Structural insights into adeno-associated virus serotype 5

Journal of Virology

Volumn 87, Issue 20, 2013, Pages 11187-11199

  Govindasamy, Lakshmanan ^a   DiMattia, Michael A ^a,c   Gurda, Brittney L ^a,d   Halder, Sujata ^a   McKenna, Robert ^a   Chiorini, John A ^b   Muzyczka, Nicholas ^a   Zolotukhin, Sergei ^a   Agbandje McKenna, Mavis ^a  

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

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CAPSID PROTEIN; DNA;

ADENO ASSOCIATED VIRUS; ANTIGENICITY; ARTICLE; CRYSTAL STRUCTURE; DNA PACKAGING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MOTIF; SEROTYPE; SIGNAL TRANSDUCTION;

CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; DEPENDOVIRUS; ELECTROCHEMISTRY; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84886935681     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00867-13     Document Type: Article

References (122)

1. Flotte TR, Carter BJ. 1995. Adeno-associated virus vectors for gene therapy. Gene Ther. 2:357-362.
2. Mingozzi F, High KA. 2011. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 12: 341-355.
3. Chiorini JA, Afione S, Kotin RM. 1999. Adeno-associated virus (AAV) type 5 Rep protein cleaves a unique terminal resolution site compared with other AAV serotypes. J. Virol. 73:4293-4298.
4. Chiorini JA, Kim F, Yang L, Kotin RM. 1999. Cloning and characterization of adeno-associated virus type 5. J. Virol. 73:1309-1319.
5. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. 2002. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. U. S. A. 99:11854-11859.
6. Muramatsu S, Mizukami H, Young NS, Brown KE. 1996. Nucleotide sequencing and generation of an infectious clone of adeno-associated virus 3. Virology 221:208-217.
7. Rutledge EA, Halbert CL, Russell DW. 1998. Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J. Virol. 72:309-319.
8. Srivastava A, Lusby EW, Berns KI. 1983. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J. Virol. 45:555-564.
9. Atchison RW, Casto BC, Hammon WM. 1965. Adenovirus-associated defective virus particles. Science 149:754-756.
10. Mori S, Wang L, Takeuchi T, Kanda T. 2004. Two novel adenoassociated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 330:375-383.
11. Schmidt M, Voutetakis A, Afione S, Zheng C, Mandikian D, Chiorini JA. 2008. Adeno-associated virus type 12 (AAV12): a novelAAVserotype with sialic acid- and heparan sulfate proteoglycan-independent transduction activity. J. Virol. 82:1399-1406.
12. Schmidt M, Katano H, Bossis I, Chiorini JA. 2004. Cloning and characterization of a bovine adeno-associated virus. J. Virol. 78:6509-6516.
13. Arbetman AE, Lochrie M, Zhou S, Wellman J, Scallan C, Doroudchi MM, Randlev B, Patarroyo-White S, Liu T, Smith P, Lehmkuhl H, Hobbs LA, Pierce GF, Colosi P. 2005. 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: 15238-15245.
14. Lochrie MA, Tatsuno GP, Arbetman AE, Jones K, Pater C, Smith PH, McDonnell JW, Zhou SZ, Kachi S, Kachi M, Campochiaro PA, Pierce GF, Colosi P. 2006. Adeno-associated virus (AAV) capsid genes isolated from rat and mouse liver genomic DNA define two new AAV species distantly related to AAV-5. Virology 353:68-82.
15. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X, Wilson JM. 2004. Clades of adeno-associated viruses are widely disseminated in human tissues. J. Virol. 78:6381-6388.
16. McLaughlin SK, Collis P, Hermonat PL, Muzyczka N. 1988. Adenoassociated virus general transduction vectors: analysis of proviral structures. J. Virol. 62:1963-1973.
17. Samulski RJ, Srivastava A, Berns KI, Muzyczka N. 1983. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV. Cell 33:135-143.
18. Samulski RJ, Chang LS, Shenk T. 1987. A recombinant plasmid from which an infectious adeno-associated virus genome can be excised in vitro and its use to study viral replication. J. Virol. 61:3096-3101.
19. - mutant and correction of terminal palindrome deletions. J. Mol. Biol. 179:1-20.
