically within the Baltimore scheme: Family, Genus and Species. Publications are listed alphabetically by first author and, where necessary, references are further divided according to research topic.
• Note a reference on “Taxonomy” is included at the end of p2.
• Multiple entries from the same first author are listed chronologically.
• For a detailed methodology of Group III viruses see OptiPrep™ Application Sheet V17. V06 is a methodological review of OptiPrep™technology

 

African horse sickness virus: see Sedoreovirinae

Birnavirus

Espirito Santo virus

Vancini, R., Paredes, A., Ribeiro, M., Blackburn, K., Ferreira, D., Kononchik, Jr. J.P., Hernandez, R. and Brown, D. (2012) Espirito Santo virus: a new Birnavirus that replicates in insect cells J. Virol., 86, 2390-2399

Orbivirus – Seadoreovirinae

African horse sickness virus
Dennis, S.J., O’Kennedy, M.M., Rutkowska, D., Tsekoa, T., Lourens, C.W., Hitzeroth, I.I., Meyers, A.E. and Rybicki, E.P. (2018) Safety and immunogenicity of plant‑produced African horse sickness virus‑like particles in horses Vet. Res. 49: 105

Dennis, S.J., Meyers, A.E., Guthrie, A.J., Hitzeroth, I.I. and Rybicki, E.P. (2018) Immunogenicity of plantproduced African horse sickness virus-like particles: implications for a novel vaccine Plant Biotech. J., 16, 442–450

Rutkowska, D.A., Mokoena, N.B., Tsekoa, T.L., Dibakwane, V.S. and O’Kennedy, M.M. (2019) Plantproduced chimeric virus-like particles – a new generation vaccine against African horse sickness BMC Veter. Res., 15: 432

Reoviridae

Banna virus
Jaafar, F.M., Attoui, H., Mertens, P.P.C., de Micco, P. and de Lamballerie, X. (2005) Structural organization of an encephalitic human isolate of Banna virus (genus Seadornavirus, family Reoviridae) J. Gen. Virol., 86, 1147-1157

Blue tongue virus
Brillault, L., Jutras, P.V., Dashti, N., Thuenemann, E.C., Morgan, G., Lomonossoff, G.P., Landsberg, M.J. and Sainsbury, F. (2017) Engineering recombinant virus-like nanoparticles from plants for cellular delivery ACS Nano,11, 3476−3484

Mokoena, N.B., Moetlhoa, B., Rutkowska. D.A., Mamputha, S., Dibakwane, V.S., Tsekoa, T.L. and O’Kennedy, M.M. (2019) Plant-produced Bluetongue chimaeric VLP vaccine candidates elicit serotype-specific immunity in sheep Vaccine, 37, 6068–6075

Thuenemann, E.C., Meyers, A.E., Verwey, J., Rybicki, E.P. and Lomonossoff, G.P. (2013) A method for rapid production of heteromultimeric protein complexes in plants: assembly of protective bluetongue virus-like particles Plant Biotechnol. J. 11, 839–846

Van Zyl, A.R., Meyers, A.E. and Rybicki, E.P. (2016) Transient Bluetongue virus serotype 8 capsid protein expression in Nicotiana benthamiana Biotech. Rep., 9, 15–24

Dinovernavirus
Attoui, H., Jaafar, F.M., Belhouchet, M., Biagini, P., Cantaloube, J-F., de Micco, P. and de Lamballerie, X. (2005) Expansion of family reoviridae to include nine-segmented dsRNA viruses: isolation and characterization of a new virus designated aedes pseudoscutellaris reovirus assigned to a proposed genes (dinovernavirus) Virology, 343, 212-223

Seadornavirus (see also item 3)

Attoui, H., Jaafar, F.M., Belhouchet, M., Tao, S., Chen, B., Liang, G., Tesh, R.B., de Micco, P. and de Lamballerie, X. (2006) Liao ning, a new Chinese seadornavirus that replicates in transformed and embryonic mammalian cells J. Gen. Virol., 87, 199-208

Rotaviruses

Cheung, W., Gill, M., Esposito, A., Kaminski, C.F., Courousse, N., Chwetzoff, S., Trugnan, G. Keshavan, N., Lever, A. and Desselberger, U. (2010) Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication J. Virol., 84, 6782-6798

Cheung, W., Gaunt, E., Lever, A. and Desselberger, U. (2016) Rotavirus replication: the role of lipid droplets in viral gastroenteritis Elsevier Inc pp 175-187

Lever, A. and Desselberger, U. (2016) Rotavirus replication and the role of cellular lipid droplets: New therapeutic targets? J. Formosan Med. Assoc., 115, 389-394

Trejo-Cerro, O., Eichwald, C., Schraner, E.M., Silva-Ayala, D., López, S., Ariasa, C.F. (2018) Actindependent nonlytic rotavirus exit and infectious virus morphogenetic pathway in nonpolarized cells J. Virol., 92: e02076-17

Taxonomy

Attoui, H., Mertens, P.P.C., Becnel, J., Belaganahalli, S., Bergoin, M., Brussaard, C.P., Chappell, J.D., Ciarlet, M., del Vas, M., Dermody, T.S. et al (2012) Dinovernavirus In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses International Committee on Taxonomy of Viruses. Elsevier Inc., pp 541-637

OptiPrep™ Reference List RV03: 2nd edition, January 2020

OptiPrep™ Reference List RV04

GROUP IV VIRUSES

• Viruses are listed alphabetically within the Baltimore scheme: Family, Genus and Species. Where necessary, references are further divided according to research topic. Publications are listed alphabetically by first author
• Multiple entries from the same first author are listed chronologically.
• For a detailed methodology of Group IV viruses see OptiPrep™ Application Sheets V18-V22. V06 is a methodological review of OptiPrep™ technology.

 

1. Arteriviridae
Porcine reproductive and respiratory syndrome virus

Chen, W-Y., Schniztlein, W.M., Calzada-Nova, G. and Zuckermann, F.A. (2018) Genotype 2 strains of porcine reproductive and respiratory syndrome virus dysregulate alveolar macrophage cytokine production via the unfolded protein response J. Virol., 92: e01251-17

Delputte, P.L., Meerts, P., Costers, S. and Nauwynck, H.J. (2004) Effect of virus-specific antibodies on attachment, internalization and infection of porcine reproductive and respiratory syndrome virus in primary macrophages Vet. Immunol. Immunopathol., 102, 179-188

Li, J. and Murtaugh, M.P. (2012) Dissociation of porcine reproductive and respiratory syndrome virus neutralization from antibodies specific to major envelope protein surface epitopes Virology, 433, 367–376

Li, J. and Murtaugh, M.P. (2015) Functional analysis of porcine reproductive and respiratory syndrome virus N-glycans in infection of permissive cells Virology, 477, 82–88

Li, J., Tao, S., Orlando, R. and Murtaugh, M.P. (2015) N-glycosylation profiling of porcine reproductive and respiratory syndrome virus envelope glycoprotein 5 Virology 478, 86–98

Van Noort, A., Nelsen, A., Pillatzki, A.E., Diel, D.G., Li, F., Nelson, E. and Wang, X. (2017) Intranasal immunization of pigs with porcine reproductive and respiratory syndrome virus-like particles plus 2′, 3′-cGAMP

VacciGrade™ adjuvant exacerbates viremia after virus challenge Virol. J., 14: 76

2. Caliciviridae

Bertolotti-Ciarlet, A., White, L.J., Chen, R., Prasad, B.V.V. and Estes, M.K. (2002) Structural requirements for the assembly of Norwalk virus-like particles J. Virol., 76, 4044-4055

Crisci, E., Fraile, L., Moreno, N., Blanco, E., Cabezónd, R., Costa, C., Mussá, T., Baratelli, M., MartinezOrellana, P., Ganges, L., Martínez, J., Bárcenac, J. and Montoya, M. (2012) Chimeric calicivirus-like particles elicit specific immune responses in pigs Vaccine 30, 2427–2439

Teixeira, L., Marques, R.M., Aguas, A.P. and Ferreira, P.G. (2011) A simple and rapid method for isolation of caliciviruses from liver of infected rabbits Res. Vet. Sci., 91, 164–166

Teixeira, L., Marques, R.M., Águas, A.P. and Ferreira, P.G. (2012) Regulatory T cells are decreased in acute RHDV lethal infection of adult rabbits Vet. Immunol. Immunopathol., 148, 343– 347

3. Coronaviridae

3a. Middle East respiratory syndrome virus

De Wit, E., Prescott, J., Baseler, L., Bushmaker, T., Thomas, T., Lackemeyer, M.G., Martellaro, C., MilnePrice, S., Haddock, E., Haagmans, B.L., Feldmann, H. and Munster, V.J. (2013) The Middle East respiratory syndrome coronavirus (MERS-CoV) does not replicate in Syrian hamsters PLoS One, 8: e69127

3b. Human-Coronavirus

Milewska, A., Kaminski, K., Ciejka, J., Kosowicz, K., Zeglen, S., Wojarski, J., Nowakowska, M., Szczubiałka, K. and Pyrc, K. (2016) HTCC: broad range inhibitor of coronavirus entry PLoS One, 11: e0156552

Milewska, A., Nowak, P., Owczarek, K., Szczepanski, A., Zarebski, M., Hoang, A., Berniak, K., Wojarski, J., Zeglen, S. et al (2018) Entry of human coronavirus NL63 into the cell J. Virol., 92: e01933-17

Naskalska, A., Dabrowska, A., Szczepanski, A., Milewska, A., Jasik, K.P. and Pyrca, K. (2019) Membrane protein of human coronavirus NL63 is responsible for interaction with the adhesion receptor J. Virol., 93:e00355-19

3c. Nidovirales

Infectious bronchitic virus

Amarasinghe, A., De Silva Senapathi1, U., Abdul-Cader, M.S., Popowich, S., Marshall, F., Cork, S.C., van der Meer, F., Gomis, S. and Abdul-Careem, M.F. (2018) Comparative features of infections of two Massachusetts (Mass) infectious bronchitis virus (IBV) variants isolated from Western Canadian layer flocks BMC Vet. Res., 14: 391

3d. SARS-Coronavirus

Beniac, D.R., deVarennes, S.L., Andonov, A., He, R. and Booth, T.F. (2007) Conformational reorganization of the SARS Coronavirus spike following receptor binding: implications for membrane fusion PLoS ONE, 10:e1082

Berry, J.D., Jones, S., Drebot, M.A., Andonov, A., Sabara, M., Yuan, X.Y., Weingartl, H., Fernando, L. et al (2004) Development and characterization of neutralizing monoclonal antibody to the SARs-coronavirus J. Virol. Methods, 120, 87-96

Gubbins, M. J., Plummer, F.A., Yuan, X.Y., Johnstone, D., Drebot, M., Andonova, M., Andonov, A. and Berry, J.D. (2004) Molecular characterization of a panel of murine monoclonal antibodies specific for the SARS-coronavirus Mol. Immunol., 42, 125-136

Hatakeyama, S., Matsuoka, Y., Ueshiba, H., Komatsu, N., Itoh, K., Shichijo, S., Kanai, T., Fukushi, M., Ishida, I., Kirikae, T., Sasazuki, T. and Miyoshi-Akiyama, T. (2008) Dissection and identification of regions required to form pseudoparticles by the interaction between the nucleocapsid (N) and membrane (M) proteins of SARS coronavirus Virology, 380, 99-108

Huang, Y., Yang, Z-Y., Kong, W-P. and Nabel, G.J. (2004) Generation of synthetic severe acute respiratory syndrome coronavirus pseudoparticles: implications for assembly and vaccine production J. Virol., 78, 12557-12565

Kuo, L., Hurst-Hess, K.R., Koetzner, C.A. and Masters, P.S. (2016) Analyses of coronavirus assembly interactions with interspecies membrane and nucleocapsid protein chimeras J. Virol., 90, 4357-4368

Milewska, A., Zarebski, M., Nowak, P., Stozek, K., Potempa, J. and Pyrca, K. (2014) Human coronavirus NL63 utilizes heparan sulfate proteoglycans for attachment to target cells J. Virol., 88, 13221–13230

Milewska, A., Kaminski, K., Ciejka, J., Kosowicz, K., Zeglen, S., Wojarski, J., Nowakowska, M., Szczubiałka, K. and Pyrc, K. (2016) HTCC: broad range inhibitor of coronavirus entry PLoS One, 11: e0156552

Tseng, Y-T., Wang, S-M., Huang, K-J., Lee, A.I-R., Chiang, C-C. and Wang, C-T. (2010) Self-assembly of severe acute respiratory syndrome coronavirus membrane protein J. Biol. Chem., 285, 12862–12872

Tseng, Y-T., Wang, S-M., Huang, K-J. and Wang, C-T. (2014) SARS-CoV envelope protein palmitoylation or nucleocapid association is not required for promoting virus-like particle production J. Biomed. Sci., 21: 34

Yang, Z-Y., Huang, Y., Ganesh, L., Leung, K., Kong, W-P., Schwartz, O., Subbarao, K. and Nabel, G.J. (2004) pH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-sign J. Virol., 78, 5642-5680

4. Flaviviridae

4a. Bovine diarrhea virus

Fredericksen, F., Delgado, F., Cabrera, C., Yáñez, A., Gonzalo, C., Villalba, M. and Olavarría, V.H. (2015) The effects of reference genes in qRT-PCR assays for determining the immune response of bovine cells (MDBK) infected with the Bovine Viral Diarrhea Virus 1 (BVDV-1) Gene, 569, 95–103

Fredericksen, F., Carrasco, G., Villalba, M. and Olavarría, V.H. (2015) Cytopathic BVDV-1 strain induces immune marker production in bovine cells through the NF-κB signaling pathway Mol. Immunol., 68, 213–222

Maurer, K., Krey, T., Moennig, V., Thiel, H-J. and Rümenapf, T. (2004) CD46 is a cellular receptor for bovine viral diarrhea virus J. Virol., 78, 1792-1799

4b. Dengue virus

Alayli, F. and Scholle, F. (2016) Dengue virus NS1 enhances viral replication and pro-inflammatory cytokine production in human dendritic cells Virology, 496, 227–236

Ayala-Nuñez, N.V., Wilschut, J. and Smit, J.M. (2011) Monitoring virus entry into living cells using DiDlabeled dengue virus particles Methods 55, 137–143

Briggs, C.M., Smith, K.M., Piper, A., Huitt, E., Spears, C.J., Quiles, M., Ribeiro, M., Thomas, M.E., Brown, D.T. and Hernandez, R. (2014) Live attenuated tetravalent dengue virus host range vaccine is immunogenic in African green monkeys following a single vaccination J. Virol., 88, 6729–6742

Hacker, K., White, L. and de Silva, A.M. (2009) N-Linked glycans on dengue viruses grown in mammalian and insect cells J. Gen. Virol., 90, 2097–2106

Hadjilaou, A., Green, A.M., Coloma, J. and Harris, E. (2015) Single-cell analysis of B cell/antibody crossreactivity using a novel multicolor FluoroSpot assay J. Immunol., 195, 3490–3496

Hallez, C., Li, X., Suspène, R., Thiers, V., Bouzidi, M.S., Dorobantu, C.M., Lucansky, V., Wain-Hobson, S., Gaudin, R. and Vartanian, J-P., (2019) Hypoxia-induced human deoxyribonuclease I is a cellular restriction factor of hepatitis B virus Nat. Microbiol., 1196, 1196–1207

Heaton, N.S., Perera, R., Berger, K.L., Khadka, S., LaCount, D.J., Kuhn, R.J. and Randall, G. (2010) Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis Proc. Natl. Acad. Sci. USA, 107, 17345–17350

Raheel, U., Jamal, M. and Zaidi, N.U.S.S. (2015) A molecular approach designed to limit the replication of mature DENV2 in host cells Viral Immunol., 28, 378–384

Rodenhuis-Zybert, I.A., van der Schaar, H.M., da Silva Voorham, J.M., van der Ende-Metselaar, H., Lei, HY., Jan Wilschut, J. and Smit, J.M. (2010) Immature dengue virus: a veiled pathogen? PLoS Pathogens, 6:e1000718

Smith, K.M., Nanda, K., McCarl, V., Spears, C.J., Piper, A., Ribeiro, M., Quiles, M., Briggs, C.M., Thomas, G.S., Thomas, M.E., Brown, D.T. and Hernandez, R. (2012) Testing of novel dengue virus 2 vaccines in African green monkeys: safety, immunogenicity, and efficacy Am. J. Trop. Med. Hyg., 87, 743–753

Vancini, R., Kramer, L.D., Ribeiro, M., Hernandez, R. and Brown, D. (2013) Flavivirus infection from mosquitoes in vitro reveals cell entry at the plasma membrane Virology 435, 406–414

Wahala, W.M.P.B., Kraus, A.A., Haymore, L.B., Accavitti-Loper, M.A. and de Silva, A.M. (2009) Dengue virus neutralization by human immune sera: Role of envelope protein domain III-reactive antibody Virology 392, 103–113

Wahala, W.M.P.B., Donaldson, E.F., de Alwis, R., Accavitti-Loper, M.A., Baric, R.S. and de Silva, A.M. (2010) Natural strain variation and antibody neutralization of dengue serotype 3 viruses PLoS Pathogens, 6:e1000821

White, L.J. Parsons, M.M., Whitmore, A.C., Williams, B.M., de Silva, A. and Johnston, R.E. (2007) An immunogenic and protective alphavirus replicon particle-based Dengue vaccine overcomes maternal antibody interference in weanling mice J. Virol., 81, 10329-10339

Zaitseva, E., Yang, S-T., Melikov, K., Pourmal, S., Chernomordik, L.V. (2010) Dengue virus ensures its fusion in late endosomes using compartment-specific lipids PloS Pathogens, 6: e1001131

Zicari, S., Arakelyan, A., Fitzgerald, W., Zaitseva, E., Chernomordik, L.V., Margolis, L. and Grivel, J-C. (2016) Evaluation of the maturation of individual Dengue virions with flow virometry Virology, 488, 20–27

Zybert, I.A., van der Ende-Metselaar, H., Wilschut, J. and Smit, J.M. (2008) Functional importance of dengue virus maturation: infectious properties of immature virions J. Gen. Virol., 89, 3047–3051

4c. Hepatitis C virus

4c-1. Anti-scavanger receptor (B type)

Vercauteren, K., Van Den Eede, N., Mesalam, A.A., Belouzard, S., Catanese, M.T. et al (2014) Successful anti-scavenger receptor class B type I (SR-BI) monoclonal antibody therapy in humanized mice after challenge with HCV variants with in vitro resistance to SR-BI-targeting agents Hepatology, 60, 1508-1518

4c-2. Assembly and cell release of virus particles

Adair, R., Patel, A.H., Corless, L., Griffin, S., Rowlands, D.J. and McCormick, C.J. (2009) Expression of hepatitis C virus (HCV) structural proteins in trans facilitates encapsidation and transmission of HCV subgenomic RNA J. Gen. Virol., 90, 833–842

Bankwitz, D., Doepke, M., Hueging, K., Weller, R., Bruening, J., Behrendt, P., Lee, J-Y., Vondran, F.W.R. et al (2017) Maturation of secreted HCV particles by incorporation of secreted ApoE protects from antibodies by enhancing infectivity J. Hepatol., 67, 480–489

Bayer, K., Banning, C., Bruss, V., Wiltzer-Bach, L. and Schindler, M. (2016) Hepatitis C virus is released via a noncanonical secretory route J. Virol., 90, 10558-10573

Belouzard, S., Danneels, A., Fénéant, L., Séron, K., Rouillé, Y. and Dubuisson, J. (2017) Entry and release of hepatitis C virus in polarized human hepatocytes J. Virol., 91: e00478-17

Benga, W.J.A., Krieger, S.E., Dimitrova, M., Zeisel, M.B., Parnot, M., Lupberger, J., Hildt, E., Luo, G., McLauchlan, J., Baumert, T.F. and Schuster, C. (2010) Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles Hepatology, 51, 43-53

Bentham, M.J., Foster, T.L., McCormick, C. and Griffin, S. (2013) Mutations in hepatitis C virus p7 reduce both the egress and infectivity of assembled particles via impaired proton channel function J. Gen. Virol., 94, 2236–2248

Counihan, N.A., Rawlinson, S.M. and Lindenbach, B.D. (2011) Trafficking of hepatitis C virus core protein during virus particle assembly PLoS Pathog., 7: e1002302

De la Fuente, C. and Catanese, M.T. (2019) Production and purification of cell culture hepatitis C virus In Hepatitis C Virus Protocols, Meth. Mol. Biol., vol. 1911 (ed. Law, M), Springer Science+Business Media LLC New York, pp 105-119

Eyre, N.S., Aloia, A.L., Joyce, M.A., Chulanetra, M., Tyrrell, D.L. and Beard, M.R. (2017) Sensitive luminescent reporter viruses reveal appreciable release of hepatitis C virus NS5A protein into the extracellular environment Virology, 507, 20–31

Fukuhara, T., Tamura, T., Ono, C., Shiokawa, M., Mori, H., Uemura, K., Yamamoto, S., Kurihara, T. et al (2017) Host-derived apolipoproteins play comparable roles with viral secretory proteins Erns and NS1 in the infectious particle formation of Flaviviridae PLoS Pathog., 13: e1006475

Hueging, K., Doepke, M., Vieyres, G., Bankwitz, D., Frentzen, A., Doerrbecker, J., Gumz, F., Haid, S., Wölk, B., Kaderali, L. and Pietschmann, T. (2014) Apolipoprotein E co-determines tissue tropism of hepatitis C virus and is crucial for viral cell-to-cell transmission by contributing to a post-envelopment step of assembly J, Virol., 88, 1433–1446

Icard, V., Diaz, O., Scholtes, C., Perrin-Cocon, L., Ramière, C., Bartenschlager, R., Penin, F., Lotteau, V. and André, P. (2009) Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins PLoS One 4: e4233

Jones, D.M., Atoom, A.M., Zhang, X., Kottilil, S. and Russell, R.S. (2011) A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus J. Virol., 85, 12351– 12361

Lassen, S., Grüttner, C., Nguyen-Dinh, V. and Herker, E. (2019) Perilipin-2 is critical for efficient lipoprotein and hepatitis C virus particle production J. Cell Sci., 132: jcs217042

Liefhebber, J.M.P., Hague, C.V., Zhang, Q., Wakelam, M.J.O. and McLauchlan, J. (2014) Modulation of triglyceride and cholesterol ester synthesis impairs assembly of infectious hepatitis C virus J. Biol. Chem., 289, 21276-21288

Long, G., Hiet, M-S., Windisch, M.P., Lee, J-Y., Lohmann, V. and Bartenschlager, R. (2011) Mouse hepatic cells support assembly of infectious hepatitis C virus particles Gastroenterology 141, 1057–1066

Ma, Y., Yates, J., Liang, Y., Lemon, S.M. and Yi, MK. (2008) NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly J. Virol., 82, 7624-7639

Ndongo, N., Selliah, S., Berthillon, P., Raymond, V-A., Trépo, C., Bilodeau, M. and Petit, M-A. (2011) Expression of E1E2 on hepatitis C RNA-containing particles released from primary cultured human hepatocytes derived from infected cirrhotic livers Intervirology, 54, 1–9

Pène, V., Lemasson, M., Harper, F., Pierron, G. and Rosenberg, A. (2017) Role of cleavage at the core-E1 junction of hepatitis C virus polyprotein in viral morphogenesis PLoS One, 12: e0175810

Puig-Basagoiti, F., Fukuhara, T., Tamura, T., Ono, C., Uemura, K., Kawachi, Y., Yamamoto, S., Mori, H. et al (2016) Human cathelicidin compensates for the role of apolipoproteins in hepatitis C virus infectious particle formation J. Virol., 90, 8464-8477

Salloum, S., Wang, H., Ferguson, C., Parton, R.G. and Tai1, A.W. (2013) Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets PLoS Pathog., 9: e1003513

Shimakami, T., Honda, M., Shirasaki, T., Takabatake, R., Liu, F., Murai, K., Shiomoto, T. et al (2014) The acyclic retinoid Peretinoin inhibits hepatitis C virus replication and infectious virus release in vitro Sci. Rep., 4:4688

Yi, M., Ma, Y., Yates, J. and Lemon, S.M. (2007) Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus J. Virol., 81, 629-638

Yi, M-K., Ma, Y., Yates, J. and Lemon, S.M. (2009) Trans-complementation of an NS2 defect in a late step in hepatitis C virus (HCV) particle assembly and maturation PLoS Pathog., 5:e1000403

Yin, C., Goonawardane, N., Stewart, H. and Harris, M. (2018) A role for domain I of the hepatitis C virus NS5A
protein in virus assembly PloS Pathog., 14: e1006834

Zayas, M., Long, G., Madan, V. and Bartenschlager, R. (2016) Coordination of hepatitis C virus assembly by distinct regulatory regions in nonstructural protein 5A PLoS Pathog., 12: e1005376

4c-3. Assembly – lipid droplets

Beilstein, F., Lemasson, M., Pène, V., Rainteau, D., Demignot, S. and Rosenberg, A.R. (2017) Lysophosphatidylcholine acyltransferase 1 is downregulated by hepatitis C virus: impact on production of lipoviro-particles Gut, 66, 2160–2169

Lee, J-Y., Cortese, M., Haselmann, U., Tabata, K., Romero-Brey, I., Funaya, C., Schieber, N.L., Qiang, Y. et al (2019) Spatiotemporal coupling of the hepatitis C virus replication cycle by creating a lipid droplet-proximal membranous replication compartment Cell Rep., 27, 3602–3617

Rösch, K., Kwiatkowski, M., Hofmann, S., Schöbel, A., Grüttner, C., Wurlitzer, M., Schlüter, H. and Herker, E. (2016) Quantitative lipid droplet proteome analysis identifies annexin A3 as a cofactor for HCV particle production Cell Rep., 16, 3219–3231

Salloum, S., Wang, H., Ferguson, C., Parton, R.G. and Tai1, A.W. (2013) Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets PLoS Pathog., 9: e1003513

Schweitzer, C.J., Zhang, F., Boyer, A., Valdez, K., Cam, M. and Liang, T.J. (2018) N-Myc downstream-regulated gene 1 restricts hepatitis C virus propagation by regulating lipid droplet biogenesis and viral assembly J. Virol., 92: e01166-17

4c-4. Cultured cell infection

Belouzard, S., Danneels, A., Fénéant, L., Séron, K., Rouillé, Y. and Dubuisson, J. (2017) Entry and release of hepatitis C virus in polarized human hepatocytes J. Virol., 91: e00478-17

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Nielsen, S.U., Neely, R.D.G., Toms, G.L. and Bassendine, M.F. (2010) Insulin resistance correlates with low density hepatitis C virus particles in genotype 1 infection J. Hepatol., 52, S319–S457

Buck, M. (2008) Direct infection and replication of naturally occurring hepatitis C virus genotypes 1, 2, 3 and 4 in normal human hepatocyte cultures PLoS One, 3:e2660

Da Costa, D., Turek, M., Felmlee, D.J., Girardi, E., Pfeffer, S., Long, G., Bartenschlager, R., Zeisel, M.B. and Baumert, D.F. (2012) Reconstitution of the entire hepatitis C virus life cycle in nonhepatic cells J. Virol., 86, 11919-11925

