Packaging capacity of adeno-associated virus serotypes: Impact of larger genomes on infectivity and postentry steps

Journal of Virology

Volumn 79, Issue 15, 2005, Pages 9933-9944

  Grieger, Joshua C ^a   Samulski, Richard J ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME INHIBITOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEGRADATION; DISEASE ASSOCIATION; DOT HYBRIDIZATION; ENCAPSULATION; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; REPORTER GENE; SEROTYPING; SIGNAL TRANSDUCTION; VIRUS INFECTIVITY; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; CAPSID PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEPENDOVIRUS; GENE DELETION; GENE EXPRESSION; GENETIC VECTORS; GENOME, VIRAL; HUMANS; VIRUS ASSEMBLY;

ADENO-ASSOCIATED VIRUS; MICE MINUTE VIRUS; MIRIDAE; PARVOVIRUS;

EID: 22544462537     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.15.9933-9944.2005     Document Type: Article

References (56)

1. Agbandje-McKenna, M., A. L. Llamas-Saiz, F. Wang, P. Tattersall, and M. G. Rossmann. 1998. Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6:1369-1381.
2. Bett, A. J., L. Prevec, and F. L. Graham. 1993. Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol. 67:5911-5921.
3. Bloss, T. A., and B. Sugden. 1994. Optimal lengths for DNAs encapsidated by Epstein-Barr virus. J. Virol. 68:8217-8222.
4. Brandenburger, A., E. Coessens, K. El Bakkouri, and T. Velu. 1999. Influence of sequence and size of DNA on packaging efficiency of parvovirus MVM-based vectors. Hum. Gene Ther. 10:1229-1238.
5. Carreira, A., M. Menendez, J. Reguera, J. M. Almendral, and M. G. Mateu. 2004. In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279:6517-6525.
6. Chang, X. B., and J. H. Wilson. 1986. Formation of deletions after initiation of simian virus 40 replication: influence of packaging limit of the capsid. J. Virol. 58:393-401.
7. Chapman, M. S., and M. G. Rossmann. 1995. Single-stranded DNA-protein interactions in canine parvovirus. Structure 3:151-162.
8. Cotmore, S. F., A. M. D'Abramo, Jr., C. M. Ticknor, and P. Tattersall. 1999. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 254:169-181.
9. Di Pasquale, G., B. L. Davidson, C. S. Stein, I. Martins, D. Scudiero, A. Monks, and J. A. Chiorini. 2003. Identification of PDGFR as a receptor for AAV-5 transduction. Nat. Med. 9:1306-1312.
10. Dong, J. Y., P. D. Fan, and R. A. Frizzell. 1996. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7:2101-2112.
11. Douar, A. M., K. Poulard, D. Stockholm, and O. Danos. 2001. Intracellular trafficking of adeno-associated virus vectors: routing to the late endosomal compartment and proteasome degradation. J. Virol. 75:1824-1833.
12. Drumm, M. L., H. A. Pope, W. H. Cliff, J. M. Rommens, S. A. Marvin, L. C. Tsui, F. S. Collins, R. A. Frizzell, and J. M. Wilson. 1990. Correction of the cystic fibrosis defect in vitro by retrovirus-mediated gene transfer. Cell 62:1227-1233.
13. Duan, D., Y. Yue, and J. F. Engelhardt, 2003. Dual vector expansion of the recombinant AAV packaging capacity. Methods Mol. Biol. 219:29-51.
14. Duan, D., Y. Yue, and J. F. Engelhardt. 2001. Expanding AAV packaging capacity with trans-splicing or overlapping vectors: a quantitative comparison Mol. Ther. 4:383-391.
15. Duan, D., Y. Yue, Z. Yan, and J. F. Engelhardt. 2000. A new dual-vector approach to enhance recombinant adeno-associated virus-mediated gene expression through intermolecular cis activation. Nat. Med. 6:595-598.
16. Duan, D., Y. Yue, Z. Yan, and J. F. Engelhardt. 2003. Trans-splicing vectors expand the packaging limits of adeno-associated virus for gene therapy applications. Methods Mol. Med. 76:287-307.