20. Kronenberg S, Kleinschmidt JA, Bottcher B. 2001. Electron cryomicroscopy and image reconstruction of adeno-associated virus type 2 empty capsids. EMBO Rep. 2:997-1002.
21. Xie Q, Bu W, Bhatia S, Hare J, Somasundaram T, Azzi A, Chapman MS. 2002. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. U. S. A. 99:10405-10410.
22. Govindasamy L, Padron E, McKenna R, Muzyczka N, Kaludov N, Chiorini JA, Agbandje-McKenna M. 2006. Structurally mapping the diverse phenotype of adeno-associated virus serotype 4. J. Virol. 80: 11556-11570.
23. Lerch TF, Xie Q, Chapman MS. 2010. The structure of adenoassociated virus serotype 3B (AAV-3B): insights into receptor binding and immune evasion. Virology 403:26-36.
24. Walters RW, Agbandje-McKenna M, Bowman VD, Moninger TO, Olson NH, Seiler M, Chiorini JA, Baker TS, Zabner J. 2004. Structure of adeno-associated virus serotype 5. J. Virol. 78:3361-3371.
25. Padron E, Bowman V, Kaludov N, Govindasamy L, Levy H, Nick P, McKenna R, Muzyczka N, Chiorini JA, Baker TS, Agbandje-McKenna M. 2005. Structure of adeno-associated virus type 4. J. Virol. 79:5047-5058.
26. Ng R, Govindasamy L, Gurda BL, McKenna R, Kozyreva OG, Samulski RJ, Parent KN, Baker TS, Agbandje-McKenna M. 2010. Structural characterization of the dual glycan binding adeno-associated virus serotype 6. J. Virol. 84:12945-12957.
27. DiMattia MA, Nam HJ, Van Vliet K, Mitchell M, Bennett A, Gurda BL, McKenna R, Olson NH, Sinkovits RS, Potter M, Byrne BJ, Aslanidi G, Zolotukhin S, Muzyczka N, Baker TS, Agbandje-McKenna M. 2012. Structural insight into the unique properties of adenoassociated virus serotype 9. J. Virol. 86:6947-6958.
28. Kronenberg S, Bottcher B, von der Lieth CW, Bleker S, Kleinschmidt JA. 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.
29. Nam HJ, Lane MD, Padron E, Gurda B, McKenna R, Kohlbrenner E, Aslanidi G, Byrne B, Muzyczka N, Zolotukhin S, Agbandje-McKenna M. 2007. Structure of adeno-associated virus serotype 8, a gene therapy vector. J. Virol. 81:12260-12271.
30. Flannery JG, Zolotukhin S, Vaquero MI, LaVail MM, Muzyczka N, Hauswirth WW. 1997. Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus. Proc. Natl. Acad. Sci. U. S. A. 94:6916-6921.
31. Flotte TR. 2005. Recent developments in recombinant AAV-mediated gene therapy for lung diseases. Curr. Gene Ther. 5:361-366.
32. Herzog RW. 2004. AAV-mediated gene transfer to skeletal muscle. Methods Mol. Biol. 246:179-194.
33. Niemeyer GP, Herzog RW, Mount J, Arruda VR, Tillson DM, Hathcock J, van Ginkel FW, High KA, Lothrop CD, Jr. 2009. Long-term correction of inhibitor-prone hemophilia B dogs treated with liverdirected AAV2-mediated factor IX gene therapy. Blood 113:797-806.
34. Maguire AM, Simonelli F, Pierce EA, Pugh EN, Jr, Mingozzi F, Bennicelli J, BanfiS, Marshall KA, Testa F, Surace EM, Rossi S, Lyubarsky A, Arruda VR, Konkle B, Stone E, Sun J, Jacobs J, Dell'Osso L, Hertle R, Ma JX, Redmond TM, Zhu X, Hauck B, Zelenaia O, Shindler KS, Maguire MG, Wright JF, Volpe NJ, McDonnell JW, Auricchio A, High KA, Bennett J. 2008. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358:2240-2248.
35. Buch PK, Bainbridge JW, Ali RR. 2008. AAV-mediated gene therapy for retinal disorders: from mouse to man. Gene Ther. 15:849-857.