Doerrbecker, J., Friesland, M., Riebesehl, N., Ginkel, C., Behrendt, P., Brown, R.J.P., Ciesek, S., Wedemeyer, H., Sarrazin, C., Kaderali, L. et al (2014) Incorporation of primary patient-derived glycoproteins into authentic infectious hepatitis C virus particles Hepatology, 60, 508-520

Haid, S., Windisch, M.P., Bartenschlager, R. and Pietschmann, T. (2010) Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line J. Virol., 84, 964-975

Helle, F., Brochot, E. Fournier, C., Descamps, V., Izquierdo, L., Hoffmann, T.W., Morel, V. et al (2013) Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus PLoS One, 8: e70809

Helle, F., Brochot, E., Fournier, C., Descamps, V., Izquierdo, L., Hoffmann, T.W., Morel, V. Herpe, Y-E. et al (2019) Correction: Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus PLoS One, 14: e0223022

Kato, T., Matsumura, T., Heller, T., Saito, S., Sapp, R.K., Murthy, K., Wakita, T. and Liang, T.J. (2007) Production of infectious hepatitis C virus of various genotypes in cell cultures J. Virol., 81, 4405-4411

Lindenbach, B.D., Meuleman, P., Ploss, A., Vanwolleghem, T., Syder, A.L., McKeating, J.A., Lanford, R.E. et al (2006) Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro Proc. Natl. Acad. Sci. USA, 103, 3805-3809

Long, G., Hiet, M-S., Windisch, M.P., Lee, J-Y., Lohmann, V. and Bartenschlager, R. (2011) Mouse hepatic cells support assembly of infectious hepatitis C virus particles Gastroenterology 2011;141:1057–1066

Mathiesen, C.K., Jensen, T.B., Prentoe, J., Krarup, H., Nicosia, A., Law, M., Bukh, J. and Gottwein, J.M. (2104) Production and characterization of high-titer serum-free cell culture grown hepatitis C virus particles of genotype 1 Virology 458-459, 190–208

Molina-Jimenez, F., Benedicto, I., , Dao Thi, V.L., Gondar, V., Lavillette, D., Marin, J.J., Briz, O. et al (2012) Matrigel-embedded 3D culture of Huh-7 cells as a hepatocyte-like polarized system to study hepatitis C virus cycle Virology, 425, 31–39

Ndongo-Thiam, N., Berthillon, P., Errazuriz, E., Bordes, I., De Sequeira, S., Trépo, C. and Petit, M-A. (2011) Long-term propagation of serum hepatitis C virus (HCV) with production of enveloped HCV particles in human HepaRG hepatocytes Hepatology, 54, 406-417

Pietschmann, T., Zayas, M., Meuleman, P., Long, G., Appel, N., Koutsoudakis, G., Kallis, S., Leroux-Roels, G., Lohmann, V. and Bartenschlager, R. (2009) Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations PLoS Pathog., 5:e1000475

Pihl, A.F., Offersgaard, A.F., Mathiesen, C.K., Prentoe, J., Fahnøe, U., Krarup, H., Bukh, J. and Gottwein, J.M. (2018) High density Huh7.5 cell hollow fiber bioreactor culture for high-yield production of hepatitis C virus and studies of antivirals Sci. Rep., 8: 17505

Podevin, P., Carpentier, A., Pène, V., Aoudjehane, L., Carriere, M., Zaïdi, S., Hernanadez, C., Calle, V. et al (2010) Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes Gastroenterology, 139, 1355-1364

Podevin, P., Carpentier, A., Pène, V., Aoudjehane, L., Hernandez, C., Calle, V., Demignot, S., Scatton, O. et al (2010) Culture of hepatitis C virus (HCV) in primary human adult hepatocytes: a physiological model for the production of authentic infectious particles J. Hepatol., 52, S183–S317

Shiokawa, M., Fukuhara, T., Ono, C., Yamamoto, S., Okamoto, T., Watanabe, N., Wakita, T. and Matsuura, Y. (2014) Novel permissive cell lines for complete propagation of hepatitis C virus J. Virol., 88, 5578–5594

Skardasi, G. and Michalak, T.I. (2013) Hepatitis C virus propogation in human CD4+ and CD8+ T lymphocytes J. Hepatol., 58, S477-S578

Skardasi, G., Chen, A.Y. and Michalak, T.I. (2018) Authentic patient-derived hepatitis C virus infects and productively replicates in primary CD4+
and CD8+ lymphocytes in vitro J. Virol., 92: e01790-17

Sugiyama, N., Murayama, A., Suzuki, R., Watanabe, N., Shiina, M., Liang, T.J., Wakita, T. and Kato, T. (2014) Single strain isolation method for cell culture-adapted hepatitis C virus by end-point dilution and infection PLoS One, 9: e98168

Yi, M., Villanueva, R.A., Thomas, D.L., Wakita, T. and Lemon, S.M. (2006) Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells Proc. Natl. Acad. Sci. USA, 103, 2310-2315

4c-5. Density heterogeneity

Andreo, U., de Jong, Y.P., Scull, M.A., Xiao, J.W., Vercauteren, K., Quirk, C., Mommersteeg, M.C., Bergaya, S. et al (2017) Analysis of hepatitis C virus particle heterogeneity in immunodeficient human liver chimeric fah- /- mice Cell. Mol. Gastroenterol. Hepatol., 4, 405–417

4c-6. Encapsidation

Steinmann, E., Brohm, C., Kallis, S., Bartenschlager, R. and Pietschmann, T. (2008) Efficient transencapsidation of hepatitis C virus RNAs into infectious virus-like particles J. Virol., 82, 7034-7046

4c-7. Entry and assembly (incl. inhibitors)

Anggakusuma, Colpitts, C.C., Schang, L.M., Rachmawati, H., Frentzen, A., Pfaender, S., Behrendt, P., Brown, R.J.P., Bankwitz, D., Steinmann, J. et al (2014) Turmeric curcumin inhibits entry of all hepatitis C virus genotypes into human liver cells Gut, 63, 1137–1149

Barth, H., Schnober, E.K., Neumann-Haeflin, C., Thumann, C., Zeisel, M.B., Diepolder, H.M., Hu, Z., Liang, T.K. et al (2008) Scavenger receptor class B is required for hepatitis C virus uptake and cross-presentation by human dendritic cells J. Virol., 82, 3466-3479

Behrendt, P., Perin, P., Menzel, N., Banda, D., Pfaender, S., Alves, M.P., Thiel, V., Meulemann, P., Colpitts, C.C. (2017) Pentagalloylglucose, a highly bioavailable polyphenolic compound present in Cortex moutan, efficiently blocks hepatitis C virus entry Antiviral Res., 147, 19-28

Bitzegeio, J., Bankwitz, D., Hueging, K., Haid, S., Brohm, C., Zeisel, M.B., Herrmann, E., Iken, M.. Ott, M., Baumert, T.F. and Pietschmann, T. (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors PLoS Pathogens, 6, e:1000978

Calland, N., Albecka, A., Belouzard, S., Wychowski, C., Duverlie, G., Descamps, V., Hober, D., Dubuisson, J., Rouill, Y. and Séron, K. (2012) (-)-Epigallocatechin-3-gallate is a new inhibitor of hepatitis C virus entry Hepatology, 55, 720-729

Calland, N., Sahuc, M.E., Belouzard, S., Pène, V., Bonnafous, P., Mesalam, A.A., Deloison, G., Descamps, V. et al (2015) Polyphenols inhibit hepatitis C virus entry by a new mechanism of action J. Virol., 89, 10053-10063

Ciesek, S. von Hahn, T., Colpitts, C.C., Schang, L.M., Friesland, M., Steinmann, J., Manns, M.P., Ott, M., Wedemeyer, H., Meuleman, P., Pietschmann, T. and Steinmann, E. (2011) The green tea polyphenol, epigallocatechin-3-gallate, inhibits hepatitis C virus entry Hepatology, 54, 1947-1955

Counihan, N.A., Rawlinson, S.M. and Lindenbach, B.D. (2011) Trafficking of hepatitis C virus core protein during virus particle assembly PLoS Pathog., 7: e1002302

Diedrich, G. (2006) How does hepatitis C virus enter cells? FEBS J., 273, 3871-3885

Kato, T., Sugiyama, N., Murayama, A., Matsumura, T., Shiina, M., Asabe, S., Wakita, T. and Imawari, M. (2013) Antimicrobial peptide LL-37 deteriorate infectivity of hepatitis C virus Hepatology, 58 (suppl), 443A444A

Maillard, P., Walic, M., Meuleman, P., Roohvand, F., Huby, T., Le Goff, W., Leroux-Roels, G., Pécheur, E.I. and Budkowska, A. (2011) Lipoprotein lipase inhibits hepatitis C virus (HCV) infection by blocking virus cell entry PLoS One, 6: e26637

Matsumura, T., Sugiyama, N., Murayama, A., Yamada, N., Shiina, M., Asabe, S., Wakita, T., Imawari, M. and Kato, T. (2016) Antimicrobial peptide LL-37 attenuates infection of hepatitis C virus Hepatol. Res., 46, 924–932

Nielsen, S.U., Bassendine, F., Burt, A.D., Bevitt, D.J. and Toms, G.L. (2004) Characterization of the genome and structural proteins of hepatitis C virus resolved from infected human liver J. Gen. Virol., 85, 1497-1507

Qian, X-J., Zhang, X-L., Zhao, P., Jin, Y-S., Chen, H-S., Xu, Q-Q., Ren, H., Zhu, S-Y. et al (2016) A schisandra-derived compound schizandronic acid inhibits entry of pan-HCV genotypes into human hepatocytes Sci. Rep., 6: 27268

Sabahi, A. (2009) Hepatitis C virus entry: the early steps in the viral replication cycle Virol. J., 6:117

Sainz Jr., B., Barretto, N., Martin, D.N., Hiraga, N., Imamura, M., Hussain, S., Marsh, K.A., Yu, X., Chayama, K., Alrefai1, W.A., and Uprichard, S.L. (2012) Identification of the Niemann-Pick C1–like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor Nat. Med., 18, 281-285

Vausselin, T., Calland, N., Belouzard, S., Descamps, V., Douam, F., Helle, F., François, C. et al (2013) The antimalarial ferroquine is an inhibitor of hepatitis C virus Hepatology, 58, 86-97

Wahid, A., Helle, F., Descamps, V., Duverlie, G., Penin, F. and Dubuisson, J. (2013) Disulfide bonds in hepatitis C virus glycoprotein E1 control the assembly and entry functions of E2 glycoprotein J. Virol., 87, 1605-1617

Xu, Y., Martinez, P., Séron, K., Luo, G., Allain, F., Dubuisson, J. and Belouzard, S. (2015) Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans J. Virol., 89, 3846-3858

Yin, C., Goonawardane, N., Stewart, H. and Harris, M. (2018) A role for domain I of the hepatitis C virus NS5A protein in virus assembly PloS Pathog., 14: e1006834

Zayas, M., Long, G., Madan, V. and Bartenschlager, R. (2016) Coordination of hepatitis C virus assembly by distinct regulatory regions in nonstructural protein 5A PLoS Pathog., 12: e1005376

4c-8. Entry/efflux processes – apolipoproteins/lipoproteins/LDL/VLDL

Albecka, A., Belouzard, S., Op de Beeck, A., Descamps, V., Goueslain, L., Bertrand-Michel, J., Tercé, F., Duverlie, G., Rouillé, Y. and Dubuisson, J. (2012) Role of low-density lipoprotein receptor in the hepatitis C virus life cycle Hepatology, 55, 998-1007

Andreo, U., Scull, M.A., De Jong, Y.P., Ramanan, V., Flatley, B., Schwartz, R.E, Ng, S., Chen, A.A., Fisher, E.A., Bhatia, S. and Rice, C.M. (2014) Novel in vitro models for assembly of VLDL and low-density hepatitis C virus particles Hepatology, 60 (Suppl), 1050A-1051A

Bankwitz, D., Doepke, M., Hueging, K., Weller, R., Bruening, J., Behrendt, P., Lee, J-Y., Vondran, F.W.R. et al (2017) Maturation of secreted HCV particles by incorporation of secreted ApoE protects from antibodies by enhancing infectivity J. Hepatol., 67, 480–489

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Toms, G.L., Neely, R.D.G. and Bassendine, M.F. (2010) Low density Hepatitis C virus particles (lipoviral particles) associate with insulin resistance in genotype 1 infection Atherosclerosis 213, e4

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Nielsen, S.U., Thomas, H.C., Taylor-Robinson, S.D., Neely,  R.D.G., Toms, G.L. and Bassendine, M.F. (2011) Insulin resistance and low-density apolipoprotein Bassociated lipoviral particles in hepatitis C virus genotype 1 infection Gut, 60, 680-687

Bridge, S., Sheridan, D., Felmlee, D., Crossey, M., Thomas, H., Taylor-Robinson, S., Toms, G., Neely, D. and Bassendine, M. (2011) P50 Apolipoprotein E and low-density, apolipoprotein B associated lipoviral particles in chronic hepatitis C infection: evidence for genotype-specific modulation of lipid pathways Gut, 60, A24

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Crossey, M.M.E., Fenwick, F.I., Lanyon, C.V., Dubuc, G., Seidah, N.G., Davignon, J. et al (2015) PCSK9, apolipoprotein E and lipoviral particles in chronic hepatitis C genotype 3: Evidence for genotype-specific regulation of lipoprotein metabolism J. Hepatol., 62, 763–770

Calattini, S., Fusil, F., Mancip, J., Thi, V.L.D., Granier, C., Gadot, N., Scoazec, J-Y., Zeisel, M.B. et al (2015) Functional and biochemical characterization of hepatitis C virus (HCV) particles produced in a humanized liver mouse model J. Biol. Chem., 290, 23173–23187

Crouchet, E., Lefèvre, M., Verrier, E.R., Oudot, M.A., Baumert, T.F. and Schuster, C. (2017) Extracellular lipid-free apolipoprotein E inhibits HCV replication and induces ABCG1-dependentcholesterol efflux Gut, 66, 896–907

Diedrich, G. (2006) How does hepatitis C virus enter cells? FEBS J., 273, 3871-3885

Fauvelle, C., Felmlee, D.J., Crouchet, E., Lee, JY., Heydmann, L., Lefèvre, M., Magri, A., Hiet, M-S., Fofana,I., Habersetzer, F. ey al (2016) Apolipoprotein E mediates evasion from hepatitis C virus neutralizing antibodies Gastroenterology 150, 206–217

Felmlee, D., Sheridan, D., Bridge, S., Packard, C., Caslake, M., Toms, G., Neely, D. and Bassendine, M. (2011) Use of Intralipid infusion to analyse apolipoprotein B (apoB) and HCV RNA kinetics in chronic infection Gut, 60, A21

Fénéant, L., Potel, J., François, C., Sané, F., Douam, F., Belouzard, S., Calland, N., Vausselin, T. et al (2015) New insights into the understanding of hepatitis C virus entry and cell-to-cell transmission by using the ionophore monensin A J. Virol., 89, 8346–8364

Fukuhara, T., Tamura, T., Ono, C., Shiokawa, M., Mori, H., Uemura, K., Yamamoto, S., Kurihara, T. et al (2017) Host-derived apolipoproteins play comparable roles with viral secretory proteins Erns and NS1 in the infectious particle formation of Flaviviridae PLoS Pathog., 13: e1006475

Hishiki, T., Shimizu, Y., Tobita, R., Sugiyama, K., Ogawa, K., Funami, K., Ohsaki, Y., Fujimoto, T. et al (2010) Infectivity of hepatitis C virus is influenced by association with apolipoprotein E isoforms J. Virol., 84, 12048-12057

Hueging, K., Doepke, M., Vieyres, G., Bankwitz, D., Frentzen, A., Doerrbecker, J., Gumz, F., Haid, S., Wölk, B., Kaderali, L. and Pietschmann, T. (2014) Apolipoprotein E co-determines tissue tropism of hepatitis C virus and is crucial for viral cell-to-cell transmission by contributing to a post-envelopment step of assembly J, Virol., 88, 1433–1446

Jammart, B., Michelet, M., Pécheur, E-I., Parent, R., Bartosch, B., Zoulim, F. and Durante, D. (2013) Verylow-density lipoprotein (VLDL)-producing and hepatitis C virus replicating HepG2 cells secrete no more lipoviroparticles than VLDL-deficient Huh7.5 cells J. Virol., 87, 5065–5080

Lee, J-Y., Acosta, E.G., Stoeck, I.K., Long, G., Hiet, M-S., Mueller, B., Fackler, O.T., Kallis, S. and Bartenschlager, R. (2014) Apolipoprotein E likely contributes to a maturation step of infectious hepatitis C virus particles and interacts with viral envelope glycoproteins J. Virol., 88, 12422–12437

Li, Z., Li, Y., Bi, Y., Zhang, H., Yao, Y., Li, Q., Cun, W., Dong, S. (2017) Extracellular interactions between hepatitis C virus and secreted apolipoprotein E J. Virol., 91: e00227-16

Maillard, P., Walic, M., Meuleman, P., Roohvand, F., Huby, T., Le Goff, W., Leroux-Roels, G., Pécheur, E.I. and Budkowska, A. (2011) Lipoprotein lipase inhibits hepatitis C virus (HCV) infection by blocking virus cell entry PLoS One, 6: e26637

Nielsen, S.U., Bassendine, M.F., Burt, A.D., Martin, C., Pumeechockchai, W. and Toms, G.L. (2006) Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients J. Virol., 80, 2418-2428

Nielsen, S., Sheridan, D., Bridge, S., Felmlee, D., Neely, D. Toms, G. and Bassendine, M. (2009) Characterization of hepatitis C virus particles in human plasma: association with immunoglobulins G1, G3 and M and apolipoproteins A-I, A-II, B, C-I and E J. Hepatol., 50 (Supp. 1) S316-S317

Oliveira, C., Fournier, C., Descamps, V., Morel, V., Scipione, C.A., Koschinsky, M.L., Boullier, A., Marcelo, P. et al (2016) Apolipoprotein(a) inhibits hepatitis C virus entry J. Clin. Virol., 82S, S82-S83

Oliveira, C., Fournier, C., Descamps, V., Morel, V., Scipione, C.A., Romagnuolo, R., Koschinsky, M.L., Boullier, A., Marcelo, P. et al (2017) Apolipoprotein(a) inhibits hepatitis C virus entry through interaction with infectious particles Hepatology, 65, 1851-1864

Owen, D.M., Huang, H., Ye, J. and Gale, M. (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor Virology 394, 99–108

Pene, V., Hernandez, C., Blanc, E., Aoudjehane, L., Le Grand, B., Carpentier, A., Méritet, J-F., Conti, F. et al (2015) Alcohol increases the production of hepatitis C virus (HCV) lipo-viro-particles in primary human hepatocytes Hepatology, 62 (Suppl) 221A-222A

Podevin, P., Carpentier, A., Pène, V., Aoudjehane, L., Hernandez, C., Calle, V., Demignot, S., Scatton, O. et al (2010) Culture of hepatitis C virus (HCV) in primary human adult hepatocytes: a physiological model for the production of authentic infectious particles J. Hepatol., 52, S183–S317

Sheridan, D., Bridge, S., Sheridan, D.A., Felmlee, D., Thomas, H., Taylor-Robinson, S., Dermot, R., Neely, G., Toms, G.L. and Bassendine, M.F. (2010) Measurement of low density apolipoprotein B associated hepatitis C virus lipoviral particles in genotype 1 infection is more clinically relevant than total viral load Gut, 59 Suppl 2, A6

Sheridan, D.A., Bridge, S.H., Felmlee, D.J., Crossey, M.M.E., Thomas, H.C., Taylor-Robinson, S.D., Toms, G.L., Neely, R.D.G. and Bassendine, M.F. (2012) Apolipoprotein-E and hepatitis C lipoviral particles in genotype 1 infection: Evidence for an association with interferon sensitivity J. Hepatol., 57, 32–38

Yang, Z., Wang, X., Chi, X., Zhao, F., Guo, J., Ma, P., Zhong, J., Niu, J., Pan, X. and Long, G. (2016) Neglected but important role of apolipoprotein E exchange in hepatitis C virus infection J. Virol., 90, 9632-9643

Zhu, W., Pei, R., Jin, R., Hu, X., Zhou, Y., Wang, Y., Wu, C., Lu, M. and Chen, X. (2014) Nuclear receptor 4 group A member 1 determines hepatitis C virus entry efficiency through the regulation of cellular receptor and apolipoprotein E expression J. Gen. Virol., 95, 1510–1521

4c-9. Entry process – glycocalyx/glycoproteins/proteins/proteoglycans

Baktash, Y., Madhav, A., Coller, K.E. and Randall, G. (2018) Single particle imaging of polarized hepatoma organoids upon hepatitis C virus infection reveals an ordered and sequential entry process Cell Host Microbe, 23, 382–394

Carlsen, T.H.R., Scheel, T,K,H, Ramirez, S., Foung, S.K.H. and Bukha, J. (2013) Characterization of hepatitis C virus recombinants with chimeric E1/E2 envelope proteins and identification of single amino acids in the E2 stem region important for entry J. Virol., 87, 1385-1399

Grigorov, B., Reungoat, E., Gentil dit Maurin, A., Varbanov, M., Blaising, J., Michelet, M., Manuel, R., Parent, R., Bartosch, B. et al (2017) Hepatitis C virus infection propagates through interactions between Syndecan-1 and CD81 and impacts the hepatocyte glycocalyx Cell. Microbiol., 19: e12711

Haid, S., Pietschmann, T. and Pécheur, E.I. (2009) Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles J. Biol. Chem., 284, 17657–17667

Haddad, J.G., Rouillé, Y., Hanoulle, X., Descamps, V., Hamze, M., Dabboussi, F., Baumert, T,F., Duverlie, G., Lavie, M. and Dubuisson, J. (2017) Identification of novel functions for hepatitis C virus envelope glycoprotein E1 in virus entry and assembly J. Virol., 91: e00048-17

Lavie, M., Sarrazin, S., Montserret, R., Descamps, V., Baumert, T.F., Duverlie, G., Séron, K., Penin, F. and Dubuissona, J. (2014) Identification of conserved residues in hepatitis C virus envelope glycoprotein E2 that modulate virus dependence on CD81 and SRB1 entry factors J. Virol., 88, 10584–10597

Tamura, T., Fukuhara, T., Uchida, T., Ono, C., Mori, H., Sato, A., Fauzyah, Y., Okamoto, T., Kurosu, T. et al (2018) Characterization of recombinant Flaviviridae viruses possessing a small reporter tag J. Virol., 92:e01582-17

Xu, Y., Martinez, P., Séron, K., Luo, G., Allain, F., Dubuisson, J. and Belouzard, S. (2015) Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans J. Virol., 89, 3846-3858

4c-10. Envelope proteins/glycoproteins (E1/E2)/structure

Atoom, A.M., Jones, D.M. and Russell, R.S. (2013) Evidence suggesting that HCV p7 protects E2 glycoprotein from premature degradation during virus production Virus Res., 176, 199– 210

Calattini, S., Fusil, F., Mancip, J., Thi, V.L.D., Granier, C., Gadot, N., Scoazec, J-Y., Zeisel, M.B. et al (2015) Functional and biochemical characterization of hepatitis C virus (HCV) particles produced in a humanized liver mouse model J. Biol. Chem., 290, 23173–23187

Carlsen, T.H.R., Scheel, T,K,H, Ramirez, S., Foung, S.K.H. and Bukha, J. (2013) Characterization of hepatitis C virus recombinants with chimeric E1/E2 envelope proteins and identification of single amino acids in the E2 stem region important for entry J. Virol., 87, 1385-1399

Catanese, M.T., Uryu, K., Kopp, M., Edwards, T.J., Andrus, L., Rice, W.J., Silvestry, M., Kuhn, R.J. and Rice, C.M. (2013) Ultrastructural analysis of hepatitis C virus particles Proc. Natl. Acad. Sci. USA, 110, 9505–9510

Denolly, S., Mialon, C., Bourlet, T., Amirache, F., Penin, F., Lindenbach, B., Boson, B. and Cosset, F-L. (2017) The amino-terminus of the hepatitis C virus (HCV) p7 viroporin and its cleavage from glycoprotein E2-p7 precursor determine specific infectivity and secretion levels of HCV particle types PLoS Pathog. 13: e1006774

Doerrbecker, J., Friesland, M., Riebesehl, N., Ginkel, C., Behrendt, P., Brown, R.J.P., Ciesek, S. et al (2014) Incorporation of primary patient-derived glycoproteins into authentic infectious hepatitis C virus particles Hepatology, 60, 508-520

Felmlee, D.J., Fauvelle, C., Heydmann, L., Hiet, M-S., Fofana, I., Bartenschlager, R., Stoll-Keller, F., Zeisel, M.B.. Fafi-Kremer, S. and Baumert, T.F. (2013) Hepatitis C virus liver transplantation escape variant is characterized by both enhanced triglyceride-rich lipoprotein association and sensitivity to apoE antibodies J. Hepatol., 58, S468

Fénéant, L., Potel, J., François, C., Sané, F., Douam, F., Belouzard, S., Calland, N., Vausselin, T. et al (2015) New insights into the understanding of hepatitis C virus entry and cell-to-cell transmission by using the ionophore monensin A J. Virol., 89, 8346–8364

Grove, J., Nielsen, S., Zhong, J., Bassendine, M.F., Drummer, H.E., Balfe, P. and McKeating, J.A. (2008) Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies J. Virol., 82, 12020–12029

Haddad, J.G., Rouillé, Y., Hanoulle, X., Descamps, V., Hamze, M., Dabboussi, F., Baumert, T,F., Duverlie, G., Lavie, M. and Dubuisson, J. (2017) Identification of novel functions for hepatitis C virus envelope glycoprotein E1 in virus entry and assembly J. Virol., 91: e00048-17

Icard, V., Diaz, O., Scholtes, C., Perrin-Cocon, L., Ramière, C., Bartenschlager, R., Penin, F., Lotteau, V. and André, P. (2009) Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins PLoS One 4: e4233

Koutsoudakis, G., Dragun, J., Pérez-del-Pulgar, S., Coto-Llerena, M., Mensa, L., Crespo, G., González, P., Navasa, M. and Forns, X. (2012) Interplay between basic residues of hepatitis C virus glycoprotein E2 with viral receptors, neutralizing antibodies and lipoproteins PLoS One, 7: e52651

Lavie, M., Sarrazin, S., Montserret, R., Descamps, V., Baumert, T.F., Duverlie, G., Séron, K., Penin, F. and Dubuissona, J. (2014) Identification of conserved residues in hepatitis C virus envelope glycoprotein E2 that modulate virus dependence on CD81 and SRB1 entry factors J. Virol., 88, 10584–10597

Lee, J-Y., Acosta, E.G., Stoeck, I.K., Long, G., Hiet, M-S., Mueller, B., Fackler, O.T., Kallis, S. and Bartenschlager, R. (2014) Apolipoprotein E likely contributes to a maturation step of infectious hepatitis C virus particles and interacts with viral envelope glycoproteins J. Virol., 88, 12422–12437

Lee, M., Yang, J., Jo, E., Lee, J-Y., Kim, H-Y., Bartenschlager, R., Shin, E-C., Bae, Y-S. and Windisch, M.P. (2017) A novel inhibitor IDPP interferes with entry and egress of HCV by targeting glycoprotein E1 in a genotype-specific manner Sci. Rep., 7: 44676

