Interaction of parvovirus B19 with human erythrocytes alters virus structure and cell membrane integrity

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11784-11791

  Bönsch, Claudia ^a   Kempf, Christoph ^a,b   Ros, Carlos ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b CSL Behring AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOLIPASE A2; PROTEIN VP1;

ANTIGEN BINDING; ARTICLE; CELL INTERACTION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ERYTHEMA INFECTIOSUM; ERYTHROCYTE; HEMOLYSIS; NONHUMAN; OSMOTIC FRAGILITY; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; VIRUS CAPSID; VIRUS MORPHOLOGY;

AMINO ACID MOTIFS; BLOOD DONORS; CAPSID; CELLS, CULTURED; ERYTHROCYTES; HEMOLYSIS; HOT TEMPERATURE; HUMANS; OSMOTIC FRAGILITY; PARVOVIRUS B19, HUMAN; PHOSPHOLIPASES A2;

MIRIDAE; PARVOVIRUS;

EID: 56449098532     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01399-08     Document Type: Article

References (45)

1. Anderson, M. J., S. E. Jones, S. P. Fisher-Hoch, E. Lewis, S. M. Hall, C. L. R. Bartlett, B. J. Cohen, P. P. Mortimer, and M. S. Pereira. 1983. Human parvovirus, the cause of erythema infectiosum (fifth disease)? Lett. Lancet 1:1378.
2. Anderson, S., M. Momoeda, M. Kawase, S. Kajigaya, and N. S. Young. 1995. Peptides derived from the unique region of B19 parvovirus minor capsid protein elicit neutralizing antibodies in rabbits. Virology 206:626-632.
3. 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.
4. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
5. Brown, T., A. Anand, L. D. Ritchie, J. P. Clewley, and T. M. Reid. 1984. Intrauterine parvovirus infection associated with hydrops fetalis. Lancet 2:1033-1034.
6. 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.
7. Cossart, Y. E., A. M. Field, B. Cant, and D. Widdows. 1975. Parvovirus-like particles in human sera. Lancet 1:72-73.
8. Cotmore, S. F., A. M. Jr. D'abramo, 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. Cotmore, S. F., V. C. McKie, L. J. Anderson, C. R. Astell, and P. Tattersall. 1986. Identification of the major structural and nonstructural proteins encoded by human parvovirus B19 and mapping of their genes by procaryotic expression of isolated genomic fragments. J. Virol. 60:548-557.
10. Crane, J., and Society of Obstetricians and Gynaecologists of Canada. 2002. Parvovirus B19 infection in pregnancy. J. Obstet. Gynaecol. Can. 24:727-743.
11. De Sena, J., and B. Mandel. 1977. Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle. Virology. 78:554-566.
12. Dorsch, S., B. Kaufmann, U. Schaible, E. Prohaska, H. Wolf, and S. Modrow. 2001. The VP1-unique region of parvovirus B19: amino acid variability and antigenic stability. J. Gen. Virol. 82:191-199.
13. 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.
14. 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.
15. Fenwick, M. L., and P. D. Cooper. 1962. Early interactions between poliovirus and ERK cells. Some observations on the nature and significance of the rejected particles. Virology 18:212-223.
16. Fletcher, K. S., E. G. Bremer, and G. A. Schwarting. 1979. P blood group regulation of glycosphingolipid levels in human erythrocytes. J. Biol. Chem. 254:11196-11198.
17. Gigler, A., S. Dorsch, A. Hemauer, C. Williams, S. Kim, N. S. Young, S. Zolla-Pazner, H. Wolf, M. K. Gorny, and S. Modrow. 1999. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 73:1974-1979.
18. 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.
19. Kaufmann, B., U. Baxa, P. R. Chipman, M. G. Rossmann, S. Modrow, and R. Seckler. 2005. Parvovirus B19 does not bind to membrane-associated globoside in vitro. Virology 332:189-198.
20. 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.
21. Kurtzman, G. J., B. J. Cohen, A. M. Field, R. Oseas, R. M. Blaese, and N. S. Young. 1989. Immune response to B19 parvovirus and an antibody defect in persistent viral infection. J. Clin. Investig. 84:1114-1123.
