Recombinant adeno-associated virus: Clinical application and development as a gene-therapy vector

Therapeutic Delivery

Volumn 3, Issue 7, 2012, Pages 835-856

  Xiao, Ping Jie ^a,b   Lentz, Thomas B ^a   Samulski, R Jude ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; ALPHA SARCOGLYCAN; ASPARTOACYLASE; BLOOD CLOTTING FACTOR 9; CAPSID PROTEIN; CARDIOVASCULAR AGENT; GENE THERAPY AGENT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; LIPOPROTEIN LIPASE; NEURTURIN; PARVOVIRUS VECTOR; PROTEIN RPE65; PROTEIN SERCA2A; TRANSMEMBRANE CONDUCTANCE REGULATOR; TUMOR NECROSIS FACTOR IMMUNOGLOBULIN FC DOMAIN FUSION PROTEIN; UNCLASSIFIED DRUG; VISUAL PIGMENT;

ABSENCE OF SIDE EFFECTS; ADENOVIRUS; ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTHRITIS; CELL INTERACTION; CYSTIC FIBROSIS; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION REGULATION; HEART FAILURE; HEMOPHILIA B; HERPES SIMPLEX VIRUS; HUMAN; HYPERLIPOPROTEINEMIA TYPE 1; IMMUNE RESPONSE; LEBER CONGENITAL AMAUROSIS; LIFE CYCLE STAGE; LIMB GIRDLE MUSCULAR DYSTROPHY; LOW DRUG DOSE; NEUROLOGIC DISEASE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN INTERACTION; RETROVIRUS; REVIEW; RNA TRANSLATION; SEROTYPE; SITE DIRECTED MUTAGENESIS; UNSPECIFIED SIDE EFFECT; VIRAL GENE DELIVERY SYSTEM; VIRUS DETECTION;

EID: 84864576522     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.63     Document Type: Review

References (253)

1. Osterman JV, Waddell A, Aposhian HV. Gene therapy systems. the need, experimental approach, and implications. Ann. NY Acad. Sci. 179, 514-519 (1971).
2. Rogers S. Gene therapy: A potentially invaluable aid to medicine and mankind. Res. Commun. Chem. Pathol. Pharmacol. 2(4), 587-600 (1971).
3. Rosenberg SA, Aebersold P, Cornetta K et al. Gene transfer into humans-immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. New Engl. J. Med 323(9), 570-578 (1990).
4. Bartel M, Schaffer D, Buning H. Enhancing the clinical potential of AAV vectors by capsid engineering to evade pre-existing immunity. Frontiers Microbiology 2, 204 (2011).
5. Mccown TJ. Adeno-associated virus (AAV) vectors in the CNS. Curr. Gene Ther. 11(3), 181-188 (2011).
6. Pacak CA, Byrne BJ. AAV vectors for cardiac gene transfer. experimental tools and clinical opportunities. Mol. Ther. 19(9), 1582-1590 (2011).
7. Stein L, Roy K, Lei L, Kaushal S. Clinical gene therapy for the treatment of RPE65- associated Leber congenital amaurosis. Exp. Opin. Biol. Ther. 11(3), 429-439 (2011).
8. Van Der Laan LJ, Wang Y, Tilanus HW, Janssen HL, Pan Q. AAV-mediated gene therapy for liver diseases. the prime candidate for clinical application? Exp. Opin. Biol. Ther. 11(3), 315-327 (2011).
9. Wang J, Faust SM, Rabinowitz JE. The next step in gene delivery. molecular engineering of adeno-associated virus serotypes. J. Mol. Cell. Cardiol. 50(5), 793-802 (2011).
10. Bartel MA, Weinstein JR, Schaffer DV. Directed evolution of novel adeno-associated viruses for therapeutic gene delivery. Gene Ther. 19(6), 694-700 (2012).
11. Griesenbach U, Alton EW. Progress in gene and cell therapy for cystic fibrosis lung disease. Curr. Pharmaceut. Design 18(5), 642-662 (2012).
12. Nonnenmacher M, Weber T. Intracellular transport of recombinant adeno-associated virus vectors. Gene Ther. 19, 649-658 (2012).
13. Grieger JC, Samulski RJ. Adeno-associated virus vectorology, manufacturing, and clinical applications. Methods Enzymol. 507, 229-254 (2012).
14. Kawabata K, Takakura Y, Hashida M. The fate of plasmid DNA after intravenous injection in mice. involvement of scavenger receptors in its hepatic uptake. Pharma. Res. 12(6), 825-830 (1995).
15. Gray SJ, Samulski RJ. Optimizing gene delivery vectors for the treatment of heart disease. Exp. Opin. Biol. Ther. 8(7), 911-922 (2008).
16. Wolff J, Lewis Dl, Herweijer H, Hegge J, Hagstrom J. Non-viral approaches for gene transfer. Acta Myol. 24(3), 202-208 (2005).
17. Yazawa H, Murakami T, Li Hm et al. Hydrodynamics-based gene delivery of naked DNA encoding fetal liver kinase-1 gene effectively suppresses the growth of pre-existing tumors. Cancer Gene Ther. 13(11), 993-1001 (2006).
18. Hoen DR, Park KC, Elrouby N et al. Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol. Biol. Evolution 23(6), 1254-1268 (2006).
19. Liu F, Shollenberger LM, Conwell CC, Yuan X, Huang L. Mechanism of naked DNA clearance after intravenous injection. J. Gene Med. 9(7), 613-619 (2007).
20. Pollard H, Remy JS, Loussouarn G, Demolombe S, Behr JP, Escande D. Polyethylenimine but not cationic lipids promotes transgene delivery to the nucleus in mammalian cells. J. Biol. Chem. 273(13), 7507-7511 (1998).
21. Bieber T, Meissner W, Kostin S, Niemann A, Elsasser HP. Intracellular route and transcriptional competence of polyethylenimine-DNA complexes. J. Control. Rel. 82(2-3), 441-454 (2002).