Moustafa, R.I., Haddad, J.G., Linna, L., Hanoulle, X., Descamps, V., Mesalam, A.A., Baumert, T.F., Duverlie, G., Meuleman, P., Dubuisson, J. and Lavie, M. (2018) Functional study of the C-terminal part of the hepatitis C virus E1 ectodomain J. Virol. 92: e00939-18

Pécheur, E-I., Diaz, O., Molle, J., Icard, V., Bonnafous, P., Lambert, O. and André, P. (2010) Morphological characterization and fusion properties of triglyceride-rich lipoproteins obtained from cells transduced with hepatitis C virus glycoproteins J. Biol. Chem., 285, 25802–25811

Pène, V., Lemasson, M., Harper, F., Pierron, G. and Rosenberg, A. (2017) Role of cleavage at the core-E1 junction of hepatitis C virus polyprotein in viral morphogenesis PLoS One, 12: e0175810

Prentoe, J., Jensen, T.B., Meuleman, P., Serre, S.B.N., Scheel, T.K.H., Leroux-Roels, G., Gottwein, J.M. and Bukh, J. (2011) Hypervariable region 1 differentially impacts viability of hepatitis C virus strains of genotypes 1 to 6 and impairs virus neutralization J. Virol., 85, 2224-2234

Prentoe, J., Velázquez-Moctezuma, R., Augestad, E.H., Galli, A., Wang, R., Law, M., Alter, H. and Bukha, J. (2019) Hypervariable region 1 and N-linked glycans of hepatitis C regulate virion neutralization by modulating envelope conformations Proc. Natl. Acad. Sci. USA 116, 0039–10047

Wahid, A., Helle, F., Descamps, V., Duverlie, G., Penin, F. and Dubuisson, J. (2013) Disulfide bonds in hepatitis C virus glycoprotein E1 control the assembly and entry functions of E2 glycoprotein J. Virol., 87, 1605-1617

4c-11. Exosome association

Elgner, F., Ren, H., Medvedev, R., Ploen, D., Himmelsbach, K., Boller, K. and Hildt, E. (2016) The intracellular cholesterol transport inhibitor U18666A inhibits the exosome-dependent release of mature hepatitis C virus J. Virol., 90, 11181-11196

Liu, Z., Zhang, X, Yu, Q. and He, J.J. (2014) Exosome-associated hepatitis C virus in cell cultures and patient plasma Biochem. Biophys. Res. Comm., 455, 218–222

4c-12. Genome/genome manipulation

Chan, K., Cheng, G., Beran, R.K.F., Yang, H., Appleby, T.C., Pokrovskii, M.V., Mo, H., Zhong, SW., Delaney IV, W.E. (2012) An adaptive mutation in NS2 is essential for efficient production of infectious 1b/2a chimeric hepatitis C virus in cell culture Virology, 422, 224–234

Nielsen, S.U., Bassendine, F., Burt, A.D., Bevitt, D.J. and Toms, G.L. (2004) Characterization of the genome and structural proteins of hepatitis C virus resolved from infected human liver J. Gen. Virol., 85, 1497-1507

Vassilaki, N., Friebe, P., Meuleman, P., Kallis, S., Kaul, A., Paranhos-Baccalà, G., Leroux-Roels, G., Mavromara, P. and Bartenschlager, R. (2008) Role of the hepatitis C virus core+1 open reading frame and core cis-acting RNA elements in viral RNA translation and replication J. Virol., 82, 11503-11515

4c-13. Immune responses/antibodies/infectivity

Angus, A.G.N., Loquet, A., Stack, S.J., Dalrymple, D., Gatherer, D., Penin, F. and Patela, A.H. (2012) Conserved glycine 33 residue in flexible domain I of hepatitis C virus core protein is critical for virus infectivity J. Virol., 86, 679-690

Bankwitz, D., Steinmann, E., Bitzegeio, J., Ciesek, S., Friesland, M., Herrmann, E., Zeisel, M.B., Baumert, T.F. et al (2010) Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes J. Virol., 84, 5751–5763

Bentham, M.J., Foster, T.L., McCormick, C. and Griffin, S. (2013) Mutations in hepatitis C virus p7 reduce both the egress and infectivity of assembled particles via impaired proton channel function J. Gen. Virol., 94, 2236–2248

Bitzegeio, J., Bankwitz, D., Hueging, K., Haid, S., Brohm, C., Zeisel, M.B., Herrmann, E., Iken, M.. Ott, M., Baumert, T.F. and Pietschmann, T. (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors PLoS Pathogens, 6, e:1000978

Blanchet, M., Sureau, C., Guévin, C., Seidah, N.G. and Labonté, P. (2015) SKI-1/S1P inhibitor PF-429242 impairs the onset of HCV infection Antiviral Res., 115, 94–104

Bocchetta, S., Maillard, P., Yamamoto, M., Gondeau, C., Douam, F., Lebreton, S., Lagaye, S., Pol, S. et al (2014) Up-regulation of the ATP-binding cassette transporter A1 inhibits hepatitis C virus infection PLoS One, 9: e92140

Brault, C., Lévy, P., Duponchel, S., Michelet, M., Sallé, A., Pécheur, E-I., Plissonnier, M-L., Parent, R., Véricel, E. et al (2016) Glutathione peroxidase 4 is reversibly induced by HCV to control lipid peroxidation and to increase virion infectivity Gut, 65, 144–154

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Nielsen, S.U., Neely, R.D.G., Toms, G.L. and Bassendine, M.F. (2010) Insulin resistance correlates with low density hepatitis C virus particles in genotype 1 infection J. Hepatol., 52, S319–S457

Bush, C.O., Pokrovskii, M.V., Saito, R., Morganelli, P., Canales, E., Clarke, M.O., Lazerwith, S.E., Golde, J. et al (2014) A small-molecule inhibitor of hepatitis C virus infectivity Antimicrob. Agents Chemother., 58, 386–396

Carlsen, T.H.R., Scheel, T,K,H, Ramirez, S., Foung, S.K.H. and Bukha, J. (2013) Characterization of hepatitis C virus recombinants with chimeric E1/E2 envelope proteins and identification of single amino acids in the E2 stem region important for entry J. Virol., 87, 1385-1399

Denolly, S., Mialon, C., Bourlet, T., Amirache, F., Penin, F., Lindenbach, B., Boson, B. and Cosset, F-L. (2017) The amino-terminus of the hepatitis C virus (HCV) p7 viroporin and its cleavage from glycoprotein E2-p7 precursor determine specific infectivity and secretion levels of HCV particle types PLoS Pathog. 13: e1006774

Elmowalid, G.A., Qiao, M., Jeong, S-H., Borg, B.B., Baumert, T.F., Sapp, R.K., Hu, Z., Murthy, K. and Liang, T.J. (2007) Immunization with hepatitis C virus-like particles results in control of hepatitis C virus infection in chimpanzees Proc. Natl. Acad. Sci. USA, 104, 8427-8432

Farquhar, M.J., Harris, H.J., Diskar, M., Jones, S., Mee,, C.J., Nielsen, S.U., Brimacombe C.L. et al (2008) Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity J. Virol., 82, 8797-8811

Fauvelle, C., Felmlee, D.J., Crouchet, E., Lee, JY., Heydmann, L., Lefèvre, M., Magri, A., Hiet, M-S., Fofana, I., Habersetzer, F. ey al (2016) Apolipoprotein E mediates evasion from hepatitis C virus neutralizing antibodies Gastroenterology 150, 206–217

Garrone, P., Fluckiger, A-C., Mangeot, P.E., Gauthier, E., Dupeyrot-Lacas, P., Mancip, J., Cangialosi, A. et al (2011) A prime-boost strategy using virus-like particles pseudotyped for HCV proteins triggers broadly neutralizing antibodies in Macaques Sci. Transl. Med., 3: 94ra71

Gastaminza, P., Kapadia, S.B. and Chisari, F. (2006) Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles J. Virol., 80, 11074-11081

Grove, J., Nielsen, S., Zhong, J., Bassendine, M.F., Drummer, H.E., Balfe, P. and McKeating, J.A. (2008) Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies J. Virol., 82, 12020–12029

Haid, S., Windisch, M.P., Bartenschlager, R. and Pietschmann, T. (2010) Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line J. Virol., 84, 964-975

Johnson, D.F., Chin, R., Earnest-Silveira, L., Zentgraf, H., Bock, T., Chua, B., Jackson, D.C. and Torresi, J. (2010) Recombinant mammalian cell derived hepatitis C virus-like particles induce neutralizing antibody responses to hepatitis C virus Clin. Microbiol. Infect., 16, S319

Jones, D.M., Atoom, A.M., Zhang, X., Kottilil, S. and Russell, R.S. (2011) A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus J. Virol., 85, 12351–12361

Koutsoudakis, G., Dragun, J., Pérez-del-Pulgar, S., Coto-Llerena, M., Mensa, L., Crespo, G., González, P., Navasa, M. and Forns, X. (2012) Interplay between basic residues of hepatitis C virus glycoprotein E2 with viral receptors, neutralizing antibodies and lipoproteins PLoS One, 7: e52651

Lambotin, M., Baumert, T.F. and Barth, H. (2010) Distinct intracellular trafficking of hepatitis C virus in myeloid and plasmacytoid dendritic cells J Virol., 84, 8964–8969

Marnata, C., Saulnier, A., Mompelat, D., Krey, T., Cohen, L., Boukadida, C., Warter, L., Fresquet, J., Vasiliauskaite, I., Escriou, N. et al (2015) Determinants involved in hepatitis C virus and GB virus B primate host restriction J. Virol., 89, 12131-12144

Mathiesen, C.K., Prentoe, J., Meredith, L.W., Jensen, T.B., Krarup, H., McKeating, J.A., Gottwein, J.M. and Bukha, J. (2015) Adaptive mutations enhance assembly and cell-to-cell transmission of a high-titer hepatitis C virus genotype 5a core-NS2 JFH1-based recombinant J. Virol., 89, 7758-7775

Meredith, L.W., Farquhar, M.J., Tarr, A.W. and McKeating, J.A. (2014) Type I interferon rapidly restricts infectious hepatitis C virus particle genesis Hepatology, 60, 1891-1901

Owen, D.M., Huang, H., Ye, J. and Gale, M. (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor Virology 394, 99–108

Plissonnier, M-L., Cottarel, J., Piver, E., Kullolli, M., Centonze, F.G., Pitteri, S., Farhan, H., Meunier, J-C., Zoulim, F. and Parent, R. (2019) LARP1 binding to hepatitis C virus particles is correlated with intracellular retention of viral infectivity Virus Res., 271: 197679

Podevin, P., Carpentier, A., Pène, V., Aoudjehane, L., Carriere, M., Zaïdi, S., Hernanadez, C., Calle, V. et al (2010) Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes Gastroenterology, 139, 1355-1364

Prentoe, J. and Bukh, J. (2011) Hepatitis C virus expressing flag-tagged envelope protein 2 has unaltered infectivity and density, is specifically neutralized by flag antibodies and can be purified by affinity chromatography Virology 409, 148–155

Prentoe, J., Jensen, T.B., Meuleman, P., Serre, S.B.N., Scheel, T.K.H., Leroux-Roels, G., Gottwein, J.M. and Bukh, J. (2011) Hypervariable region 1 differentially impacts viability of hepatitis C virus strains of genotypes 1 to 6 and impairs virus neutralization J. Virol., 85, 2224-2234

Sabahi, A., Marsh, K.A., Dahari, H., Corcoran, P., Lamora, J.M., Yu, X., Garry, R.F. and Uprichard, S.L. (2010) The rate of hepatitis C virus infection initiation in vitro is directly related to particle density Virology, 407, 110–119

Sheridan, D.A., Bridge, S.H., Felmlee, D.J., Crossey, M.M.E., Thomas, H.C., Taylor-Robinson, S.D., Toms, G.L., Neely, R.D.G. and Bassendine, M.F. (2012) Apolipoprotein-E and hepatitis C lipoviral particles in genotype 1 infection: Evidence for an association with interferon sensitivity J. Hepatol., 57, 32–38

Sheridan, D.A., Hajarizadeh, B., Fenwick, F.I., Matthews, G.V., Applegate, T., Douglas, M., Neely, D., Askew, B. Dore, G.J., et al (2016) Maximum levels of hepatitis C virus lipoviral particles are associated with early and persistent infection Liver Int., 36, 1774–1782

Shimizu, Y., Hishiki, T., Sugiyama, K., Ogawa, K., Funami, K., Kato, A., Ohsaki, Y., Fujimoto, T., Takaku, H. and Shimotohno, K. (2010) Lipoprotein lipase and hepatic triglyceride lipase reduce the infectivity of hepatitis C virus (HCV) through their catalytic activities on HCV-associated lipoproteins Virology, 407, 152-159

Vausselin, T., Séron, K., Lavie, M., Mesalam, A.A., Lemasson, M., Belouzard, S., Fénéant, L., Danneels, A., Rouillé, Y. et al (2016) Identification of a new benzimidazole derivative as an antiviral against hepatitis C virus J. Virol., 90, 8422-8434

Vercauteren, K., Van Den Eede, N., Mesalam, A.A., Belouzard, S., Catanese, M.T. et al (2014) Successful anti-scavenger receptor class B type I (SR-BI) monoclonal antibody therapy in humanized mice after challenge with HCV variants with invitro resistance to SR-BI-targeting agents Hepatology, 60, 1508-1518

4c-14. Insulin resistance

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Nielsen, S.U., Neely, R.D.G., Toms, G.L. and Bassendine, M.F. (2010) Insulin resistance correlates with low density hepatitis C virus particles in genotype 1 infection J. Hepatol., 52, S319–S457

Bridge, S.H., Sheridan, D.A., Felmlee, D.J., Nielsen, S.U., Thomas, H.C., Taylor-Robinson, S.D., Neely, R.D.G., Toms, G.L. and Bassendine, M.F. (2011) Insulin resistance and low-density apolipoprotein Bassociated lipoviral particles in hepatitis C virus genotype 1 infection Gut, 60, 680-687

Das, G.C. and Hollinger, F.B. (2012) Molecular pathways for glucose homeostasis, insulin signaling and autophagy in hepatitis C virus induced insulin resistance in a cellular model Virology, 434, 5–17

4c-15. Intracellular trafficking

Baktash. Y. and Randall, G. (2019) Live cell imaging of hepatitis C virus trafficking In Hepatocytes In Hepatitis C Virus Protocols, Meth. Mol. Biol., vol. 1911 (ed. Law, M), Springer Science+Business Media LLC New York, pp 263-274

4c-16. LARP-1

Plissonnier, M-L., Cottarel, J., Piver, E., Kullolli, M., Centonze, F.G., Pitteri, S., Farhan, H., Meunier, J-C., Zoulim, F. and Parent, R. (2019) LARP1 binding to hepatitis C virus particles is correlated with intracellular retention of viral infectivity Virus Res., 271: 197679

4c-17. Lipids and lipoprotein metabolism (see also “Phospholipases”)

Boyer, A., Park, S.B., de Boer, Y.S., Li, Q. and Liang, T.J. (2018) TM6SF2 Promotes lipidation and secretion of hepatitis C virus in infected hepatocytes Gastroenterology 115, 1923–1935

Brault, C., Lévy, p., Duponchel, s., Michelet, M., Sallé, A., Pécheur, E-I., Plissonnier, M-L., Parent, R., Véricel, E. et al (2016) Glutathione peroxidase 4 is reversibly induced by HCV to control lipid peroxidation and to increase virion infectivity Gut, 65, 144–154

Caldwell, S., Hoehn, K.K. and Hahn, Y.S. (2013) The strange and critical intersection of hepatitis C and lipoprotein metabolism: ‘‘C-zing’’ the Oil Hepatology, 57, 1684-1687

Maillard, P., Walic, M., Meuleman, P., Roohvand, F., Huby, T., Le Goff, W., Leroux-Roels, G., Pécheur, E.I. and Budkowska, A. (2011) Lipoprotein lipase inhibits hepatitis C virus (HCV) infection by blocking virus cell entry PLoS One, 6: e26637

Denolly, S., Granier, C., Fontaine, N., Pozzetto, B., Bourlet, T., Guérin, M., Cosset, F-L. (2019) A serum protein factor mediates maturation and apoB-association of HCV particles in the extracellular milieu J. Hepatol., 70, 626–638

Merz, A., Long, G., Hiet, M-S., Brügger, B., Chlanda, P., Andre, P., Wieland, F., Krijnse-Locker, J. and Bartenschlager, R. (2011) Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome J. Biol. Chem., 286, 3018-3032

Shimizu, Y., Hishiki, T., Sugiyama, K., Ogawa, K., Funami, K., Kato, A., Ohsaki, Y., Fujimoto, T., Takaku, H. and Shimotohno, K. (2010) Lipoprotein lipase and hepatic triglyceride lipase reduce the infectivity of hepatitis C virus (HCV) through their catalytic activities on HCV-associated lipoproteins Virology, 407, 152-159

Shimizu, Y., Hishiki, T., Ujino, S., Sugiyama, K., Funami, K. and Shimotohno, K. (2011) Lipoprotein component associated with hepatitis C virus is essential for virus infectivity Curr. Opin. Virol., 1, 19–26

Shirasaki, T., Honda, M., Shimakami, T., Horii, R., Yamashita, T., Sakai, Y., Sakai, A. et al (2013) MicroRNA27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells J. Virol., 87, 5270–5286

Yamane, D., McGivern, D.R., Wauthier, E., Yi, M., Madden, V.J., Welsch, C., Antes, I., Wen, Y., Chugh, P.E., McGee, C.E. et al (2014) Regulation of the hepatitis C virus RNA replicase by endogenous lipid peroxidation Nature Med., 20, 927-935

4c-18. Mi-RNAs

Bourhill, T., Arbuthnot, P. and Ely, A. (2016) Successful disabling of the 5’UTR of HCV using adenoassociated viral vectors to deliver modular multimeric primary microRNA mimics J. Virol. Meth., 235, 26–33

Shirasaki, T., Honda, M., Shimakami, T., Horii, R., Yamashita, T., Sakai, Y., Sakai, A., Okada, H. et al (2013) MicroRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells J. Virol., 87, 5270–5286

4c-19. Morphology

Lussignol, M., Kopp, M., Molloy, K., Vizcay-Barrena, G., Fleck, R.A., Dorner, M., Bell, K.L., Chait, B.T., Rice, C.M. and Catanese, M.T. (2016) Proteomics of HCV virions reveals an essential role for the nucleoporin Nup98 in virus morphogenesis Proc. Natl. Acad. Sci. USA, 113, 2484-2489

Pène, V., Lemasson, M., Harper, F., Pierron, G. and Rosenberg, A. (2017) Role of cleavage at the core-E1 junction of hepatitis C virus polyprotein in viral morphogenesis PLoS One, 12: e0175810

Romero-Brey, I., Merz, A., Chiramel, A., Lee, J-Y., Chlanda, P., Haselman, U., Santarella-Mellwig, R. et al (2012) Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication PLoS Pathog., 8: e1003056

Yu, X., Qiao, M., Atanasov, I., Hu, Z., Kato, T., Liang, T.J. and Zhou, Z.H. (2007) Cryo-electron microscopy and three-dimensional reconstructions of hepatitis C virus particles Virology, 126, 126-134

4c-20. NS5A protein

Eyre, N.S., Aloia, A.L., Joyce, M.A., Chulanetra, M., Tyrrell, D.L. and Beard, M.R. (2017) Sensitive luminescent reporter viruses reveal appreciable release of hepatitis C virus NS5A protein into the extracellular environment Virology, 507, 20–31

Salloum, S., Wang, H., Ferguson, C., Parton, R.G. and Tai1, A.W. (2013) Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets PLoS Pathog., 9: e1003513

Shanmugam, S., Nichols, A.K., Saravanabalaji, D., Welsch, C. and Yi, MK. (2018) HCV NS5A dimer interface residues regulate HCV replication by controlling its selfinteraction, hyperphosphorylation, subcellular localization and interaction with cyclophilin A PLoS Pathog., 14: e1007177

Yin, C., Goonawardane, N., Stewart, H. and Harris, M. (2018) A role for domain I of the hepatitis C virus NS5A protein in virus assembly PloS Pathog., 14: e1006834

4c-21. Nuclear factor a

Vallianou, I., Dafou, D., Vassilaki, N., Mavromara, P., Hadzopoulou-Cladaras, M. (2016) Hepatitis C virus suppresses Hepatocyte Nuclear Factor 4 alpha, a keyregulator of hepatocellular carcinoma Int. J. Biochem. Cell Biol., 78, 315–326

4c-22. Particle heterogeneity

Andreo, U., de Jong, Y.P., Scull, M.A., Xiao, J.W., Vercauteren, K., Quirk, C., Mommersteeg, M.C., Bergaya, S. et al (2017) Analysis of hepatitis C virus particle heterogeneity in immunodeficient human liver chimeric fah-/- mice Cell. Mol. Gastroenterol. Hepatol., 4, 405–417

Felmlee, D.J., Sheridan, D.A., Bridge, S.H., Nielsen, S.U., Milne, R.W., Packard, C.J., Caslake, M.J. et al (2010) Intravascular transfer contributes to postprandial increase in numbers of very-low-density hepatitis C virus particles Gastroenterology 139, 1774–1783

Felmlee, D.J., Fauvelle, C., Heydmann, L., Hiet, M-S., Fofana, I., Bartenschlager, R., Stoll-Keller, F., Zeisel, M.B.. Fafi-Kremer, S. and Baumert, T.F. (2013) Hepatitis C virus liver transplantation escape variant is characterized by both enhanced triglyceride-rich lipoprotein association and sensitivity to apoE antibodies J. Hepatol., 58, S468

Mathiesen, C.K., Prentoe, J., Meredith, L.W., Jensen, T.B., Krarup, H., McKeating, J.A., Gottwein, J.M. and Bukha, J. (2015) Adaptive mutations enhance assembly and cell-to-cell transmission of a high-titer hepatitis C virus genotype 5a core-NS2 JFH1-based recombinant J. Virol., 89, 7758-7775

Nielsen, S.U., Bassendine, M.F., Martin, C., Lowther, D., Purcell, P.J., King, B.J., Neely, D., Toms, G.L. (2008) Characterization of hepatitis C RNA-containing particles from human liver by density and size J. Gen. Virol., 89, 2507-2517

Simmonds, P., Becher, P., Collett, M.S., Gould, E.A., Heinz, F.X., Meyers, G., Monath, T., Pletnev, A. et al (2012) Hepacivirus In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses International Committee on Taxonomy of Viruses. Elsevier Inc., pp 1003-1020

Sugiyama, N., Murayama, A., Suzuki, R., Watanabe, N., Shiina, M., Liang, T.J., Wakita, T. and Kato, T. (2014) Single strain isolation method for cell culture-adapted hepatitis C virus by end-point dilution and infection PLoS One, 9: e98168

Thi, V.L.D., Granier, C., Zeisel, M.B., Guérin, M., Mancip, J., Granio, O., Penin, F. et al (2012) Characterization of hepatitis C virus particle subpopulations reveals multiple usage of the scavenger receptor BI for entry steps J. Biol., Chem., 287, 31242–31257

4c-23. Patient sources

Bartolomé, J., López-Alcorocho, J.M., Castillo, I., Rodriguez-Iñigo, E., Quiroga, J.A., Palacios, R. and Carreño, V. (2007) Ultracentrifugation of serum samples allows detection of hepatitis C virus RNA in patients with occult hepatitis C. J. Virol., 81, 7710-7715

Eyre, N.S., Aloia, A.L., Joyce, M.A., Chulanetra, M., Tyrrell, D.L. and Beard, M.R. (2017) Sensitive luminescent reporter viruses reveal appreciable release of hepatitis C virus NS5A protein into the extracellular environment Virology, 507, 20–31

Liu, Z., Zhang, X, Yu, Q. and He, J.J. (2014) Exosome-associated hepatitis C virus in cell cultures and patient plasma Biochem. Biophys. Res. Comm., 455, 218–222
Sheridan, D.A., Bridge, S.H., Crossey, M.M.E., Felmlee, D.J., Fenwick, F.I., Thomas, H.C., Neely, R.D.G.,

Taylor-Robinson, S.D. and Bassendine, M.F. (2014) Omega-3 fatty acids and/or fluvastatin in hepatitis C prior non-responders to combination antiviral therapy – a pilot randomized clinical trial Liver Int., 34, 737–747

4c-24. Phospholipases

Menzel, N., Fischl, W., Hueging, K., Bankwitz, D., Frentzen, A., Haid, S., Gentzsch, J.et al (2012) MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious hepatitis C virus particles PLoS Pathog., 8: e1002829

4c-25. Proteins

Adair, R., Patel, A.H., Corless, L., Griffin, S., Rowlands, D.J. and McCormick, C.J. (2009) Expression of hepatitis C virus (HCV) structural proteins in trans facilitates encapsidation and transmission of HCV subgenomic RNA J. Gen. Virol., 90, 833–842

Bentham, M.J., Foster, T.L., McCormick, C. and Griffin, S. (2013) Mutations in hepatitis C virus p7 reduce both the egress and infectivity of assembled particles via impaired proton channel function J. Gen. Virol., 94, 2236–2248

Lussignol, M., Kopp, M., Molloy, K., Vizcay-Barrena, G., Fleck, R.A., Dorner, M., Bell, K.L., Chait, B.T., Rice, C.M. and Catanese, M.T. (2016) Proteomics of HCV virions reveals an essential role for the nucleoporin Nup98 in virus morphogenesis Proc. Natl. Acad. Sci. USA, 113, 2484-2489

Nielsen, S.U., Bassendine, F., Burt, A.D., Bevitt, D.J. and Toms, G.L. (2004) Characterization of the genome and structural proteins of hepatitis C virus resolved from infected human liver J. Gen. Virol., 85, 1497-1507

Prentoe, J. and Bukh, J. (2011) Hepatitis C virus expressing flag-tagged envelope protein 2 has unaltered infectivity and density, is specifically neutralized by flag antibodies and can be purified by affinity chromatography Virology 409, 148–155

Salloum, S., Wang, H., Ferguson, C., Parton, R.G. and Tai1, A.W. (2013) Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets PLoS Pathog., 9: e1003513

4c-26. Purification

De la Fuente, C. and Catanese, M.T. (2019) Production and purification of cell culture hepatitis C virus In Hepatitis C Virus Protocols, Meth. Mol. Biol., vol. 1911 (ed. Law, M), Springer Science+Business Media LLC New York, pp 105-119

4c-27. Replication

Bankwitz, D., Steinmann, E., Bitzegeio, J., Ciesek, S., Friesland, M., Herrmann, E., Zeisel, M.B., Baumert, T.F., Keck, Z-y., Foung, S.K.H., Pécheur, E.I. and Pietschmann, T. (2010) Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes J. Virol., 84, 5751–5763

Jammart, B., Michelet, M., Pécheur, E-I., Parent, R., Bartosch, B., Zoulim, F. and Durante, D. (2013) Verylow-density lipoprotein (VLDL)-producing and hepatitis C virus replicating HepG2 cells secrete no more lipoviroparticles than VLDL-deficient Huh7.5 cells J. Virol., 87, 5065–5080

