Pathways of cell infection by parvoviruses and adeno-associated viruses

Journal of Virology

Volumn 78, Issue 13, 2004, Pages 6709-6714

  Vihinen Ranta, Maija ^a   Suikkanen, Sanna ^a   Parrish, Colin R ^b  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME INHIBITOR; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; VIRUS DNA; VIRUS RECEPTOR;

ADENO ASSOCIATED VIRUS; CELL NUCLEUS; CELL SURFACE; CHEMICAL MODIFICATION; DNA DETERMINATION; INTRACELLULAR TRANSPORT; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CELL LINE; DEPENDOVIRUS; DOGS; HUMANS; MICE; PARVOVIRIDAE INFECTIONS; PARVOVIRUS;

EID: 2942650156     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.13.6709-6714.2004     Document Type: Short Survey

References (91)

1. 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.
2. 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.
3. Ball-Goodrich, L. J., and P. Tattersall. 1992. Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. J. Virol. 66:3415-3423.
4. Bantel-Schaal, U., B. Hub, and J. Kartenbeck. 2002. Endocytosis of adeno-associated virus type 5 leads to accumulation of virus particles in the Golgi compartment. J. Virol. 76:2340-2349.
5. Barbis, D. P., S.-F. Chang, and C. R. Parrish. 1992. Mutations adjacent to the dimple of canine parvovirus capsid structure affect sialic acid binding. Virology 191:301-308.
6. 2 antibody. Nat. Biotechnol. 17:181-186.
7. Bartlett, J. S., R. Wilcher, and R. J. Samulski. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74:2777-2785.
8. Basak, S., and H. Turner. 1992. Infectious entry pathway for canine parvovirus. Virology 186:368-376.
9. Becerra, S. P., F. Koczot, P. Fabisch, and J. A. Rose. 1988. Synthesis of adeno-associated virus structural proteins requires both alternative mRNA splicing and alternative initiations from a single transcript. J. Virol. 62:2745-2754.
10. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
11. Brown, K. E., N. S. Young, and J. M. Liu. 1994. Molecular, cellular and clinical aspects of parvovirus B19 infection. Crit. Rev. Oncol. Hematol. 16:1-31.
12. Brownstein, D. G., A. L. Smith, R. O. Jacoby, E. A. Johnson, G. Hansen, and P. Tattersall. 1991. Pathogenesis of infection with a virulent allotropic variant of minute virus of mice and regulation by host genotype. Lab. Investig. 65:357-364.
13. Brunstein, J., and C. R. Astell. 1997. Analysis of the internal replication sequence indicates that there are three elements required for efficient replication of minute virus of mice minigenomes. J. Virol. 71:9087-9095.
14. Chang, S. F., J. Y. Sgro, and C. R. Parrish. 1992. Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties. J. Virol. 66:6858-6867.
15. Chiorini, J. A., S. M. Wiener, L. Yang, R. H. Smith, B. Safer, N. P. Kilcoin, Y. Liu, E. Urcelay, and R. M. Kotin. 1996. The roles of AAV Rep proteins in gene expression and targeted integration. Curr. Top. Microbiol. Immunol. 218:25-33.
16. 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.
17. Cotmore, S. F., and P. Tattersall. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
18. Cotmore, S. F., and P. Tattersall. 1988. The NS-1 polypeptide of minute virus of mice is covalently attached to the 5′ termini of duplex replicative form DNA and progeny single strands. J. Virol. 62:851-860.
19. 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.
20. 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.
21. Duan, D., Q. Li, A. W. Kao, Y. Yue, J. E. Pessin, and J. F. Engelhardt. 1999. Dynamin is required for recombinant adeno-associated virus type 2 infection. J. Virol. 73:10371-10376.
22. Fauquet, C. M., and M. A. Mayo. 2001. The 7th ICTV report. Arch. Virol. 146:189-194.
23. Girod, A., M. Ried, C. Wobus, H. Lahm, K. Leike, J. Kleinschmidt, G. Deleage, and M. Hallek. 1999. Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat. Med. 5:1052-1056.
24. Girod, A., C. E. Wobus, Z. Zadori, M. Ried, K. Leike, P. Tüssen, 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.
25. Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell. Dev. Biol. 15:607-660.
26. Greber, U. F. 2002. Signalling in viral entry. Cell. Mol. Life Sci. 59:608-626.
27. 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.
28. Hansen, J., K. Qing, and A. Srivastava. 2001. Infection of purified nuclei by adeno-associated virus 2. Mol. Ther. 4:289-296.
29. Hoque, M., K.-I. Ishizu, A. Matsumoto, S.-I. Han, F. Arisaka, M. Takayama, K. Suzuki, K. Kato, T. Kanda, H. Watanabe, and H. Handa. 1999. Nuclear transport of the major capsid protein is essential for adeno-associated virus capsid formation. J. Virol. 73:7912-7915.