22. Dean DA, Strong DD, Zimmer WE. Nuclear entry of nonviral vectors. Gene Ther. 12(11), 881-890 (2005).
23. Watson P, Jones AT, Stephens DJ. Intracellular trafficking pathways and drug delivery. fluorescence imaging of living and fixed cells. Adv. Drug Deliv. Rev. 57(1), 43-61 (2005).
24. Luo D, Saltzman WM. Synthetic DNA delivery systems. Nat. Biotechnol. 18(1), 33-37 (2000).
25. Chen T, Wang Z, Wang R, Lu T, Wang W. Polyethylenimine-DNA solid particles for gene delivery. J. Drug Target. 15(10), 714-720 (2007).
26. Gupta B, Levchenko TS, Torchilin VP. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv. Drug Deliv. Rev. 57(4), 637-651 (2005).
27. Hashida M, Nishikawa M, Yamashita F, Takakura Y. Cell-specific delivery of genes with glycosylated carriers. Adv. Drug Deliv. Rev. 52(3), 187-196 (2001).
28. Yu W, Zhang N, Li C. Saccharide modified pharmaceutical nanocarriers for targeted drug and gene delivery. Curr. Pharmaceut. Design 15(32), 3826-3836 (2009).
29. Wells DJ. Electroporation and ultrasound enhanced non-viral gene delivery in vitro and in vivo. Cell Biol. Toxicol. 26(1), 21-28 (2010).
30. Rissanen TT, Yla-Herttuala S. Current status of cardiovascular gene therapy. Mol. Ther. 15(7), 1233-1247 (2007).
31. Osten P, Grinevich V, Cetin A. Viral vectors: A wide range of choices and high levels of service. Handb. Exp. Pharmacol. 178, 177-202 (2007).
32. Goff SP. Retroviridae: The retroviruses and their replication. In: Fields Virology, Knipe DM, Howley PM (Eds). Lippincott-Raven Publishers, PA, USA, 1871-1940 (2001).
33. Miller DG, Adam MA, Miller AD. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell. Biol. 10(8), 4239-4242 (1990).
34. Robbins PD, Ghivizzani SC. Viral vectors for gene therapy. Pharmacol. Ther. 80(1), 35-47 (1998).
35. Chinen J, Davis J, De Ravin SS et al. Gene therapy improves immune function in preadolescents with X-linked severe combined immunodeficiency. Blood 110(1), 67-73 (2007).
36. Gaspar HB, Parsley KL, Howe S et al. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364(9452), 2181-2187 (2004).
37. Cavazzana-Calvo M, Fischer A. Gene therapy for severe combined immunodeficiency. Are we there yet? J. Clin. Investig. 117(6), 1456-1465 (2007).
38. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J. Virol. 72(10), 8150-8157 (1998).
39. Bahner I, Sumiyoshi T, Kagoda M et al. Lentiviral vector transduction of a dominant-negative Rev gene into human CD34+ hematopoietic progenitor cells potently inhibits human immunodeficiency virus-1 replication. Mol. Ther. 15(1), 76-85 (2007).
40. Schnell T, Foley P, Wirth M, Munch J, Uberla K. Development of a self-inactivating, minimal lentivirus vector based on simian immunodeficiency virus. Hum. Gene Ther. 11(3), 439-447 (2000).
41. Bank A, Dorazio R, Leboulch P. A Phase I/II clinical trial of beta-globin gene therapy for beta-thalassemia. Ann. NY Acad. Sci. 1054, 308-316 (2005).
42. Cartier N, Hacein-Bey-Abina S, Bartholomae CC et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326(5954), 818-823 (2009).
43. Li Mj, Kim J, Li S et al. Long-term inhibition of HIV-1 infection in primary hematopoietic cells by lentiviral vector delivery of a triple combination of anti-HIV shRNA, anti- CCR5 ribozyme, and a nucleolar-localizing TAR decoy. Mol. Ther. 12(5), 900-909 (2005).
44. Williams DA. ESCGT 2008: progress in clinical gene therapy. Mol. Ther. 17(1), 1-2 (2009).
45. Bonci D, Cittadini A, Latronico MV et al. 'Advanced' generation lentiviruses as efficient vectors for cardiomyocyte gene transduction in vitro and in vivo. Gene Ther. 10(8), 630-636 (2003).
46. Ellis J. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum. Gene Ther. 16(11), 1241-1246 (2005).
47. Towers GJ. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4, 40 (2007).
48. Campos SK, Barry MA. Current advances and future challenges in Adenoviral vector biology and targeting. Curr. Gene Ther. 7(3), 189-204 (2007).
49. Kovesdi I, Brough DE, Bruder JT, Wickham TJ. Adenoviral vectors for gene transfer. Curr. Opin. Biotechnol. 8(5), 583-589 (1997).
50. Chen HH, Mack LM, Kelly R, Ontell M, Kochanek S, Clemens PR. Persistence in muscle of an adenoviral vector that lacks all viral genes. Proc. Natl Acad. Sci. USA 94(5), 1645-1650 (1997).
51. Ghosh SS, Gopinath P, Ramesh A. Adenoviral vectors: A promising tool for gene therapy. Appl. Biochem. Biotechnol. 133(1), 9-29 (2006).
52. Mata-Espinosa DA, Mendoza-Rodriguez V, Aguilar-Leon D, Rosales R, Lopez-Casillas F, Hernandez-Pando R. Therapeutic effect of recombinant adenovirus encoding interferon-gamma in a murine model of progressive pulmonary tuberculosis. Mol. Ther. 16(6), 1065-1072 (2008).
53. Roth JA. Adenovirus p53 gene therapy. Exp. Opin. Biol. Ther. 6(1), 55-61 (2006).
54. Douglas JT. Adenoviral vectors for gene therapy. Mol. Biotech. 36(1), 71-80 (2007).
55. Fink DJ, Glorioso JC. Engineering herpes simplex virus vectors for gene transfer to neurons. Nat. Med. 3(3), 357-359 (1997).
56. Geller AI. Herpes simplex virus-1 plasmid vectors for gene transfer into neurons. Adv. Neurol. 72, 143-148 (1997).
57. Kass SU, Landsberger N, Wolffe AP. DNA methylation directs a time-dependent repression of transcription initiation. Curr. Biol. 7(3), 157-165 (1997).