Lindenbach, B.D., Evans, M.J., Syder, A.J., Wolk, B., Tellinghuisen, T.L., Liu, C.C., Maruyama, T., Hynes, R.O., Burton, D.R., McKeating, J.A. and Rice, C.M. (2005) Complete replication of hepatitis C virus in cell culture Science, 309, 623-626

Pietschmann, T., Zayas, M., Meuleman, P., Long, G., Appel, N., Koutsoudakis, G., Kallis, S., Leroux-Roels, G., Lohmann, V. and Bartenschlager, R. (2009) Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations PLoS Pathog., 5:e1000475

Salloum, S., Wang, H., Ferguson, C., Parton, R.G. and Tai1, A.W. (2013) Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets PLoS Pathog., 9: e1003513

Shimakami, T., Honda, M., Shirasaki, T., Takabatake, R., Liu, F., Murai, K., Shiomoto, T., Funaki, M. et al (2014) The acyclic retinoid Peretinoin inhibits hepatitis C virus replication and infectious virus release in vitro Sci. Rep., 4: 4688

Shiokawa, M., Fukuhara, T., Ono, C., Yamamoto, S., Okamoto, T., Watanabe, N., Wakita, T. and Matsuura, Y. (2014) Novel permissive cell lines for complete propagation of hepatitis C virus J. Virol., 88, 5578–5594

Shirasaki, T., Honda, M., Shimakami, T., Horii, R., Yamashita, T., Sakai, Y., Sakai, A., Okada, H. et al (2013) MicroRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells J. Virol., 87, 5270–5286

Vassilaki, N., Friebe, P., Meuleman, P., Kallis, S., Kaul, A., Paranhos-Baccalà, G., Leroux-Roels, G., Mavromara, P. and Bartenschlager, R. (2008) Role of the hepatitis C virus core+1 open reading frame and core cis-acting RNA elements in viral RNA translation and replication J. Virol., 82, 11503-11515

4d. Japanese encephalitis virus

Tamura, T., Igarashi, M., Enkhbold, B., Suzuki, T., Okamatsu, M., Ono, C., Mori, H., Izumi, T. et al (2019) In Vivo dynamics of reporter Flaviviridae viruses J. Virol., 93: e01191-19

4e. Pestivirus

Tamura, T., Igarashi, M., Enkhbold, B., Suzuki, T., Okamatsu, M., Ono, C., Mori, H., Izumi, T. et al (2019) In Vivo dynamics of reporter Flaviviridae viruses J. Virol., 93: e01191-19

4f. West Nile virus

Thompson, B.S., Moesker, B., Smit, J.M., Wilschut, J., Diamond, M.S. and Fremont, D.H. (2009) A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes PLoS Pathog., 5:e1000453

Vancini, R., Kramer, L.D., Ribeiro, M., Hernandez, R. and Brown, D. (2013) Flavivirus infection from mosquitoes in vitro reveals cell entry at the plasma membrane Virology 435, 406–414

Vogt, M.R., Moesker, B., Goudsmit, J., Jongeneelen, M., Austin, K., Oliphant, T., Nelson, S., Pierson, T.C., Wilschut, J., Throsby, M. and Diamond, M.S. (2009) Human monoclonal antibodies against West Nile Virus induced by natural infection neutralize at a post-attachment step J. Virol., 83, 6494–6507

4g. Yellow fever virus

Patkar, C.G., Jones, C.T., Chang, Y-h., Warrier, R. and Kuhn, R.J. (2007) Functional requirements of the yellow fever virus capsid protein J. Virol., 81, 6471-6481

4h. Zika virus

Andrade, P., Gimblet-Ochieng, C., Modirian, F., Collins, M., Cárdenas, M., Katzelnick, L.C. Montoya, M., Michlmayr, D., Kuan, G. et al (2019) Impact of pre-existing dengue immunity on human antibody and memory B cell responses to Zika Nat. Commun., 10: 938

Betancourt, D., de Queiroz, N.M.G.P., Xia, T., Ahn, J. and Barber, G.N. (2017) Cutting edge: innate immune augmenting vesicular stomatitis virus expressing Zika virus proteins confers protective immunity J. Immunol., 198, 3023–3028

Garg, H., Mehmetoglu-Gurbuz, T., Ruddy, G.M. and Joshi, A. (2019) Capsid containing virus like particle vaccine against Zika virus made from a stable cell line Vaccine, 37, 7123–7131

Heinzelman, P., Low, A., Simeon, R., Wright, G.A. and Chen, Z. (2019) De novo isolation & affinity maturation of yeast-displayed virion-binding human fibronectin domains by flow cytometric screening against virions J. Biol. Engineer., 13: 76

Taguwa, S., Yeh, M-T., Rainbolt, T.K., Nayak, A., Shao, H., Gestwicki, J.E., Andino, R. and Frydman, J. (2019) Zika virus dependence on host Hsp70 provides a protective strategy against infection and disease Cell Rep., 26, 906–920

5. Hepeviridae

5.1 Hepatitis E

Allweiss, L., Gass, S., Giersch, K., Groth, A., Kah, J., Volz, T., Rapp, G., Schöbel, A. et al (2016) Human liver chimeric mice as a new model of chronic hepatitis E virus infection and preclinical drug evaluation J. Hepatol., 64, 1033–1040

Ankcorn, M.J., Ijaz, S., Haywood, B., Neuberger, J., Elsharkawy, A.M., Maggs, J. and Tedder, R.S. (2018) Confirmation of specificity of reactivity in a solid phase ELISA for the detection of hepatitis E viral antigen improves utility of the assay J. Virol. Meth., 252, 42–48

Behrendt, P., Bremer, B., Todt, D., Brown, R.J.P., Heim, A., Manns, M.P., Steinmann, E. and Wedemeyer, H. (2016) Hepatitis E virus (HEV) ORF2 antigen levels differentiate between acute and chronic HEV infection J. Infect. Dis., 214, 361–368

Bochud, M., Schäfer, W., Roth, N.J. and Ros, C. (2019) Characterization of a quasi-enveloped, fast replicating hepevirus from fish and its use as hepatitis E virus surrogate J. Virol. Meth., 263, 111–119

Capelli, N., Marion, O., Dubois, M., Allart, S., Bertrand-Michel, J., Lhomme, S., Abravanel, F., Izopet, J. and Chapuy-Regaud, S. (2019) Vectorial release of hepatitis E virus in polarized human hepatocytes J. Virol., 93: e01207-18

Chapuy-Regaud, S., Dubois, M., Plisson-Chastang, C., Bonnefois, T., Lhomme, S., Bertrand-Michel, J., You, B., Simoneau, S. et al (2017) Characterization of the lipid envelope of exosome encapsulated HEV particles protected from the immune response Biochimie, 141, 70-79

Emerson, S.U., Nguyen, H.T., Torian, U., Burke, D., Engle, R. and Purcell, R.H. (2010) Release of genotype 1 hepatitis E virus from cultured hepatoma and polarized intestinal cells depends on open reading frame 3 protein and requires an intact PXXP motif J. Virol., 84, 9059–9069

Feng, Z. and Lemon, S.M. (2014) Peek-a-boo: membrane hijacking and the pathogenesis of viral hepatitis Trends Microbiol., 22, 59-64

Izopet, J., Lhomme, S., Chapuy-Regaud, S., Mansuy, J-M., Kamar, N. and Abravanel, F. (2017) HEV and transfusion-recipient risk Transfusion Clinique et Biologique, 24, 176–181

Knegendorf, L., Drave, S.A., Thi, V.L.D., Debing, Y., Brown, R.J.P., Vondran, F.W.R., Resner, K., Friesland, M., Khera, T. et al (2018) Hepatitis E virus replication and interferon responses in human placental cells Hepatol. Comm., 2, 173-187

Marion, O., Capelli, N., Lhomme, S., Dubois, M., Pucelle, M., Abravanel, F., Kamar, N. and Izopet, J. (2019) Hepatitis E virus genotype 3 and capsid protein in the blood and urine of immunocompromised patients J. Infect., 78, 232–240

Montpellier, C. et al (2018) Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein J. Hepatol., 68 (Suppl. 1) Abstr. SAT-386

Montpellier, C., Wychowski, C., Sayed, I.M., Meunier, J-C., Saliou, J-M., Ankavay, M., Bull, A., Pillez, A. et al (2018) Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein Gastroenterology 154, 211–223

Nagashima, S., Takahashi, M., Kobayashi, T., Nishizawa, T.T., Nishiyama, T., Primadharsini, P.P. and Okamoto, H. (2017) Characterization of the quasi-enveloped hepatitis E virus particles released by the cellular exosomal pathway J. Virol., 91: e00822-17

Sayed, I.M., Verhoye, L., Cocquerel, L., Abravanel, F., Foquet, L., Montpellier, C., Debing, Y., Farhoudi, A. Wychowski, C. (2017) Study of hepatitis E virus infection of genotype 1 and 3 in mice with humanised liver Gut 66, 920–929

Sayed, I.M., Verhoye, L., Montpellier, C., Abravanel, F., Izopet, J., Cocquerel, L. and Meuleman, P. (2019) Hepatitis E virus (HEV) open reading frame 2 antigen kinetics in human-liver chimeric mice and its impact on HEV diagnosis J. Infect. Dis., 220, 811–819

Todt, D., Friesland, M., Moeller, N., Praditya, D., Kinast, V., Brüggemann, Y., Knegendorf, L., Burkard, T., Steinmann, J., Burm, R. (2020) Robust hepatitis E virus infection and transcriptional response in human hepatocytes Proc. Natl. Acad. Sci. USA 117, 1731–1741

Von Nordheim, M., Boinay, M., Leisi, R., Kempf, C. and Ros, C. (2016) Cutthroat trout virus—towards a virus model to support hepatitis E research Viruses, 8: 289

Yin, X., Ambardekar, C., Lu, Y. and Feng, Z. (2016) Distinct entry mechanisms for nonenveloped and quasienveloped hepatitis E viruses J. Virol., 90, 4232-4242

6. Nidovirales

6.1 Wobbly possum disease

Giles, J.C., Perrott, M.R. and Dunowska, M. (2015) Primary possum macrophage cultures support the growth of a nidovirus associated with wobbly possum disease J. Virol. Methods, 222, 66–71

Giles, J., Perrott, M., Roe, W. and Dunowska, M. (2016) The aetiologyof wobbly possum disease: Reproduction of the disease with purified nidovirus Virology, 491, 20–26

Giles, J., Perrott, M., Roe, W., Shrestha, K., Aberdein, D., Morel, P. and Dunowska, M. (2018) Viral RNA load and histological changes in tissues following experimental infection with an arterivirus of possums (wobbly possum disease virus) Virology, 522, 73–80

7. Nodaviridae

7.1 Orsay virus

Jiang, H., Franz, C.J., Wu, G., Renshaw, H., Zhao, G., Firth, A.E. and Wang, D. (2014) Orsay virus utilizes ribosomal frameshifting to express a novel protein that is incorporated into virions Virology 450-451, 213–221

8. Picornaviridae

8.1 Coxsackie virus

Müller, L.M.E., Holmes, M., Michael, J.L., Scott, G.B., West, E.J., Scott, K.J., Parrish, C., Hall, K., Stäble, S. et al (2019) Plasmacytoid dendritic cells orchestrate innate and adaptive anti-tumor immunity induced by oncolytic coxsackievirus A21 J. ImmunoTher. Cancer, 7: 164

Petrik, J. (2016) Immunomodulatory effects of exosomes produced by virus-infected cells Transfus. Apher. Sci., 55, 84–91

Robinson, S.M., Tsueng, G., Sin, J., Mangale, V., Rahawi, S., McIntyre, L.L., Williams, W., Kha, N. et al (2014) Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers PLoS Pathog., 10: e1004045

8.2 Hepatitis A

Costafreda, M.I. and Kaplan, G. (2019) Reply to Das et al., “TIM1 (HAVCR1): an essential ‘receptor’ or an ‘accessory attachment factor’ for Hepatitis A virus?” J. Virol., 93, e02040-18

Das, A., Hirai-Yuki, A., González-López, O., Rhein, B., Moller-Tank, S., Brouillette, R., Hensley, L., Misumi, I. et al (2017) TIM1 (HAVCR1) is not essential for cellular entry of either quasi-enveloped or naked hepatitis A virions mBIO, 8: e00969-17

Feng, Z. and Lemon, S.M. (2014) Peek-a-boo: membrane hijacking and the pathogenesis of viral hepatitis Trends Microbiol., 22, 59-64

Feng, Z., Hensley, L., McKnight, K.L., Hu, F., Madden, V., Ping, L-F., Jeong, S-H., Walker, C., Lanford, R.E. and Lemon, S.M. (2013) A pathogenic picornavirus acquires an envelope by hijacking cellular membranes Nature 496, 367-371

Hirai-Yuki, A., Hensley, L., Whitmire, J.K. and Lemon, S.M. (2016) Biliary secretion of quasi-enveloped human hepatitis A virus mBio, 7: e01998-16

Hofer, U. (2013) Cloak and dagger Nat. Rev. Microbiol., 11, 3026

Kapsch, A-M., Farcet, M.R., Antoine, G. and Kreil, T.R. (2017) A nonenveloped virus with a lipid envelope: hepatitis A virus as used in virus-reduction studies Transfusion 57, 1433–1439

McKnighta, K.L., Xiec, L., González-Lópeza, O., Rivera-Serrano, E.E., Chen, X. and Lemon, S.M. (2017) Protein composition of the hepatitis A virus quasi-envelope Proc. Natl. Acad. Sci. USA, 114, 6587–6592

Vaughan, G., Goncalves Rossi, L.M., Forbi, J.C., de Paula, V.S, Purdy, M.A., Xia, G. and Khudyakov, Y.E. (2014) Hepatitis A virus: Host interactions, molecular epidemiology and evolution Infect. Genet. Evol., 21, 227–243

8.3 Human enterovirus

Liu, Y., Sheng, J., van Vliet, A.L.W., Buda, G., van Kuppeveld, F.J.M. and Rossmann, M.G. (2018) Molecular basis for the acid-initiated uncoating of human enterovirus D68 Proc. Natl. Acad. Sci. USA, 115, E12209–E12217

8.4 Kobuviruses

Canh, V.D., Kasuga, I., Furumai, H. and Katayama, H. (2019) Viability RT-qPCR combined with sodium deoxycholate pre-treatment for selective quantification of infectious viruses in drinking water samples Food Environ. Virol., 11, 40–51

8.5 Rhinovirus

Simpson, J.L., Carroll, M., Yang, I.A., Reynolds, P.N., Hodge, S., James, A.L., Gibson, P.G. and Upham, J.W. (2016) Reduced antiviral interferon production in poorly controlled asthma is associated with neutrophilic inflammation and high-dose inhaled corticosteroids Chest, 149, 704-713

Xi, Y., Finlayson, A., White, O.J., Carroll, M.L., and Upham, J.W. (2015) Rhinovirus stimulated IFN-α production: how important are plasmacytoid DCs, monocytes and endosomal pH? Clin. Translat. Immunol., 4, e46

9. Picornavirales Secoviridae

9.1 Cowpea mosaic virus

Thuenemann, E.C., Meyers, A.E., Verwey, J., Rybicki, E.P. and Lomonossoff, G.P. (2013) A method for rapid production of heteromultimeric protein complexes in plants: assembly of protective bluetongue virus-like particles Plant Biotechnol. J. 11, 839–846

10. Porcine sapelovirus

Li, Y., Du, L., Jin, T., Cheng, Y., Zhang, X., Jiao, S., Huang, T., Zhang, Y. et al (2019) Characterization and epidemiological survey of porcine sapelovirus in China Vet. Microbiol., 232, 13–21

11. Togaviridae

11.1 Alphavirus

Akahata, W. and Nabel, G. J. (2012) A specific domain of the Chikungunya virus E2 protein regulates particle formation in human cells: implications for alphavirus vaccine design J. Virol., 86, 8879-8883

Jin, J., Sherman, M.B., Chafets, D., Dinglasan, N., Lu, K., Lee, T-H., Carlson, L-A., Muench, M.O. and Simmons, G. (2018) An attenuated replication-competent chikungunya virus with a fluorescently tagged envelope PLoS Negl. Trop. Dis., 12: e0006693

Jose, J., Przybyla, L., Edwards, T.J., Perera, R., Burgner II, J.W. and Kuhn, R.J. (2012) Interactions of the cytoplasmic domain of Sindbis virus E2 with nucleocapsid cores promote alphavirus budding J. Virol., 86, 2585-2599

Snyder, J.E., Azizgolshani, O., Wu, B., He, Y., Lee, A.C., Jose, J., Suter, D.M., Knobler, C.M., Gelbart, W.M. and Kuhn, R.J. (2011) Rescue of infectious particles from preassembled alphavirus nucleocapsid cores J. Virol., 85, 5773–5781

Snyder, J.E., Berrios, C.J., Edwards, T.J., Jose, J., Perera, R. and Kuhn, R.J. (2012) Probing the early temporal and spatial interaction of the Sindbis virus capsid and E2 proteins with reverse genetics J. Virol., 86, 12372-12383

Snyder, J.E., Kulcsar, K.A., Schultz, K.L.W., Riley, C.P., Neary, J.T., Marr, S., Jose, J., Griffin, D.E. and Kuhn, R.J. (2013) Functional characterization of the alphavirus TF protein J. Virol., 87, 8511–8523

Sokoloski, K.J., Snyder, A.J., Liu, N.H., Hayes, C.A., Mukhopadhyay, S. and Hardy, R.W. (2013) Encapsidation of host-derived factors correlates with enhanced infectivity of Sindbis virus J. Virol., 87, 12216–12226

Tang, J., Jose, J., Chipman, P., Zhang, W., Kuhn, R.J. and Baker, T.S. (2011) Molecular links between the E2 envelope glycoprotein and nucleocapsid core in sindbis virus J. Mol. Biol., 414, 442–459

Urakami, A., Sakurai, A., Ishikawa, M., Yap, M.L., Flores-Garcia, Y., Haseda, Y., Aoshi, T., Zavala, F.P. et al (2017) Development of a novel virus-like particle vaccine platform that mimics the immature form of alphavirus Clin. Vacc. Immunol., 24: e00090-17

Yap, M.L., Klose, T., Urakamic, A., Hasana, S.S., Akahata, W. and Rossmann, M.G. (2017) Structural studies of Chikungunya virus maturation Proc. Natl. Acad. Sci., 114, 13703–13707

Chikungunya virus – see 11.1 Alphavirus

11.2 Rubella virus

Battisti, A.J., Yoder, J.D., Plevka, P., Winkler, D.C., Prasad, V.M., Kuhn, R.J., Frey, T.K., Steven, A.C. and Rossmann, M.G. (2012) Cryo-electron tomography of rubella virus J. Virol., 86, 11078-11085

11.3 Semliki Forest virus

Hammarstedt, M., Wallengren, K., Pedersen, K.W., Roos, N. and Garoff, H. (2000) Minimal exclusion of plasma membrane proteins during retrovirus envelope formation Proc. Natl. Acad. Sci. USA, 97, 7527-7532

Kalvodova, L., Sampaio, J.L., Cordo, S., Ejsing, C.S., Shevchenko, A. and Simons, K. (2009) The lipidomes of vesicular stomatitis virus, Semliki Forest virus and the host plasma membrane analyzed by quantitative shotgun mass spectrometry J. Virol., 83, 7996-8003

Sjøberg, M. and Garoff, H. (2003) Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion J. Virol., 77, 3441-3450

Sindbis virus – see 11.1 Alphavirus

11.4 Venezuelan/eastern equine encephalitis virus

Hasan, S.S., Sun, C., Kim, A.S., Watanabe, Y., Chen, C-L., Klose, T., Buda, G., Crispin, M., Diamond, M.S., Klimstra, W.B. and Rossmann, M.G. (2018) Cryo-EM structures of eastern equine encephalitis virus reveal mechanisms of virus disassembly and antibody neutralization Cell Rep., 25, 3136–3147

Jurgens, C.K., Young, K.R., Madden, V.J., Johnson, P.R. and Johnston, R.E. (2012) A novel self-replicating chimeric lentivirus-like particle J. Virol., 86, 246-261

Ko, S-Y., Akahata, W., Yang, E.S., Kong, W-P., Burke, C.W., Honnold, S.P., Nichols, D.K., Huang, Y-J.S., Schieber, G.L., Carlton, K. et al (2019) A virus-like particle vaccine prevents equine encephalitis virus infection in nonhuman primates Sci. Transl. Med., 11: eaav3113

Lamb, K., Lokesh, G.L., Sherman, M. and Watowich, S. (2010) Structure of a Venezuelan equine encephalitis virus assembly intermediate isolated from infected cells Virology 406, 261–269

Porta, J., Jose, J., Roehrig, J.T., Blair, C.D., Kuhn, R.J. and Rossmann, M.G. (2014) Locking and blocking the viral landscape of an alphavirus with neutralizing antibodies J. Virol., 88, 9616–9623

12. Tombusviridae (Dianthovirus)

12.1 Red clover mosaic virus

Lockney, D.M., Guenther, R.N., Loo, L., Overton, W., Antonelli, R., Clark, J., Hu, M., Luft, C., Lommel, S.A. and Franzen, S. (2011) The Red clover necrotic mosaic virus capsid as a multifunctional cell targeting plant viral nanoparticle Bioconjugate Chem. 22, 67–73

Lockney, D., Franzen, S. and Lommel, S. (2011) Viruses as nanomaterials for drug delivery In Biomedical Nanotechnology: Methods and Protocols, Methods Mol. Biol., 726 (ed. Hurst, S.J.), Springer Science+Business Media, pp 207-221

OptiPrep™ Reference List RV04: 4th edition, January 2020

OptiPrep™ Reference List RV05

GROUP V VIRUSES

• Viruses are listed alphabetically within the Baltimore scheme: Family, Genus and Species. Publications are listed alphabetically by first author and, where necessary, references are further divided according to research topic
• Multiple entries from the same first author are listed chronologically.
• For a detailed methodology of Group V viruses see OptiPrep™ Application Sheets V23-V28. V06 is a methodological review of OptiPrep™ technology.

 

1 Arenaviridae

Arenavirus

Junin virus
Chou, Y-y., Cuevas, C., Carocci, M., Stubbs, S.H., Ma, M., Cureton, D.K., Luke Chao, L., Evesson, F. et al (2016) Identification and characterization of a novel broad-spectrum virus entry inhibitor J. Virol., 90, 4494- 4510

Gaudin, R. and Barteneva, N.S. (2015) Sorting of small infectious virus particles by flow virometry reveals distinct infectivity profiles Nat. Commun, 6: 6022

Gaudin, R. and Kirchhausen, T. (2015) Superinfection exclusion is absent during acute Junin virus infection of Vero and A549 cells Sci. Rep., 5: 15990

Lassa virus
Baird, N.L., York, J. and Nunberg, J.H. (2012) Arenavirus infection induces discrete cytosolic structures for RNA replication J. Virol., 86, 11301-11310

Eichler, R., Lenz, O., Strecker, T. and Garten, W. (2003) Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length FEBS Lett., 538, 203-206

Lenz, O., Ter Meulen, J., Feldmann, H., Klenk, H-D. and Garten, W. (2000) Identification of a novel consensus sequence at the cleavage site of the Lassa virus glycoprotein J. Virol., 74, 11418-11421

Strecker, T., Eichler, R., ter Meulen, J., Weissenhorn, W., Klenk, H.D., Garten, W. and Lenz, O. (2003) Lassa virus Z protein is a matrix protein sufficient for the release of virus-like particles J. Virol., 77, 10700-10705

Ziegler, C.M., Eisenhauer, P., Bruce, E.A., Weir, M.E., King, B.R., Klaus, J.P., Krementsov, D.N. et al (2016) The lymphocytic choriomeningitis virus matrix protein PPXY late domain drives the production of defective interfering particles PLoS Pathog., 12: e1005501

2 Bunyaviridae

Bunyamweravirus

Ariza, A., Tanner, S.J., Walter, C.T., Dent, K.C., Shepherd, D.A., Wu, W., Matthews, S.V., Hiscox, J.A., Green, T.J. et al (2013) Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization Nucleic Acids Res., 41, 5912–5926

Cabezas, P. and Risco, C. (2006) Studying cellular architecture in three dimensions with improved resolution: Ta replicas revisited Cell Biol. Int., 30, 747-754

Hover, S., Foster, B., Fontana, J., Kohl, A., Goldstein, S.A.N., Barr, J.N. and Mankouri, J. (2018) Bunyavirus requirement for endosomal K+ reveals new roles of cellular ion channels during infection PLoS Pathog 14: e1006845

Novoa, R.R., Calderita, G., Cabezas, P., Elliott, R.M. and Risco, C. (2005) Key Golgi factors for structural and functional maturation of bunyamwera virus J. Virol., 79, 10852-10863

Hantavirus

Bisoffi, M., Hjelle, B., Brown, D.C., Branch, D.W., Edwards, T.L., Brozik, S.M., Bondu-Hawkins, V.S. and Larson, R.S. (2008) Detection of viral bioagents using a shear horizontal surface acoustic wave biosensor Biosens. Bioelectron., 23, 1397-1403

Buranda, T., Wu, Y., Perez, D., Jett, S.D., BonduHawkins, V., Ye, C., Edwards, B., Hall, P., Larson, R.S., Lopez, G.P., Sklar, L.A. and Hjelle, B. (2010) Recognition of decay accelerating factor and avb3 by inactivated hantaviruses: Toward the development of high-throughput screening flow cytometry assays Anal. Biochem., 402, 151–160

Guo, Y., Wang, W., Sun, Y., Ma, C., Wang, X., Wang, X., Liu, P., Shen, S. et al (2016) Crystal structure of the core region of hantavirus nucleocapsid protein reveals the mechanism for ribonucleoprotein complex formation J. Virol., 90, 1048-1061

Hall, P.R., Hjelle, B., Brown, D.C., Ye, C., Bondu-Hawkins, V., Kilpatrick, K.A. and Larson, R.S. (2008) Multivalent presentation of anti-hantavirus peptides on nanoparticles enhances infection blockade Antimicrob. Agents Chemother., 52, 2079-2088

Huiskonen, J.T., Hepojoki, J., Laurinmäki, P., Vaheri, A., Lankinen, H., Butcher, S.J. and Grünewald, K. (2010) Electron cryotomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses J. Virol., 84, 4889–4897

Li, S., Rissanen, I., Zeltina, A., Hepojoki, J., Raghwani, J., Harlos, K., Pybus, O.G., Huiskonen, J.T. and Bowden, T.A. (2016) A molecular-level account of the antigenic hantaviral surface Cell Rep., 15, 959–967

Prescott, J.B., Hall, P.R., Bondu-Hawkins, V.S., Ye, C. and Hjelle, B. (2007) Early innate immune responses to Sin Nombre Hantavirus occur independently of IFN regulatory factor 3, characterized pattern recognition receptors and viral entry J. Immunol., 179, 1796-1802

Nairoviridae

Surtees, R., Dowall, S.D., Shaw, A., Armstrong, S., Hewson, R., Carroll, M.W., Mankouri, J., Edwards, T.A., Hiscox, J.A. and Barr. J.N. (2016) Heat shock protein 70 family members interact with Crimean-Congo hemorrhagic fever virus and Hazara virus nucleocapsid proteins and perform a functional role in the nairovirus replication cycle J. Virol., 90, 9305-9326