36. Cideciyan AV. 2010. Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog. Retin. Eye Res. 29:398-427.
37. Cideciyan AV, Hauswirth WW, Aleman TS, Kaushal S, Schwartz SB, Boye SL, Windsor EA, Conlon TJ, Sumaroka A, Pang JJ, Roman AJ, Byrne BJ, Jacobson SG. 2009. Human RPE65 gene therapy for Leber congenital amaurosis: persistence of early visual improvements and safety at 1 year. Hum. Gene Ther. 20:999-1004.
38. Dinculescu A, Estreicher J, Zenteno JC, Aleman TS, Schwartz SB, Huang WC, Roman AJ, Sumaroka A, Li Q, Deng WT, Min SH, Chiodo VA, Neeley A, Liu X, Shu X, Matias-Florentino M, Buentello-Volante B, Boye SL, Cideciyan AV, Hauswirth WW, Jacobson SG. 2012. Gene therapy for retinitis pigmentosa caused by MFRP mutations: human phenotype and preliminary proof of concept. Hum. Gene Ther. 23:367-376.
39. Jacobson SG, Acland GM, Aguirre GD, Aleman TS, Schwartz SB, Cideciyan AV, Zeiss CJ, Komaromy AM, Kaushal S, Roman AJ, Windsor EA, Sumaroka A, Pearce-Kelling SE, Conlon TJ, Chiodo VA, Boye SL, Flotte TR, Maguire AM, Bennett J, Hauswirth WW. 2006. Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol. Ther. 13:1074-1084.
40. Jacobson SG, Boye SL, Aleman TS, Conlon TJ, Zeiss CJ, Roman AJ, Cideciyan AV, Schwartz SB, Komaromy AM, Doobrajh M, Cheung AY, Sumaroka A, Pearce-Kelling SE, Aguirre GD, Kaushal S, Maguire AM, Flotte TR, Hauswirth WW. 2006. Safety in nonhuman primates of ocular AAV2-RPE65, a candidate treatment for blindness in Leber congenital amaurosis. Hum. Gene Ther. 17:845-858.
41. Mendell JR, Rodino-Klapac L, Sahenk Z, Malik V, Kaspar BK, Walker CM, Clark KR. 2012. Gene therapy for muscular dystrophy: lessons learned and path forward. Neurosci. Lett. 527:90-99.
42. Mendell JR, Rodino-Klapac LR, Rosales XQ, Coley BD, Galloway G, Lewis S, Malik V, Shilling C, Byrne BJ, Conlon T, Campbell KJ, Bremer WG, Taylor LE, Flanigan KM, Gastier-Foster JM, Astbury C, Kota J, Sahenk Z, Walker CM, Clark KR. 2010. Sustained alphasarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D. Ann. Neurol. 68:629-638.
43. Virella-Lowell I, Zusman B, Foust K, Loiler S, Conlon T, Song S, Chesnut KA, Ferkol T, Flotte TR. 2005. Enhancing rAAV vector expression in the lung. J. Gene Med. 7:842-850.
44. Zabner J, Seiler M, Walters R, Kotin RM, Fulgeras W, Davidson BL, Chiorini JA. 2000. Adeno-associated virus type 5 (AAV5) but not AAV2 binds to the apical surfaces of airway epithelia and facilitates gene transfer. J. Virol. 74:3852-3858.
45. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, Zolotukhin S, Reier PJ, Mandel RJ, Muzyczka N. 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.
46. Nathwani AC, Gray JT, McIntosh J, Ng CY, Zhou J, Spence Y, Cochrane M, Gray E, Tuddenham EG, DavidoffAM. 2007. Safe and efficient transduction of the liver after peripheral vein infusion of selfcomplementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109:1414-1421.
47. Duan D, Yan Z, Yue Y, Ding W, Engelhardt JF. 2001. Enhancement of muscle gene delivery with pseudotyped adeno-associated virus type 5 correlates with myoblast differentiation. J. Virol. 75:7662-7671.
48. Lipshutz GS, Titre D, Brindle M, Bisconte AR, Contag CH, Gaensler KM. 2003. Comparison of gene expression after intraperitoneal delivery of AAV2 or AAV5 in utero. Mol. Ther. 8:90-98.