58. Lilley CE, Groutsi F, Han Z et al. Multiple immediate-early gene-deficient herpes simplex virus vectors allowing efficient gene delivery to neurons in culture and widespread gene delivery to the central nervous system in vivo. J. Virol. 75(9), 4343-4356 (2001).
59. Sun M, Zhang GR, Kong L et al. Correction of a rat model of Parkinson's disease by coexpression of tyrosine hydroxylase and aromatic amino acid decarboxylase from a helper virus-free herpes simplex virus type 1 vector. Hum. Gene Ther. 14(5), 415-424 (2003).
60. Suzuki M, Chiocca EA, Saeki Y. Stable transgene expression from HSV amplicon vectors in the brain: potential involvement of immunoregulatory signals. Mol. Ther. 16(10), 1727-1736 (2008).
61. Fraefel C, Song S, Lim F et al. Helper virus-free transfer of herpes simplex virus type 1 plasmid vectors into neural cells. J. Virol. 70(10), 7190-7197 (1996).
62. Mueller C, Flotte TR. Clinical gene therapy using recombinant adeno-associated virus vectors. Gene therapy 15(11), 858-863 (2008).
63. Berns KI, Pinkerton TC, Thomas GF, Hoggan MD. Detection of adeno-associated virus (AAV)-specific nucleotide sequences in DNA isolated from latently infected Detroit 6 cells. Virology 68(2), 556-560 (1975).
64. Rabinowitz JE, Rolling F, Li C et al. 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(2), 791-801 (2002).
65. Atchison RW, Casto BC, Hammon WM. Adenovirus-associated defective virus particles. Science 149(3685), 754-756 (1965).
66. Hoggan MD, Blacklow NR, Rowe WP. Studies of small DNA viruses found in various adenovirus preparations. physical, biological, and immunological characteristics. Proc. Natl Acad. Sci. USA 55(6), 1467-1474 (1966).
67. Ding W, Zhang L, Yan Z, Engelhardt JF. Intracellular trafficking of adeno-associated viral vectors. Gene Ther. 12(11), 873-880 (2005).
68. Mccarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther. 10(26), 2112-2118 (2003).
69. Kyostio SR, Owens RA, Weitzman MD, Antoni BA, Chejanovsky N, Carter BJ. Analysis of adeno-associated virus (AAV) wild-type and mutant Rep proteins for their abilities to negatively regulate AAV p5 and p19 mRNA levels. J. Virol. 68(5), 2947-2957 (1994).
70. Buning H, Braun-Falco M, Hallek M. Progress in the use of adeno-associated viral vectors for gene therapy. Cells Tissues Organs 177(3), 139-150 (2004).
71. Johnson JS, Li C, Diprimio N, Weinberg MS, Mccown TJ, Samulski RJ. Mutagenesis of adeno-associated virus type 2 capsid protein VP1 uncovers new roles for basic amino acids in trafficking and cell-specific transduction. J. Virol. 84(17), 8888-8902 (2010).
72. Sonntag F, Kother K, Schmidt K et al. The assembly-activating protein promotes capsid assembly of different adeno-associated virus serotypes. J. Virol. 85(23), 12686-12697 (2011).
73. Sonntag F, Schmidt K, Kleinschmidt JA. A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc. Natl Acad. Sci. USA 107(22), 10220-10225 (2010).
74. Summerford C, Samulski RJ. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72(2), 1438-1445 (1998).
75. Qing K, Mah C, Hansen J, Zhou S, Dwarki V, Srivastava A. Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat. Med. 5(1), 71-77 (1999).
76. Summerford C, Bartlett JS, Samulski RJ. AlphaVbeta5 integrin. a co-receptor for adeno-associated virus type 2 infection. Nat. Med. 5(1), 78-82 (1999).
77. Kaminsky PM, Keiser NW, Yan Z, Lei-Butters DC, Engelhardt JF. Directing integrin-linked endocytosis of recombinant AAV enhances productive FAK-dependent transduction. Mol. Ther. 20(5), 972-983 (2012).
78. Girod A, Wobus CE, Zadori Z et al. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J. General Virol. 83(Pt 5), 973-978 (2002).
79. Xiao W, Warrington KH Jr, Hearing P, Hughes J, Muzyczka N. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J. Virol. 76(22), 11505-11517 (2002).
80. Grieger JC, Snowdy S, Samulski RJ. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 80(11), 5199-5210 (2006).
81. Samulski RJ, Zhu X, Xiao X et al. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J. 10(12), 3941-3950 (1991).
82. Giraud C, Winocour E, Berns KI. Recombinant junctions formed by site-specific integration of adeno-associated virus into an episome. J. Virol. 69(11), 6917-6924 (1995).
83. Kotin RM, Linden RM, Berns KI. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J. 11(13), 5071-5078 (1992).
84. Miller DG, Trobridge GD, Petek LM, Jacobs MA, Kaul R, Russell DW. Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J. Virol. 79(17), 11434-11442 (2005).
85. Nakai H, Wu X, Fuess S et al. Large-scale molecular characterization of adeno-associated virus vector integration in mouse liver. J. Virol. 79(6), 3606-3614 (2005).
86. Grossman Z, Winocour E, Berns KI. Recombination between simian virus 40 and adeno-associated virus. virion coinfection compared to DNA cotransfection. Virology 134(1), 125-137 (1984).
87. Walz C, Deprez A, Dupressoir T, Durst M, Rabreau M, Schlehofer JR. Interaction of human papillomavirus type 16 and adeno-associated virus type 2 co-infecting human cervical epithelium. J. General Virol. 78 ( Pt 6), 1441-1452 (1997
88. Yakobson B, Koch T, Winocour E. Replication of adeno-associated virus in synchronized cells without the addition of a helper virus. J. Virol. 61(4), 972-981 (1987).
89. Yalkinoglu AO, Heilbronn R, Burkle A, Schlehofer JR, zur Hausen H. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res. 48(11), 3123-3129 (1988).