Wang, X., Li, B., Guo, Y., Shen, S., Zhao, L., Zhang, P., Sun, Y., Sui, S-F., Deng, F. and Lou, Z. (2016) Molecular basis for the formation of ribonucleoprotein complex of Crimean-Congo hemorrhagic fever virus J. Struct. Biol., 196, 455–465

Phlebovirus

Freiberg, A.N., Sherman, M.B., Morais, M.C., Holbrook, M.R. and Watowich, S.J. (2008) Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography J. Virol., 82, 10341-10348

Mbewana, S., Myers, A.E., Rybicki, E.P. (2019) Chimaeric rift valley fever virus-like particle vaccine candidate production in Nicotiana benthamiana Biotechnol. J., 14: 1800238

Weingart, H.M., Zhang, S., Marszal, P., McGreevy, A., Burton, L. and Wilson, W.C. (2014) Rift valley fever virus incorporates the 78 kDa glycoprotein into virions matured in mosquito C6/36 cells PLoS One, 9: e87385

Wolf, M.C., Freiberg, A.N., Zhang, T., Akyol-Ataman, Z., Grock, A., Hong, P.W., Li, J., Watson, N.F., et al (2010) A broad-spectrum antiviral targeting entry of enveloped viruses Proc. Natl. Acad. Sci. USA, 107, 3157–3162

3 Deltavirus

Hepatitis D
Perez-Vargas, J., Amirache, F., Boson, B., Mialon, C., Freitas, N., Sureau, C., Fusil, F. and Cosset, F-L. (2019) Enveloped viruses distinct from HBV induce dissemination of hepatitis D virus in vivo Nature Comm., 10: 2098

Verrier, E.R., Colpitts, C.C., Bach, C., Heydmann, L., Weiss, A., Renaud, M., Durand, S.C., Habersetzer, F., Durante, D. et al (2016) A targeted functional RNA interference screen uncovers glypican 5 as an entry factor for hepatitis B and D viruses Hepatology, 36, 35-48

4 Filoviridae

Ebola virus

Gélinas, J-F., Azizi, H., Kiesslich, S., Lanthier, S., Perdersen, J., Chahal, P.S., Ansorge, S., Kobinger, G. et al (2019) Production of rVSV-ZEBOV in serum-free suspension culture of HEK 293SF cells Vaccine, 37, 6624–6632

Huang, Y., Xu, L., Sun, Y. and Nabel, G.J. (2002) The assembly of Ebola virus nucleocapsid requires virionassociated proteins 35 and 24 and posttranslational modification of nucleoprotein Mol. Cell, 10, 307-316

Kim, J-O., Chakrabarti, B.K., Guha-Niyogi, A., Louder, M.K., Mascola, J.R., Ganesh, L. and Nabel, G.J. (2007) Lysis of human immunodeficiency virus type 1 by a specific secreted human phospholipase A2 J. Virol., 81, 1441-1450

Pastor, A.R., González-Domínguez, G., Díaz-Salinas, M.A., Ramírez, O.T. and Palomares, L.A. (2019) Defining the multiplicity and time of infection for the production of Zaire Ebola virus-like particles in the insect cell-baculovirus expression system Vaccine 37, 6962–6969

5 Orthomyxoviridae

Influenza virus
Bungener, L., Serre, K., Bijl, L., Leserman, L., Wilschut, J., Daemen, T. and Machy, P. (2002) Virosomemediated delivery of protein antigens to dendritic cells Vaccine, 20, 2287-2295

Bungener, L., Huckreide, A., de Mare, A., de Vries-Idema, J., Wilschut, J. and Daemen, T. (2005) Virosomemediated delivery of protein antigens in vivo: efficient induction of class I MHC-restricted cytotoxic T lymphocyte activity Vaccine, 23, 1232-1241

Chlanda, P., Mekhedov, E., Waters, H., Sodt, A., Schwartz, C., Nair, V., Blank, P.S. and Zimmerberg, J. (2017) Palmitoylation contributes to membrane curvature in influenza A virus assembly and hemagglutininmediated membrane fusion J. Virol. 91, e00947-17

Chou, Y-Y., Vafabakhsh, R., Doganay, S., Gao, Q., Ha, T. and Palese (2012) One influenza virus particle packages eight unique viral RNAs as shown by FISH analysis Proc. Natl. Acad. Sci. USA, 109, 9101–9106

Das, D.K., Govindan, R., Nikić-Spiegel, I., Krammer, F., Lemke, E.A. and Munro, J.B. (2018) Direct visualization of the conformational dynamics of single influenza hemagglutinin trimers Cell, 174, 926–937

Galarza, J.M., Latham, T. and Cupo, A. (2005) Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge Viral Immunol., 18, 244-251

Galarza, J.M., Latham, T. and Cupo, A. (2005) Virus like particle vaccine conferred complete protection against a lethal influenza virus challenge Viral Immunol., 18, 365-372

Herbert, A.S., Heffron, L., Sundick, R. and Roberts, P.C. (2009) Incorporation of membrane-bound, mammalian-derived immunomodulatory proteins into influenza whole virus vaccines boosts immunogenicity and protection against lethal challenge Virol. J., 6:42

Hutchinson, E.C., Charles, P.D., Hester, S.S., Thomas, B., Trudgian, D., Martınez-Alonso, M. and Fodor, E. (2014) Conserved and host-specific features of influenza virion architecture Nat. Commun., 5: 4816

Hutchinson, E.C. and Stegmann, M. (2018) Purification and proteomics of influenza virions In Influenza Virus Methods and Protocols, Meth. Mol. Biol., vol. 1836 (ed. Yamauchi, Y.) Springer Science+Business Media New York LLC, pp 89-120

Khan, T., Heffron, C.L., High, K.P. and Roberts, P.C. (2014) Tailored vaccines targeting the elderly using whole inactivated influenza vaccines bearing cytokine immunomodulators J. Interferon Cytokine Res., 34,129-139

Latham, T. and Galarza, J.M. (2001) Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins J. Virol., 75, 6154-6165

LeBouder, F., Morello, E., Rimmelzwaan, G.F., Bosse, F., Pechoux, C., Delmas, B. and Riteau, B. (2008) Annexin II incorporated into influenza virus particles supports virus replication by converting plasminogen into plasmin J. Virol., 82, 6820-6828

Le Rua, A., Jacob, D., Transfiguracion, J., Ansorge, S., Henry, O. and Kamena, A.A. (2010) Scalable production of influenza virus in HEK-293 cells for efficient vaccine manufacturing Vaccine, 28, 3661–3671

Makarkov, A.I., Patel, A.R., Bainov, V. and Ward, B.J. (2018) A novel serological assay for influenza based on DiD fluorescence dequenching that is free from observer bias and potentially automatable – A proof of concept study Vaccine, 36, 4485–4493

Matassov, D., Cupo, A. and Galarza, J.M. (2007) A novel intranasal virus-like particle (VLP) vaccine designed to protect against the pandemic 1918 influenza A virus (H1N1) Viral Immunol., 20, 441-452

Shaw, M.L., Stone, K.L., Colangelo, C.M., Gilcicek, E.E. and Palese, P. (2008) Cellular proteins in influenza virus particles PLoS Pathog., 4:e1000085

Smith, T., O’Kennedy, M.M., Wandrag, D.B.R., Adeyemi, M. and Abolnik, C. (2020) Efficacy of a plantproduced virus-like particle vaccine in chickens challenged with Influenza A H6N2 virus Plant Biotech. J., 18, 502–512

Speshock, J.L., Doyon-Reale, N., Rabah, R., Neely, M.N. and Roberts, P.C. (2007) Filamentous influenza virus A infection predisposes mice to fatal septicemia following superinfection with Streptococcus pneumoniae Serotype 3 Infect. Immun., 75, 3102-3111

Su, W-C., Yu, W-Y., Huang, S-H. and Laia, M.M.C. (2018) Ubiquitination of the cytoplasmic domain of influenza A virus M2 protein is crucial for production of infectious virus particles J. Virol., 92: e01972-17

Sulli, C., Banik, S.S.R., Schilling, J., Moser, A., Xiang, X., Payne, R., Wanless, A., Willis, S.H., Paes, C., Rucker, J.B. and Doranz, B.J. (2013) Detection of proton movement directly across viral membranes to identify novel influenza virus M2 inhibitors J. Virol., 87, 10679-10686

Thompson, C.M., Petiot, E., Lennaertz, A., Henry, O. and Kamen, A.A. (2013) Analytical technologies for influenza virus-like particle candidate vaccines: challenges and emerging approaches Virol. J. 10: 141

Thompson, C.M., Petiot, E., Mullick, A., Aucoin, M.G., Henry, O. and Kamen, A.A. (2015) Critical assessment of influenza VLP production in Sf9 and HEK293 expression systems BMC Biotechnol., 15: 31

Yang, X., Steukers, L., Forier, K., Xiong, R., Braeckmans, K., Van Reeth, K. and Nauwynck, H. (2014) A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus PLoS One, 9: e110026

Yang, Y., Leggat, D., Herbert, A., Roberts, P.C. and Sundick, R.S. (2009) A novel method to incorporate bioactive cytokines as adjuvants on the surface of virus particles J. Interferon Cytokine Res., 29, 9-23

6 Paramyxoviridae

Henipavirus
Akiyama, H., Miller, C., Patel, H.V., Hatch, S.C., Archer, J., Ramirez, N-G.P. and Gummuluru, S. (2014) Virus particle release from glycosphingolipid-enriched microdomains is essential for dendritic cell-mediated capture and transfer of HIV-1 and Henipavirus J. Virol., 88, 8813–8825

Paramyxovirinae

Avlulavirus
Newcastle disease virus

Biswas, M., Johnson, J.B., Kumar, S.R.P., Parks, G.D. and Subbiaha, E. (2012) Incorporation of host complement regulatory proteins into Newcastle disease virus enhances complement evasion J. Virol., 86, 12708-12716

Morbillivirus
Measles virus
Brindley, M.A. and Plemper, R.K. (2010) Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H J. Virol., 84, 12174-12184

Liljeroos, L., Huiskonen, J.T., Ora, A., Susi, P. and Butcher, S.J. (2011) Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions Proc. Natl. Acad. Sci. USA, 108, 18085–18090

Hallak, L.K., Merchan, J.R., Storgard, C.M., Loftus, J.C. and Russell, S.J. (2005) Targeted measles virus vector displaying echistatin infects endothelial cells via v3 and leads to tumor regression Cancer Res., 65, 5292-5300

Pneumovirinae
Human respiratory syncytial virus
Gias, E., Nielsen, S.U., Morgan, L.A.F. and Toms, G.L. (2008) Purification of human respiratory syncytial virus by ultracentrifugation in iodixanol density gradient J. Virol. Methods, 147, 328-332

Murawski, M.R., Bowen, G.N., Cerny, A.M., Anderson, L.J., Haynes, L.M., Tripp, R.A., Kurt-Jones, E.A. and Finberg, R.W. (2009) Respiratory syncytial virus activates innate immunity through Toll-Like receptor 2 J. Virol., 83, 1492-1500

Respirovirus
Swine paramyxovirus
Qiao, D., Janke, B.H. and Elankumaran, S. (2009) Molecular characterization of glycoprotein genes and phylogenetic analysis of two swine paramyxoviruses isolated from United States Virus Genes, 39, 53–65

6 Rhabdoviridae

Lyssavirus
Rabies virus
Chatterjee, S., Sullivan, H.A., MacLennan, B.J., Xu, R., Hou, Y.Y., Lavin, T.K., Lea, N.E., Michalski, J.E., Babcock, K.R. et al (2018) Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons Nat. Neurosci., 638, 638–646

Finke, S. and Conzelmann, K-K. (2003) Dissociation of rabies virus matrix protein functions in regulation of viral RNA synthesis and virus assembly J. Virol., 77, 12704-12082

Finke, S., Brzozka, K. and Conzelmann, K-K. (2004) Tracking fluorescence-labeled rabies virus: enhanced green fluorescent protein-tagged phosphoprotein P supports virus gene expression and formation of infectious particles J. Virol., 78, 12333-12343

Fontana, D., Kratje, R., Etcheverrigaray, M. and Prieto, C. (2015) Immunogenic virus-like particles continuously expressed inmammalian cells as a veterinary rabies vaccine candidate Vaccine, 33, 4238–4246

Fontana, D., Etcheverrigaray, M., Kratje, R. and Prieto, C. (2016) Development of rabies virus-like particles for vaccine applications: production, characterization, and protection studies In Vaccine Design: Methods and Protocols, Vol. 1: Vaccines for Human Diseases, Methods in Molecular Biology, vol. 1403 (ed. Thomas, S.) Springer Science+Business Media New York pp 155-166

Fontana, D., Marsili, F., Garay, E., Battagliotti, J., Etcheverrigaray, M., Kratje, R. and Prieto, C. (2019) A simplified roller bottle platform for the production of a new generation VLPs rabies vaccine for veterinary applications Comp. Immunol. Microbiol. Infect. Dis., 65, 70–75

Hidaka, Y., Lim, C-K., Takayama-Ito, M., Park, C-H., Kimitsuki, K., Shiwa, N., Inoue, K-i., Itou, T. (2018) Segmentation of the rabies virus genome Vir. Res., 252, 68–75

Klingen, Y., Conzelmann, K-K. and Finke, S. (2008) Double-labeled rabies virus: live tracking of enveloped virus transport J. Virol., 82, 237-245

Marschalek A., Drechsel, L. amd Conzelmann, K-K. (2012) The importance of being short: The role of rabies virus phosphoprotein isoforms assessed by differential IRES translation initiation Eur. J. Cell Biol., 91, 17– 23

Vesiculovirus
Vesicular stomatitis virus
Andreu-Moreno, I. and Sanjuán, R. (2018) Collective infection of cells by viral aggregates promotes early viral proliferation and reveals a cellular-level Allee effect Curr, Biol., 28, 3212–3219

Arulanandam, R., Batenchuk, C., Varette, O., Zakaria, C., Garcia, V., Forbes, N.E., Davis, C. Krishnan, R. et al (2015) Microtubule disruption synergizes with oncolytic virotherapy by inhibiting interferon translation and potentiating bystander killing Nat. Commun., 6: 6410

Betancourt, D., Ramos, J.C. and Barber, G.N. (2015) Retargeting oncolytic vesicular stomatitis virus to human T-cell lymphotropic virus Type 1-associated adult T-cell leukemia J. Virol., 89, 11786-11800

Betancourt, D., de Queiroz, N.M.G.P., Xia, T., Ahn, J. and Barber, G.N. (2017) Cutting edge: innate immune augmenting vesicular stomatitis virus expressing Zika virus proteins confers protective immunity J. Immunol., 198, 3023–3028

Beug, S.T., Beauregard, C.E., Healy, C., Sanda, T., St-Jean, M., Chabot, J., Walker, D.E., Mohan, A., Earl, N. et al (2017) Smac mimetics synergize with immune checkpoint inhibitors to promote tumour immunity against glioblastoma Nat. Comm., 8: 14278

Beug, S.T., Pichette, S.J., St-Jean, M., Holbrook, J., Walker, D.E., LaCasse, E.C. and Korneluk, R.G. (2018) Combination of IAP antagonists and TNF-α-armed oncolytic viruses induce tumor vascular shutdown and tumor regression Mol. Ther: Oncolytics, 10, 28-39

Cuevas, J.M., Durán-Moreno, M. and Sanjuán, R. (2017) Multi-virion infectious units arise from free viral particles in an enveloped virus Nat. Microbiol., 2: 17078

Diallo, J-S., Le Boeuf, F., Lai, F., Cox, J., Vaha-Koskela, M., Abdelbary, H., MacTavish, H., Waite, K., Falls, T. et al (2010) A high-throughput pharmacoviral approach identifies novel oncolytic virus sensitizers Mol. Ther., 18, 1123-1129

Diallo, J-S., Vähä-Koskela, M., Le Boeuf, F. and Bell, J. (2011) Propagation, purification, and in vivo testing of oncolytic vesicular stomatitis virus strains In Methods Mol. Biol., 797, Oncolytic Viruses: Methods and Protocols, (ed. Kirn, D.H. et al.), Springer Science+Business Media, pp 127-140

Domingo-Calap, P., Segredo-Otero, E., Durán-Moreno, M. and Sanjuán, R. (2019) Social evolution of innate immunity evasion in a virus Nat. Microbiol., 4, 1006–1013

Dornan, M.H., Krishnan, R., Macklin, A.M., Selman, M., El Sayes, N., Son, H.H., Davis, C., Chen, A., Keillor, K., Le, P.J. et al (2016) First-in-class small molecule potentiators of cancer virotherapy Sci. Rep., 6: 26786

Garijo, R., Hernández-Alonso, P., Rivas, C., Diallo, J-S. and Sanjuán, R. (2014) Experimental evolution of an oncolytic vesicular stomatitis virus with increased selectivity for p53-deficient cells PLoS One, 9: e102365

Gélinas, J-F., Azizi, H., Kiesslich, S., Lanthier, S., Perdersen, J., Chahal, P.S., Ansorge, S., Kobinger, G. et al (2019) Production of rVSV-ZEBOV in serum-free suspension culture of HEK 293SF cells Vaccine, 37, 6624–6632

Hastie, E., Besmer, D.M., Shah, N.R., Murphy, A.M., Moerdyk-Schauwecker, M., Molestina, C., Das Roy, L., Curry, J.M., Mukherjee, P. and Grdzelishvili, V.Z. (2013) Oncolytic vesicular stomatitis virus in an immunocompetent model of MUC1-positive or MUC1-null pancreatic ductal adenocarcinoma J. Virol., 87, 10283–10294

Kalvodova, L., Sampaio, J.L., Cordo, S., Ejsing, C.S., Shevchenko, A. and Simons, K. (2009) The lipidomes of vesicular stomatitis virus, Semliki Forest virus and the host plasma membrane analyzed by quantitative shotgun mass spectrometry J. Virol., 83, 7996-8003

Kim, D-S., Dastidar, H., Zhang, C., Zemp, F.J., Lau, K., Ernst, M., Rakic, A., Sikdar, S., Rajwani, J. et al (2017) Smac mimetics and oncolytic viruses synergize in driving anticancer T-cell responses through complementary mechanisms Nat. Comm., 8: 344

Moerdyk-Schauwecker, M,. Hwang, S-I., Grdzelishvili, V.Z. (2014) Cellular proteins associated with the interior and exterior of vesicular stomatitis virus virions. PLoS One, 9: e104688

Rodriguez, S.E., Cross, R.W., Fenton, K.A., Bente, D.A., Mire, C.E. and Geisbert, T.W. (2019) Vesicular stomatitis virus-based vaccine protects mice against Crimean-Congo hemorrhagic fever Sci. Rep., 9: 7755

Selman, M., Ou, P., Rousso, C., Bergeron, A., Krishnan, R., Pikor, L., Chen, A., Keller, B.A., Ilkow, C., Bell, J.C. and Diallo, J-S. (2018) Dimethyl fumarate potentiates oncolytic virotherapy through NF-κB inhibition Sci. Transl. Med., 10: eaao1613

OptiPrep™ Reference List RV05: 3rd edition, January 2020

OptiPrep™ Reference List RV06

GROUP VI VIRUSES

• Viruses are listed alphabetically within the Baltimore scheme: Family, Genus and Species. Publications are listed alphabetically by first author and, where necessary, references are further divided according to research topic
• Multiple entries from the same first author are listed chronologically.
• For a detailed methodology of Group VI viruses see OptiPrep™ Application Sheets V29-V35. V06 is a methodological review of OptiPrep™ technology.
• For a comparative structural analysis of all Group VI virsues refer to: Martin, J.L., Cao, S., Maldonado, J.O., Zhang, W. and Mansky, L.M. (2016) Distinct particle morphologies revealed through comparative parallel analyses of retrovirus-like particles J. Virol., 90, 8074-8084

 

1. Alpharetroviridae

Rous sarcoma virus

Lee, E-G., Yeo, A., Kraemer, B., Wickens, M. and Linial, M.L. (1999) The Gag domains required for avian retroviral RNA encapsidation determined by using two independent assays J. Virol, 73, 6282-6292

Ochsenbauer-Jambor, C., Delos, S.E., Accavitti, M.A., White, J.M. and Hunter, E. (2002) Novel monoclonal antibody directed at the receptor binding site on the avian sarcoma and leukosis virus env complex J. Virol., 76, 7518-7527

2. Betaretroviridae

Mason-Pfizer Monkey virus (Simian retrovirus)

Fuzik, T., Pichalova, R., Schur, F.K.M., Strohalmova, K., Križova, I., Hadravova, R., Rumlova, M., Briggs, J.A.G., Ulbrich, P. and Ruml, T. (2016) Nucleic acid binding by Mason-Pfizer monkey virus CA promotes virus assembly and genome packaging J. Virol., 90, 4593-4603

Gottwein, E., Bodem, J., Müller, B., Schmechel, A., Zentgraf, H. and Kräusslich, H-G. (2003) The MasonPfizer monkey virus PPPY and PSAP motifs both contribute to virus release J. Virol., 77, 9474-9485

Voráčková, I., Ulbrich, P., Diehl, W.E. and Ruml, T. (2104) Engineered retroviral virus-like particles for receptor targeting Arch.Virol., 159, 677–688

Wildová, M., Hadravová, R. Štokrová, J., Křížová, I., Ruml, T., Hunter, E., Pichová, I. and Rumlová, M. (2008) The effect of point mutations within the N-terminal domain of Mason-Pfizer monkey virus capsid protein on virus core assembly and infectivity Virology, 380, 157-163

3. Deltaretroviridae

Human T-cell lymphotropic virus (HTLV-1)

Cao, S., Maldonado, J.O., Grigsby, I.F., Mansky, L.M. and Zhang, W. (2015) Analysis of human T-cell leukemia virus type 1 particles by using cryo-electron tomography J. Virol., 89, 2182-2191

Hémonnot, B., Molle, D., Bardy, M., Gay, B., Laune, D., Devaux, C. and Briant, L. (2006) Phosphorylation of the HTLV-1 matrix L-domain-containing protein by virus-associated ERK-2 kinase Virology, 349, 430-439

Martin, J.L., Mendonça, M., Marusinec, R., Zuczek, J., Angert, I., Blower, R.J., Mueller, J.D., Perilla, J.R. et al (2018) Critical role of the human T-cell leukemia virus type 1 capsid N-terminal domain for Gag-Gag interactions and virus particle assembly J. Virol., 14: e00333-18

Meissner, M.E., Mendonça, L.M., Zhang, W. and Mansky, L.M. (2017) Polymorphic nature of human T-cell leukemia virus type 1 particle cores as revealed through characterization of a chronically infected cell line J. Virol., 91: e00369-17-pfizer

Møller-Larsen, A. and Christensen, T. (1998) Isolation of a retrovirus from multiple sclerosis patients in selfgenerated iodixanol gradients J. Virol. Methods, 73, 151-161

4. Gammaretroviridae

Moloney murine leukaemia virus

Courtney, D.G., Chalem, A., Bogerd, H.P., Law, B.A., Kennedy, E.M., Holley, C.L. and Cullen, B.R. (2019) Extensive epitranscriptomic methylation of A and C residues on murine leukemia virus transcripts enhances viral gene expression mBio 10: e01209-19

Eckwahl, M.J., Sim, S.,. Smith, D., Telesnitsky, A. and Wolin, S.L. (2015) A retrovirus packages nascent host noncoding RNAs from a novel surveillance pathway Genes Devel., 29, 646–657

Leblanc, P., Alais, S., Porto-Carriero, I., Lehmann, S., Grassi, J., Raposo, G. and Darlix, J.L. (2006) Retrovirus infection strongly enhances scrapie infectivity release in cell culture EMBO J., 25, 2674-2685

Onafuwa-Nuga, A.A., King, S.R. and Telesnitsky, A. (2005) Nonrandom packaging of host RNAs in moloney murine leukemia virus J. Virol., 79, 13528-13537

Qu, K., Glass, B., Doelžal, M., Schur, F.K.M., Murciano, B., Rein, A., Rumlová, M., Ruml, T., Kräusslich, H.G. and Briggs, J.A.G. (2018) Structure and architecture of immature and mature murine leukemia virus capsids Proc. Natl. Acad. Sci. USA, 115, E11751–E11760

Segura, M.M., Garnier, A., Di Falco, M.R., Whissell, G., Meneses-Acosta, A., Arcand, N. and Kamen, A. (2008) Identification of host proteins associated with retroviral vector particles by proteomic analysis of highly purified vector preparations J. Virol., 82 1107-1117

Murine oncornavirus

Fujisawa, R., McAtee, F.J., Favara, C., Hayes, S.F. and Portis, J.L. (2001) N-terminal cleavage fragment of
glycosylated Gag is incorporated into murine oncornavirus particles J. Virol., 75, 11239-11243

5 Lentivirus

Feline immunodeficiency virus

Ammersbach, M. and Bienzle, D. (2011) Methods for assessing feline immunodeficiency virus infection, infectivity and purification Vet. Immunol. Immunopathol.,143, 202– 214

Human endogenous retroviruses

Li, M., Radvanyi, L., Yin, B., Li, J., Chivukula, R., Lin, K., Lu, Y., Shen, J.J., Chang, D.Z. et al (2017) Downregulation of human endogenous retrovirus type K (HERV-K) viral env RNA in pancreatic cancer cells decreases cell proliferation and tumor growth Clin Cancer Res., 23, 5892–5911

Human immunodeficiency virus-1 (HIV-1)

Actin
Popova, S., Popova, E., Inoue, M., Wu, Y. and Göttlinger, H. (2018) HIV-1 gag recruits PACSIN2 to promote virus spreading Proc. Natl. Acad. Sci. USA, 115, 7093–7098

Stauffer, S., Rahman, S.A., de Marco, A., Carlson, L-A., Glass, B., Oberwinkler, H., Herold, N., Briggs, J.A.G., Müller, B., Grünewald, K. and Kräusslich, H-G. (2014) The nucleocapsid domain of Gag is dispensable for actin incorporation into HIV-1 and for association of viral budding sites with cortical F-actin J. Virol., 88, 7893–7903

Adenosine deaminase
Orecchini, E., Federico, M., Doria, M., Arenaccio, C., Giuliani, E., Ciafrè, S.A. and Michienzi, A. (2015) The ADAR1 editing enzyme is encapsidated into HIV-1 virions Virology, 485, 475–480

Antiretroviral agents/therapy
De Silva Feelixge, H.S., Stone, D., Pietz, H.L., Roychoudhury, P., Greninger, A.L., Schiffer, J.T., Aubert, M. and Jerome, K.R. (2016) Detection of treatment-resistant infectious HIV after genome-directed antiviral endonuclease therapy Antiviral Res., 126, 90-98

Frezza, C., Grelli, S., Federico, M., Marino-Merlo, F., Mastino, A. and Macchi, B. (2016) Testing anti-HIV activity of antiretroviral agents in vitro using flow cytometry analysis of CEM-GFP cells infected with transfection-derived HIV-1 NL4-3 J. Med. Virol. 88, 979–986

Henriet, S., Mercenne, G., Bernacchi, S., Paillart, J-C. and Marquet, R. (2009) Tumultuous relationship between the human immunodeficiency virus type 1 viral infectivity factor (Vif) and the human APOBEC-3G and APOBEC-3F restriction factors Microbiol. Mol. Biol. Rev., 73, 211-232

