Surface-exposed adeno-associated virus Vp1-NLS capsid fusion protein rescues infectivity of noninfectious wild-type Vp2/Vp3 and Vp3-only capsids but not that of fivefold pore mutant virions

Journal of Virology

Volumn 81, Issue 15, 2007, Pages 7833-7843

  Grieger, Joshua C ^a,b   Johnson, Jarrod S ^b   Gurda Whitaker, Brittney ^c   Agbandje McKenna, Mavis ^c   Samulski, R Jude ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALANINE; CAPSID PROTEIN; CYSTEINE; HYBRID PROTEIN; LEUCINE; PHOSPHOLIPASE A2; TRYPTOPHAN; UNCLASSIFIED DRUG; VIRUS CAPSID PROTEIN 1; VIRUS CAPSID PROTEIN 2; VIRUS CAPSID PROTEIN 3;

ADENO ASSOCIATED VIRUS; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS MUTATION; WESTERN BLOTTING; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CAPSID; CAPSID PROTEINS; CELL LINE; CHEMOKINES, CX3C; DEPENDOVIRUS; HUMANS; MEMBRANE PROTEINS; MODELS, MOLECULAR; NUCLEAR LOCALIZATION SIGNALS; PROTEIN STRUCTURE, QUATERNARY; RATS; RECOMBINANT FUSION PROTEINS; VIRION;

ADENO-ASSOCIATED VIRUS; MIRIDAE; RATTUS;

EID: 34547117580     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00580-07     Document Type: Article

References (54)

1. Agbandje, M., S. Kajigaya, R. McKenna, N. S. Young, and M. G. Rossmann. 1994. The structure of human parvovirus B19 at 8 Å resolution. Virology 203:106-115.
2. Agbandje, M., R. McKenna, M. G. Rossmann, M. L. Strassheim, and C. R. Parrish. 1993. Structure determination of feline panleukopenia virus empty particles. Proteins 16:155-171.
3. 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.
4. Asokan, A., J. B. Hamra, L. Govindasamy, M. Agbandje-McKenna, and R. J. Samulski. 2006. Adeno-associated virus type 2 contains an integrin α5β1 binding domain essential for viral cell entry. J. Virol. 80:8961-8969.
5. Atchison, R. W., B. C. Casto, and W. M. Hammon. 1965. Adenovirus-associated defective virus particles. Science 149:754-756.
6. Bleker, S., F. Sonntag, and J. A. Kleinschmidt. 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.
7. Buller, R. M., J. E. Janik, E. D. Sebring, and J. A. Rose. 1981. Herpes simplex virus types 1 and 2 completely help adenovirus-associated virus replication. J. Virol. 40:241-247.
8. Canaan, S., Z. Zadori, F. Ghomashchi, J. Bollinger, M. Sadilek, M. E. Moreau, P. Tyssen, and M. H. Gelb. 2004. Interfacial enzymology of parvovirus phospholipases A2. J. Biol. Chem. 279:14502-14508.
9. 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.
10. Chejanovsky, N., and B. J. Carter. 1989. Mutagenesis of an AUG codon in the adeno-associated virus rep gene: effects on viral DNA replication. Virology 173:120-128.
11. Clark, K. R., F. Voulgaropoulou, D. M. Fraley, and P. R. Johnson. 1995. Cell lines for the production of recombinant adeno-associated virus. Hum. Gene Ther. 6:1329-1341.
12. Clark, K. R., F. Voulgaropoulou, and P. R. Johnson. 1996. A stable cell line carrying adenovirus-inducible rep and cap genes allows for infectivity titration of adeno-associated virus vectors. Gene Ther. 3:1124-1132.
13. Cotmore, S. F., M. A. 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.
14. 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.
15. Dorsch, S., G. Liebisch, B. Kaufmann, P. von Landenberg, J. H. Hoffmann, W. Drobnik, and S. Modrow. 2002. The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. J. Virol. 76:2014-2018.
16. 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.
17. Farr, G. A., and P. Tattersall. 2004. A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 323:243-256.
18. Farr, G. A., L. G. Zhang, and P. Tattersall. 2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 102:17148-17153.
19. Grieger, J. C., S. Snowdy, and R. J. Samulski. 2006. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 80:5199-5210.
20. 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.
21. 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.
22. 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.
23. King, J. A., R. Dubielzig, D. Grimm, and J. A. Kleinschmidt. 2001. DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282-3291.
24. Kronenberg, S., B. Bottcher, C. W. von der Lieth, S. Bleker, and J. A. Kleinschmidt. 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.
25. 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.
26. Llamas-Saiz, A. L., M. Agbandje-McKenna, W. R. Wikoff, J. Bratton, P. Tattersall, and M. G. Rossmann. 1997. Structure determination of minute virus of mice. Acta Crystallogr, D 53:93-102.
27. Lombardo, E., J. C. Ramirez, J. Garcia, and J. M. Almendral. 2002. Complementary roles of multiple nuclear targeting signals in the capsid proteins of the parvovirus minute virus of mice during assembly and onset of infection. J. Virol. 76:7049-7059.
28. + entry by human parvovirus B19 capsid protein VP1. J. Virol. 80:11370-11380.
29. 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.
30. Lux, K., N. Goerlitz, S. Schlemminger, L. Perabo, D. Goldnau, J. Endell, K. Leike, D. M. Koffer, S. Finke, M. Hallek, and H. Buning. 2005. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J. Virol. 79:11776-11787.
31. McKenna, R., N. H. Olson, P. R. Chipman, T. S. Baker, T. F. Booth, J. Christensen, B. Aasted, J. M. Fox, M. E. Bloom, J. B. Wolfinbarger, and M. Agbandje-McKenna. 1999. Three-dimensional structure of Aleutian mink disease parvovirus: implications for disease pathogenicity. J. Virol. 73:6882-6891.
32. 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.
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. Schwede T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
35. Simpson, A. A., P. R. Chipman, T. S. Baker, P. Tijssen, and M. G. Rossmann. 1998. The structure of an insect parvovirus (Galleria mellonella densovirus) at 3.7 Å resolution. Structure 6:1355-1367.
36. Sonntag, F., S. Bleker, B. Leuchs, R. Fischer, and J. A. Kleinschmidt. 2006. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J. Virol. 80:11040-11054.
37. 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.
38. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316: 267-280.
39. Summerford, C., J. S. Bartlett, and R. J. Samulski. 1999. αVβ5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat. Med. 5:78-82.
40. 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.
41. Tsao, J., M. S. Chapman, M. Agbandje, W. Keller, K. Smith, H. Wu, M. Luo, T. J. Smith, M. G. Rossmann, R. W. Compans, et al. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464.
42. Vihinen-Ranta, M., D. Wang, W. S. Weichert, and C. R. Parrish. 2002. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 76:1884-1891.
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. 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.
45. 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.
46. Wu, H., and M. G. Rossmann. 1993. The canine parvovirus empty capsid structure. J. Mol. Biol. 233:231-244.
47. Wu, P., W. Xiao, T. Conlon, J. Hughes, M. Agbandje-McKenna, T. Ferkol, T. Flotte, and N. Muzyczka. 2000. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J. Virol. 74:8635-8647.
48. Xiao, W., K. H. Warrington, Jr., P. Hearing, J. Hughes, and N. Muzyczka. 2002. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J. Virol. 76:11505-11517.
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 Å resolution. J. Mol. Biol. 264:497-520.
51. Yan, 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. 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.
54. 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.