90. Chang LS, Shenk T. The adenovirus DNA-binding protein stimulates the rate of transcription directed by adenovirus and adeno-associated virus promoters. J. Virol. 64(5), 2103-2109 (1990).
91. Duan D, Sharma P, Dudus L et al. Formation of adeno-associated virus circular genomes is differentially regulated by adenovirus E4 ORF6 and E2a gene expression. J. Virol. 73(1), 161-169 (1999).
92. Shi Y, Seto E, Chang LS, Shenk T. Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67(2), 377-388 (1991).
93. Ferrari FK, Samulski T, Shenk T, Samulski RJ. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70(5), 3227-3234 (1996).
94. Fisher KJ, Gao GP, Weitzman MD, Dematteo R, Burda JF, Wilson JM. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70(1), 520-532 (1996).
95. Samulski RJ, Berns Ki, Tan M, Muzyczka N. Cloning of adeno-associated virus into pBR322: Rescue of intact virus from the recombinant plasmid in human cells. Proc. Natl Acad. Sci. USA 79(6), 2077-2081 (1982).
96. Samulski RJ, Srivastava A, Berns KI, Muzyczka N. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV. Cell 33(1), 135-143 (1983).
97. Xiao X, Xiao W, Li J, Samulski RJ. A novel 165-base-pair terminal repeat sequence is the sole cis requirement for the adeno-associated virus life cycle. J. Virol. 71(2), 941-948 (1997).
98. Grieger JC, Choi VW, Samulski RJ. Production and characterization of adeno-associated viral vectors. Nat. Protoc. 1(3), 1412-1428 (2006).
99. Samulski RJ, Chang LS, Shenk T. Helper-free stocks of recombinant adeno-associated viruses: Normal integration does not require viral gene expression. J. Virol. 63(9), 3822-3828 (1989).
100. Miao CH, Snyder RO, Schowalter DB et al. The kinetics of rAAV integration in the liver. Nat. Genet. 19(1), 13-15 (1998).
101. Nakai H, Yant SR, Storm TA, Fuess S, Meuse L, Kay MA. Extrachromosomal recombinant adeno-associated virus vector genomes are primarily responsible for stable liver transduction in vivo. J. Virol. 75(15), 6969-6976 (2001).
102. Flotte TR, Zeitlin Pl, Reynolds TC et al. Phase I trial of intranasal and endobronchial administration of a recombinant adeno-associated virus serotype 2 (rAAV2)-CFTR vector in adult cystic fibrosis patients. a two-part clinical study. Hum. Gene Ther. 14(11), 1079-1088 (2003).
103. Wagner JA, Messner AH, Moran ML et al. Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope 109(2 Pt 1), 266-274 (1999).
104. Wagner JA, Nepomuceno IB, Messner AH et al. A Phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum. Gene Ther. 13(11), 1349-1359 (2002).
105. Aitken ML, Moss RB, Waltz DA et al. A phase I study of aerosolized administration of tgAAVCF to cystic fibrosis subjects with mild lung disease. Hum. Gene Ther. 12(15), 1907-1916 (2001).
106. Moss RB, Rodman D, Spencer LT et al. Repeated adeno-associated virus serotype 2 aerosol-mediated cystic fibrosis transmembrane regulator gene transfer to the lungs of patients with cystic fibrosis. a multicenter, double-blind, placebo-controlled trial. Chest 125(2), 509-521 (2004).
107. Moss RB, Milla C, Colombo J et al. Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: A randomized placebo-controlled phase 2B trial. Hum. Gene Ther. 18(8), 726-732 (2007).
108. Lu Y, Choi YK, Campbell-Thompson M et al. Therapeutic level of functional human alpha 1 antitrypsin (hAAT) secreted from murine muscle transduced by adeno-associated virus (rAAV1) vector. J. Gene Med. 8(6), 730-735 (2006).
109. Song S, Scott-Jorgensen M, Wang J et al. Intramuscular administration of recombinant adeno-associated virus 2 alpha-1 antitrypsin (rAAV-SERPINA1) vectors in a nonhuman primate model. safety and immunologic aspects. Mol. Ther. 6(3), 329-335 (2002).
110. Brantly ML, Chulay JD, Wang L et al. Sustained transgene expression despite T lymphocyte responses in a clinical trial of rAAV1-AAT gene therapy. Proc. Natl Acad. Sci. USA 106(38), 16363-16368 (2009).
111. Flotte TR, Brantly ML, Spencer LT et al. Phase I trial of intramuscular injection of a recombinant adeno-associated virus alpha 1-antitrypsin (rAAV2-CB-hAAT) gene vector to AAT-deficient adults. Hum. Gene Ther. 15(1), 93-128 (2004).
112. Brantly ML, Spencer LT, Humphries M et al. Phase I trial of intramuscular injection of a recombinant adeno-associated virus serotype 2 alphal-antitrypsin (AAT) vector in AAT-deficient adults. Hum. Gene Ther. 17(12), 1177-1186 (2006).
113. Flotte TR, Trapnell BC, Humphries M et al. Phase 2 clinical trial of a recombinant adeno-associated viral vector expressing alpha1-antitrypsin. interim results. Hum. Gene Ther. 22(10), 1239-1247 (2011).
114. Flotte TR, Mueller C. Gene therapy for alpha-1 antitrypsin deficiency. Hum. Mol. Genet. 20(R1), R87-92 (2011).
115. Stone EM. Leber congenital amaurosis - a model for efficient genetic testing of heterogeneous disorders. LXIV Edward Jackson Memorial Lecture. Am. J. Ophthalmol. 144(6), 791-811 (2007).
116. Den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog. Retinal Eye Res. 27(4), 391-419 (2008).
117. Acland GM, Aguirre GD, Ray J et al. Gene therapy restores vision in a canine model of childhood blindness. Nat. Genetics 28(1), 92-95 (2001).
118. Maguire AM, Simonelli F, Pierce EA et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358(21), 2240-2248 (2008).
119. Bainbridge JW, Smith AJ, Barker SS et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med 358(21), 2231-2239 (2008).
120. Cideciyan AV, Aleman TS, Boye SL et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc. Natl Acad. Sci. USA 105(39), 15112-15117 (2008).