Ingemarsdotter, C.K., Zeng, J., Long, Z., Lever, A.M.L. and Kenyon, J.C. (2018) An RNA‑binding compound that stabilizes the HIV‑1 gRNA packaging signal structure and specifically blocks HIV‑1 RNA encapsidation Retrovirology, 15: 25

Lassen, K.G., Wissing, S., Lobritz, M.A., Santiago, M. and Greene, W.C. (2010) Identification of two APOBEC3F splice variants displaying HIV-1 antiviral activity and contrasting sensitivity to Vif J. Biol. Chem., 285, 29326–29335

Mangeat, B., Turelli, P., Caron, G., Friedil, M., Perrin, L. and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Nature, 424, 99-103

Soros, V.B., Yonemoto, W. and Greene, W.C. (2007) Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA and subsequently activated by RNase H PLoS Pathog., 3:e15

Yukl, S.A., Shergill, A.K., McQuaid, K., Gianella, S., Lampiris, H., Hare, C.B., Pandori, M., Sinclair, E., Günthard, H.F., Fischer, M., Wong, J.K. and Havlir, D.V. (2010) Effect of raltegravir-containing intensification on HIV burden and T-cell activation in multiple gut sites of HIV-positive adults on suppressive antiretroviral therapy AIDS , 24, 2451–2460

Yukl, S.A., Gianella, S., Sinclair, E., Epling, L., Li, Q., Duan, L., Choi, A.L.M., Girling, V., Ho, T., Li, P., Fujimoto, K., et al (2010) Differences in HIV burden and immune activation within the gut of HIV-positive patients receiving suppressive antiretroviral therapy J. Infect. Dis., 202, 1553–1561

Autophagy
Campbell, G.R., Rawat, P., Bruckman, R.S. and Spector, S.A. (2015) Human immunodeficiency virus type 1 Nef inhibits autophagy through transcription factor EB sequestration PLoS Pathog 11: e1005018

Campbell, G.R., Bruckman, R.S., Chu, Y-L., Trout, R.N. and Spector, S.A., (2018) SMAC mimetics induce autophagy-dependent apoptosis of HIV-1-infected resting memory CD4+ T cells Cell Host & Microbe 24, 689–702

Budding
Carlson, L-A., Briggs, J.A.G., Glass, B., Riches, J.D., Simon, M.N., Johnson, M.C., Müller, B., Grünewald, K., Kräusslich, H-G. (2008) Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis Cell Host Microbe 4, 592-599

Leblanc, P., Alais, S., Porto-Carriero, I., Lehmann, S., Grassi, J., Raposo, G. and Darlix, J.L. (2006) Retrovirus infection strongly enhances scrapie infectivity release in cell culture EMBO J., 25, 2674-2685

Meckes, Jr. D.G. and Raab-Traub, N. (2011) Microvesicles and viral infection J. Virol., 85, 12844–12854 Park, I-W. and He, J.J. (2010) HIV-1 is budded from CD4+ T lymphocytes independently of exosomes Virol. J., 7: 234

Perez-Caballero, D., Zang, T., Ebrahimi, A., McNatt, M.W., Gregory, D.A., Johnson, M.C. and Bieniasz, P.D. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells Cell 139, 499–511

Stauffer, S., Rahman, S.A., de Marco, A., Carlson, L-A., Glass, B., Oberwinkler, H., Herold, N., Briggs, J.A.G., Müller, B., Grünewald, K. and Kräusslich, H-G. (2014) The nucleocapsid domain of Gag is dispensable for actin incorporation into HIV-1 and for association of viral budding sites with cortical F-actin J. Virol., 88, 7893–7903

Stuchell, M.D., Garrus, J.E., Müller, B., Stray, K.M., Ghaffarian, S., McKinnon, R., Kräusslich, H-G., Morham, S.G. and Sundquist, W.I. (2004) The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding J. Biol. Chem., 279, 36059-36071

Von Schwedler, U.K., Stuchell, M., Muller, B., Ward, D. M., Chung, H-Y., Morita, E., Wang, H.E. et al (2003) The protein network of HIV budding Cell, 114, 701-713

Zhao, W-L., Zhang, F., Feng, D., Wu, J., Chen, S. and Sui, S-F. (2009) A novel sorting strategy of trichosanthin for hijacking human immunodeficiency virus type 1 Biochem. Biophys. Res. Commun., 384, 347–351

Capsid assembly/disassembly and structure
Martin, J.L., Mendonça, L.M., Angert, I., Mueller, J.D., Zhang, W. and Manskya, L.M. (2017) Disparate contributions of human retrovirus capsid subdomains to Gag-Gag oligomerization, virus morphology, and particle biogenesis J. Virol., 91: e00298-17

Mattei, S., Flemming, A., Anders-Össwein, M., Kräusslich, H-G., Briggs, J.A.G. and Müller, B. (2015) RNA and nucleocapsid are dispensable for mature HIV-1 capsid assembly J. Virol., 89, 9739-9747

Rankovic, S., Varadarajan, J., Ramalho, R., Aiken, C. and Rousso, I. (2017) Reverse transcription mechanically initiates HIV-1 capsid disassembly J. Virol., 91: e00289-17

Rankovic, S., Ramalho, R., Aiken, C. and Rousso, I. (2018) PF74 reinforces the HIV-1 capsid to impair reverse transcription-induced uncoating J. Virol. 92: e00845-18

Cellular interactions/entry/transfer
Akiyama, H., Miller, C., Patel, H.V., Hatch, S.C., Archer, J., Ramirez, N-G.P. and Gummuluru, S. (2014) Virus particle release from glycosphingolipid-enriched microdomains is essential for dendritic cell-mediated capture and transfer of HIV-1 and Henipavirus J. Virol., 88, 8813–8825

Dobrowsky, T.M., Zhou, Y., Sun, S.X., Siliciano, R.F. and Wirtz, D. (2008) Monitoring early fusion dynamics of human immunodeficiency virus type 1 at single-molecule resolution J. Virol., 82, 7022-7033

Gilbert, C., Cantin, R., Barat, C. and Tremblay, M.J. (2007) Human immunodeficiency virus type 1 replication in dendritic cell-T-cell co-cultures is increased upon incorporation of host LFA-1 due to higher levels of virus production in immature dendritic cells J. Virol., 81, 7672-7682

Harman, A.N., Wilkinson, J., Byem C.R., Bosnjak, L., Stern, J.L., Nicholle, M., Lai, J. and Cunningham (2006) HIV induces maturation of monocyte-derived dendritic cells and Langerhans cells J. Immunol., 177, 7103-7113

Izquierdo-Useros, N., Lorizate, M., Contreras, F-X., Rodriguez-Plata, M.T., Glass, B., Erkizia, I., Prado, J.G. et al (2012) Sialyllactose in viral membrane gangliosides is a novel molecular recognition pattern for mature dendritic cell capture of HIV-1 PLoS Biol., 10: e1001315

Pang, H-B., Hevroni, L., Kol, N., Eckert, D.M., Tsvitov, M., Kay, M.S. and Rousso, I. (2013) Virion stiffness regulates immature HIV-1 entry Retrovirology, 10: 4

Popova, S., Popova, E., Inoue, M., Wu, Y. and Göttlinger, H. (2018) HIV-1 gag recruits PACSIN2 to promote virus spreading Proc. Natl. Acad. Sci. USA, 115, 7093–7098

Sirois, M., Robitaille, L., Sasik, R., Estaquier, J., Fortin, J. and Corbeil, J. (2008) R5 and X4 HIV viruses differentially modulate host gene expression in resting CD4+ T cells AIDS Res. Hum. Retrovir., 24, 485-493

Smith, A.L., Ganesh, L., Leung, K., Jongstra-Bilen, J., Jongstra, J. and Nabel, G.J. (2007) Leukocyte-specific protein 1 interacts with DC-SIGN and mediates transport of HIV to the proteasome of dendritic cells J. Exp. Med., 204, 421-430

St-Pierre, C., Ouellet, M., Tremblay, M.J. and Sato, S. (2010) Galectin-1 and HIV-1 infection Methods Enzymol., 480, 267-294

Zhao, W-L., Zhang, F., Feng, D., Wu, J., Chen, S. and Sui, S-F. (2009) A novel sorting strategy of trichosanthin for hijacking human immunodeficiency virus type 1 Biochem. Biophys. Res. Commun., 384, 347–351

Chikungunya virus assay
Kishishita, N., Takeda, N., Anuegoonpipat, A. and Anantapreechac, S. (2013) Development of a pseudotypedlentiviral-vector-based neutralization assay for Chikungunya virus infection J. Clin. Microbiol., 51, 1389–1395

Cholesterol (membrane)
Campbell, S. M., Crowe, S. M. and Mak, J. (2002) Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity AIDS, 16, 2253-2261

Campbell, S., Gaus, K., Bittman, R., Jessup, W., Crowe, S. and Mak, J. (2004) The raft-promoting property of virion-associated cholesterol, but not the presence of virion-associated Brij 98 rafts, is a determinant of human immunodeficiency virus type 1 infectivity J. Virol., 78, 10556-10565

Pollock, S., Nichita, N.B., Böhmer, A., Radulescu, C., Dwek, R.A. and Zitzmann, N. (2010) Polyunsaturated liposomes are antiviral against hepatitis B and C viruses and HIV by decreasing cholesterol levels in infected cells Proc. Natl. Acad. Sci. USA, 107, 17176–17181

Sundaram, R.V.K., Li, H., Bailey, L., Rashad, A.A., Aneja, R., Weiss, K., Huynh, J., Bastian, A.R., et al (2016) Impact of HIV‑1 membrane cholesterol on cell-independent lytic inactivation and cellular infectivity Biochemistry, 55, 447−458

Cytotoxicity
Alsahafi, N., Bakouche, N., Kazemi, M., Richard, J., Ding, S., Bhattacharyya, S., Das, D., Anand, S.P. et al (2019) An asymmetric opening of HIV-1 envelope mediates antibody-dependent cellular cytotoxicity Cell Host Microbe, 25, 578–587

Defective core virus
Joshi, P., Sloan, B., Torbett, B.E. and Stoddart, C.A. (2013) Heat shock protein 90AB1 and hyperthermia rescue infectivity of HIV with defective cores Virology, 436, 162–172

Endosomal sorting complex
Meng, B., Ip, N.C.Y., Prestwood, L.J., Abbink, T.E.M. and Lever, A.M.L. (2015) Evidence that the endosomal sorting complex required for transport-II (ESCRT-II) is required for efficient human immunodeficiency virus-1 (HIV-1) production Retrovirology, 12: 72

Envelope components/structure/function
Alsahafi, N., Bakouche, N., Kazemi, M., Richard, J., Ding, S., Bhattacharyya, S., Das, D., Anand, S.P. et al (2019) An asymmetric opening of HIV-1 envelope mediates antibody-dependent cellular cytotoxicity Cell Host Microbe, 25, 578–587

Aneja, R., Rashad, A.A., Li, H., Sundaram, R.V.K., Duffy, C., Bailey, L.D. and Chaiken, I. (2015) Peptide triazole inactivators of HIV‑1 utilize a conserved two-cavity binding site at the junction of the inner and outer domains of Env gp120 J. Med. Chem., 58, 3843−3858

Bailey, L.D., Sundaram, R.V.K., Li, H., Duffy, C., Aneja, R., Bastian, A.R., Holmes, A.P., Kamanna, K., Rashad, A.A. and Chaiken, I. (2015) Disulfide sensitivity in the Env protein underlies lytic inactivation of HIV‑1 by peptide triazole thiols ACS Chem. Biol., 10, 2861−2873

Barat, C., Martin, G., Beaudoin, A.R., Sévingy, J. and Tremblay, M.J. (2007) The nucleoside triphosphate diphosphohydrolase-1/CD39 is incorporated into human immunodeficiency type 1 particles, where it remains biologically active J. Mol. Biol., 371, 269-282

Bastian, A.R., Contarino, M., Bailey, L.D., Aneja, R., Moreira, D.R.M., Freedman, K., McFadden, K. et al (2013) Interactions of peptide triazole thiols with Env gp120 induce irreversible breakdown and inactivation of HIV-1 virions Retrovirology 10: 153

Bastian, A.R., Ang, C.G., Kamannaa, K., Shaheen, F., Huang, Y-H., McFadden, K., Duffy, C., Bailey, L.D. et al (2017) Targeting cell surface HIV-1 Env protein to suppress infectious virus formation Virus Res., 235, 33–36

Brügger, B., Glass, B., Haberkant, P., Leibrecht, I., Wieland, F.T. and Kräusslich, H-G. (2006) The HIV lipodome: a raft with an unusual composition Proc. Natl. Acad, Sci. USA, 108, 2641-2646

Chojnacki, J., Waithe, D., Carravilla, P., Huarte, N., Galiani, S., Enderlein, J. and Eggeling, C. (2017) Envelope glycoprotein mobility on HIV-1 particles depends on the virus maturation state Nat. Comm. 8: 545

Contarino, M., Bastian, A.R., Sundaram, R.V.K., McFadden, K., Duffy, C., Gangupomu, V., Baker, M., Abrams, C. and Chaiken, I. (2013) Chimeric cyanovirin-MPER recombinantly engineered proteins cause cellfree virolysis of HIV-1 J. Virol., 87, 4743-4750

Gurer, C., Cimarelli, A. and Luban, J. (2002) Specific incorporation of heat shock protein 70 family members into primate Lentiviral virions J. Virol., 76, 4666-4670

Habermann, A., Krijnse-Locker, J., Oberwinkler, H., Eckhardt, M., Homann, S., Andrew, A., Strebel, K. and Kräusslich, H-G. (2010) CD317/tetherin is enriched in the HIV-1 envelope and downregulated from the plasma membrane upon virus infection J. Virol., 84, 4646-4658

Henderson, R., Lu, M., Zhou, Y., Mu, Z., Parks, R., Han, Q., Hsu, A.L., Carter, E. et al (2020) Disruption of the HIV-1 Envelope allosteric network blocks CD4-induced rearrangements Nat. Comm., 11: 520

Henriksson, P., Pfeiffer, T., Zentgraf, H., Alke, A. and Bosch, V. (1999) Incorporation of wild-type and Cterminally truncated human epidermal growth factor receptor into human immunodeficiency virus-like particles: insight into the processes governing glycoproteins incorporation into retroviral particles J. Virol, 73, 9294-9302

Herrera, C., Klasse, P.J., Michael, E., Kake, S., Barnes, K., Kibler, C.W., Campbell-Gardeneer, L., Si, Z., Sodroski, J., Moore, J.P. and Beddows, S. (2005) The impact of envelope glycoprotein cleavage on the antigenicity, infectivity, and neutralization sensitivity of Env-pseudotyped human immunodeficiency virus type 1 particles Virology, 338, 154-172

Herrera, C., Klasse, P.J., Kibler, C.W., Michael, E., Moore, J.P. and Beddows, S. (2006) Dominant-negative effect of hetero-oligomerization on the function of the human immunodeficiency virus type 1 envelope glycoprotein complex Virology, 351, 121-132

Huarte, N., Carravilla, P., Cruz, A., Lorizate, M., Nieto-Garai, J.A., Kräusslich, H-G., Pérez-Gil, J., RequejoIsidro, J. and Nieva, J.L. (2016) Functional organization of the HIV lipid envelope Sci. Rep., 6: 34190

Izquierdo-Useros, N., Lorizate, M., Contreras, F-X., Rodriguez-Plata, M.T., Glass, B., Erkizia, I., Prado, J.G., Casas, J., Fabriàs, G., Kräusslich, H-G. and Martinez-Picado, J. (2012) Sialyllactose in viral membrane gangliosides is a novel molecular recognition pattern for mature dendritic cell capture of HIV-1 PLoS Biol., 10: e1001315

Leaman, D.P., Kinkead, H. and Zwick, M.B. (2010) In-solution virus capture assay helps deconstruct heterogeneous antibody recognition of human immunodeficiency virus type 1 J. Virol., 84, 3382–3395

Lorizate, M., Brügger, B., Akiyama, H., Glass, B., Müller, B., Anderluh, G., Wieland, F.T. and Kräusslich, HG. (2009) Probing HIV-1 membrane liquid order by Laurdan staining reveals producer cell-dependent differences J. Biol. Chem., 284, 22238-22247

Lu, M., Ma, X., Castillo-Menendez, L.R., Gorman, J., Alsahafi, N., Ermel, U., Terry, D.S., Chambers, M., Peng, D., Zhang, B. et al (2019) Associating HIV-1 envelope glycoprotein structures with states on the virus observed by smFRET Nature, 568, 415-419

Lu, W., Chen, S., Yu, J., Behrens, R., Wiggins, J., Sherer, N., Liu, S-L., Xiong, Y., Xiang, S-H. and Wu, L. (2019) The polar region of the HIV-1 envelope protein determines viral fusion and infectivity by stabilizing the gp120-gp41 association J. Virol., 93: e02128-18

Mücksch, F., Citir, M., Lüchtenborg, C., Glass, B., Traynor-Kaplan, A., Schultz, C., Brügger, B. and Kräusslich, H-G. (2019) Quantification of phosphoinositides reveals strong enrichment of PIP2 in HIV-1 compared to producer cell membranes Sci. Rep., 9: 17661

Pancera, M., Zhou, T., Druz, A., Georgiev, I.S. et al (2014) Structure and immune recognition of trimeric prefusion HIV-1 Env Nature, 514, 455-461

Parajuli, B., Acharya, K., Yu, R., Ngo, B., Rashad, A.A., Abrams, C.F. and Chaiken, I.M. (2016) Lytic inactivation of human immunodeficiency virus by dual engagement of gp120 and gp41 domains in the virus env protein trimer Biochemistry, 55, 6100−6114

Parajuli, B., Acharya, K., Bach, H.C., Parajuli, B., Zhang, S., Smith, III, A.B., Abrams, C.F. and Chaiken, I. (2018) Restricted HIV-1 Env glycan engagement by lectin-reengineered DAVEI protein chimera is sufficient for lytic inactivation of the virus Biochem. J., 475, 931–957

Rashad, A.A., Song, L-R., Holmes, A.P., Acharya, K., Zhang, S., Wang, Z-L., Gary, E., Xie, X et al (2018) Bifunctional chimera that coordinately targets human immunodeficiency virus 1 envelope gp120 and the hostcell CCR5 coreceptor at the virus−cell interface J. Med. Chem. 2018, 61, 5020−5033

Roy, J., Martin, G., Giguere, J-F., Belanger, D., Petrin, M. and Tremblay, M.J. (2005) HIV type 1 can act as an APC upon acquisition from the host cell of peptide-loaded HLA-DR and CD86 molecules J. Immunol., 174, 4779-4788

Stano, A., Leaman, D.P., Kim, A.S., Zhang, L., Autin, L., Ingale, J., Gift, S.K. et al (2017) Dense array of spikes on HIV-1 virion particles J. Virol., 91: e00415-17

Taylor, B.M., Foulke, J.S., Flinko, R., Heredia, A., DeVico, A. and Reitz, M. (2008) An alteration of human immunodeficiency virus gp41 leads to reduced CCR5 dependence and CD4 independence J. Virol., 82, 5460-5471

Vyas, G.N., Stoddart, C.A., Killian, S., Brennan, T.V., Goldberg, T. Ziman, A. and Bryson, Y. (2012) Derivation of non-infectious envelope proteins from virions isolated from plasma negative for HIV antibodies Biologicals 40,15-20

Wilson, S.J., Schoggins, J.W., Zang, T., Kutluay, S.B., Jouvenet, N., Alim, M.A., Bitzegeio, J., Rice, C.M. and Bieniasz, P.D. (2012) Inhibition of HIV-1 particle assembly by 2’,3’-cyclic-nucleotide 3’-phospho-diesterase Cell Host Microbe 12, 585–597

Yang, Z-Y., Chakrabati, B.K., Xu, L., Welcher, B., Kong, W-p., Leung, K., Panet, A., Mascola, J.R. and Nabel, G.J. (2004) Selective modification of variable loops alters tropism and enhances immunogenicity of human immunodeficiency virus type 1 envelope J. Virol., 78, 4029-4036

Exosomes
Böker, K.O., Lemus-Diaz, N., Ferreira, R.R., Schiller, L., Schneider, S. and Gruber, J. (2018) The impact of the CD9 tetraspanin on lentivirus infectivity and exosome secretion Mol. Ther., 26, 634-647

Chiozzini, C., Arenaccio, C., Olivetta, E., Anticoli, S., Manfredi, F., Ferrantelli, F., d’Ettorre, G., Schietroma, I., Andreotti, M. and Federico, M. (2017) Trans-dissemination of exosomes from HIV-1-infected cells fosters both HIV-1 trans-infection in resting CD4+ T lymphocytes and reactivation of the HIV-1 reservoir Arch. Virol., 162, 2565–2577

Ducloux, C., Mougel, M., Goldschmidt, V., Didierlaurent, L., Marquet, R. and Isel, C. (2012) A pyrophosphatase activity associated with purified HIV-1 particles Biochimie, 94, 2498-2507

Meckes, Jr. D.G. and Raab-Traub, N. (2011) Microvesicles and viral infection J. Virol., 85, 12844–12854

Park, I-W., Fan, Y., Luo, X., Ryou, M-G., Liu. J., Green, L. and He, J.J. (2014) HIV-1 Nef is transferred from expressing T cells to hepatocytic cells through conduits and enhances HCV replication PLoS One, 9: e99545

Gag protein interactions (see “HIV assembly”)

c-GAMP expression

Bridgeman, A, Maelfait, J., Davenne, T., Partridge, T., Peng, Y., Mayer, A., Dong, T., Kaever, V., Borrow, P. and Rehwinkel, J. (2015) Viruses transfer the antiviral second messenger cGAMP between cells Science 349, 1228-1232

Gene expression
Courtney, D.G., Tsai, K., Bogerd, H.P., Kennedy, E.M., Law, B.A., Emery, A., Swanstrom, R., Holley, C.L. and Cullen, B.R. (2019) Epitranscriptomic addition of m5C to HIV-1 transcripts regulates viral gene expression Cell Host Microbe 26, 217–227

Rahimian, P. and He, J.J. (2016) HIV-1 Tat-shortened neurite outgrowth through regulation of microRNA-132 and its target gene expression J. Neuroinflamm., 13: 247
2-17.

Genome delivery
De las Mercedes Segura, M., Kamen, A. and Garnier, A. (2006) Downstream processing of oncoretroviral and lentiviral gene therapy vectors Biotechnol. Adv., 24, 321-337

McDonald, D., Vodicka, M. A., Lucero, G., Svitkina, T. M., Borisy, G. G., Emerman, M. and Hope, T. J. (2002) Visualization of the intracellular behavior of HIV in living cells J. Cell Biol., 159, 441-452

Priet, S., Navarro, J-M., Querat, G. and Sire, J. (2003) Reversion of the lethal phenotype of an HIV-1 integrase mutant virus by overexpression of the same integrase mutant protein J. Biol. Chem., 278, 20724-20730

Glycolipid/glycosphingolipid domains
Akiyama, H., Miller, C., Patel, H.V., Hatch, S.C., Archer, J., Ramirez, N-G.P. and Gummuluru, S. (2014) Virus particle release from glycosphingolipid-enriched microdomains is essential for dendritic cell-mediated capture and transfer of HIV-1 and Henipavirus J. Virol., 88, 8813–8825

Izquierdo-Useros, N., Lorizate, M., Contreras, F-X., Rodriguez-Plata, M.T., Glass, B., Erkizia, I., Prado, J.G. et al (2012) Sialyllactose in viral membrane gangliosides is a novel molecular recognition pattern for mature dendritic cell capture of HIV-1 PLoS Biol., 10: e1001315

Growth factors
Desimmie, B.A., Weydert, C., Schrijvers, R., Vets, S., Demeulemeester, J., Proost, P., Paron, I., De Rijck, J. et al (2015) HIV-1 IN/Pol recruits LEDGF/p75 into viral particles Retrovirology, 12: 16

Heat shock proteins
Joshi, P., Sloan, B., Torbett, B.E. and Stoddart, C.A. (2013) Heat shock protein 90AB1 and hyperthermia rescue infectivity of HIV with defective cores Virology, 436, 162–172

Joshi, P., Maidji, E. and Stoddart, C.A. (2016) Inhibition of heat shock protein 90 prevents HIV rebound J. Biol. Chem., 291, 10332–10346

Helicase
Kristina, A., Serquiña, P., Das, S.R., Popova, E., Ojelabi, O.A., Roy, C.K. and Göttlinger, H.G. (2013) UPF1 is crucial for the infectivity of human immunodeficiency virus type 1 progeny virions J. Virol., 87, 8853–8861

Hepatitis C replication
Park, I-W., Fan, Y., Luo, X., Ryou, M-G., Liu. J., Green, L. and He, J.J. (2014) HIV-1 Nef is transferred from expressing T cells to hepatocytic cells through conduits and enhances HCV replication PLoS One, 9: e99545

HIV assembly
De Marco, A., Heuser, A-M., Glass, B., Kräusslich, H-G., Müller, B. and Briggs, J.A.G. (2012) Role of the SP2 domain and its proteolytic cleavage in HIV-1 structural maturation and infectivity J. Virol., 86, 13708-13716

Engeland, C.E., Oberwinkler, H., Schümann, M., Krause, E., Müller, G.A. and Kräusslich, H-G. (2011) The cellular protein lyric interacts with HIV-1 Gag J. Virol., 85, 13322–13332

Hemonnot, B., Cartier, C., Gay, B., Rebuffat, S., Bardy, M., Devaux, C., Boyer, V. and Briant, L. (2004) The host cell MAP kinase ERK-2 regulates viral assembly and release by phosphorylating the p6gag protein of HIV-1 J. Biol. Chem., 279, 32426-32434

Kessans, S.A., Linhart, M.D., Matoba, N. and Mor, T. (2013) Biological and biochemical characterization of HIV-1 Gag/dgp41 virus-like particles expressed in Nicotiana benthamiana Plant Biotech. J., 11, 681–690

Kol, N., Tsvitov, M., Hevroni, L., Wolf, S.G., Pang, H-B., Kay, M.S. and Rousso, I. (2010) The effect of purification method on the completeness of the immature HIV-1 Gag shell J. Virol. Methods 169, 244–247

Leung, K., Kim, J-O., Ganesh, L., Kabat, J., Schwartz, O. and Nabel, G.J. (2008) HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions Cell Host Microbe, 3, 285-292

L’Hernault, A., Weiss, E.U., Greatorex, J.S. and Lever, A.M. (2012) HIV-2 genome dimerization is required for the correct processing of Gag: a second-site reversion in matrix can restore both processes in dimerizationimpaired mutant viruses J. Virol., 86, 5867-5876

Martin, J.L., Mendonça, L.M., Angert, I., Mueller, J.D., Zhang, W. and Manskya, L.M. (2017) Disparate contributions of human retrovirus capsid subdomains to Gag-Gag oligomerization, virus morphology, and particle biogenesis J. Virol., 91: e00298-17

Müller, B., Patschinsky, T. and Kräusslich, H-G. (2002) The late-domain-containing protein p6 is the predominant phosphoprotein of human immunodeficiency virus type 1 particles J. Virol., 76, 1015-1024

Popova, S., Popova, E., Inoue, M., Wu, Y. and Göttlinger, H. (2018) HIV-1 gag recruits PACSIN2 to promote virus spreading Proc. Natl. Acad. Sci. USA, 115, 7093–7098

