Adeno-associated virus structural biology as a tool in vector development

Future Virology

Volumn 8, Issue 12, 2013, Pages 1183-1199

  Drouin, Lauren M ^a   Agbandje Mckenna, Mavis ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

adeno associated virus; capsid structure; chimera; directed evolution; gene therapy; rational design; tissue tropism

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOVIRUS VECTOR; ALIPOGENE TIPARVOVEC; AMINO ACID; BLOOD CLOTTING FACTOR 9; CLATHRIN; DIMER; DYNAMIN; DYSTROPHIN; ENDONUCLEASE; FIBROBLAST GROWTH FACTOR RECEPTOR; HELICASE; HEPARAN; IMMUNOGLOBULIN; IMMUNOGLOBULIN F(AB) FRAGMENT; INTEGRIN; LAMININ RECEPTOR; MOLECULAR MOTOR; MONOMER; NEUTRALIZING ANTIBODY; PHENYLALANINE; PHOSPHOLIPASE A2; PROTEIN VP1; PROTEOHEPARAN SULFATE; RESTRICTION ENDONUCLEASE; RPE65 PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRUS DNA; VISUAL PIGMENT;

ADENO ASSOCIATED VIRUS; ADENOVIRUS; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANTIBODY RESPONSE; CHIMERA; CHROMOSOME; CLINICAL TRIAL (TOPIC); CRYOELECTRON MICROSCOPY; DNA SHUFFLING; DUCHENNE MUSCULAR DYSTROPHY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; GENOME; HELPER VIRUS; HEMATOPOIETIC STEM CELL; HEMOPHILIA B; HERPES VIRUS; HUMAN; HYPERLIPOPROTEINEMIA TYPE 1; IMAGE RECONSTRUCTION; IMMUNE RESPONSE; INVERTED TERMINAL REPEAT; LEBER CONGENITAL AMAUROSIS; MELANOMA CELL; MICROTUBULE; MOLECULAR DOCKING; MUSCULOSKELETAL DISEASE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OPEN READING FRAME; PHENOTYPE; PHYLOGENETIC TREE; PLASMID; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; RHESUS MONKEY; SEROPREVALENCE; SEROTYPE; START CODON; TROPISM; VIRUS CAPSID; VIRUS PARTICLE; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

EID: 84889571789     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.13.112     Document Type: Review

References (111)

1. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: Progress and challenges. Nat. Rev. Genet. 12(5), 341-355 (2011
2. Yanez RJ, Porter AC. Therapeutic gene targeting. Gene Ther. 5(2), 149-159 (1998 (Pubitemid 28077741)
3. Peng KW. Strategies for targeting therapeutic gene delivery. Mol. Med. Today 5(10), 448-453 (1999
4. Raper SE, Chirmule N, Lee FS et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Genet. Metab. 80(1-2), 148-158 (2003
5. Hacein-Bey-Abina S, Garrigue A, Wang GP et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118(9), 3132-3142 (2008
6. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin. Microbiol. Rev. 21(4), 583-593 (2008
7. Flotte TR, Carter BJ. Adeno-associated virus vectors for gene therapy. Gene Ther. 2(6), 357-362 (1995
8. Chapman M, Agbandje-McKenna M. Atomic structure of viral particles. In: Parvoviruses. Kerr JR Cotmore SF, Bloom ME, Linden RM, Parrish CR (Eds). Edward Arnold Ltd, NY, USA (2006
9. 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
10. 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
11. Naumer M, Sonntag F, Schmidt K et al. Properties of the adeno-associated virus assembly-activating protein. J. Virol. 86(23), 13038-13048 (2012
12. Ding W, Zhang L, Yan Z, Engelhardt JF. Intracellular trafficking of adeno-associated viral vectors. Gene Ther. 12(11), 873-880 (2005 (Pubitemid 40852205)
13. 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 (Pubitemid 28116931)
14. Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3 and 9. J. Virol. 80(19), 9831-9836 (2006 (Pubitemid 44435657)
15. Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ. Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J. Virol. 80(18), 8961-8969 (2006 (Pubitemid 44359970)
16. Kashiwakura Y, Tamayose K, Iwabuchi K et al. Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J. Virol. 79(1), 609-614 (2005 (Pubitemid 39648414)
17. 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 (Pubitemid 29051001)
18. 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 (Pubitemid 29051002)
19. Uhrig S, Coutelle O, Wiehe T, Perabo L, Hallek M, Buning H. Successful target cell transduction of capsid-engineered rAAV vectors requires clathrin-dependent endocytosis. Gene Ther. 19(2), 210-218 (2012
20. Nonnenmacher M, Weber T. Adeno-associated virus 2 infection requires endocytosis through the CLIC/GEEC pathway. Cell Host Microbe 10(6), 563-576 (2011
21. 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. Gen. Virol. 83(Pt 5), 973-978 (2002 (Pubitemid 34477268)
22. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. 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(22), 11040-11054 (2006 (Pubitemid 44706545)
23. Zadori Z, Szelei J, Lacoste MC et al. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell. 1(2), 291-302 (2001 (Pubitemid 33653063)
24. 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
25. Kronenberg S, Bottcher B, von der Lieth CW, Bleker S, Kleinschmidt JA. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J. Virol. 79(9), 5296-5303 (2005 (Pubitemid 40548198)
26. Xiao PJ, Samulski RJ. Cytoplasmic trafficking, endosomal escape and perinuclear accumulation of adeno-associated virus type 2 particles are facilitated by microtubule network. J. Virol. 86(19), 10462-10473 (2012
27. 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 (Pubitemid 35231307)
28. Dubielzig R, King JA, Weger S, Kern A, Kleinschmidt JA. Adeno-associated virus type 2 protein interactions: Formation of pre-encapsidation complexes. J. Virol. 73(11), 8989-8998 (1999 (Pubitemid 29487052)
29. Duan D, Sharma P, Yang J et al. Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J. Virol. 72(11), 8568-8577 (1998 (Pubitemid 28471794)
30. Kotin RM, Siniscalco M, Samulski RJ et al. Site-specific integration by adeno-associated virus. Proc. Natl Acad. Sci. USA 87(6), 2211-2215 (1990
31. Atchison RW, Casto BC, Hammon WM. Adenovirus-associated defective virus particles. Science 149(3685), 754-756 (1965
32. Srivastava A, Lusby EW, Berns KI. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J. Virol. 45(2), 555-564 (1983 (Pubitemid 13225420)
33. Muramatsu S, Mizukami H, Young NS, Brown KE. Nucleotide sequencing and generation of an infectious clone of adeno-associated virus 3. Virology 221(1), 208-217 (1996 (Pubitemid 26266557)
34. 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 (Pubitemid 28048842)
35. Chiorini JA, Kim F, Yang L, Kotin RM. Cloning and characterization of adeno-associated virus type 5. J. Virol. 73(2), 1309-1319 (1999 (Pubitemid 29036786)
36. Chiorini JA, Yang L, Liu Y, Safer B, Kotin RM. Cloning of adeno-associated virus type 4 (AAV4) and generation of recombinant AAV4 particles. J. Virol. 71(9), 6823-6833 (1997 (Pubitemid 27355343)
37. Schmidt M, Grot E, Cervenka P, Wainer S, Buck C, Chiorini JA. Identification and characterization of novel adeno-associated virus isolates in ATCC virus stocks. J. Virol. 80(10), 5082-5085 (2006
38. Schmidt M, Govindasamy L, Afione S, Kaludov N, Agbandje-McKenna M, Chiorini JA. Molecular characterization of the heparin-dependent transduction domain on the capsid of a novel adeno-associated virus isolate, AAV(VR-942). J. Virol. 82(17), 8911-8916 (2008