121. Simonelli F, Maguire AM, Testa F et al. Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol. Ther. 18(3), 643-650 (2010).
122. High KA. Gene therapy for haemophilia: A long and winding road. J. Thromb. Haemost. 9(Suppl. 1), 2-11 (2011).
123. Kay MA, Manno CS, Ragni MV et al. Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat. Genetics 24(3), 257-261 (2000).
124. Manno CS, Chew AJ, Hutchison S et al. AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101(8), 2963-2972 (2003).
125. Manno CS, Pierce GF, Arruda VR et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12(3), 342-347 (2006).
126. Mingozzi F, Maus MV, Hui DJ et al. CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat. Med. 13(4), 419-422 (2007).
127. Nathwani Ac, Tuddenham EG, Rangarajan S et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 365(25), 2357-2365 (2011).
128. Leone P, Janson CG, Mcphee SJ, During MJ. Global CNS gene transfer for a childhood neurogenetic enzyme deficiency. Canavan disease. Curr. Opin. Mol. Ther. 1(4), 487-492 (1999).
129. Janson C, Mcphee S, Bilaniuk L et al. Clinical protocol. Gene therapy of Canavan disease: AAV-2 vector for neurosurgical delivery of aspartoacylase gene (ASPA) to the human brain. Hum. Gene Ther. 13(11), 1391-1412 (2002).
130. Mcphee SW, Janson CG, Li C et al. Immune responses to AAV in a Phase I study for Canavan disease. J. Gene Med. 8(5), 577-588 (2006).
131. Carlsson T, Bjorklund T, Kirik D. Restoration of the striatal dopamine synthesis for Parkinson's disease: viral vector-mediated enzyme replacement strategy. Curr. Gene Therapy 7(2), 109-120 (2007).
132. Mochizuki H, Mizuno Y. Gene therapy for Parkinson's disease. J. Neural Transm. (65), 205-213 (2003).
133. Marks WJ Jr, Ostrem JL, Verhagen L et al. Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: An open-label, Phase I trial. Lancet Neurol. 7(5), 400-408 (2008).
134. Christine CW, Starr PA, Larson PS et al. Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 73(20), 1662-1669 (2009).
135. Eberling JL, Jagust WJ, Christine CW et al. Results from a Phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70(21), 1980-1983 (2008).
136. Muramatsu S, Fujimoto K, Kato S et al. A Phase I study of aromatic l-amino acid decarboxylase gene therapy for Parkinson's disease. Mol. Ther. 18(9), 1731-1735 (2010).
137. Luo J, Kaplitt MG, Fitzsimons HL et al. Subthalamic GAD gene therapy in a Parkinson's disease rat model. Science 298(5592), 425-429 (2002).
138. Kaplitt MG, Feigin A, Tang C et al. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease. an open label, Phase I trial. Lancet 369(9579), 2097-2105 (2007).
139. Weinberg MS, Samulski RJ, Mccown TJ. Adeno-associated virus (AAV) gene therapy for neurological disease. Neuropharmacology doi:org/10.1016/j. neuropharm.2012.03.004 (2012) (Epub ahead of print).
140. Mendell JR, Rodino-Klapac LR, Rosales XQ et al. Sustained alpha-sarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D. Ann. Neurol. 68(5), 629-638 (2010).
141. Mendell JR, Rodino-Klapac LR, Rosales- Quintero X et al. Limb-girdle muscular dystrophy type 2D gene therapy restores alpha-sarcoglycan and associated proteins. Ann. Neurol. 66(3), 290-297 (2009).
142. Herson S, Hentati F, Rigolet A et al. A Phase I trial of adeno-associated virus serotype 1-gamma-sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C. Brain 135(2), 483-492 (2012).
143. Bowles DE, Mcphee SW, Li C et al. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol. Ther. 20(2), 443-455 (2011).
144. Mendell JR, Campbell K, Rodino-Klapac L et al. Dystrophin immunity in Duchenne's muscular dystrophy. N. Engl. J. Med. 363(15), 1429-1437 (2011).
145. Diprimio N, Mcphee SW, Samulski RJ. Adeno-associated virus for the treatment of muscle diseases: Toward clinical trials. Curr. Opin. Mol. Ther. 12(5), 553-560 (2010).
146. Mease PJ, Hobbs K, Chalmers A et al. Local delivery of a recombinant adenoassociated vector containing a tumour necrosis factor alpha antagonist gene in inflammatory arthritis. a phase 1 dose-escalation safety and tolerability study. Ann. Rheum. Dis. 68(8), 1247-1254 (2009).
147. Hajjar RJ, Zsebo K, Deckelbaum L et al. Design of a phase 1/2 trial of intracoronary administration of AAV1/SERCA2a in patients with heart failure. J. Cardiac Failure 14(5), 355-367 (2008).
148. Lipskaia L, Chemaly ER, Hadri L, Lompre AM, Hajjar RJ. Sarcoplasmic reticulum Ca(2+) ATPase as a therapeutic target for heart failure. Exp. Opin. Biol. Ther. 10(1), 29-41 (2010).
149. Stroes ES, Nierman MC, Meulenberg JJ et al. Intramuscular administration of AAV1- lipoprotein lipase S447X lowers triglycerides in lipoprotein lipase-deficient patients. Arterioscler. Thromb. Vasc. Biol. 28(12), 2303-2304 (2008).
150. Mingozzi F, Meulenberg JJ, Hui DJ et al. AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-dependent activation of capsid-specific T cells. Blood 114(10), 2077-2086 (2009).
151. Mingozzi F, High KA. Immune responses to AAV in clinical trials. Curr. Gene Ther. 11(4), 321-330 (2011).
152. Martin KR, Klein RL, Quigley HA. Gene delivery to the eye using adeno-associated viral vectors. Methods 28(2), 267-275 (2002).
153. Rogers GL, Martino AT, Aslanidi GV, Jayandharan GR, Srivastava A, Herzog RW. Innate immune responses to AAV vectors. Front. Microbiol. 2, 194 (2011).