22. Lehmann, H. W., P. von Landenberg, and S. Modrow. 2003. Parvovirus B19 infection and autoimmune disease. Autoimmun. Rev. 2:218-223.
23. 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.
24. Mani, B., C. Baltzer, N. Valle, J. M. Almendral, C. Kempf, and C. Ros. 2006. 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. J. Virol. 80:1015-1024.
25. Munakata, Y., T. Saito-Ito, K. Kumura-Ishii, J. Huang, T. Kodera, T. Ishii, Y. Hirabayashi, Y. Koyanagi, and T. Sasaki. 2005. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 106:3449-3456.
26. Ozawa, K., and N. Young. 1987. Characterization of capsid and noncapsid proteins of B19 parvovirus propagated in human erythroid bone marrow cell cultures. J. Virol. 61:2627-2630.
27. Racaniello, V. R. 1996. Early events in poliovirus infection: virus-receptor interactions. Proc. Natl. Acad. Sci. USA 93:11378-11381.
28. Reid, D. M., T. M. Reid, T. Brown, J. A. Rennie, and C. J. Eastmond. 1985. Human parvovirus-associated arthritis: a clinical and laboratory description. Lancet 1:422-425.
29. 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.
30. Ros, C., M. Gerber, and C. Kempf. 2006. Conformational changes in the VP1-unique region of native human parvovirus B19V lead to exposure of internal sequences playing a role in virus neutralization and infectivity. J. Virol. 80:12017-12024.
31. Saikawa, T., S. Anderson, M. Momoeda, S. Kajigaya, and N. S. Young. 1993. Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J. Virol. 67:3004-3009.
32. Serjeant, G. R., J. M. Topley, K. Mason, B. E. Serjeant, J. R. Pattison, S. E. Jones, and R. Mohamed. 1981. Outbreak of aplastic crises in sickle cell anaemia associated with parvovirus-like agent. Lancet 2:595-597.
33. Sonntag, F., S. Bleker, B. Leuchs, R. Fischer, and J. A. Kleinschmidt. 2006. AAV2 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.
34. Suikkanen, S., M. Antila, A. Jaatinen, M. Vihinen-Ranta, and M. Vuento. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
35. Tsang, S. K., B. M. McDermott, V. R. Racaniello, and J. M. Hogle. 2001. Kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J. Virol. 75:4984-4989.
36. Tzang, B. S., G. J. Tsay, Y. J. Lee, C. Li, Y. S. Sun, and T. C. Hsu. 2007. The association of VP1 unique region protein in acute parvovirus B19 infection and anti-phospholipid antibody production. Clin. Chim. Acta 378:59-65.
37. Tzang, B. S., Y. J. Lee, T. P. Yang, G. J. Tsay, J. Y. Shi, C. C. Tsai, and T. C. Hsu. 2007. Induction of antiphospholipid antibodies and antiphospholipid syndrome-like autoimmunity in naive mice with antibody against human parvovirus B19 VP1 unique region protein. Clin. Chim. Acta 382:31-36.
38. Vaysse, J., P. Pilardeau, L. Gattegno, and M. Garnier. 1987. Osmotic properties of human erythrocytes treated by phospholipase A2 from bee venom. Br. J. Haematol. 65:361-365.
39. 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.
40. von dem Borne, A. E., M. J. Bos, N. Joustra-Maas, J. F. Tromp, M. B. van't Veer, R. van Wijngaarden-du Bois, and P. A. Tetteroo. 1986. A murine monoclonal IgM antibody specific for blood group P antigen (globoside). Br. J. Haematol. 63:35-46.
41. Von Landenberg, P., H. W. Lehmann, A. Knoll, S. Dorsch, and S. Modrow. 2003. Antiphospholipid antibodies in pediatric and adult patients with rheumatic disease are associated with parvovirus B19 infection. Arthritis Rheum. 48:1939-1947.
42. 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. 75:4110-4116.
43. Weigel-Kelley, K. A., M. C. Yoder, and A. Srivastava. 2003. α5β1 Integrin as a cellular coreceptor for human parvovirus B19: requirement of functional activation of beta1 integrin for viral entry. Blood 102:3927-3933.
44. 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.
45. Zuffi, E., E. Manaresi, G. Gallinella, G. A. Gentilomi, S. Venturoli, M. Zerbini, and M. Musiani. 2001. Identification of an immunodominant peptide in the parvovirus B19 VP1 unique region able to elicit a long-lasting immune response in humans. Viral Immunol. 14:151-158.