30. Hueffer, K., L. Govindasamy, M. Agbandje-McKenna, and C. R. Parrish. 2003. Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses. J. Virol. 77:10099-10105.
31. Hueffer, K., J. S. Parker, W. S. Weichert, R. E. Geisel, J. Y. Sgro, and C. R. Parrish. 2003. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J. Virol. 77:1718-1726.
32. Kaludov, N., K. E. Brown, R. W. Walters, J. Zabner, and J. A. Chiorini. 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.
33. Kotin, R. M., R. M. Linden, and K. I. Berns. 1992. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J. 11:5071-5078.
34. Linser, P., H. Bruning, and R. W. Armentrout. 1979. Uptake of minute virus of mice into cultured rodent cells. J. Virol. 31:537-545.
35. Liu, J. M., S. W. Green, T. Shimada, and N. S. Young. 1992. A block in full-length transcript maturation in cells nonpermissive for B19 parvovirus. J. Virol. 66:4686-4692.
36. Lombardo, E., J. C. Ramirez, M. Agbandje-McKenna, and J. M. Almendral. 2000. A beta-stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J. Virol. 74:3804-3814.
37. 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.
38. Luby-Phelps, K. 2000. Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int. Rev. Cytol. 192:189-221.
39. Mabit, H., M. Y. Nakano, U. Prank, B. Saam, K. Dohner, B. Sodeik, and U. F. Greber. 2002. Intact microtubules support adenovirus and herpes simplex virus infections. J. Virol. 76:9962-9971.
40. Muzyczka, N. 1992. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 158:97-129.
41. Muzyczka, N., and K. I. Berns. 2001. Parvoviridae: the viruses and their replication, p. 2327-2359. In D. M. Knipe, P. M. Howley, D. E. Griffen, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, vol. 2. Lippincott Williams and Wilkins, Philadelphia, Pa.
42. Nigg, E. A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature (London) 386:779-787.
43. Opie, S. R., K. H. Warrington, Jr., M. Agbandje-McKenna, S. Zolotukhin, and N. Muzyczka. 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.
44. Parker, J. S., and C. R. Parrish. 2000. Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 74:1919-1930.
45. Parker, J. S. L., W. J. Murphy, D. Wang, S. J. O'Brien, and C. R. Parrish. 2001. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75:3896-3902.
46. Parrish, C. R. 1990. Emergence, natural history, and variation of canine, mink, and feline parvoviruses. Adv. Virus Res. 38:403-450.
47. Pasquale, G. D., 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.
48. Pelkmans, L., and A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
49. Prasad, K. M., and J. P. Trempe. 1995. The adeno-associated virus Rep78 protein is covalently linked to viral DNA in a preformed virion. Virology 214:360-370.
50. Qing, K., J. Hansen, K. A. Weigel-Kelley, M. Tan, S. Zhou, and A. Srivastava. 2001. Adeno-associated virus type 2-mediated gene transfer: role of cellular FKBP52 protein in transgene expression. J. Virol. 75:8968-8976.
51. 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.
52. Qiu, J., and K. E. Brown. 1999. Integrin alphaVbeta5 is not involved in adeno-associated virus type 2 (AAV2) infection. Virology 264:436-440.
53. Qiu, J., A. Handa, M. Kirby, and K. E. Brown. 2000. The interaction of heparin sulfate and adeno-associated virus 2. Virology 269:137-147.
54. Ried, M. U., A. Girod, K. Leike, H. Buning, and M. Hallek. 2002. Adeno-associated virus capsids displaying immunoglobulin-binding domains permit antibody-mediated vector retargeting to specific cell surface receptors. J. Virol. 76:4559-4566.
55. Ros, C., C. J. Burckhardt, and C. Kempf. 2002. Cytoplasmic trafficking of minute virus of mice: low-pH requirement, routing to late endosomes, and proteasome interaction. J. Virol. 76:12634-12645.
56. Samulski, R. J. 1993. Adeno-associated virus: integration at a specific chromosomal locus. Curr. Opin. Genet. Dev. 3:74-80.
57. Sanlioglu, S., P. K. Benson, J. Yang, E. M. Atkinson, T. Reynolds, and J. F. Engelhardt. 2000. Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by Rac1 and phosphatidylinositol-3 kinase activation. J. Virol. 74:9184-9196.
58. Seisenberger, G., M. U. Ried, T. Endress, H. Buning, M. Hallek, and C. Brauchle. 2001. Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294:1929-1932.
59. Seksek, O., J. Biwersi, and A. S. Verkman. 1997. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell Biol. 138:131-142.
