1887

Abstract

The envelope of bovine viral diarrhea virus (BVDV) contains the glycoproteins E, E1 and E2. Complementation of a recombinant vesicular stomatitis virus (VSV) with BVDV glycoproteins resulted in infectious pseudotyped viruses. To elucidate the specific role of each of the single envelope glycoproteins during viral entry, pseudotypes were generated bearing the BVDV envelope proteins in different combinations. Pseudoviruses that contained E1 and E2 but not E were infectious, indicating that E is dispensable for virus entry. VSV/BVDV pseudotypes with chimeric proteins (the ectodomain of the BVDV glycoprotein and the transmembrane domain of the VSV-G protein) were not infectious. The fact that E1–E2 heterodimers were not detected if one of the proteins was chimeric indicated that the heterodimers are crucial for BVDV entry. It was shown by site-directed mutagenesis that the charged amino acids in the transmembrane domains of BVDV E1 (lysine and arginine) and the charged amino acid in the transmembrane domain of E2 (arginine) play a key role in heterodimer formation. Pseudoviruses bearing the mutation E2-R/A, where the charged amino acid was substituted by alanine, were not infectious, supporting the hypothesis that E1–E2 heterodimers are essential for BVDV entry.

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2008-09-01
2024-04-19
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References

  1. Bartosch B., Dubuisson J., Cosset F. L. 2003; Infectious hepatitis C virus pseudo-particles containing functional E1–E2 envelope protein complexes. J Exp Med 197:633–642 [CrossRef]
    [Google Scholar]
  2. Bolin S., Moennig V., Kelso Gourley N. E., Ridpath J. 1988; Monoclonal antibodies with neutralizing activity segregate isolates of bovine viral diarrhea virus into groups. Arch Virol 99:117–123 [CrossRef]
    [Google Scholar]
  3. Cathomen T., Buchholz C. J., Spielhofer P., Cattaneo R. 1995; Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 214:628–632 [CrossRef]
    [Google Scholar]
  4. Ciczora Y., Callens N., Montpellier C., Bartosch B., Cosset F. L., Op D. B., Dubuisson J. 2005; Contribution of the charged residues of hepatitis C virus glycoprotein E2 transmembrane domain to the functions of the E1E2 heterodimer. J Gen Virol 86:2793–2798 [CrossRef]
    [Google Scholar]
  5. Ciczora Y., Callens N., Penin F., Pecheur E. I., Dubuisson J. 2006; The transmembrane domains of HCV envelope glycoproteins: residues involved in E1E2 heterodimerization and involvement of these domains in virus entry. J Virol 81:2372–2381
    [Google Scholar]
  6. Cocquerel L., Wychowski C., Minner F., Penin F., Dubuisson J. 2000; Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J Virol 74:3623–3633 [CrossRef]
    [Google Scholar]
  7. Cocquerel L., Op D. B., Lambot M., Roussel J., Delgrange D., Pillez A., Wychowski C., Penin F., Dubuisson J. 2002; Topological changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J 21:2893–2902 [CrossRef]
    [Google Scholar]
  8. Crofts A. J., Leborgne-Castel N., Hillmer S., Robinson D. G., Phillipson B., Carlsson L. E., Ashford D. A., Denecke J. 1999; Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell 11:2233–2248 [CrossRef]
    [Google Scholar]
  9. Donis R. O., Dubovi E. J. 1987; Characterization of bovine viral diarrhoea-mucosal disease virus-specific proteins in bovine cells. J Gen Virol 68:1597–1605 [CrossRef]
    [Google Scholar]
  10. Dubuisson J. 2000; Folding, assembly and subcellular localization of hepatitis C virus glycoproteins. Curr Top Microbiol Immunol 242:135–148
    [Google Scholar]
  11. Fetzer C., Tews B. A., Meyers G. 2005; The carboxy-terminal sequence of the pestivirus glycoprotein Erns represents an unusual type of membrane anchor. J Virol 79:11901–11913 [CrossRef]
    [Google Scholar]
