Parvovirus B19 uptake is a highly selective process controlled by VP1u, a novel determinant of viral tropism

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13161-13167

  Leisi, Remo ^a,b   Ruprecht, Nico ^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

RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VP1U PROTEIN;

ARTICLE; CONTROLLED STUDY; ERYTHROID CELL; HUMAN; HUMAN CELL; HUMAN PARVOVIRUS B19; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; VIRAL TROPISM; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS ENTRY; VP1 UNIQUE REGION;

AMINO ACID MOTIFS; CAPSID PROTEINS; CELL LINE; HUMANS; PARVOVIRIDAE INFECTIONS; PARVOVIRUS B19, HUMAN; VIRAL TROPISM; VIRUS INTERNALIZATION;

EID: 84888033635     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02548-13     Document Type: Article

References (37)

1. Cossart YE, Field AM, Cant B, Widdows D. 1975. Parvovirus-like particles in human sera. Lancet i:72-73.
2. Heegaard ED, Brown KE. 2002. Human parvovirus B19. Clin. Microbiol. Rev. 15:485-505.
3. Servey JT, Reamy BV, Hodge J. 2007. Clinical presentations of parvovirus B19 infection. Am. Fam. Physician 75:373-376.
4. Ozawa K, Kurtzman G, Young N. 1986. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233:883-886.
5. Brown KE, Anderson SM, Young NS. 1993. Erythrocyte P antigen:cellular receptor for B19 parvovirus. Science 262:114-117.
6. Pallier C, Greco A, Le Junter J, Saib A, Vassias I, Morinet F. 1997. The 3' untranslated region of the B19 parvovirus capsid protein mRNAs inhibits its own mRNA translation in nonpermissive cells. J. Virol. 71:9482-9489.
7. Brunstein J, Soderlund-Venermo M, Hedman K. 2000. Identification of a novel RNA splicing pattern as a basis of restricted cell tropism of erythrovirus B19. Virology 274:284-291.
8. Gallinella G, Manaresi E, Zuffi E, Venturoli S, Bonsi L, Bagnara GP, Musiani M, Zerbini M. 2000. Different patterns of restriction to B19 parvovirus replication in human blast cell lines. Virology 278:361-367.
9. Guan W, Cheng F, Yoto Y, Kleiboeker S, Wong S, Zhi N, Pintel DJ, Qiu J. 2008. Block to the production of full-length B19 virus transcripts by internal polyadenylation is overcome by replication of the viral genome. J. Virol. 82:9951-9963.
10. Chen AY, Guan W, Lou S, Liu Z, Kleiboeker S, Qiu J. 2010. Role of erythropoietin receptor signaling in parvovirus B19 replication in human erythroid progenitor cells. J. Virol. 84:12385-12396.
11. Weigel-Kelley KA, Yoder MC, Srivastava A. 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.
12. Weigel-Kelley KA, Yoder MC, Srivastava A. 2003. Alpha5beta1 integrin as a cellular coreceptor for human parvovirus B19:requirement of functional activation of β1 integrin for viral entry. Blood 102:3927-3933.
13. Munakata Y, Saito-Ito T, Kumura-Ishii K, Huang J, Kodera T, Ishii T, Hirabayashi Y, Koyanagi Y, Sasaki T. 2005. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 106:3449-3456.
14. Kaufmann B, Baxa U, Chipman PR, Rossmann MG, Modrow S, Seckler R. 2005. Parvovirus B19 does not bind to membrane-associated globoside in vitro. Virology 332:189-198.
15. Cotmore SF, McKie VC, Anderson LJ, Astell CR, Tattersall P. 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.
16. Ozawa K, Young N. 1987. Characterization of capsid and noncapsid proteins of B19 parvovirus propagated in human erythroid bone marrow cell cultures. J. Virol. 61:2627-2630.
17. Saikawa T, Anderson S, Momoeda M, Kajigaya S, Young NS. 1993. Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J. Virol. 67:3004-3009.
18. Anderson S, Momoeda M, Kawase M, Kajigaya S, Young NS. 1995. Peptides derived from the unique region of B19 parvovirus minor capsid protein elicit neutralizing antibodies in rabbits. Virology 206:626-632.
19. Kurtzman GJ, Cohen BJ, Field AM, Oseas R, Blaese RM, Young NS. 1989. Immune response to B19 parvovirus and an antibody defect in persistent viral infection. J. Clin. Invest. 84:1114-1123.
20. Suikkanen S, Antila M, Jaatinen A, Vihinen-Ranta M, Vuento M. 2003. Release of canine parvovirus from endocytic vesicles. Virology 316:267-280.
21. Mani B, Baltzer C, Valle N, Almendral JM, Kempf C, Ros C. 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.
22. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. 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.
23. Zadori Z, Szelei J, Lacoste MC, Li Y, Gariepy S, Raymond P, Allaire M, Nabi IR, Tijssen P. 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1:291-302.
24. Dorsch S, Liebisch G, Kaufmann B, von Landenberg P, Hoffmann JH, Drobnik W, Modrow S. 2002. The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. J. Virol. 76:2014-2018.
25. Girod A, Wobus CE, Zadori Z, Ried M, Leike K, Tijssen P, Kleinschmidt JA, Hallek M. 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.
26. Farr GA, Zhang LG, Tattersall P. 2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. U.S.A. 102:17148-17153.
27. Qu XW, Liu WP, Qi ZY, Duan ZJ, Zheng LS, Kuang ZZ, Zhang WJ, Hou YD. 2008. Phospholipase A2-like activity of human bocavirus VP1 unique region. Biochem. Biophys. Res. Commun. 365:158-163.
28. Vihinen-Ranta M, Wang D, Weichert WS, Parrish CR. 2002. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 76:1884-1891.
29. Grieger JC, Snowdy S, Samulski RJ. 2006. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 80:5199-5210.
30. Bonsch C, Kempf C, Ros C. 2008. Interaction of parvovirus B19 with human erythrocytes alters virus structure and cell membrane integrity. J. Virol. 82:11784-11791.
31. Bonsch C, Zuercher C, Lieby P, Kempf C, Ros C. 2010. The globoside receptor triggers structural changes in the B19 virus capsid that facilitate virus internalization. J. Virol. 84:11737-11746.
32. Gigler A, Dorsch S, Hemauer A, Williams C, Kim S, Young NS, Zolla-Pazner S, Wolf H, Gorny MK, Modrow S. 1999. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 73:1974-1979.
33. Kankaanpaa P, Paavolainen L, Tiitta S, Karjalainen M, Paivarinne J, Nieminen J, Marjomaki V, Heino J, White DJ. 2012. BioImageXD:an open, general-purpose and high-throughput image-processing platform. Nature methods. 9:683-689.
34. Dorsch S, Kaufmann B, Schaible U, Prohaska E, Wolf H, Modrow S. 2001. The VP1-unique region of parvovirus B19:amino acid variability and antigenic stability. J. Gen. Virol. 82:191-199.
35. Ros C, Gerber M, Kempf C. 2006. Conformational changes in the VP1-unique region of native human parvovirus B19 lead to exposure of internal sequences that play a role in virus neutralization and infectivity. J. Virol. 80:12017-12024.
36. Bonvicini F, Filippone C, Manaresi E, Zerbini M, Musiani M, Gallinella G. 2008. HepG2 hepatocellular carcinoma cells are a non-permissive system for B19 virus infection. J. Gen. Virol. 89:3034-3038.
37. Takahashi T, Ozawa K, Takahashi K, Asano S, Takaku F. 1990. Susceptibility of human erythropoietic cells to B19 parvovirus in vitro increases with differentiation. Blood 75:603-610.