60. Shaughnessy, E., D. Lu, S. Chatterjee, and K. K. Wong. 1996. Parvoviral vectors for the gene therapy of cancer. Semin. Oncol. 23:159-171.
61. Shi, W., G. S. Arnold, and J. S. Bartlett. 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.
62. Shi, W., and J. S. Bartlett. 2003. RGD inclusion in VP3 provides adeno-associated virus type 2 (AAV2)-based vectors with a heparan sulfate-independent cell entry mechanism. Mol. Ther. 7:515-525.
63. Sieczkarski, S. B., and G. R. Whittaker. 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545.
64. Simpson, A. A., V. Chandrasekar, B. Hebert, G. M. Sullivan, M. G. Rossmann, and C. R. Parrish. 2000. Host range and variability of calcium binding by surface loops in the capsids of canine and feline parvoviruses. J. Mol. Biol. 300:597-610.
65. 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.
66. Sodeik, B. 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8:465-472.
67. Suikkanen, S., T. Aaltonen, M. Nevalainen, O. Valilehto, L. Lindholm, M. Vuento, and M. Vihinen-Ranta. 2003. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77:10270-10279.
68. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
69. Suikkanen, S., K. Saajarvi, J. Hirsimaki, O. Valilehto, H. Reunanen, M. Vihinen-Ranta, and M. Vuento. 2002. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 76:4401-4411.
70. 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.
71. 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.
72. Tattersall, P., A. J. Shatkin, and D. C. Ward. 1977. Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111:775-794.
73. Tresnan, D. B., L. Southard, W. Weichert, J. Y. Sgro, and C. R. Parrish. 1995. Analysis of the cell and erythrocyte binding activities of the dimple and canyon regions of the canine parvovirus capsid. Virology 211:123-132.
74. Tsao, J., M. S. Chapman, M. Agbandje, W. Keller, K. Smith, H. Wu, M. Luo, T. J. Smith, M. G. Rossmann, R. W. Compans, and C. R. Parrish. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464.
75. Tsao, J., M. S. Chapman, H. Wu, M. Agbandje, W. Keller, and M. G. Rossmann. 1992. Structure determination of monoclinic canine parvovirus. Acta Crystallogr. Sect. B Struct. Sci. 48:75-88.
76. Tullis, G. E., L. R. Burger, and D. J. Pintel. 1992. The trypsin-sensitive RVER domain in the capsid proteins of minute virus of mice is required for efficient cell binding and viral infection but not for proteolytic processing in vivo. Virology 191:846-857.
77. Vihinen-Ranta, M., L. Kakkola, A. Kalela, P. Vilja, and M. Vuento. 1997. Characterization of a nuclear localization signal of canine parvovirus capsid proteins. Eur. J. Biochem. 250:389-394.
78. 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.
79. Vihinen-Ranta, M., W. Yuan, and C. R. Parrish. 2000. Cytoplasmic trafficking of the canine parvovirus capsid and its role in infection and nuclear transport. J. Virol. 74:4853-4859.
80. Walters, R. W., S. Yi, S. Keshavjee, K. E. Brown, M. J. Welsh, J. A. Chiorini, and J. Zabner. 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.
81. Wang, D., and C. R. Parrish. 1999. A heterogeneous nuclear ribonucleoprotein A/B-related protein binds to single-stranded DNA near the 5′ end or within the genome of feline parvovirus and can modify virus replication. J. Virol. 73:7761-7768.
82. Weichert, W. S., J. S. Parker, A. T. M. 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.
83. Weigel-Kelley, K. A., M. C. Yoder, and A. Srivastava. 2001. Recombinant human parvovirus B19 vectors: erythrocyte P antigen is necessary but not sufficient for successful transduction of human hematopoietic cells. J. Virol. 75:4110-5116.
84. Whittaker, G. R., and A. Helenius. 1998. Nuclear import and export of viruses and virus genomes. Virology 246:1-23.
85. 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.
86. 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.
87. Xie, Q., and M. S. Chapman. 1996. Canine parvovirus capsid structure, analyzed at 2.9 Å resolution. J. Mol. Biol. 264:497-520.
88. 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.
89. Yang, Q., M. Mamounas, G. Yu, S. Kennedy, B. Leaker, J. Merson, F. Wong-Staal, M. Yu, and J. R. Barber. 1998. Development of novel cell surface CD34-targeted recombinant adenoassociated virus vectors for gene therapy. Hum. Gene Ther. 9:1929-1937.
90. Young, S. M., Jr., W. Xiao, and R. J. Samulski. 2000. Site-specific targeting of DNA plasmids to chromosome 19 using AAV cis and trans sequences. Methods Mol. Biol. 133:111-126.
91. Zadori, Z., J. Szelei, M.-C. Lacoste, 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.