154. Bantel-Schaal U, Zur Hausen H. Characterization of the DNA of a defective human parvovirus isolated from a genital site. Virology 134(1), 52-63 (1984).
155. Chao H, Liu Y, Rabinowitz J, Li C, Samulski RJ, Walsh CE. Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol. Ther. 2(6), 619-623 (2000).
156. Gao G, Vandenberghe LH, Alvira MR et al. Clades of Adeno-associated viruses are widely disseminated in human tissues. J. Virol. 78(12), 6381-6388 (2004).
157. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl Acad. Sci. USA 99(18), 11854-11859 (2002).
158. Grimm D, Kay MA. From virus evolution to vector revolution. use of naturally occurring serotypes of adeno-associated virus (AAV) as novel vectors for human gene therapy. Curr. Gene Ther. 3(4), 281-304 (2003).
159. Mori S, Wang L, Takeuchi T, Kanda T. Two novel adeno-associated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 330(2), 375-383 (2004).
160. Pacak CA, Mah CS, Thattaliyath BD et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ. Res. 99(4), e3-e9 (2006).
161. Rutledge EA, Halbert CL, Russell DW. Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J. Virol. 72(1), 309-319 (1998).
162. Flotte TR, Conlon TJ, Poirier A, Campbell- Thompson M, Byrne BJ. Preclinical characterization of a recombinant adeno-associated virus type 1-pseudotyped vector demonstrates dose-dependent injection site inflammation and dissemination of vector genomes to distant sites. Hum. Gene Ther. 18(3), 245-256 (2007).
163. Sun X, Pawlyk B, Xu X et al. Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations. Gene Ther. 17(1), 117-131 (2010).
164. Limberis MP, Vandenberghe LH, Zhang L, Pickles RJ, Wilson JM. Transduction efficiencies of novel AAV vectors in mouse airway epithelium in vivo and human ciliated airway epithelium in vitro. Mol. Ther. 17(2), 294-301 (2008).
165. Cooper M, Nayak S, Hoffman BE, Terhorst C, Cao O, Herzog RW. Improved induction of immune tolerance to factor IX by hepatic AAV-8 gene transfer. Hum. Gene Ther. 20(7), 767-776 (2009).
166. Blacklow NR, Hoggan MD, Rowe WP. Serologic evidence for human infection with adenovirus-associated viruses. J. Natl Cancer Instit. 40(2), 319-327 (1968).
167. Erles K, Sebokova P, Schlehofer JR. Update on the prevalence of serum antibodies (IgG and IgM) to adeno-associated virus (AAV). J. Med. Virol. 59(3), 406-411 (1999).
168. Georg-Fries B, Biederlack S, Wolf J, Zur Hausen H. Analysis of proteins, helper dependence, and seroepidemiology of a new human parvovirus. Virology 134(1), 64-71 (1984).
169. Parks WP, Boucher DW, Melnick JL, Taber LH, Yow MD. Seroepidemiological and ecological studies of the adenovirus-associated satellite viruses. Infect. Immun. 2(6), 716-722 (1970).
170. Sondhi D, Hackett NR, Peterson DA et al. Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-associated virus vector. Mol. Ther. 15(3), 481-491 (2007).
171. Arbetman AE, Lochrie M, Zhou S et al. Novel caprine adeno-associated virus (AAV) capsid (AAV-Go.1) is closely related to the primate AAV-5 and has unique tropism and neutralization properties. J. Virol. 79(24), 15238-15245 (2005).
172. Bossis I, Chiorini JA. Cloning of an avian adeno-associated virus (AAAV) and generation of recombinant AAAV particles. J. Virol. 77(12), 6799-6810 (2003).
173. Dutta SK. Isolation and characterization of an adenovirus and isolation of its adenovirus-associated virus in cell culture from foals with respiratory tract disease. Am. J. Veterinary Res. 36(3), 247-250 (1975).
174. Farkas SL, Zadori Z, Benko M, Essbauer S, Harrach B, Tijssen P. A parvovirus isolated from royal python (Python regius) is a member of the genus Dependovirus. J. Gen. Virol. 85(Pt 3), 555-561 (2004).
175. Jacobson ER, Kopit W, Kennedy FA, Funk RS. Coinfection of a bearded dragon, Pogona vitticeps, with adenovirus- and dependovirus-like viruses. Vet. Pathol. 33(3), 343-346 (1996).
176. Olson Ej, Haskell SR, Frank RK et al. Isolation of an adenovirus and an adeno-associated virus from goat kids with enteritis. J. Vet. Diagn. Invest. 16(5), 461-464 (2004).
177. Schmidt M, Katano H, Bossis I, Chiorini JA. Cloning and characterization of a bovine adeno-associated virus. J. Virol. 78(12), 6509-6516 (2004).
178. Girod A, Ried M, Wobus C et al. Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat. Med. 5(9), 1052-1056 (1999).
179. Shi W, Arnold GS, Bartlett JS. 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(14), 1697-1711 (2001).
180. Wu P, Xiao W, Conlon T et al. Mutational analysis of the adeno-associated
181. Grifman M, Trepel M, Speece P et al. Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol. Ther. 3(6), 964-975 (2001).
182. Nicklin SA, Buening H, Dishart KL et al. Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol. Ther. 4(3), 174-181 (2001).
183. Shi W, Bartlett JS. RGD inclusion in VP3 provides adeno-associated virus type 2 (AAV2)-based vectors with a heparan sulfate-independent cell entry mechanism. Mol. Ther. 7(4), 515-525 (2003).
184. White AF, Mazur M, Sorscher EJ, Zinn KR, Ponnazhagan S. Genetic modification of adeno-associated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells. Hum. Gene Ther. 19(12), 1407-1414 (2008).
185. White SJ, Nicklin SA, Buning H et al. Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109(4), 513-519 (2004).
186. Work LM, Buning H, Hunt E et al. Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Mol. Ther. 13(4), 683-693 (2006).
187. Yu Cy, Yuan Z, Cao Z et al. A muscle-targeting peptide displayed on AAV2 improves muscle tropism on systemic delivery. Gene Therapy 16(8), 953-962 (2009).