17. Flotte, T. R., S. A. Afione, C. Conrad, S. A. McGrath, R. Solow, H. Oka, P. L. Zeitlin, W. B. Guggino, and B. J. Carter. 1993. Stable in vivo expression of the cystic fibrosis transmembrane conductance regulator with an adeno-associated virus vector. Proc. Natl. Acad. Sci. USA 90:10613-10617.
18. Flotte, T. R., S. A. Afione, R. Solow, M. L. Drumm, D. Markakis, W. B. Guggino, P. L. Zeitlin, and B. J. Carter. 1993. Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-associated virus promoter. J. Biol. Chem. 268:3781-3790.
19. Girod, A., C. E. Wobus, Z. Zadori, M. Ried, K. Leike, P. Tijssen, J. A. Kleinschmidt, and M. Hallek. 2002. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J. Gen. Virol. 83:973-978.
20. Haberman, R. A., G. Kroner-Lux, and R. J. Samulski. 1999. Production of recombinant adeno-associated viral vectors. Curr. Protoc. Hum. Genet. 23(Suppl.):12.9.1-12.9.17.
21. Haberman, R. P., T. J. McCown, and R. J. Samulski. 2000. Novel transcriptional regulatory signals in the adeno-associated virus terminal repeat A/D junction element. J. Virol. 74:8732-8739.
22. Hansen, J., K. Qing, and A. Srivastava. 2001. Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J. Virol. 75:4080-4090.
23. Hermonat, P. L., J. G. Quirk, B. M. Bishop, and L. Han. 1997. The packaging capacity of adeno-associated virus (AAV) and the potential for wild-type-plus AAV gene therapy vectors. FEBS Lett. 407:78-84.
24. Jones, N., and T. Shenk. 1979. Isolation of adenovirus type 5 host range deletion mutants defective for transformation of rat embryo cells. Cell 17:683-689.
25. Kashiwakura, Y., K. Tamayose, K. Iwabuchi, Y. Hirai, T. Shimada, K. Matsumoto, T. Nakamura, M. Watanabe, K. Oshimi, and H. Daida. 2005. Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J. Virol. 79:609-614.
26. Kawase, M., M. Momoeda, N. S. Young, and S. Kajigaya. 1995. Most of the VP1 unique region of B19 parvovirus is on the capsid surface. Virology 211:359-366.
27. Kronenberg, S., J. A. Kleinschmidt, and B. Bottcher. 2001. Electron cryomicroscopy and image reconstruction of adeno-associated virus type 2 empty capsids. EMBO Rep. 2:997-1002.
28. Lusby, E., K. H. Fife, and K. I. Berns. 1980. Nucleotide sequence of the inverted terminal repetition in adeno-associated virus DNA. J. Virol. 34:402-409.
29. McCarty, D. M., S. M. Young, Jr., and R. J. Samulski. 2004. Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38:819-845.
30. Muralidhar, S., S. P. Becerra, and J. A. Rose. 1994. Site-directed mutagenesis of adeno-associated virus type 2 structural protein initiation codons: effects on regulation of synthesis and biological activity. J. Virol. 68:170-176.
31. Qing, K., C. Mah, J. Hansen, S. Zhou, V. Dwarki, and A. Srivastava. 1999. Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat. Med. 5:71-77.
32. Rabinowitz, J. E., F. Rolling, C. Li, H. Conrath, W. Xiao, X. Xiao, and R. J. Samulski. 2002. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J. Virol. 76:791-801.
33. Reguera, J., A. Carreira, L. Riolobos, J. M. Almendral, and M. G. Mateu. 2004. Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid. Proc. Natl. Acad. Sci. USA 101:2724-2729.
34. Rosenfeld, S. J., K. Yoshimoto, S. Kajigaya, S. Anderson, N. S. Young, A. Field, P. Warrener, G. Bansal, and M. S. Collett. 1992. Unique region of the minor capsid protein of human parvovirus B19 is exposed on the virion surface. J. Clin. Investig. 89:2023-2029.
35. 34a.Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
36. Sarkar, R., R. Tetreault, G. Gao, L. Wang, P. Bell, R. Chandler, J. M. Wilson, and H. H. Kazazian, Jr. 2004. Total correction of hemophilia A mice with canine FVIII using an AAV 8 serotype. Blood 103:1253-1260.
