Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome

Journal of Virology

Volumn 80, Issue 2, 2006, Pages 1015-1024

  Mani, Bernhard ^a   Baltzer, Claudia ^a   Valle, Noelia ^c   Almendral, José M ^c   Kempf, Christoph ^a,b   Ros, Carlos ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b ZLB Behring   (Switzerland)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; PROTEIN VP1; PROTEIN VP2; SINGLE STRANDED DNA; STRUCTURAL PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; LYSOSOME; LYSOSOME MEMBRANE; MOUSE; NONHUMAN; PARVOVIRUS; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; TRANSPORT KINETICS; VIRION; VIRUS CAPSID; VIRUS GENOME; VIRUS PARTICLE;

ANIMALS; CAPSID PROTEINS; CELL LINE; DNA, VIRAL; ENDOSOMES; HYDROGEN-ION CONCENTRATION; MICE; MINUTE VIRUS OF MICE; PARVOVIRIDAE INFECTIONS; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

ANIMALIA; MINUTE VIRUS OF MICE; MIRIDAE; PARVOVIRUS;

EID: 30344459715     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.2.1015-1024.2006     Document Type: Article

References (56)

1. 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.
2. 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.
3. Basak, S., and H. Turner. 1992. Infectious entry pathway for canine parvovirus. Virology 186:368-376.
4. 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.
5. Canaan, S., Z. Zadori, F. Ghomashchi, J. Bollinger, M. Sadilek, M. E. Moreau, P. Tijssen, and M. H. Gelb. 2004. Interfacial enzymology of parvovirus phospholipases A2. J. Biol. Chem. 279:14502-14508.
6. Clinton, G. M., and M. Hayashi. 1976. The parvovirus MVM: a comparison of heavy and light particle infectiviry and their density conversion in vitro. Virology 74:57-63.
7. 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.
8. Cotmore, S. F., and P. Tattersall. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
9. de Duve, C. 1983. Lysosomes revisited. Eur. J. Biochem. 137:391-397.
10. Ding, W., L. Zhang, Z. Yan, and J. F. Engelhardt. 2005. Intracellular trafficking of adeno-associated viral vectors. Gene Ther. 12:873-880.
11. 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.
12. 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.
13. Dunn, W. A., Jr. 1994. Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol. 4:139-143.
14. Evans, C. J., and R. J. Aguilera. 2003. DNase II: genes, enzymes and function. Gene 322:1-15.
15. 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 infectiviry. J. Gen. Virol. 83:973-978.
16. 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.
17. Hauck, B., W. Zhao, K. High, and W. Xiao. 2004. Intracellular viral processing, not single-stranded DNA accumulation, is crucial for recombinant adeno-associated virus transduction. J. Virol. 78:13678-13686.
18. Hernando, E., A. L. Llamas-Saiz, C. Foces-Foces, R. McKenna, I. Portman, M. Agbandje-McKenna, and J. M. Almendral. 2000. Biochemical and physical characterization of parvovirus minute virus of mice virus-like particles. Virology 267:299-309.
19. Hogle, J. M. 2002. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56:677-702.
20. Reference deleted.
21. 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.
22. Lombardo, E., J. C. Ramírez, J. García, 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.
23. Lombardo, E., J. C. Ramírez, M. Agbandje-Mckenna, and J. M. Almendral. 2000. A β-stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nuclei for viral assembly. J. Virol. 74:3804-3814.
24. Lopez-Bueno, A., M. G. Mateu, and J. M. Almendral. 2003. High mutant frequency in populations of a DNA virus allows evasion from antibody therapy in an immunodeficient host. J. Virol. 77:2701-2708.
25. Lux, K., N. Goerlitz, S. Schlemminger, L. Perabo, D. Goldnau, J. Endell, K. Leike, D. M. Kofler, 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.
26. Lyon, C. J., and R. J. Aguilera. 1997. Purification and characterization of the immunoglobulin switch sequence-specific endonuclease (Endo-SR) from bovine spleen. Mol. Immunol. 34:209-219.
27. Maroto, B., J. C. Ram irez, and J. M. Almendral. 2000. Phosphorylation status of the parvovirus minute virus of mice particle: mapping and biological relevance of the major phosphorylation sites. J. Virol. 74:10892-10902.
28. Maroto, B., N. Valle, R. Saffrich, and J. M. Almendral. 2004. Nuclear export of the nonenveloped parvovirus virion is directed by an unordered protein signal exposed on the capsid surface. J. Virol. 78:10685-10694.
29. Mortimore, G. E. 1987. Mechanism and regulation of induced and basal protein degradation in liver, p. 415-444. In H. Glaumann and F. J. Ballard (ed.), Lysosomes: their role in protein breakdown. Academic Press, New York, N.Y.
30. Mothes, W., A. L. Boerger, S. Narayan, J. M. Cunningham, and J. A. T. Young. 2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679-689.
31. . Nurani, G., B. Lindqvist, and J. M. Casasnovas. 2003. Receptor priming of major group human rhinoviruses for uncoating and entry at mild low-pH environments. J. Virol. 77:11985-11991.
32. Pajusola, K., M. Gruchala, H. Joch, T. F. Luscher, S. Yla-Herttuala, and H. Bueler. 2002. Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J. Virol. 76:11530-11540.
33. 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.
34. Poranen, M. M., R. Daugelavicius, and D. H. Bamford. 2002. Common principles in viral entry. Annu. Rev. Microbiol. 56:521-538.
35. Ros, C., and C. Kempf. 2004. The ubiquitin-proteasome machinery is essential for nuclear translocation of incoming minute virus of mice. Virology 324:350-360.
36. 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.
37. Ros, C., C. Baltzer, B. Mani, and C. Kempf. Parvovirus uncoating in vitro reveals a mechanism of DNA release without capsid disassembly and striking differences in encapsidated DNA stability. Virology, in press.
38. 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.
39. Rossmann, M. G., Y. He, and R. J. Kuhn. 2002. Picornavirus-receptor interactions. Trends Microbiol. 10:324-331.
40. Rubio, M. P., A. Lopez-Bueno, and J. M. Almendral. 2005. Virulent variants emerging in mice infected with the apathogenic prototype strain of the parvovirus minute virus of mice exhibit a capsid with low avidity for a primary receptor. J. Virol. 79:11280-11290.
41. 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.
42. 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.
43. Slor, H., H. Bustan, and T. Lev. 1973. Deoxyribonuclease II activity in relation to cell cycle in synchronized HeLa S3 cells. Biochem. Biophys. Res. Commun. 52:556-561.
44. Smith, A. E., and A. Helenius. 2004. How viruses enter animal cells. Science 304:237-242.
45. 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.
46. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
47. Tattersall, P., A. J. Shatkin, and D. C. Ward. 1977. Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111:375-394.
48. 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.
49. Vihinen-Ranta, M., A. Kalela, P. Mäkinen, L. Kakkola, V. Marjomäki, and M. Vuento. 1998. Intracellular route of canine parvovirus entry. J. Virol. 72:802-806.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. Yamamoto, M. 1971. Purification and some properties of an acid deoxyribonuclease from testes of chinook salmon Oncorhynchus tshawytscha. Biochim. Biophys. Acta 228:95-104.
56. 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.