188. Michelfelder S, Lee MK, Delima-Hahn E et al. Vectors selected from adeno-associated viral display peptide libraries for leukemia cell-targeted cytotoxic gene therapy. Exp. Hematol. 35(12), 1766-1776 (2007).
189. Muller OJ, Kaul F, Weitzman MD et al. Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotech. 21(9), 1040-1046 (2003).
190. Perabo L, Buning H, Kofler DM et al. In vitro selection of viral vectors with modified tropism: The adeno-associated virus display. Mol. Ther. 8(1), 151-157 (2003).
191. Waterkamp DA, Muller OJ, Ying Y, Trepel M, Kleinschmidt JA. Isolation of targeted AAV2 vectors from novel virus display libraries. J. Gene Med. 8(11), 1307-1319 (2006).
192. Grimm D, Lee JS, Wang L et al. In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82(12), 5887-5911 (2008).
193. Michelfelder S, Kohlschutter J, Skorupa A et al. 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(4), e5122 (2009).
194. Boucas J, Lux K, Huber A et al. Engineering adeno-associated virus serotype 2-based targeting vectors using a new insertion site-position 453-and single point mutations. J. Gene Med. 11(12), 1103-1113 (2009).
195. Maheshri N, Koerber JT, Kaspar BK, Schaffer DV. Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat. Biotechnol. 24(2), 198-204 (2006).
196. Perabo L, Endell J, King S et al. Combinatorial engineering of a gene therapy vector. directed evolution of adeno-associated virus. J. Gene Med. 8(2), 155-162 (2006).
197. Koerber JT, Jang JH, Schaffer DV. DNA Shuffling of adeno-associated virus yields functionally diverse viral progeny. Mol. Ther. 16(10), 1703-1709 (2008).
198. Li W, Asokan A, Wu Z et al. Engineering and selection of shuffled AAV genomes. a new strategy for producing targeted biological nanoparticles. Mol. Ther. 16(7), 1252-1260 (2008).
199. Asokan A, Conway JC, Phillips JL et al. Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat. Biotechnol. 28, 79-82 (2010).
200. Gray SJ, Blake BL, Criswell HE, Nicolson SC, Samulski RJ, Mccown TJ. Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood- brain barrier (BBB). Mol. Ther. 18(3), 570-578 (2009).
201. Yang L, Jiang J, Drouin LM et al. A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection. Proc. Natl Acad. Sci. USA 106(10), 3946-3951 (2009).
202. Excoffon KJ, Koerber JT, Dickey DD et al. Directed evolution of adeno-associated virus to an infectious respiratory virus. Proc. Natl Acad. Sci. USA 106(10), 3865-3870 (2009).
203. Li W, Zhang L, Johnson JS et al. Generation of novel AAV variants by directed evolution for improved CFTR delivery to human ciliated airway epithelium. Mol. Ther. 17(12), 2067-2077 (2009).
204. Petrs-Silva H, Dinculescu A, Li Q et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol. Ther. 17(3), 463-471 (2009).
205. Zhang HG, Xie J, Dmitriev I et al. Addition of six-His-tagged peptide to the C terminus of adeno-associated virus VP3 does not affect viral tropism or production. J. Virol. 76(23), 12023-12031 (2002).
206. Zhong L, Li B, Mah CS et al. Next generation of adeno-associated virus 2 vectors. point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc. Natl Acad. Sci. USA 105(22), 7827-7832 (2008).
207. Bleker S, Sonntag F, Kleinschmidt JA. 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(4), 2528-2540 (2005).
208. Diprimio N, Asokan A, Govindasamy L, Agbandje-Mckenna M, Samulski RJ. Surface loop dynamics in adeno-associated virus capsid assembly. J. Virol. 82(11), 5178-5189 (2008).
209. Kern A, Schmidt K, Leder C et al. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77(20), 11072-11081 (2003).
210. Opie SR, Warrington KH Jr, Agbandje- Mckenna M, Zolotukhin S, Muzyczka N. 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(12), 6995-7006 (2003).
211. Wu Z, Asokan A, Grieger JC, Govindasamy L, Agbandje-Mckenna M, Samulski RJ. Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J. Virol. 80(22), 11393-11397 (2006).
212. Kaludov N, Padron E, Govindasamy L, Mckenna R, Chiorini JA, Agbandje-Mckenna M. Production, purification and preliminary x-ray crystallographic studies of adeno-associated virus serotype 4. Virology 306(1), 1-6 (2003).
213. Kronenberg S, Kleinschmidt JA, Bottcher B. Electron cryo-microscopy and image reconstruction of adeno-associated virus type 2 empty capsids. EMBO Rep. 2(11), 997-1002 (2001).
214. Lerch TF, Xie Q, Ongley HM, Hare J, Chapman MS. Twinned crystals of adeno-associated virus serotype 3b prove suitable for structural studies. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65(Pt 2), 177-183 (2009).
215. Miller EB, Gurda-Whitaker B, Govindasamy L et al. Production, purification and preliminary x-ray crystallographic studies of adeno-associated virus serotype 1. Acta Crystallogr. Sect F Struct. Biol. Cryst. Commun. 62(Pt 12), 1271-1274 (2006).
216. Mitchell M, Nam HJ, Carter A et al. Production, purification and preliminary x-ray crystallographic studies of adeno-associated virus serotype 9 Acta Crystallogr. Sect F Struct. Biol. Cryst. Commun. 65(Pt 7), 715-718 (2009).
217. Nam H-J, Lane MD, Padron E et al. Structure of adeno-associated virus serotype 8, a gene therapy vector. J. Virol. 81(22), 12260-12271 (2007).
218. O'Donnell J, Taylor KA, Chapman MS. Adeno-associated virus-2 and its primary cellular receptor - Cryo-EM structure of a heparin complex. Virology 385(2), 434-443 (2009).
219. Quesada O, Gurda B, Govindasamy L et al. Production, purification and preliminary x-ray crystallographic studies of adeno-associated virus serotype 7. Acta Crystallogr. Sect F Struct. Biol. Cryst. Commun. 63(Pt 12), 1073-1076 (2007).