39. Schmidt M, Voutetakis A, Afione S, Zheng C, Mandikian D, Chiorini JA. Adeno-associated virus type 12 (AAV12): A novel AAV serotype with sialic acid- And heparan sulfate proteoglycan-independent transduction activity. J. Virol. 82(3), 1399-1406 (2008
40. 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 (Pubitemid 39572844)
41. 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 (Pubitemid 38715936)
42. 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 (Pubitemid 34994488)
43. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 16(6), 1073-1080 (2008 (Pubitemid 351737072)
44. 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(1), 79-82 (2010
45. Asokan A, Schaffer DV, Samulski RJ. The AAV vector toolkit: Poised at the clinical crossroads. Mol. Ther. 20(4), 699-708 (2012
46. Kotchey NM, Adachi K, Zahid M et al. A potential role of distinctively delayed blood clearance of recombinant adeno-associated virus serotype 9 in robust cardiac transduction. Mol. Ther. 19(6), 1079-1089 (2011
47. DiMattia MA, Nam HJ, Van Vliet K et al. Structural insight into the unique properties of adeno-associated virus serotype 9. J. Virol. 86(12), 6947-6958 (2012
48. Govindasamy L, DiMattia MA, Gurda BL et al. Structural insights into adeno-associated virus serotype 5. J. Virol. 87(20), 11187-11199 (2013
49. Govindasamy L, Padron E, McKenna R et al. Structurally mapping the diverse phenotype of adeno-associated virus serotype 4. J. Virol. 80(23), 11556-11570 (2006 (Pubitemid 44788870)
50. 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 (Pubitemid 33130605)
51. Lerch TF, Xie Q, Chapman MS. The structure of adeno-associated virus serotype 3B (AAV-3B): Insights into receptor binding and immune evasion. Virology 403(1), 26-36 (2010
52. Nam HJ, Gurda BL, McKenna R et al. Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking. J. Virol. 85(22), 11791-11799 (2011
53. Nam HJ, Lane MD, Padron E et al. Structure of adeno-associated virus serotype 8, a gene therapy vector. J. Virol. 81(22), 12260-12271 (2007 (Pubitemid 350085841)
54. Ng R, Govindasamy L, Gurda BL et al. Structural characterization of the dual glycan binding adeno-associated virus serotype 6. J. Virol. 84(24), 12945-12957 (2010
55. Walters RW, Agbandje-McKenna M, Bowman VD et al. Structure of adeno-associated virus serotype 5. J. Virol. 78(7), 3361-3371 (2004 (Pubitemid 38568277)
56. 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
57. Venkatakrishnan B, Yarbrough J, Domsic J et al. Structure and dynamics of adeno-associated virus serotype 1 VP1-unique N-terminal domain and its role in capsid trafficking. J. Virol. 87(9), 4974-4984 (2013
58. McCraw DM, O'Donnell JK, Taylor KA, Stagg SM, Chapman MS. Structure of adeno-associated virus-2 in complex with neutralizing monoclonal antibody A20. Virology 431(1-2), 40-49 (2012
59. Gurda BL, DiMattia MA, Miller EB et al. Capsid antibodies to different adeno-associated virus serotypes bind common regions. J. Virol. 87(16), 9111-9124 (2013
60. Gurda BL, Raupp C, Popa-Wagner R et al. Mapping a neutralizing epitope onto the capsid of adeno-associated virus serotype 8. J. Virol. 86(15), 7739-7751 (2012
61. 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 (Pubitemid 37204297)
62. Levy HC, Bowman VD, Govindasamy L et al. Heparin binding induces conformational changes in adeno-associated virus serotype 2. J. Struct. Biol. 165(3), 146-156 (2009
63. Lochrie MA, Tatsuno GP, Christie B et al. Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J. Virol. 80(2), 821-834 (2006 (Pubitemid 43062894)
64. 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
65. 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 (Pubitemid 36666892)
66. Wobus CE, Hugle-Dorr B, Girod A, Petersen G, Hallek M, Kleinschmidt JA. Monoclonal antibodies against the adeno-associated virus type 2 (AAV-2) capsid: Epitope mapping and identification of capsid domains involved in AAV-2-cell interaction and neutralization of AAV-2 infection. J. Virol. 74(19), 9281-9293 (2000
67. Wu P, Xiao W, Conlon T et al. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J. Virol. 74(18), 8635-8647 (2000 (Pubitemid 30666714)
68. Bleker S, Pawlita M, Kleinschmidt JA. Impact of capsid conformation and Rep-capsid interactions on adeno-associated virus type 2 genome packaging. J. Virol. 80(2), 810-820 (2006 (Pubitemid 43062893)
69. Hermonat PL, Muzyczka N. Use of adeno-associated virus as a mammalian DNA cloning vector: Transduction of neomycin resistance into mammalian tissue culture cells. Proc. Natl Acad. Sci. USA 81(20), 6466-6470 (1984 (Pubitemid 15221855)
70. McLaughlin SK, Collis P, Hermonat PL, Muzyczka N. Adeno-associated virus general transduction vectors: Analysis of proviral structures. J. Virol. 62(6), 1963-1973 (1988
71. Matsushita T, Elliger S, Elliger C et al. Adeno-associated virus vectors can be efficiently produced without helper virus. Gene Ther. 5(7), 938-945 (1998 (Pubitemid 28371911)
72. Kohlbrenner E, Aslanidi G, Nash K et al. Successful production of pseudotyped rAAV vectors using a modified baculovirus expression system. Mol. Ther. 12(6), 1217-1225 (2005 (Pubitemid 41723056)
73. Urabe M, Ding C, Kotin RM. Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum. Gene Ther. 13(16), 1935-1943 (2002 (Pubitemid 35341035)