37. Sirninger, J., C. Muller, S. Braag, Q. Tang, H. Yue, C. Detrisac, T. Ferkol, W. B. Guggino, and T. R. Flotte. 2004. Functional characterization of a recombinant adeno-associated virus 5-pseudotyped cystic fibrosis transmembrane conductance regulator vector. Hum. Gene Ther. 15:832-841.
38. Srivastava, A., E. W. Lusby, and K. I. Berns. 1983. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J. Virol. 45:555-564.
39. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
40. Summerford, C., J. S. Bartlett, and R. J. Samulski. 1999. AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat. Med. 5:78-82.
41. Summerford, C., and R. J. Samulski. 1998. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72:1438-1445.
42. Sun, L., J. Li, and X. Xiao. 2000. Overcoming adeno-associated virus vector size limitation through viral DNA heterodimerization. Nat. Med. 6:599-602.
43. Walters, R. W., M. Agbandje-McKenna, V. D. Bowman, T. O. Moninger, N. H. Olson, M. Seiler, J. A. Chiorini, T. S. Baker, and J. Zabner. 2004. Structure of adeno-associated virus serotype 5. J. Virol. 78:3361-3371.
44. Wang, D., H. Fischer, L. Zhang, P. Fan, R. X. Ding, and J. Dong. 1999. Efficient CFTR expression from AAV vectors packaged with promoters-the second generation. Gene Ther. 6:667-675.
45. Warrington, K. H., Jr., O. S. Gorbatyuk, J. K. Harrison, S. R. Opie, S. Zolotukhin, and N. Muzyczka. 2004. Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at its N terminus. J. Virol. 78:6595-6609.
46. Weichert, W. S., J. S. Parker, A. T. Wahid, S. F. Chang, E. Meier, and C. R. Parrish. 1998. Assaying for structural variation in the parvovirus capsid and its role in infection. Virology 250:106-117.
47. Wobus, C. E., B. Hugle-Dorr, A. Girod, G. Petersen, M. Hallek, and J. A. Kleinschmidt. 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.
48. Wu, H., and M. G. Rossmann. 1993. The canine parvovirus empty capsid structure. J. Mol. Biol. 233:231-244.
49. Xie, Q., W. Bu, S. Bhatia, J. Hare, T. Somasundaram, A. Azzi, and M. S. Chapman. 2002. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. USA 99:10405-10410.
50. Xie, Q., and M. S. Chapman. 1996. Canine parvovirus capsid structure, analyzed at 2.9 A resolution. J. Mol. Biol. 264:497-520.
51. Van, Z., R. Zak, G. W. Luxton, T. C. Ritchie, U. Bantel-Schaal, and J. F. Engelhardt. 2002. Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J. Virol. 76:2043-2053.
52. Yan, Z., R. Zak, Y. Zhang, W. Ding, S. Godwin, K. Munson, R. Peluso, and J. F. Engelhardt. 2004. Distinct classes of proteasome-modulating agents cooperatively augment recombinant adeno-associated virus type 2 and type 5-mediated transduction from the apical surfaces of human airway epithelia. J. Virol. 78:2863-2874.
53. Yan, Z., Y. Zhang, D. Duan, and J. F. Engelhardt. 2000. Trans-splicing vectors expand the utility of adeno-associated vims for gene therapy. Proc. Natl. Acad. Sci. USA 97:6716-6721.
54. Zadori, Z., J. Szelei, M. C. Lacoste, Y. Li, S. Gariepy, P. Raymond, M. Allaire, I. R. Nabi, and P. Tijssen. 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1:291-302.
55. Zhang, L., D. Wang, H. Fischer, P. D. Fan, J. H. Widdicombe, Y. W. Kan, and J. Y. Dong. 1998. Efficient expression of CFTR function with adeno-associated virus vectors that carry shortened CFTR genes. Proc. Natl. Acad. Sci. USA 95:10158-10163.
56. Zolotukhin, S., B. J. Byrne, E. Mason, I. Zolotukhin, M. Potter, K. Chesnut, C. Summerford, R. J. Samulski, and N. Muzyczka. 1999. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther. 6:973-985.