Orecchini, E., Federico, M., Doria, M., Arenaccio, C., Giuliani, E., Ciafrè, S.A. and Michienzi, A. (2015) The ADAR1 editing enzyme is encapsidated into HIV-1 virions Virology, 485, 475–480

Sova, P., Volsky, D.J., Wang, L. and Chao, W. (2001) Vif is largely absent from human immunodeficiency virus type 1 mature virions and associates with viral particles containing unprocessed Gag J. Virol., 75, 5504-5517

Stauffer, S., Rahman, S.A., de Marco, A., Carlson, L-A., Glass, B., Oberwinkler, H., Herold, N., Briggs, J.A.G., Müller, B., Grünewald, K. and Kräusslich, H-G. (2014) The nucleocapsid domain of Gag is dispensable for actin incorporation into HIV-1 and for association of viral budding sites with cortical F-actin J. Virol., 88, 7893–7903

Tritel, M. and Resh, M.D. (2000) Kinetic analysis of human immunodeficiency virus type 1 assembly reveals the presence of sequential intermediates J. Virol., 74, 5845-5855

Tritel, M. and Resh, M.D. (2001) The late stage of human immunodeficiency virus type 1 assembly is an energy-dependent process J. Virol., 75, 5473-5481

Wilson, S.J., Schoggins, J.W., Zang, T., Kutluay, S.B., Jouvenet, N., Alim, M.A., Bitzegeio, J., Rice, C.M. and Bieniasz, P.D. (2012) Inhibition of HIV-1 particle assembly by 2’,3’-cyclic-nucleotide 3’-phospho-diesterase Cell Host Microbe 12, 585–597

Zhang, F., Zang, T., Wilson, S.J., Johnson, M.C. and Bieniasz, P.D. (2011) Clathrin facilitates the morphogenesis of retrovirus particles PLoS Pathog., 7: e1002119

Host cell-HIV interactions
Desimmie, B.A., Weydert, C., Schrijvers, R., Vets, S., Demeulemeester, J., Proost, P., Paron, I., De Rijck, J. et al (2015) HIV-1 IN/Pol recruits LEDGF/p75 into viral particles Retrovirology, 12: 16

Rashad, A.A., Song, L-R., Holmes, A.P., Acharya, K., Zhang, S., Wang, Z-L., Gary, E., Xie, X et al (2018) Bifunctional chimera that coordinately targets human immunodeficiency virus 1 envelope gp120 and the hostcell CCR5 coreceptor at the virus−cell interface J. Med. Chem. 2018, 61, 5020−5033

Trautz, B., Wiedemann, H., Lüchtenborg, C., Pierini, V., Kranich, J., Glass, B., Kräusslich, H-G. et al (2017) The host-cell restriction factor SERINC5 restricts HIV-1 infectivity without altering the lipid composition and organization of viral particles J. Biol. Chem., 292, 3702–13713

Immune responses/immunogenicity/vaccines
Akahata, W., Yang, Z-y. and Nabel, G.J. (2005) Comparative immunogenicity of human immunodeficiency virus particles and corresponding polypeptides in a DNA vaccine J. Virol., 79, 626-631

Barat, C., Martin, G., Beaudoin, A.R., Sévingy, J. and Tremblay, M.J. (2007) The nucleoside triphosphate diphosphohydrolase-1/CD39 is incorporated into human immunodeficiency type 1 particles, where it remains biologically active J. Mol. Biol., 371, 269-282

Deml, L., Speth, C., Dierich, M.P., Wolf, H. and Wagner, R. (2004) Recombinant HIV-1 Pr55gag virus-like particles: potent stimulators of innate and acquired immune responses Mol. Immunol., 42, 259-277

Ganesh, L., Leung, K., Loré, K., Levin, R., Panet, A., Schwartz, O., Koup, R.A. and Nabel, G.J. (2004) Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cellmediated transmission of virus resistant to broadly neutralizing antibodies J. Virol., 78, 11980-11987

Kim, M., Qiao, Z., Yu, J., Montefiori, D. and Reinherz, E.L. (2007) Immunogenicity of recombinant immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state Vaccine, 25, 5102-5114

Sirois, M., Robitaille, L., Allary, R., Shah, M., Woelk, C.H., Estaquier, J. and Corbeil, J. (2011) TRAF6 and IRF7 control HIV replication in macrophages PLoS One, 6: e28125

Vyas, G.N., Stoddart, C.A., Killian, S., Brennan, T.V., Goldberg, T. Ziman, A. and Bryson, Y. (2012) Derivation of non-infectious envelope proteins from virions isolated from plasma negative for HIV antibodies Biologicals 40,15-20

Yang, Z-Y., Chakrabati, B.K., Xu, L., Welcher, B., Kong, W-p., Leung, K., Panet, A., Mascola, J.R. and Nabel, G.J. (2004) Selective modification of variable loops alters tropism and enhances immunogenicity of human immunodeficiency virus type 1 envelope J. Virol., 78, 4029-4036

Young, K.R., McBurney, S.P., Karkhanis, L.U. and Ross, T.M. (2006) Virus-like particles: Designing an effective AIDS vaccine Methods, 40, 98-117

Zaldívar, I., Muñoz-Fernández, M.A., Alarcón, B. and San José, E. (2009) Expression of a modified form of CD4 results in the release of an anti-HIV factor derived from the Env sequence J. Immunol., 183, 1188-1196

Inactivation/inactivators
Aneja, R., Rashad, A.A., Li, H., Sundaram, R.V.K., Duffy, C., Bailey, L.D. and Chaiken, I. (2015) Peptide triazole inactivators of HIV‑1 utilize a conserved two-cavity binding site at the junction of the inner and outer domains of Env gp120 J. Med. Chem., 58, 3843−3858

Aneja, R., Grigoletto, A., Nangarlia, A., Rashad, A.A., Wrenn, S., Jacobson, J.M., Pasut, G. and Chaiken, I. (2019) Pharmacokinetic stability of macrocyclic peptide triazole HIV‐1 inactivators alone and in liposomes J. Pep. Sci., 25: e3155

Bailey, L.D., Sundaram, R.V.K., Li, H., Duffy, C., Aneja, R., Bastian, A.R., Holmes, A.P., Kamanna, K., Rashad, A.A. and Chaiken, I. (2015) Disulfide sensitivity in the Env protein underlies lytic inactivation of HIV‑1 by peptide triazole thiols ACS Chem. Biol., 10, 2861−2873

Bastian, A.R., Contarino, M., Bailey, L.D., Aneja, R., Moreira, D.R.M., Freedman, K., McFadden, K. et al (2013) Interactions of peptide triazole thiols with Env gp120 induce irreversible breakdown and inactivation of HIV-1 virions Retrovirology 10: 153

Bastian, A.R., Nangarlia, A., Bailey, L.D., Holmes, A., Sundaram, R.V.K., Ang, C., Moreira, D.R.M. et al (2015) Mechanism of multivalent nanoparticle encounter with HIV-1 for potency enhancement of peptide triazole virus inactivation J. Biol. Chem., 290, 529–543

Parajuli, B., Acharya, K., Yu, R., Ngo, B., Rashad, A.A., Abrams, C.F. and Chaiken, I.M. (2016) Lytic inactivation of human immunodeficiency virus by dual engagement of gp120 and gp41 domains in the virus env protein trimer Biochemistry, 55, 6100−6114

Parajuli, B., Acharya, K., Bach, H.C., Parajuli, B., Zhang, S., Smith, III, A.B., Abrams, C.F. and Chaiken, I. (2018) Restricted HIV-1 Env glycan engagement by lectin-reengineered DAVEI protein chimera is sufficient for lytic inactivation of the virus Biochem. J., 475, 931–957

Rashad, A.A., Sundaram, R.V.K., Aneja, R., Duffy, C. and Chaiken, I. (2015) Macrocyclic envelope glycoprotein antagonists that irreversibly inactivate HIV‑1 before host cell encounter J. Med. Chem., 58, 7603−7608

Rashad, A.A., Acharya, K., Haftl, A., Aneja, R., Dick, A., Holmes, A.P. and Chaiken, I. (2017) Chemical optimization of macrocyclic HIV-1 inactivators for improving potency and increasing the structural diversity at the triazole ring Org. Biomol. Chem., 15, 7770-7782

Infectivity
Chiozzini, C., Arenaccio, C., Olivetta, E., Anticoli, S., Manfredi, F., Ferrantelli, F., d’Ettorre, G., Schietroma, I., Andreotti, M. and Federico, M. (2017) Trans-dissemination of exosomes from HIV-1-infected cells fosters both HIV-1 trans-infection in resting CD4+ T lymphocytes and reactivation of the HIV-1 reservoir Arch. Virol., 162, 2565–2577

De Marco, A., Heuser, A-M., Glass, B., Kräusslich, H-G., Müller, B. and Briggs, J.A.G. (2012) Role of the SP2 domain and its proteolytic cleavage in HIV-1 structural maturation and infectivity J. Virol., 86, 13708-13716

Lu, W., Tirumuru, N., St. Gelais, C., Koneru, P.C., Liu, C., Kvaratskhelia, M., He, C. and Wu, L. (2018) N

Methyladenosine–binding proteins suppress HIV-1 infectivity and viral production J. Biol. Chem., 293, 12992–13005

Lu, W., Chen, S., Yu, J., Behrens, R., Wiggins, J., Sherer, N., Liu, S-L., Xiong, Y., Xiang, S-H. and Wu, L. (2019) The polar region of the HIV-1 envelope protein determines viral fusion and infectivity by stabilizing the gp120-gp41 association J. Virol., 93: e02128-18

Manganaro, L., Hong, P., Hernandez, M.M., Argyle, D., Mulder, L.C.F., Potla, U., Diaz-Griffero, F., Lee, B., Fernandez-Sesma, A. and Simon, V. (2018) IL-15 regulates susceptibility of CD4+ T cells to HIV infection Proc. Natl. Acad. Sci. USA, 115, E9659–E9667

Mendonca¸ L.M., Poeys, S.C., Abreu, C.M., Tanuri, A., Costa, L.J. (2014) HIV-1 Nef inhibits protease activity and its absence alters protein content of mature viral particles PLoS One, 9: e95352

Ouellet, M., St-Pierre, C., Tremblay, M.J. and Sato, S. (2015) Effect of galectins on viral transmission In Galectins: Methods and Protocols, Methods in Molecular Biology, vol. 1207 (eds. Stowell, S.R. and Cummings, R.D.), Springer Science+Business Media New York, pp 397-420

Sundaram, R.V.K., Li, H., Bailey, L., Rashad, A.A., Aneja, R., Weiss, K., Huynh, J., Bastian, A.R., et al (2016) Impact of HIV‑1 membrane cholesterol on cell-independent lytic inactivation and cellular infectivity Biochemistry, 55, 447−458

Usami, Y., Wu, Y. and Göttlinger, H.G. (2015) SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef Nature, 526, 218-223

Integrase oligomerization probe
Borrenberghs, D., Thys, W., Rocha, S., Demeulemeester, J., Weydert, C., Dedecker, P., Hofkens, J., Debyser, Z. and Hendrix, J. (2014) HIV virions as nanoscopic test tubes for probing oligomerization of the integrase enzyme ACS Nano 8, 3531–3545

Interferon-induced transmembrane proteins
Compton, A.A., Bruel, T., Porrot, F., Mallet, A., Sachse, M., Euvrard, M., Liang, C., Casartelli, N. and Schwartz, O. (2014) IFITM proteins incorporated into HIV-1 virions impair viral fusion and spread Cell Host Microbe, 16, 736–747

Compton, A.A., Roy, N., Porrot, F., Billet, A., Casartelli, N., Yount, J.S., Liang, C. and Schwartz, O. (2016) Natural mutations in IFITM3 modulate post-translational regulation and toggle antiviral specificity EMBO Rep., 17, 1657-1671

Latency
Dahabieh, M.S., Ooms, M., Simon, V. and Sadowskia, I. (2013) A doubly fluorescent HIV-1 reporter shows that the majority of integrated HIV-1 is latent shortly after infection J. Virol., 87, 4716-4727

Lentiviral vector analysis
Anderson, G.R., Semenov, A., Song, J.H. and Martemyanov, K.A. (2007) The membrane anchor R7BP controls the proteolytic stability of the striatal specific RGS protein, RGS9-2 J. Biol. Chem., 282, 4772-4781

Anderson, G.R., Cao, Y., Davidson, S., Truong, H.V., Pravetoni, M., Thomas, M.J., Wickman, K., Giesler, G.J. and Martemyanov, K.A. (2010) R7BP complexes with RGS9-2 and RGS7 in the striatum differentially control motor learning and locomotor responses to cocaine Neuropsychopharmacology, 35, 1040–1050

Giacca, M. and Zacchigna, S. (2012) Virus-mediated gene delivery for human gene therapy J. Control. Release, 161, 377–388

Hossain, M.I., Hoque, A., Lessene, G., Kamaruddin, M.A., Chu, P.W.Y., Ng, I.H.W., Irtegun, S. et al (2015) Dual role of Src kinase in governing neuronal survival Brain Res., 1594, 1–14

Huentelmann, M.J., Zubcevic, J., Katovich, M.J. and Raizada, M.K. (2004) Cloning and characterization of a secreted form of angiotensin-converting enzyme 2 Regul. Pept., 122, 61-67

Kibaly, C., Lin, H-Y., Loh, H.H., Law, P-Y. (2017) Spinal or supraspinal phosphorylation deficiency at the MOR C-terminus does not affect morphine tolerance in vivo Pharmacol. Res., 119, 153–168

Kishishita, N., Takeda, N., Anuegoonpipat, A. and Anantapreechac, S. (2013) Development of a pseudotypedlentiviral-vector-based neutralization assay for Chikungunya virus infection J. Clin. Microbiol., 51, 1389–1395

Kotzin, J.J., Spencer, S.P., McCright, S.J., Uthaya Kumar, D.B., Collet, M.A., Mowel, W.K., Elliott, E.N., Uyar, A., Makiya, M.A. and Dunagin, M.C. (2016) The long non-coding RNA Morrbid regulates Bim and shortlived myeloid cell lifespan Nature, 537, 239-243

Ricks, D.M., Kutner, R., Zhang, X-Y., Welsh, D.A. and Reiser, J. (2008) Optimized lenitviral transduction of mouse bone marrow-derived mesenchymal stem cells Stem Cells Dev., 17, 441-450

Segura, M.M., Kamen, A.A. and Garnier, A. (2011) Overview of current scalable methods for purification of viral vectors In, Viral Vectors for Gene Therapy: Methods and Protocols, Methods in Molecular Biology, 737 (eds. Merten O.W. and Al-Rubeai, M.) Springer Science+Business Media, pp 89-116

Yu, H., Fischer, G., Jia, G., Reiser, J., Park, F. and Hogan, Q.H. (2011) Lentiviral gene transfer into the dorsal root ganglion of adult rats Mol. Pain, 7: 63

Lipid composition/organization
Trautz, B., Wiedemann, H., Lüchtenborg, C., Pierini, V., Kranich, J., Glass, B., Kräusslich, H-G. et al (2017) The host-cell restriction factor SERINC5 restricts HIV-1 infectivity without altering the lipid composition and organization of viral particles J. Biol. Chem., 292, 3702–13713

Maturation
Chojnacki, J., Waithe, D., Carravilla, P., Huarte, N., Galiani, S., Enderlein, J. and Eggeling, C. (2017) Envelope glycoprotein mobility on HIV-1 particles depends on the virus maturation state Nat. Comm. 8: 545

de Marco, A., Müller, B., Glass, B., Riches, J.D., Kräusslich, H-G. and Briggs, J.A.G. (2010) Structural analysis of HIV-1 maturation using cryo-electron tomography PloS Pathogens, 6: e1001215

de Marco, A., Heuser, A-M., Glass, B., Kräusslich, H-G., Müller, B. and Briggs, J.A.G. (2012) Role of the SP2 domain and its proteolytic cleavage in HIV-1 structural maturation and infectivity J. Virol., 86, 13708-13716

Mattei, S., Anders, M., Konvalinka, J., Kräusslich, H-G., Briggs, J.A.G. and Müller, B. (2014) Induced maturation of human immunodeficiency virus J. Virol., 88, 13722–13731

Mattei, S., Tan, A., Glass, B., Müller, B., Kräusslich, H-G. and Briggs, J.A.G. (2018) High-resolution structures of HIV-1 Gag cleavage mutants determine structural switch for virus maturation Proc. Natl. Acad. Sci. USA 115, E9401-E9410

Molecular clones
Tebit, D.M., Zekeng, L., Kaptue, J., Fräusslich, H-G- and Herchenröder, O. (2003) Construction and characterization of a full-length infectious molecular clone from a fast replicating, X4-tropic HIV-1 CRF02.AG primary isolate Virology, 313, 645-652

Morphogenesis
Radestock, B., Morales, I., Rahman, S.A., Radau, S., Glass, B., Zahedi, R.P., Müller, B. and Kräusslich, H.G. (2013) Comprehensive mutational analysis reveals p6Gag phosphorylation to be dispensable for HIV-1 morphogenesis and replication J. Virol., 87, 724-734

Nef protein
Campbell, G.R., Rawat, P., Bruckman, R.S. and Spector, S.A. (2015) Human immunodeficiency virus type 1 Nef inhibits autophagy through transcription factor EB sequestration PLoS Pathog 11: e1005018

Cavrois, M., Neidleman, J., Yonemoto, W., Fenard, D. and Greene, W.C. (2004) HIV-1 virion fusion assay: uncoating not required and no effect of Nef on fusion Virology, 328, 36-44

Lundquist, C.A., Zhou, J. and Aiken, C. (2004) Nef stimulates human immunodeficiency virus type 1 replication in primary T cells by enhancing virion-associated gp120 levels: coreceptor-dependent requirement for Nef in viral replication J. Virol., 78, 6287-6296

Mendonca¸ L.M., Poeys, S.C., Abreu, C.M., Tanuri, A., Costa, L.J., (2014) HIV-1 Nef inhibits protease activity and its absence alters protein content of mature viral particles PLoS One, 9: e95352

Park, I-W., Fan, Y., Luo, X., Ryou, M-G., Liu. J., Green, L. and He, J.J. (2014) HIV-1 Nef is transferred from expressing T cells to hepatocytic cells through conduits and enhances HCV replication PLoS One, 9: e99545

Usami, Y., Wu, Y. and Göttlinger, H.G. (2015) SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef Nature, 526, 218-223

Neuron survival studies
Hossain, M.I., Hoque, A., Lessene, G., Kamaruddin, M.A., Chu, P.W.Y., Ng, I.H.W., Irtegun, S. et al (2015) Dual role of Src kinase in governing neuronal survival Brain Res., 1594, 1–14

Neutralizing antibodies
Li, H., Zony, C., Chen, P. and Chen, B.K. (2017) Reduced potency and incomplete neutralization of broadly neutralizing antibodies against cell-to-cell transmission of HIV-1 with transmitted founder Envs J. Virol., 91: e02425-16

Nuclear entry/nucleic acid interactions/nucleocapsid
Borrenberghs, D., Dirix, L., De Wit, F., Rocha, S., Blokken, J., De Houwer, S., Gijsbers, R., Christ, F., Hofkens, J., Hendrix, J. and Debyser, Z. (2016) Dynamic oligomerization of integrase orchestrates HIV nuclear entry Sci. Rep., 6: 36485

Chen, S., Khorchid, A., Javanbakht, H., Gabor, J., Stello, T., Shiba, K., Musier-Forsyth, K. and Kleiman, L. (2001) Incorporation of lysyl-tRNA synthetase into human immunodeficiency virus type 1 J. Virol., 75, 5043-5048

Mangeat, B., Turelli, P., Caron, G., Friedil, M., Perrin, L. and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Nature, 424, 99-103

Mattei, S., Flemming, A., Anders-Össwein, M., Kräusslich, H-G., Briggs, J.A.G. and Müller, B. (2015) RNA and nucleocapsid are dispensable for mature HIV-1 capsid assembly J. Virol., 89, 9739-9747

Mouland, A.J., Mercier, J., Luo, M., Bernier, L., DesGroseillers, L and Cohen E. (2000) The double-stranded RNA-binding protein Staufen is incorporated in human Immunodeficiency virus type 1: evidence for a role in genomic encapsidation J. Virol., 74, 5441-5451

Müller, B., Tessmer, U., Schubert, U. and Kräusslich, H.G. (2000) Human immunodeficiency virus type 1 Vpr protein is incorporated into the virion in significantly smaller amounts than Gag and is phosphorylated in infected cells J. Virol., 74, 9727-9731

Priet, S., Navarro, J-M., Gros, N., Querat, G. and Sire, J. (2003) Functional role of HIV-1 virion-associated uracil DNA glycosylase 2 in the correction of G:U mispairs to G:C pairs J. Biol. Chem., 278, 4566-4571

Phosphoinositides/Phospholipids/Phospholipase A2
Kim, J-O., Chakrabarti, B.K., Guha-Niyogi, A., Louder, M.K., Mascola, J.R., Ganesh, L. and Nabel, G.J. (2007) Lysis of human immunodeficiency virus type 1 by a specific secreted human phospholipase A2 J. Virol., 81, 1441-1450

Mücksch, F., Citir, M., Lüchtenborg, C., Glass, B., Traynor-Kaplan, A., Schultz, C., Brügger, B. and Kräusslich, H-G. (2019) Quantification of phosphoinositides reveals strong enrichment of PIP2 in HIV-1 compared to producer cell membranes Sci. Rep., 9: 17661

Preintegration complex
Borrenberghs, D., Dirix, L., De Wit, F., Rocha, S., Blokken, J., De Houwer, S., Gijsbers, R., Christ, F., Hofkens, J., Hendrix, J. and Debyser, Z. (2016) Dynamic oligomerization of integrase orchestrates HIV nuclear entry Sci. Rep., 6: 36485

Protein content/interactions/proteomics
Alais, S., Soto-Rifo, R., Balter, V., Gruffat, H., Manet, E., Schaeffer, L., Darlix, J.L., Cimarelli, A., Raposo, G., Ohlmann, T. and Leblanc, P. (2012) Functional mechanisms of the cellular prion protein (PrPC) associated anti-HIV-1 properties Cell. Mol. Life Sci., 69, 1331–1352

Compton, A.A., Roy, N., Porrot, F., Billet, A., Casartelli, N., Yount, J.S., Liang, C. and Schwartz, O. (2016) Natural mutations in IFITM3 modulate post-translational regulation and toggle antiviral specificity EMBO Rep., 17, 1657-1671

Graham, D.R.M. (2016) Proteomic Studies of HIV-1 In HIV-1 Proteomics (eds. Graham, D.R.M. and Ott, D.E.) Springer Science+Business Media New York, pp 39-58

Lin, H-Y., Law, P-Y. and Loh, H.H. (2012) Activation of protein kinase C (PKC) or PKC as an approach to increase morphine tolerance in respiratory depression and lethal overdose J. Pharmacol. Exp. Therapeut., 341, 115-125

Linde, M.E., Colquhoun, D.R., Mohien, C.U., Kole, T., Aquino, V., Cotter, R., Edwards, N., Hildreth, J.E.K. and Graham, D.R. (2013) The conserved set of host proteins incorporated into HIV‑1 virions suggests a common egress pathway in multiple cell types J. Proteome Res., 12, 2045-2054

Mendonca¸ L.M., Poeys, S.C., Abreu, C.M., Tanuri, A., Costa, L.J., (2014) HIV-1 Nef inhibits protease activity and its absence alters protein content of mature viral particles PLoS One, 9: e95352

Pseudoviruses
Parajuli, B., Acharya, K., Bach, H.C., Parajuli, B., Zhang, S., Smith, III, A.B., Abrams, C.F. and Chaiken, I. (2018) Restricted HIV-1 Env glycan engagement by lectin-reengineered DAVEI protein chimera is sufficient for lytic inactivation of the virus Biochem. J., 475, 931–957

Rashad, A.A., Sundaram, R.V.K., Aneja, R., Duffy, C. and Chaiken, I. (2015) Macrocyclic envelope glycoprotein antagonists that irreversibly inactivate HIV‑1 before host cell encounter J. Med. Chem., 58, 7603−7608

Sundaram, R.V.K., Li, H., Bailey, L., Rashad, A.A., Aneja, R., Weiss, K., Huynh, J., Bastian, A.R., et al (2016) Impact of HIV‑1 membrane cholesterol on cell-independent lytic inactivation and cellular infectivity Biochemistry, 55, 447−458

Purification protocols
Coleman J.E., Huentelman, M.J., Kasparov, S., Metcalfe, B.L., Paton, J.F.R., Katovich, M.J., SempleRowland, S.L. and Raizada, M.K. (2003) Efficient large scale production and concentration of HIV-1-based lentiviral vectors for use in vivo Physiol. Genomics, 12, 221-228

Dettenhofer, M. and Yu, X.F. (1999) Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif virions J. Virol., 73, 1460-1467

Henriksson, P., Pfeiffer, T., Zentgraf, H., Alke, A. and Bosch, V. (1999) Incorporation of wild-type and Cterminally truncated human epidermal growth factor receptor into human immunodeficiency virus-like particles: insight into the processes governing glycoproteins incorporation into retroviral particles J. Virol, 73, 9294-9302

Kol, N., Tsvitov, M., Hevroni, L., Wolf, S.G., Pang, H-B., Kay, M.S. and Rousso, I. (2010) The effect of purification method on the completeness of the immature HIV-1 Gag shell J. Virol. Methods 169, 244–247

Wojtkiewicz, M. and Ciborowski, P. (2012) Profiling of HIV proteins in cerebrospinal fluid In Expression Profiling in Neuroscience, Neuromethods, vol. 64 (Ed..Karamanos, Y.) Springer Science+Business Media, pp 225-244

Pyrophosphatase
Ducloux, C., Mougel, M., Goldschmidt, V., Didierlaurent, L., Marquet, R. and Isel, C. (2012) A pyrophosphatase activity associated with purified HIV-1 particles Biochimie, 94, 2498-2507

Replication control
De Wit, F., Pillalamarri, S.R., Sebastián-Martín, A., Venkatesham, A., Van Aerschot, A. and Debyser, Z. (2019) Design of reverse transcriptase–specific nucleosides to visualize early steps of HIV-1 replication by click labeling J. Biol. Chem. (2019) 294, 11863–11875

Radestock, B., Morales, I., Rahman, S.A., Radau, S., Glass, B., Zahedi, R.P., Müller, B. and Kräusslich, H.G. (2013) Comprehensive mutational analysis reveals p6Gag phosphorylation to be dispensable for HIV-1 morphogenesis and replication J. Virol., 87, 724-734

Sirois, M., Robitaille, L., Allary, R., Shah, M., Woelk, C.H., Estaquier, J. and Corbeil, J. (2011) TRAF6 and IRF7 control HIV replication in macrophages PLoS One, 6: e28125

Reservoir markers
Sharaf, R.R. and Li, J.Z. (2017) The Alphabet Soup of HIV Reservoir Markers Curr. HIV/AIDS Rep., 14, 72–81

Restriction factor
Trautz, B., Wiedemann, H., Lüchtenborg, C., Pierini, V., Kranich, J., Glass, B., Kräusslich, H-G. et al (2017) The host-cell restriction factor SERINC5 restricts HIV-1 infectivity without altering the lipid composition and organization of viral particles J. Biol. Chem., 292, 3702–13713