49. Auricchio A, O'Connor E, Weiner D, Gao GP, Hildinger M, Wang L, Calcedo R, Wilson JM. 2002. Noninvasive gene transfer to the lung for systemic delivery of therapeutic proteins. J. Clin. Invest. 110:499-504.
50. Lin DS, Hsiao CD, Liau I, Lin SP, Chiang MF, Chuang CK, Wang TJ, Wu TY, Jian YR, Huang SF, Liu HL. 2011. CNS-targeted AAV5 gene transfer results in global dispersal of vector and prevention of morphological and function deterioration in CNS of globoid cell leukodystrophy mouse model. Mol. Genet. Metab. 103:367-377.
51. Agbandje-McKenna M, Kleinschmidt J. 2011. AAV capsid structure and cell interactions. Methods Mol. Biol. 807:47-92.
52. Xie Q, Lerch TF, Meyer NL, Chapman MS. 2011. Structure-function analysis of receptor-binding in adeno-associated virus serotype 6 (AAV-6). Virology 420:10-19.
53. Allocca M, Doria M, Petrillo M, Colella P, Garcia-Hoyos M, Gibbs D, Kim SR, Maguire A, Rex TS, Di Vicino U, Cutillo L, Sparrow JR, Williams DS, Bennett J, Auricchio A. 2008. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J. Clin. Invest. 118:1955-1964.
54. Wu Z, Yang H, Colosi P. 2010. Effect of genome size on AAV vector packaging. Mol. Ther. 18:80-86.
55. Dong B, Nakai H, Xiao W. 2010. Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther. 18:87-92.
56. Lai Y, Yue Y, Duan D. 2010. Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome≥8.2 kb. Mol. Ther. 18:75-79.
57. DiMattia M, Govindasamy L, Levy HC, Gurda-Whitaker B, Kalina A, Kohlbrenner E, Chiorini JA, McKenna R, Muzyczka N, Zolotukhin S, Agbandje-McKenna M. 2005. Production, purification, crystallization and preliminary X-ray structural studies of adeno-associated virus serotype 5. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61:917-921.
58. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
59. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
60. Brünger AT. 1993. Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr. D Biol. Crystallogr. 49:24-36.
61. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47:110-119.
62. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
63. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. 1996. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR8:477-486.
64. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
65. Kleywegt GJ, Zou JY, Kjeldgaard M, Jones TA. 2001. Around O, p 353-356. In Rossmann MG, Arnold E (ed), International tables for crystallography, vol F. Kluwer Academic Publishers, Dordrecht, The Netherlands.
66. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. Mol-Probity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
67. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60:2256-2268.
68. Xiao C, Rossmann MG. 2007. Interpretation of electron density with stereographic roadmap projections. J. Struct. Biol. 158:182-187.
69. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. 2009. The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37:D387-392.
70. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
71. Kaufmann B, Chipman PR, Kostyuchenko VA, Modrow S, Rossmann MG. 2008. Visualization of the externalized VP2 N termini of infectious human parvovirus B19. J. Virol. 82:7306-7312.
72. Halder S, Ng R, Agbandje-McKenna M. 2012. Parvoviruses: structure and infection. Future Virol. 7:253-278.
73. Chapman MS, Agbandje-McKenna M. 2006. Atomic structure of viral particles, p 107-123. In Kerr JR, Cotmore SF, Bloom ME, Linden RM, Parrish CR (ed), Parvoviruses. Hodder Arnold, London, United Kingdom.
74. Gekko K, TimasheffSN. 1981. Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry 20:4667-4676.
75. Gekko K, TimasheffSN. 1981. Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677-4686.
76. Coker SF, Lloyd AJ, Mitchell E, Lewis GR, Coker AR, Shoolingin-Jordan PM. 2010. The high-resolution structure of pig heart succinyl-CoA:3-oxoacid coenzyme A transferase. Acta Crystallogr. D Biol. Crystallogr. 66:797-805.
77. Chen S, Kapturczak M, Loiler SA, Zolotukhin S, Glushakova OY, Madsen KM, Samulski RJ, Hauswirth WW, Campbell-Thompson M, Berns KI, Flotte TR, Atkinson MA, Tisher CC, Agarwal A. 2005. Efficient transduction of vascular endothelial cells with recombinant adeno-associated virus serotype 1 and 5 vectors. Hum. Gene Ther. 16:235-247.