  12. Greiser-Wilke I., Dittmar K. E., Liess B., Moennig V. 1991; Immunofluorescence studies of biotype-specific expression of bovine viral diarrhoea virus epitopes in infected cells. J Gen Virol 72:2015–2019 [CrossRef]
    [Google Scholar]
  13. Grummer B., Beer M., Liebler-Tenorio E., Greiser-Wilke I. 2001; Localization of viral proteins in cells infected with bovine viral diarrhoea virus. J Gen Virol 82:2597–2605
    [Google Scholar]
  14. Hanika A., Larisch B., Steinmann E., Schwegmann-Weßels C., Herrler G., Zimmer G. 2005; Use of influenza C virus glycoprotein HEF for generation of vesicular stomatitis virus pseudotypes. J Gen Virol 86:1455–1465 [CrossRef]
    [Google Scholar]
  15. Hsu M., Zhang J., Flint M., Logvinoff C., Cheng-Mayer C., Rice C. M., McKeating J. A. 2003; Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci U S A 100:7271–7276 [CrossRef]
    [Google Scholar]
  16. Hulst M. M., Moormann R. J. 1997; Inhibition of pestivirus infection in cell culture by envelope proteins Erns and E2 of classical swine fever virus: Erns and E2 interact with different receptors. J Gen Virol 78:2779–2787
    [Google Scholar]
  17. Hulst M. M., Van Gennip H. G., Vlot A. C., Schooten E., De Smit A. J., Moormann R. J. 2001; Interaction of classical swine fever virus with membrane-associated heparan sulfate: role for virus replication in vivo and virulence. J Virol 75:9585–9595 [CrossRef]
    [Google Scholar]
  18. Iqbal M., Flick-Smith H., McCauley J. W. 2000; Interactions of bovine viral diarrhoea virus glycoprotein Erns with cell surface glycosaminoglycans. J Gen Virol 81:451–459
    [Google Scholar]
  19. Köhl W., Zimmer G., Greiser-Wilke I., Haas L., Moennig V., Herrler G. 2004; The surface glycoprotein E2 of bovine viral diarrhoea virus contains an intracellular localization signal. J Gen Virol 85:1101–1111 [CrossRef]
    [Google Scholar]
  20. Lagging L. M., Meyer K., Owens R. J., Ray R. 1998; Functional role of hepatitis C virus chimeric glycoproteins in the infectivity of pseudotyped virus. J Virol 72:3539–3546
    [Google Scholar]
  21. Lefrancois L., Lyles D. S. 1982; The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 121:168–174 [CrossRef]
    [Google Scholar]
  22. Mendez E., Ruggli N., Collett M. S., Rice C. M. 1998; Infectious bovine viral diarrhea virus (strain NADL) RNA from stable cDNA clones: a cellular insertion determines NS3 production and viral cytopathogenicity. J Virol 72:4737–4745
    [Google Scholar]
  23. Ren X., Glende J., Al Falah M., Schwegmann-Wessels C., Qu X., Tan L., Tschernig T., Deng H., Naim H. Y., Herrler G. 2006; Analysis of ACE2 in polarized epithelial cells: surface expression and function as receptor for severe acute respiratory syndrome-associated coronavirus. J Gen Virol 87:1691–1695 [CrossRef]
    [Google Scholar]
  24. Rümenapf T., Unger G., Strauss J. H., Thiel H. J. 1993; Processing of the envelope glycoproteins of pestiviruses. J Virol 67:3288–3294
    [Google Scholar]
  25. Thiel H. J., Stark R., Weiland E., Rumenapf T., Meyers G. 1991; Hog cholera virus: molecular composition of virions from a pestivirus. J Virol 65:4705–4712
    [Google Scholar]
  26. van Rijn P. A., Miedema G. K., Wensvoort G., van Gennip H. G., Moormann R. J. 1994; Antigenic structure of envelope glycoprotein E1 of hog cholera virus. J Virol 68:3934–3942
    [Google Scholar]
  27. Wang Z., Nie Y., Wang P., Ding M., Deng H. 2004; Characterization of classical swine fever virus entry by using pseudotyped viruses: E1 and E2 are sufficient to mediate viral entry. Virology 330:332–341 [CrossRef]
    [Google Scholar]
  28. Weiland E., Stark R., Haas B., Rumenapf T., Meyers G., Thiel H. J. 1990; Pestivirus glycoprotein which induces neutralizing antibodies forms part of a disulfide-linked heterodimer. J Virol 64:3563–3569
    [Google Scholar]
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