Retrotransposon
Perugi, F., Freslon-Evain, C., Batard, L., Guillet. P. and Schwamborn, K. (2019) The duck EB66® cell substrate reveals a novel retrotransposon Biologicals, 61, 22–31

Reverse transcription
De Wit, F., Pillalamarri, S.R., Sebastián-Martín, A., Venkatesham, A., Van Aerschot, A. and Debyser, Z. (2019) Design of reverse transcriptase–specific nucleosides to visualize early steps of HIV-1 replication by click labeling J. Biol. Chem. (2019) 294, 11863–11875

Ducloux, C., Mougel, M., Goldschmidt, V., Didierlaurent, L., Marquet, R. and Isel, C. (2012) A pyrophosphatase activity associated with purified HIV-1 particles Biochimie, 94, 2498-2507

Lin, M-H., Apolloni, A., Cutillas, V., Sivakumaran, H., Martin, S., Li, D., Wei, T., Wang, R., Jin, H., Spann, K. and Harrich, D. (2015) A mutant Tat protein inhibits HIV-1 reverse transcription by targeting the reverse transcription complex J. Virol, 89, 4827-4836

Rankovic, S., Varadarajan, J., Ramalho, R., Aiken, C. and Rousso, I. (2017) Reverse transcription mechanically initiates HIV-1 capsid disassembly J. Virol., 91: e00289-17

Warrilow, D., Meredith, L., Davis, A., Burrell, C., Li, P. and Harrich, D. (2008) Cell factors stimulate human immunodeficiency virus type 1 reverse transcription in vitro J. Virol., 82, 1425-1437

Warrilow, D., Warren, K. and Harrich, D. (2010) Strand transfer and elongation of HIV-1 reverse transcription is facilitated by cell factors in vitro PloS Pathogens, 5: e13229

RNA
Bogerd, H.P., Kennedy, E.M., Whisnant, A.W. and Cullen, B.R. (2017) Induced packaging of cellular microRNAs into HIV-1 virions can inhibit infectivity mBio, 8: e02125-16

Eckwahl, M.J., Arnion, H., Kharytonchyk, S., Zang, T., Bieniasz, P.D., Telesnitsky, A. and Wolin, S.L. (2016) Analysis of the human immunodeficiency virus-1 RNA packageome RNA, 22, 228–1238

Lassen, K.G., Wissing, S., Lobritz, M.A., Santiago, M. and Greene, W.C. (2010) Identification of two APOBEC3F splice variants displaying HIV-1 antiviral activity and contrasting sensitivity to Vif J. Biol. Chem., 285, 29326–29335

L’Hernault, A., Weiss, E.U., Greatorex, J.S. and Lever, A.M. (2012) HIV-2 genome dimerization is required for the correct processing of Gag: a second-site reversion in matrix can restore both processes in dimerizationimpaired mutant viruses J. Virol., 86, 5867-5876

Mattei, S., Flemming, A., Anders-Össwein, M., Kräusslich, H-G., Briggs, J.A.G. and Müller, B. (2015) RNA and nucleocapsid are dispensable for mature HIV-1 capsid assembly J. Virol., 89, 9739-9747

Onafuwa-Nuga, A.A., Telesnitsky, A. and King, S.R. (2006) 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles RNA, 12, 542-546

Orecchini, E., Federico, M., Doria, M., Arenaccio, C., Giuliani, E., Ciafrè, S.A. and Michienzi, A. (2015) The ADAR1 editing enzyme is encapsidated into HIV-1 virions Virology, 485, 475–480

Rahimian, P. and He, J.J. (2016) HIV-1 Tat-shortened neurite outgrowth through regulation of microRNA-132 and its target gene expression J. Neuroinflamm., 13: 24

Šimonová, A., Svojanovská, B., Trylčová, J., Hubálek, M., Moravčík, O., Zavřel, M., Pávová, M., Hodek, J. et al (2019) LC/MS analysis and deep sequencing reveal the accurate RNA composition in the HIV-1 virion Sci. Rep., 9: 8697

Soros, V.B., Yonemoto, W. and Greene, W.C. (2007) Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA and subsequently activated by RNase H PLoS Pathog., 3:e15

Yukl, S.A., Li, P., Fujimoto, K., Lampiris, H., Lu, C.M., Hare, C.B. Deeks, S.G., Liegler, T., Pandori, M., Havlir, D.V. and Wong, J.K. (2011) Modification of the Abbott RealTime assay for detection of HIV-1 plasma RNA viral loads less than one copy per milliliter J. Virol. Methods, 175, 261– 265

Tat protein
Lin, M-H., Apolloni, A., Cutillas, V., Sivakumaran, H., Martin, S., Li, D., Wei, T., Wang, R., Jin, H., Spann, K. and Harrich, D. (2015) A mutant Tat protein inhibits HIV-1 reverse transcription by targeting the reverse transcription complex J. Virol, 89, 4827-4836

Rahimian, P. and He, J.J. (2016) HIV-1 Tat-shortened neurite outgrowth through regulation of microRNA-132 and its target gene expression J. Neuroinflamm., 13: 247

Tumour necrosis factor (TNF)
Roesch, F., Richard, L., Rua, R., Porrot, F., Casartelli, N. and Schwartz, O. (2015) Vpr enhances tumor necrosis factor production by HIV-1-infected Tcells J. Virol., 89, 12118-12130

Vaccine development/production
Bridgeman, A., Maelfait, J., Davenne, T., Partridge, T., Peng, Y., Mayer, A., Dong, T., Kaever, V., Borrow, P. and Rehwinkel, J. (2015) Viruses transfer the antiviral second messenger cGAMP between cells Science 349, 1228-1232

Perugi, F., Freslon-Evain, C., Batard, L., Guillet. P. and Schwamborn, K. (2019) The duck EB66® cell substrate reveals a novel retrotransposon Biologicals, 61, 22–31

Viral rebound
Joshi, P., Maidji, E. and Stoddart, C.A. (2016) Inhibition of heat shock protein 90 prevents HIV rebound J. Biol. Chem., 291, 10332–10346

Virus cores
Warrilow, D., Stenzel, D. and Harrich, D. (2007) Isolated HIV-1 core is active for reverse transcription Retrovirology, 4:77

Virus inactivation
Contarino, M., Bastian, A.R., Sundaram, R.V.K., McFadden, K., Duffy, C., Gangupomu, V., Baker, M., Abrams, C. and Chaiken, I. (2013) Chimeric cyanovirin-MPER recombinantly engineered proteins cause cellfree virolysis of HIV-1 J. Virol., 87, 4743-4750

Virus Infectivity Factor (Vif)
Baraz, L. and Kotler, M. (2003) The Vif protein of human immunodeficiency virus type 1 (HIV-1): enigmas and solutions Curr. Med. Chem. 11, 221-231

Dettenhofer, M. and Yu, X.F. (1999) Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif virions J. Virol., 73, 1460-1467

Henriet, S., Mercenne, G., Bernacchi, S., Paillart, J-C. and Marquet, R. (2009) Tumultuous relationship between the human immunodeficiency virus type 1 viral infectivity factor (Vif) and the human APOBEC-3G and APOBEC-3F restriction factors Microbiol. Mol. Biol. Rev., 73, 211-232

Lassen, K.G., Wissing, S., Lobritz, M.A., Santiago, M. and Greene, W.C. (2010) Identification of two APOBEC3F splice variants displaying HIV-1 antiviral activity and contrasting sensitivity to Vif J. Biol. Chem., 285, 29326–29335

Mangeat, B., Turelli, P., Caron, G., Friedil, M., Perrin, L. and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Nature, 424, 99-103

Stopak, K., de Noronha, C., Yonemoto, W. and Greene, W.C. (2003) HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability Mol. Cell, 12, 591-601

Virus-like particle production
Jurgens, C.K., Young, K.R., Madden, V.J., Johnson, P.R. and Johnston, R.E. (2012) A novel self-replicating chimeric lentivirus-like particle J. Virol., 86, 246-261

Kessans, S.A., Linhart, M.D., Matoba, N. and Mor, T. (2013) Biological and biochemical characterization of HIV-1 Gag/dgp41 virus-like particles expressed in Nicotiana benthamiana Plant Biotech. J., 11, 681–690

Li, L., Wang, X-H., Banerjee, S., Volsky, B., Williams, C., Virland, D., Nadas, A., Seaman, M.S., Chen, X., Spearman, P., Zolla-Pazner, S. and Gorny, M.K. (2012) Different pattern of immunoglobulin gene usage by HIV-1 compared to non-HIV-1 antibodies derived from the same infected subject PLoS One, 7: e39534

Lynch, A.G., Tanzer, F., Fraser, M.J., Shephard, E.G., Williamson, A-L. and Rybicki, E.P. (2010) Use of the piggyBac transposon to create HIV-1 gag transgenic insect cell lines for continuous VLP production BMC Biotechnology 2010, 10:30

Lynch, A., Meyers, A.E., Williamson, A-L. and Rybicki, E.P. (2012) Stability studies of HIV-1 Pr55gag virus-like particles made in insect cells after storage in various formulation media Virol. J., 9: 210

Meador, L.R., Kessans, S.A., Kilbourne, J., Kibler, K.V., Pantaleo, G., Esteban Roderiguez, M., Blattman, J.N., Jacobs, B.L. and Mor, T.S. (2017) A heterologous prime-boosting strategy with replicating Vaccinia virus vectors and plant-produced HIV-1 Gag/dgp41 virus-like particles Virology, 507, 242–256

Muratori, C., D’Aloja, P., Superti, F., Tinari, A., Sol-Foulon, N., Sparacio, S., Bosch, V., Schwartz, O. and Federico, M. (2006) Generation and characterization of a stable cell population releasing fluorescent HIV-1- based virus like particles in an inducible way BMC Biotechnol., 6:52

Stano, A., Leaman, D.P., Kim, A.S., Zhang, L., Autin, L., Ingale, J., Gift, S.K. et al (2017) Dense array of spikes on HIV-1 virion particles J. Virol., 91: e00415-17

6 Spumaviridae

Spumavirus – Foamy virus
Capsid assembly/particle release
Hamann, M.V., Müllers, E., Reh, J., Stanke, N., Effantin, G., Weissenhorn, W. Lindemann, D. (2014) The cooperative function of arginine residues in the prototype foamy virus Gag C-terminus mediates viral and cellular RNA encapsidation Retrovirology, 11: 87

Envelope glycoproteins/proteins
Geiselhart, V., Schwantes, A., Bastone, P., Frech, M. and Lochelt, M. (2003) Features of the Env leader protein and the N-terminal Gag domain of feline foamy virus important for virus morphogenesis Virology, 310, 235-244

Geiselhart, V., Bastone, P., Kempf, T., Schnölzer, M. and Löchelt, M. (2004) Furin-mediated cleavage of the feline foamy virus Env leader protein J. Virol., 78, 13573-13581

Life, R.B., Lee, E-G., Eastman, S.W. and Linial, M.L. (2008) Mutations in the amino terminus of foamy virus Gag disrupt morphology and infectivity but do not target cell assembly J. Virol., 82, 6109-6119

Lindemann, D., Pietschmann, T., Picard-Maurreau, M., Berg, A., Heinkelein, M., Thurow, J., Knaus, P., Zentgraf, H. and Rethwilm, A. (2001) A particle-associated glycoprotein signal peptide essential for virus maturation and infectivity J. Virol., 75, 5762-5771

Shaw, K.L., Lindemann, D., Mulligan, M.J. and Goepfert, P.A. (2003) Foamy virus envelope glycoprotein is sufficient for particle budding and release J. Virol., 77, 2338-2348

Wilk, T., Geiselhart, V., Frech, M., Fuller, S.D., Flügel, R.M. and Löchelt, M. (2001) Specific interaction of a novel foamy virus env leader protein with the N-terminal Gag domain J. Virol., 75, 7995-8007

Immune response
Rua, R., Lepelley, A., Gessain, A. and Schwartz, O. (2012) Innate sensing of foamy viruses by human hematopoietic cells J. Virol., 86, 909-918

Pol incorporation
Baldwin, D.N. and Linial, M.L. (1999) Proteolytic activity, the carboxy terminus of Gag, and the primer binding site are not required for Pol incorporation into foamy virus particles J. Virol., 73, 6387-6393

Cartellieri, M., Rudolph, W., Herchenröder, O., Lindemann, D. and Rethwilm, A. (2005) Determination of the relative amounts of Gag and Pol proteins in foamy virus particles Retrovirology, 2:44

Lee, E-G. and Linial, M.L. (2008) The C terminus of foamy retrovirus Gag contains determinants for encapsidation of Pol protein into virions J. Virol., 82, 10803-10810

Lee, E-G., Sinicrope, A., Jackson, D.L., Yu, S.F. and Linial, M.L. (2012) Foamy virus Pol protein expressed as Gag-Pol fusion retains enzymatic activities, allowing for infectious virus production J. Virol., 86, 5992–6001

Spannaus, R. and Bodem, J. (2014) Determination of the protease cleavage site repertoire-the RNase H but not the RT domain is essential for foamy vireyal protease activity Virology, 454-455, 145–156

Swiersy, A., Wiek, C., Reh, J., Zentgraf, H. and Lindemann, D. (2011) Orthoretroviral-like prototype foamy virus gag-pol expression is compatible with viral replication Retrovirology, 8: 66

Purification
Spannaus, R., Miller, C., Lindemann, D. and Bodem, J. (2017) Purification of foamy viral particles Virology 506, 28–33

OptiPrep™ Reference List RV06: 2nd edition, January 2020

OptiPrep™ Reference List RV07

GROUP VII VIRUSES

• Hepatitis B is the only Group VII virus that has been reported to be effectively purified in an iodixanol gradient, prepared from OptiPrep™.
• Publications are listed alphabetically by first author and, where necessary, references are further divided according to research topic.
• Multiple entries from the same first author are listed chronologically.
• For a detailed methodology of Group VII viruses see OptiPrep™Application Sheet V36. V06 is a methodological review of OptiPrep™ technology.

 

Hepatitis B virus

Abdul, F., Ndeboko, B., Buronfosse, T., Zoulim, F., Kann, M., Nielsen, P.E. and Cova, L. (2012) Potent inhibition of late stages of hepadnavirus replication by a modified cell penetrating peptide PLoS One, 7: e48721

Aillot, L., Bonnin, M., Ait-Goughoulte, M., Bendriss-Vermare, N., Maadadi, S., Dimier, L., Subic, M., Scholtes, C., Najera, I. et al (2018) Interaction between toll-like receptor 9-CpG oligodeoxynucleotides and

hepatitis B virus virions leads to entry inhibition in hepatocytes and reduction of alpha interferon production by plasmacytoid dendritic cells Antimicrob. Agents Chemother., 62: e01741-17

Bardens, A., Döring, T., Stieler, J. and Prange, R. (2011) Alix regulates egress of hepatitis B virus naked capsid particles in an ESCRT-independent manner Cell. Microbiol., 13, 602–619

Burwitz, B.J., Wettenge, L.M., Mück-Häus, M.A., Ringelhan, M., Ko, C., Festag, M.M., Hammond, K.B., Northrup, M. et al (2017) Hepatocytic expression of human sodium taurocholate co-transporting polypeptide enables hepatitis B virus infection of macaques Nat. Comm., 8: 2146

Faure-Dupuy, S., Delphin, M., Ailot, L., Dimier, L….. Heikenwalder, M., Durantel, D., Lucifora, J. et al (2019) Hepatitis B virus-incuded modulation of liver macrophage function promotes hepatocyte infection J. Hepatol., 71, 1086-1098

Feng, X., Liu, H., Chu, X., Sun, P., Huang, W., Liu, C., Yang, X., Sun, W., Bai, H. and Ma, Y. (2019) Recombinant virus-like particles presenting IL-33 successfully modify the tumor microenvironment and facilitate antitumor immunity in a model of breast cancer Acta Biomaterialia, 100, 316–325

Hallez, C., Li, X., Suspène, R., Thiers, V., Bouzidi, M.S., Dorobantu, C.M., Lucansky, V., Wain-Hobson, S., Gaudin, R. and Vartanian, J-P., (2019) Hypoxia-induced human deoxyribonuclease I is a cellular restriction factor of hepatitis B virus Nat. Microbiol., 1196, 1196–1207

Inoue, J. et al (2017) Rab5B determines HBV release pathways by promoting transport of LHBs from ER to MVB Hepatology, 66 (Suppl.) Abstr. #1491

Kim, S., Lee, J. and Ryu, W-S. (2009) Four conserved cysteine residues of the hepatitis B virus polymerase are critical for RNA pregenome encapsidation J. Virol., 83, 8032-8040

Komatsu, H., Inui, A., Murano, T., Tsunoda, T., Sogo, T. 2 and Fujisawa, T. (2015) Lack of infectivity of HBV in feces from patients with chronic hepatitis B virus infection, and infection using chimeric mice BMC Res. Notes, 8: 366

Kratochwil, N.A., Triyatni, M., Mueller, M.B., Klammers, F., Leonard, B., Turley, D., Schmaler, J., Ekiciler, A., Molitor, B. et al (2018) Simultaneous assessment of clearance, metabolism, induction, and drug-drug interaction potential using a long-term in vitro liver model for a novel hepatitis B virus inhibitor J. Pharmacol. Exp. Ther., 365, 237–248

Li, F., Cheng, L., Murphy, C.M., Reszka-Blanco, N.J., Wu, Y., Chi, L., Hu, J. and Su, L. (2016) Minicircle HBV cccDNA with a Gaussia luciferase reporter for investigating HBV cccDNA biology and developing cccDNA-targeting drugs Sci. Rep., 6: 36483

Lam, A.M., Ren, S., Espiritu, C., Kelly, M., Lau, V., Zheng, L., Hartman, G.D., Flores, O.A. and Klumpp, K. (2017) Hepatitis B virus capsid assembly modulators, but not nucleoside analogs, inhibit the production of extracellular pregenomic RNA and spliced RNA variants Antimicrob. Agents Chemother., 61: e00680-17

Maepa, M.B., Ely, A., Grayson, W. and Arbuthnot, P. (2017) Sustained inhibition of HBV replication in vivo after systemic injection of AAVs encoding artificial antiviral primary microRNAs Mol. Ther. Nucleic Acids, 7, 190-199

Montpellier, C. et al (2018) Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein J. Hepatol., 68 (Suppl. 1) Abstr. SAT-386

Scott, T., Moyo, B., Nicholson, S., Maepa, M.B., Watashi, K., Ely, A., Weinberg, M.S. and Arbuthnot, P. (2017) ssAAVs containing cassettes encoding SaCas9 and guides targeting hepatitis B virus inactivate replication of the virus in cultured cells Sci. Rep., 7: 7401

Verrier, E.R., Colpitts, C.C., Bach, C., Heydmann, L., Weiss, A., Renaud, M., Durand, S.C., Habersetzer, F., Durante, D. et al (2016) A targeted functional RNA interference screen uncovers glypican 5 as an entry factor for hepatitis B and D viruses Hepatology, 36, 35-48

Wang, H., Kim, S. and Ryu, W-S. (2009) DDX3 DEAD-box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids J.Virol., 83, 5815–5824

Yao, Y., Yang, B., Chen, Y., Wang, H., Hu, X., Zhou, Y., Gao, X., Lu, M., Niu, J. et al (2019) RNA-binding motif protein 24 (RBM24) is involved in pregenomic RNA packaging by mediating interaction between hepatitis B virus polymerase and the epsilon element J. Virol., 93, e02161-18

Zannetti, C., Roblot, G., Charrier, E., Ainouze, M., Tout, I., Briat, F., Isorce, N., Faure-Dupuy, S., Michelet, M. et al (2016) Characterization of the inflammasome in human Kupffer cells in response to synthetic agonists and pathogens J. Immunol., 197, 356-367

OptiPrep™ Reference List RV07: 2nd edition, January 2020

OptiPrep™ Reference List RV08

UNCLASSIFIED VIRUSES & SURVEYS

• Some viruses have not been classified according to the Baltimore system. This Reference List describes applications of these viruses that have been purified in OptiPrep™-based gradients.
• This Reference List also includes papers describing disease surveys (Section 8)

 

1. Archaeal viruses

Sulfolobus

Monocaudavirus
Uldahl, K.B., Wu, L., Hall, A., Papathanasiou, P., Peng, X. and Moghimi, S.M. (2016) Recognition of extremophilic archaeal viruses by eukaryotic cells: a promising nanoplatform from the third domain of life Sci. Rep., 6: 37966

Uldahl, K.B., Walk, S.T., Olshefsky, S.C., Young, M.J. and Peng, X. (2017) SMV1, an extremely stable thermophilic virus platform for nanoparticle trafficking in the mammalian GI tract J. Appl. Microbiol., 123, 1286-1297

Wu, L., Uldahl, K.B., Chen, F., Benasutti, H., Logvinski, D., Vu, V., Banda, N.K., Peng, X., Simberg, D. and Moghimi, S.M. (2017) Interaction of extremophilic archaeal viruses with human and mouse complement system and viral biodistribution in mice Mol. Immunol., 90, 273-279

Spindle-shaped virus 2
Uldahl, K.B., Wu, L., Hall, A., Papathanasiou, P., Peng, X. and Moghimi, S.M. (2016) Recognition of extremophilic archaeal viruses by eukaryotic cells: a promising nanoplatform from the third domain of life Sci. Rep., 6: 37966

Thermococcus prieurii virus 1
Gorlas, A., Koonin, E.V., Bienvenu, N., Prieur, D. and Geslin, C. (2012) TPV1, the first virus isolated from the hyperthermophilic genus Thermococcus Environ. Microbiol., 14, 503–516

2. Bovine serum viruses

Funk, M., Gunst, K., Lucansky, V., Müller, H., zur Hausen, H., de Villiers, E-M. (2014) Isolation of proteinassociated circular DNA from healthy cattle serum Genome Announce., 2: e00846-14

3. Circovirus (Circoviridae)

Parras-Moltó, M., Rodríguez-Galet, A., Suárez-Rodríguez, P. and López-Bueno, A. (2018) Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses Microbiome, 6: 119

Wang, H., Zhang, K., Lin, C., Zhou, J., Jin, Y., Dong, W., Gu, J., Zhou, J. (2019) Conformational changes and nuclear entry of porcine circovirus without disassembly J. Virol., 93: e00824-19

4. Hepatitis A Virus (Picornaviridae)

Costafreda, M.I. and Kaplan, G. (2019) Reply to Das et al., “TIM1 (HAVCR1): an essential ‘receptor’ or an ‘accessory attachment factor’ for Hepatitis A virus?” J. Virol., 93, e02040-18

Das, A., Maury, W., Lemon, S.M. (2019) TIM1 (HAVCR1): an essential “receptor” or an “accessory attachment factor” for hepatitis A virus? J. Virol., 93, e01793-18

5. Human T cell lymphotropic (leukaemia) virus (HTLV1) Deltaretrovirus

Cao, S., Maldonado, J.O., Grigsby, I.F., Mansky, L.M. and Zhang, W. (2015) Analysis of human T-cell leukemia virus type 1 particles by using cryo-electron tomography J. Virol., 89, 2182-2191

Hémonnot, B., Molle, D., Bardy, M., Gay, B., Laune, D., Devaux, C. and Briant, L. (2006) Phosphorylation of the HTLV-1 matrix L-domain-containing protein by virus-associated ERK-2 kinase Virology, 349, 430-439

Martin, J.L., Mendonça, M., Marusinec, R., Zuczek, J., Angert, I., Blower, R.J., Mueller, J.D., Perilla, J.R. et al (2018) Critical role of the human T-cell leukemia virus type 1 capsid N-terminal domain for Gag-Gag interactions and virus particle assembly J. Virol., 14: e00333-18

Meissner, M.E., Mendonça, L.M., Zhang, W. and Mansky, L.M. (2017) Polymorphic nature of human T-cell leukemia virus type 1 particle cores as revealed through characterization of a chronically infected cell line J. Virol., 91: e00369-17

Møller-Larsen, A. and Christensen, T. (1998) Isolation of a retrovirus from multiple sclerosis patients in selfgenerated iodixanol gradients J. Virol. Methods, 73, 151-161

6. Malaria (virus-like particle production)

SpyTag-AP205 VLPs
Singh, S.K., Thrane, S., Janitzek, C.M., Nielsen, M.A., Theander, T.G., Theisen, M., Salanti, A. and Sander, A.F. (2017) Improving the malaria transmission-blocking activity of a Plasmodium falciparum 48/45 based vaccine antigen by SpyTag/SpyCatcher mediated virus-like display Vaccine, 35, 3726–3732

7. Malarial vaccine

Janitzek, C.M., Peabody, J., Thrane, S., Carlsen, P.H.R., Theander, T.G., Salanti, A., Chackerian, B., Nielsen, M.A. and Sander, A.F. (2019) A proof-of-concept study for the design of a VLP-based combinatorial HPV and placental malaria vaccine Sci. Rep., 9: 5260

8. Metagenomic surveys

Parras-Moltó, M., Rodríguez-Galet, A., Suárez-Rodríguez, P. and López-Bueno, A. (2018) Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses Microbiome, 6: 119

Dugat-Bony, E., Lossouarn, J., De Paepe, M., Sarthou, A-S., Fedala, Y., Petit, M.A. and Chaillou, S. (2020) Viral metagenomic analysis of the cheese surface: a comparative study of rapid procedures for extracting viral particles Food Microbiology 85 (2020) 103278

9. Nodavirus

Macrobrachium rosenbergii
Gangnonngiw, W., Bunnontae, M., Phiwsaiya, K., Senapin, S. and Dhar, A.K. (2020) In experimental challenge with infectious clones of Macrobrachium rosenbergii nodavirus (MrNV) and extra small virus (XSV), MrNV alone can cause mortality in freshwater prawn (Macrobrachium rosenbergii) Virology, 540, 30–37

10. Oncolytic viruses

Selman, M., Rousso, C., Bergeron, A., Son, H.H., Krishnan, R., El-Sayes, N.A., Varette, O., Chen, A. et al (2018) Multi-modal potentiation of oncolytic virotherapy by vanadium compounds Mol. Ther., 26, 56-69

11. Plant virus-like particles

Van Zyl, A.R. and Hitzeroth, I.I. (2016) Purification of virus-like particles (VLPs) from plants In Vaccine Design: Methods and Protocols, Vol. 2: Vaccines for Veterinary Diseases, Methods in Molecular Biology, vol. 1404 (ed. Thomas, S.) Springer Science+Business Media New York pp 569-579

12. Plasmids

Antarctic haloarchaeon

Erdmann, S., Tschitschko, B., Zhong, L., Raftery, M.J. and Cavicchioli, R. (2017) A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells Nat. Microbiol., 1446, 1446–1455

13. Saliva viruses

Parras-Moltó, M., Rodríguez-Galet, A., Suárez-Rodríguez, P. and López-Bueno, A. (2018) Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses Microbiome, 6: 119

14. Vaccine manufacture

Zhao, M., Vandersluis, M., Stout, J., Haupts, U., Sanders, M. and Jacquemart, R. (2019) Affinity chromatography for vaccines manufacturing: Finally ready for prime time? Vaccine, 37, 5491–5503

OptiPrep™ Reference List RV08: 1st edition, January 2020