78. Wu Z, Miller E, Agbandje-McKenna M, Samulski RJ. 2006. α2,3 and α2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J. Virol. 80:9093-9103.
79. Li W, Zhang L, Wu Z, Pickles RJ, Samulski RJ. 2011. AAV-6 mediated efficient transduction of mouse lower airways. Virology 417:327-333.
80. Summerford C, Samulski RJ. 1998. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72:1438-1445.
81. Messina EL, Nienaber J, Daneshmand M, Villamizar N, Samulski J, Milano C, Bowles DE. 2012. Adeno-associated viral vectors based on serotype 3b use components of the fibroblast growth factor receptor signaling complex for efficient transduction. Hum. Gene Ther. 23:1031-1042.
82. Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA. 2001. 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. 75:6884-6893.
83. Walters RW, Pilewski JM, Chiorini JA, Zabner J. 2002. Secreted and transmembrane mucins inhibit gene transfer with AAV4 more efficiently than AAV5. J. Biol. Chem. 277:23709-23713.
84. Walters RW, Yi SM, Keshavjee S, Brown KE, Welsh MJ, Chiorini JA, Zabner J. 2001. Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J. Biol. Chem. 276:20610-20616.
85. Wu Z, Asokan A, Grieger JC, Govindasamy L, Agbandje-McKenna M, Samulski RJ. 2006. Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J. Virol. 80:11393-11397.
86. Bell CL, Vandenberghe LH, Bell P, Limberis MP, Gao GP, Van Vliet K, Agbandje-McKenna M, Wilson JM. 2011. The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J. Clin. Invest. 121:2427-2435.
87. Shen S, Bryant KD, Brown SM, Randell SH, Asokan A. 2011. Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem. 286:13532-13540.
88. Shen S, Bryant KD, Sun J, Brown SM, Troupes A, Pulicherla N, Asokan A. 2012. Glycan binding avidity determines the systemic fate of adeno-associated virus type 9. J. Virol. 86:10408-10417.
89. Di Pasquale G, Davidson BL, Stein CS, Martins I, Scudiero D, Monks A, Chiorini JA. 2003. Identification of PDGFR as a receptor for AAV-5 transduction. Nat. Med. 9:1306-1312.
90. O'Donnell J, Taylor KA, Chapman MS. 2009. Adeno-associated virus-2 and its primary cellular receptor-cryo-EM structure of a heparin complex. Virology 385:434-443.
91. Opie SR, Warrington KH, Jr, Agbandje-McKenna M, Zolotukhin S, 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.
92. Kern A, Schmidt K, Leder C, Muller OJ, Wobus CE, Bettinger K, Von der Lieth CW, King JA, Kleinschmidt JA. 2003. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77:11072-11081.
93. Levy HC, Bowman VD, Govindasamy L, McKenna R, Nash K, Warrington K, Chen W, Muzyczka N, Yan X, Baker TS, Agbandje-McKenna M. 2009. Heparin binding induces conformational changes in adeno-associated virus serotype 2. J. Struct. Biol. 165:146-156.
94. Raupp C, Naumer M, Muller OJ, Gurda BL, Agbandje-McKenna M, Kleinschmidt JA. 2012. The threefold protrusions of adeno-associated virus type 8 are involved in cell surface targeting as well as postattachment processing. J. Virol. 86:9396-9408.
95. Kotchey NM, Adachi K, Zahid M, Inagaki K, Charan R, Parker RS, Nakai H. 2011. A potential role of distinctively delayed blood clearance of recombinant adeno-associated virus serotype 9 in robust cardiac transduction. Mol. Ther. 19:1079-1089.
96. Pulicherla N, Shen S, Yadav S, Debbink K, Govindasamy L, Agbandje-McKenna M, Asokan A. 2011. Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol. Ther. 19:1070-1078.
97. Lochrie MA, Tatsuno GP, Christie B, McDonnell JW, Zhou S, Surosky R, Pierce GF, Colosi P. 2006. Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J. Virol. 80:821-834.
98. Wu P, Xiao W, Conlon T, Hughes J, Agbandje-McKenna M, Ferkol T, Flotte T, Muzyczka N. 2000. Mutational analysis of the adenoassociated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J. Virol. 74:8635-8647.