74. Urabe M, Nakakura T, Xin KQ et al. Scalable generation of high-titer recombinant adeno-associated virus type 5 in insect cells. J. Virol. 80(4), 1874-1885 (2006 (Pubitemid 43228727)
75. Dong B, Nakai H, Xiao W. Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther. 18(1), 87-92 (2010
76. Dong JY, Fan PD, Frizzell RA. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7(17), 2101-2112 (1996 (Pubitemid 26400735)
77. Hirsch ML, Agbandje-McKenna M, Samulski RJ. Little vector, big gene transduction: Fragmented genome reassembly of adeno-associated virus. Mol. Ther. 18(1), 6-8 (2010
78. Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol. Ther. 18(1), 80-86 (2010
79. Yan Z, Zhang Y, Duan D, Engelhardt JF. Trans-splicing vectors expand the utility of adeno-associated virus for gene therapy. Proc. Natl Acad. Sci. USA 97(12), 6716-6721 (2000 (Pubitemid 30412780)
80. Ginn SL, Alexander IE, Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2012 - An update. J. Gene Med. 15(2), 65-77 (2013
81. Maguire AM, High KA, Auricchio A et al. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: A Phase 1 dose-escalation trial. Lancet 374(9701), 1597-1605 (2009
82. 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 (Pubitemid 351724453)
83. 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
84. 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 (Pubitemid 43355084)
85. 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
86. Gaudet D, de Wal J, Tremblay K et al. Review of the clinical development of alipogene tiparvovec gene therapy for lipoprotein lipase deficiency. Atheroscler. Suppl. 11(1), 55-60 (2010
87. Boutin S, Monteilhet V, Veron P et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8 and 9 in the healthy population: Implications for gene therapy using AAV vectors. Hum. Gene Ther. 21(6), 704-712 (2010
88. 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 (Pubitemid 32611306)
89. Srivastava A. Hematopoietic stem cell transduction by recombinant adeno-associated virus vectors: Problems and solutions. Hum. Gene Ther. 16(7), 792-798 (2005 (Pubitemid 40982328)
90. Loiler SA, Conlon TJ, Song S et al. Targeting recombinant adeno-associated virus vectors to enhance gene transfer to pancreatic islets and liver. Gene Ther. 10(18), 1551-1558 (2003 (Pubitemid 37063260)
91. 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 (Pubitemid 351866056)
92. 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 (Pubitemid 32851280)
93. Calcedo R, Vandenberghe LH, Gao G, Lin J, Wilson JM. Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J. Infect. Dis. 199(3), 381-390 (2009
94. Moskalenko M, Chen L, van Roey M et al. Epitope mapping of human anti-adeno-associated virus type 2 neutralizing antibodies: Implications for gene therapy and virus structure. J. Virol. 74(4), 1761-1766 (2000 (Pubitemid 30434033)
95. Rapti K, Louis-Jeune V, Kohlbrenner E et al. Neutralizing antibodies against AAV serotypes 1, 2, 6 and 9 in sera of commonly used animal models. Mol. Ther. 20(1), 73-83 (2012
96. Raupp C, Naumer M, Muller OJ, Gurda BL, Agbandje-McKenna M, Kleinschmidt JA. The threefold protrusions of adeno-associated virus type 8 are involved in cell surface targeting as well as postattachment processing. J. Virol. 86(17), 9396-9408 (2012
97. 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 (2012
98. Pulicherla N, Shen S, Yadav S et al. Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol. Ther. 19(6), 1070-1078 (2011
99. Wu Z, Asokan A, Samulski RJ. Adeno-associated virus serotypes: Vector toolkit for human gene therapy. Mol. Ther. 14(3), 316-327 (2006 (Pubitemid 44184972)
100. 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
101. Emsley P, Cowtan K. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60(Pt 12 Pt 1), 2126-2132 (2004 (Pubitemid 41742764)
102. Carrillo-Tripp M, Shepherd CM, Borelli IA et al. VIPERdb2: An enhanced and web API enabled relational database for structural virology. Nucleic Acids Res. 37(Database issue), D436-D442 (2009
103. Pettersen EF, Goddard TD, Huang CC et al. UCSF chimera - A visualization system for exploratory research and analysis. J. Comput. Chem. 25(13), 1605- 1612 (2004
104. Xiao C, Rossmann MG. Interpretation of electron density with stereographic roadmap projections. J. Struct. Biol. 158(2), 182-187 (2007 (Pubitemid 46719989)
105. 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 (Pubitemid 351822263)
106. Lerch TF, O'Donnell JK, Meyer NL et al. Structure of AAV-DJ, a retargeted gene therapy vector: Cryo-electron microscopy at 4.5 A resolution. Structure 20(8), 1310-1320 (2012
107. 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
108. Zhong L, Li B, Jayandharan G et al. Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381(2), 194-202 (2008
109. Zhong L, Li BZ, 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 (Pubitemid 351872723)
110. Aslanidi GV, Rivers AE, Ortiz L et al. Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: The final threshold? PLoS ONE 8(3), e59142 (2013
111. Larkin MA, Blackshields G, Brown NP et al. Clustal W and Clustal X version 2.0. Bioinformatics 23(21), 2947-2948 (2007).