220. Walters RW, Agbandje-Mckenna M, Bowman VD et al. Structure of adeno-associated virus serotype 5. J. Virol. 78(7), 3361-3371 (2004).
221. Xie Q, Bu W, Bhatia S et al. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl Acad. Sci. USA 99(16), 10405-10410 (2002).
222. Hauck B, Chen L, Xiao W. Generation and characterization of chimeric recombinant AAV vectors. Mol. Ther. 7(3), 419-425 (2003).
223. Rabinowitz JE, Bowles DE, Faust SM, Ledford JG, Cunningham SE, Samulski RJ. Cross-dressing the virion: The transcapsidation of adeno-associated virus serotypes functionally defines subgroups. J. Virol. 78(9), 4421-4432 (2004).
224. Johnson JS, Samulski RJ. Enhancement of AAV infection by mobilizing capsids into and out of the nucleolus. J. Virol. 83(6), 2632-2644 (2008).
225. Xiao PJ, Li C, Neumann A, Samulski RJ. Quantitative 3D tracing of gene-delivery viral vectors in human cells and animal tissues. Mol. Ther. 20(2), 317-328 (2011
226. Ashtari M, Cyckowski LL, Monroe JF et al. The human visual cortex responds to gene therapy-mediated recovery of retinal function. J. Clin. Investig. 121(6), 2160-2168 (2011).
227. Mittermeyer G, Christine CW, Rosenbluth KH et al. Long-term evaluation of a Phase 1 study of AADC gene therapy for Parkinson's disease. Hum. Gene Ther. 23(4), 377-381 (2012).
228. Worgall S, Sondhi D, Hackett NR et al. Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum. Gene Ther. 19(5), 463-474 (2008).
229. Wu Z, Miller E, Agbandje-Mckenna M, Samulski RJ. Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J. Virol. 80(18), 9093-9103 (2006).
230. Yan Z, Lei-Butters DC, Liu X et al. Unique biologic properties of recombinant AAV1 transduction in polarized human airway epithelia. J. Biol. Chem. 281(40), 29684-29692 (2006).
231. Wang C, Wang CM, Clark KR, Sferra TJ. Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther. 10(17), 1528-1534 (2003).
232. Auricchio A, Kobinger G, Anand V et al. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics. the retina as a model. Hum. Mol. Genet. 10(26), 3075-3081 (2001).
233. Loiler SA, Tang Q, Clarke T et al. Localized gene expression following administration of adeno-associated viral vectors via pancreatic ducts. Mol. Ther. 12(3), 519-527 (2005).
234. Koeberl DD, Alexander IE, Halbert CL, Russell DW, Miller AD. Persistent expression of human clotting factor IX from mouse liver after intravenous injection of adeno-associated virus vectors.Proc. Natl Acad. Sci. USA 94(4), 1426-1431 (1997).
235. Alexander IE, Russell DW, Spence AM, Miller AD. Effects of gamma irradiation on the transduction of dividing and nondividing cells in brain and muscle of rats by adeno-associated virus vectors. Hum. Gene Ther. 7(7), 841-850 (1996).
236. Bartlett JS, Samulski RJ, McCown TJ. Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum. Gene Ther. 9(8), 1181-1186 (1998).
237. Takeda S, Takahashi M, Mizukami H et al. Successful gene transfer using adeno-associated virus vectors into the kidney. Comparison among adeno-associated virus serotype 1-5 vectors in vitro and in vivo. Nephron 96(4), e119-e126 (2004).
238. Schmidt OW, Cooney MK, Foy HM. Adeno-associated virus in adenovirus type 3 conjunctivitis. Infection Immunity 11(6), 1362-1370 (1975).
239. Parks WP, Melnick JL, Rongey R, Mayor HD. Physical assay and growth cycle studies of a defective adeno-satellite virus. J. Virol. 1(1), 171-180 (1967).
240. Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J. Virol. 75(15), 6884-6893 (2001).
241. Weber M, Rabinowitz J, Provost N et al. Recombinant adeno-associated virus serotype 4 mediates unique and exclusive long-term transduction of retinal pigmented epithelium in rat, dog, and nonhuman primate after subretinal delivery. Mol. Ther. 7(6), 774-781 (2003).
242. Walters RW, Pilewski JM, Chiorini JA, Zabner J. Secreted and transmembrane mucins inhibit gene transfer with AAV4 more efficiently than AAV5. J. Biol. Chem. 277(26), 23709-23713 (2002).
243. Davidson BL, Stein CS, Heth JA et al. Recombinant adeno-associated virus type 2, 4, and 5 vectors. transduction of variant cell types and regions in the mammalian central nervous system. Proc. Natl Acad. Sci. USA 97(7), 3428-3432 (2000).
244. Blankinship MJ, Gregorevic P, Allen JM et al. Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol. Ther. 10(4), 671-678 2004).
245. Zincarelli C, Soltys S, Rengo G, Koch WJ, Rabinowitz JE. Comparative cardiac gene delivery of adeno-associated virus serotypes 1-9 reveals that AAV6 mediates the most efficient transduction in mouse heart. Clin. Transl. Sci. 3(3), 81-89 (2010).
246. Allocca M, Mussolino C, Garcia-Hoyos M et al. Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J. Virol. 81(20), 11372-11380 (2007).
247. Taymans JM, Vandenberghe LH, Haute CV et al. Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum. Gene Ther. 18(3), 195-206 (2007).
248. Wang Z, Zhu T, Qiao C et al. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat. Biotechnol. 23(3), 321-328 (2005).
249. Bell CL, Vandenberghe LH, Bell P et al. The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J. Clin. Investig. 121(6), 2427-2435 (2011).
250. Shen S, Bryant KD, Brown SM, Randell SH, Asokan A. Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem. 286(15), 13532-13540 (2011).
251. Inagaki K, Fuess S, Storm TA et al. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol. Ther. 14(1), 45-53 (2006).
252. Foust KD, Nurre E, Montgomery Cl, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol. 27(1), 59-65 (2009).
253. Bostick B, Ghosh A, Yue Y, Long C, Duan D. Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Ther. 14(22), 1605-1609 (2007).