99. Li W, Asokan A, Wu Z, Van Dyke T, DiPrimio N, Johnson JS, Govindaswamy L, Agbandje-McKenna M, Leichtle S, Redmond DE, Jr, McCown TJ, Petermann KB, Sharpless NE, Samulski RJ. 2008. Engineering and selection of shuffled AAV genomes: a new strategy for producing targeted biological nanoparticles. Mol. Ther. 16:1252-1260.
100. Gurda BL, Raupp C, Popa-Wagner R, Naumer M, Olson NH, Ng R, McKenna R, Baker TS, Kleinschmidt JA, Agbandje-McKenna M. 2012. Mapping a neutralizing epitope onto the capsid of adeno-associated virus serotype 8. J. Virol. 86:7739-7751.
101. Wobus CE, Hugle-Dorr B, Girod A, Petersen G, Hallek M, Kleinschmidt JA. 2000. 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. 74:9281-9293.
102. Excoffon KJ, Koerber JT, Dickey DD, Murtha M, Keshavjee S, Kaspar BK, Zabner J, Schaffer DV. 2009. Directed evolution of adenoassociated virus to an infectious respiratory virus. Proc. Natl. Acad. Sci. U. S. A. 106:3865-3870.
103. Dickey DD, Excoffon KJ, Koerber JT, Bergen J, Steines B, Klesney-Tait J, Schaffer DV, Zabner J. 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.
104. DiPrimio N, Asokan A, Govindasamy L, Agbandje-McKenna M, Samulski RJ. 2008. Surface loop dynamics in adeno-associated virus capsid assembly. J. Virol. 82:5178-5189.
105. Bleker S, Pawlita M, Kleinschmidt JA. 2006. Impact of capsid conformation and Rep.-capsid interactions on adeno-associated virus type 2 genome packaging. J. Virol. 80:810-820.
106. Bleker S, Sonntag F, Kleinschmidt JA. 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.
107. Dubielzig R, King JA, Weger S, Kern A, Kleinschmidt JA. 1999. Adeno-associated virus type 2 protein interactions: formation of preencapsidation complexes. J. Virol. 73:8989-8998.
108. King JA, Dubielzig R, Grimm D, Kleinschmidt JA. 2001. DNA helicasemediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282-3291.
109. Prasad KM, Trempe JP. 1995. The adeno-associated virus Rep78 protein is covalently linked to viral DNA in a preformed virion. Virology 214:360-370.
110. Prasad KM, Zhou C, Trempe JP. 1997. Characterization of the Rep78/adeno-associated virus complex. Virology 229:183-192.
111. Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ. 2006. Adeno-associated virus type 2 contains an integrin α5β1 binding domain essential for viral cell entry. J. Virol. 80:8961-8969.
112. Shi W, Arnold GS, Bartlett JS. 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.
113. Hida K, Won SY, Di Pasquale G, Hanes J, Chiorini JA, Ostermeier M. 2010. Sites in the AAV5 capsid tolerant to deletions and tandem duplications. Arch. Biochem. Biophys. 496:1-8.
114. McCraw DM, O'Donnell JK, Taylor KA, Stagg SM, Chapman MS. 2012. Structure of adeno-associated virus-2 in complex with neutralizing monoclonal antibody A20. Virology 431:40-49.
115. Grieger JC, Samulski RJ. 2005. Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J. Virol. 79:9933-9944.
116. Warrington KH, Jr, Gorbatyuk OS, Harrison JK, Opie SR, Zolotukhin S, Muzyczka N. 2004. Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at itsNterminus. J. Virol. 78:6595-6609.
117. Myers MW, Carter BJ. 1980. Assembly of adeno-associated virus. Virology 102:71-82.
118. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
119. Esnouf R. 1999. Further additions to Molscript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 55:938-940.
120. Merritt EA, Murphy MEP. 1994. Raster3D version 2.0: a program for photorealistic molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 50:869-873.
121. Merritt EA, Bacon DJ. 1997. Raster3D-photorealistic molecular graphics. Methods Enzymol. 277:505-524.
122. Bell CL, Gurda BL, Van Vliet K, Agbandje-McKenna M, Wilson JM. 2012. Identification of the galactose binding domain of the adenoassociated virus serotype 9 capsid. J Virol. 86:7326-7333