1887

Abstract

Vaccinia virus (VV) produces two antigenically and structurally distinct infectious virions, intracellular mature virus (IMV) and extracellular enveloped virus (EEV). EEV is important for the efficient dissemination of virus both and where it causes formation of comet-shaped virus plaques. Here, we show that EEV, in contrast to IMV, is resistant to neutralization by antibodies bound to its surface. However, antibodies against EEV can prevent comet formation in cell culture. To explain this apparent paradox, we investigated the mechanism by which antibodies inhibit comet formation and demonstrated that antibodies prevent EEV release from infected cells, and consequently comet formation, by agglutination of the virus on the cell surface. Two complementary observations allowthis conclusion: first, electron microscopy showed that infected cells incubated with medium containing anti-vaccinia virus antibodies have virus aggregates on their surface; second, culture medium from these cells contained a 4 log fold reduction in the physical particle/ml titre in comparison with control culture. A mechanism by which antibodies to EEV proteins provide immunological protection is thus restriction of EEV release rather than neutralization of free EEV particles.

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1997-08-01
2024-04-25
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References

  1. Alcami A., Smith G. L. 1996; A mechanism for the inhibition offever by a virus. Proceedings of the National Academy of Sciences, USA 93:11029–11034
    [Google Scholar]
  2. Appleyard G., Andrews C. 1974; Neutralizing activities of antisera to poxvirus soluble antigens. Journal of General Virology 23:197–200
    [Google Scholar]
  3. Appleyard G., Hapel A. J., Boulter E. A. 1971; An antigenic difference between intracellular and extracellular rabbitpox virus. Journal of General Virology 13:9–17
    [Google Scholar]
  4. Blasco R., Moss B. 1992; Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. Journal of Virology 66:4170–4179
    [Google Scholar]
  5. Boulter E. A. 1969; Protection against poxviruses. Proceedings of the Royal Society of Medicine 62:295–297
    [Google Scholar]
  6. Boulter E. A., Appleyard G. 1973; Differences between extracellular and intracellular forms of poxviruses and their implications. Progress in Medical Virology 16:86–108
    [Google Scholar]
  7. Cudmore S., Cossart P., Griffiths G., Way M. 1995; Actin-based motility of vaccinia virus. Nature 378:636–638
    [Google Scholar]
  8. Czerny C. P., Mahnel H. 1990; Structural and functional analysis of orthopoxvirus epitopes with neutralizing monoclonal antibodies. Journal of General Virology 71:2341–2352
    [Google Scholar]
  9. Doms R. W., Blumenthal R., Moss B. 1990; Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane. Journal of Virology 64:4884–4892
    [Google Scholar]
  10. Duncan S. A., Smith G. L. 1992; Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. Journal of Virology 66:1610–1621
    [Google Scholar]
  11. Engelstad M., Smith G. L. 1993; The vaccinia virus 42 kDa envelope protein is required for envelopment and egress of extracellular virus and for virulence. Virology 194:627–637
    [Google Scholar]
  12. Engelstad M., Howard S. T., Smith G. L. 1992; A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 188:801–810
    [Google Scholar]
  13. Essani K., Dales S. 1979; Biogenesis of vaccinia: evidence for more than 100 polypeptides in the virion. Virology 95:385–394
    [Google Scholar]
  14. Hanson C. V., Riggs J. L., Lennette E. H. 1978; Photochemical inactivation of DNA and RNA viruses by psoralen derivatives. Journal of General Virology 40:345–358
    [Google Scholar]
  15. Hirt P., Hiller G., Wittek R. 1986; Localization and fine structure of a vaccinia virus gene encoding an envelope antigen. Journal of Virology 58:757–764
    [Google Scholar]
  16. Ichihashi Y. 1996; Extracellular enveloped vaccinia virus escapes neutralization. Virology 217:478–485
    [Google Scholar]
  17. Ichihashi Y., Matsumoto S., Dales S. 1971; Biogenesis of poxviruses: role of A-type inclusions and host cell membranes in virus dissemination. Virology 46:507–532
    [Google Scholar]
  18. Isaacs S. N., Moss B. 1994; Inhibition of complement activation by vaccinia virus. In Viroceptors, Virokines and Related Immune Modulators Encoded by DNA Viruses pp. 55–66 McFadden G. Edited by Austin: R. G. Landes;
    [Google Scholar]
  19. Isaacs S. N., Wolffe E. J., Payne L. G., Moss B. 1992; Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. Journal of Virology 66:7217–7224
    [Google Scholar]
  20. McIntosh A. A. G., Smith G. L. 1996; Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. Journal of Virology 70:272–281
    [Google Scholar]
  21. Mackett M., Smith G. L., Moss B. 1985; The construction and characterization of vaccinia virus recombinants expressing foreign genes. In DNA Cloning: A Practical Approach pp. 191–211 Glover D. M. Edited by Oxford: IRL Press;
    [Google Scholar]
  22. Mason P. W., Rieder E., Baxt B. 1994; RGD sequence of foot-and- mouth disease virus is essential for infecting cells via the natural receptor but can be bypassed by an antibody-dependent enhancement pathway. Proceedings of the National Academy of Sciences, USA 91:1932–1936
    [Google Scholar]
  23. Parkinson J. E., Smith G. L. 1994; Vaccinia virus gene A36R encodes a Mr 43–50K protein on the surface of extracellular enveloped virus. Virology 204:376–390
    [Google Scholar]
  24. Payne L. G. 1978; Polypeptide composition ofextracellular enveloped vaccinia virus. Journal of Virology 27:28–37
    [Google Scholar]
  25. Payne L. G. 1979; Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus. Journal of Virology 31:147–155
    [Google Scholar]
  26. Payne L. G. 1980; Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia virus. Journal of General Virology 50:89–100
    [Google Scholar]
  27. Payne L. G. 1992; Characterization of vaccinia virus glycoproteins by monoclonal antibody preparations. Virology 187:251–260
    [Google Scholar]
  28. Payne L. G., Kristensson K. 1985; Extracellular release of enveloped vaccinia virus from mouse nasal epithelial cells in vivo . Journal of General Virology 66:643–646
    [Google Scholar]
  29. Payne L. G., Norrby E. 1976; Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles. Journal of General Virology 32:63–72
    [Google Scholar]
  30. Roos N., Cyrklaff M., Cudmore S., Blasco R., Krijnse-Locker J., Griffiths G. 1996; A novel immunogold cryoelectron microscopic approach to investigate the structure of the intracellular and extracellular forms of vaccinia virus. EMBO Journal 15:2343–2355
    [Google Scholar]
  31. Roper R. L., Payne L. G., Moss B. 1996; Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. Journal of Virology 70:3753–3762
    [Google Scholar]
  32. Sanderson C. M., Parkinson J. E., Hollinshead M., Smith G. L. 1996; Overexpression of the vaccinia virus A38L integral membrane protein promotes Ca2+ influx into infected cells. Journal of Virology 70:905–914
    [Google Scholar]
  33. Schmelz M., Sodeik B., Ericsson M., Wolffe E. J., Shida H. G. H., Griffiths G. 1994; Assembly of vaccinia virus : the second wrapping cisterna is derived from the trans Golgi network. Journal of Virology 68:130–147
    [Google Scholar]
  34. Shida H. 1986; Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150:451–462
    [Google Scholar]
  35. Tooze J., Hollinshead M., Reis B., Radsak K., Kern H. 1993; Progeny vaccinia viruses and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. European Journal of Cell Biology 60:163–178
    [Google Scholar]
  36. Turner G. S., Squires E. J. 1971; Inactivated smallpox vaccine: immunogenicity of inactivated intracellular and extracellular vaccinia virus. Journal of General Virology 13:19–25
    [Google Scholar]
  37. Vanderplasschen A., Smith G. L. 1997; An novel virus binding assay using confocal microscopy: demonstration that the intracellular and extracellular vaccinia virions bind to different cellular receptors. Journal of Virology 71:4032–4041
    [Google Scholar]
  38. Wand S., He R., Patarapotikul J., Innis B. L., Anderson R. 1995; Antibody-enhanced binding of dengue-2 virus to human platelets. Virology 213:254–257
    [Google Scholar]
  39. Wolffe E. J., Isaacs S. N., Moss B. 1993; Deletion of the vaccinia virus B5R gene encoding a 42-kiloDalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. Journal of Virology 67:4732–4741
    [Google Scholar]
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