1887

Abstract

During vaccinia virus (VV) morphogenesis intracellular mature virus (IMV) is wrapped by two additional membranes to form intracellular enveloped virus (IEV). IEV particles can nucleate the formation of actin tails which aid movement of IEVs to the cell surface where the outer IEV membrane fuses with the plasma membrane forming cell- associated enveloped virus (CEV) which remains attached to the cell, or extracellular enveloped virus (EEV) which is shed from the cell. In this report, we have used a collection of VV mutants lacking individual EEV-specific proteins to compare the roles of these proteins in the formation of IEV and IEV-associated actin tails and fusion of infected cells after a low pH shock. Data presented here show that p45–50 (A36R) is not required for IEV formation or for acid-induced cell-cell fusion, but is required for formation of IEV-associated actin tails. In contrast, gp86 (Δ 56R), the virus haemagglutinin, is not required for formation of either IEV or IEV- associated actin tails. Data presented also confirm that p37 (gene F13L), gp42 (B5R) and gp22–24 (A34R) are needed for formation of IEV-associated actin tails and for cell-cell fusion after low pH shock. The phenotypes of these mutants were not affected by the host cell type as similar results were obtained in a range of different cells. Lastly, comparisons of the phenotypes of VV strains Western Reserve, ΔA34R and ΔA36R demonstrate that actin tails are not required for low pH-induced cell-cell fusion.

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1998-06-01
2022-01-16
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References

  1. Alcamí A., Smith G. L. 1992; A soluble receptor for interleukin-1^ encoded by vaccinia virus : a novel mechanism of virus modulation of the host response to infection. Cell 71:153–167
    [Google Scholar]
  2. Blasco R., Moss B. 1991; Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein. Journal of Virology 65:5910–5920
    [Google Scholar]
  3. 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]
  4. Cossart P. 1995; Actin based bacterial motility. Current Opinion in Cell Biology 7:94–101
    [Google Scholar]
  5. Cossart P., Kocks C. 1994; The actin-based motility of the facultative intracellular pathogen Listeria monocytogenes . Molecular Microbiology 13:395–402
    [Google Scholar]
  6. Cudmore S., Cossart P., Griffiths G., Way M. 1995; Actin-based motility of vaccinia virus. Nature 378:636–638
    [Google Scholar]
  7. Cudmore S., Reckmann I., Griffiths G., Way M. 1996; Vaccinia virus: a model system for actin-membrane interactions. Journal of Cell Science 109:1739–1747
    [Google Scholar]
  8. Dales S., Pogo B. G. T. 1981; Biology of poxviruses. In Virology Monographs pp. 1–101 Kingsbury D. W., zur Hausen H. Edited by Berlin: Springer-Verlag;
    [Google Scholar]
  9. Duncan S. A. 1992 Analysis of three vaccinia virus genes, one of which is essential for plaque formation D. Phil University of Oxford, Oxford, UK:
    [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 virus gene encodes a 42 kDa glycoprotein related to complement control factors that forms part of the extracellular envelope. Virology 188:801–810
    [Google Scholar]
  13. Fenner F., Anderson D. A., Arita I., Jezek Z., Ladnyi I. D. 1988 Smallpox and its Eradication Geneva: World Health Organization;
    [Google Scholar]
  14. Gong S. C., Lai C. F., Dallo S., Esteban M. 1989; A single point mutation of Ala-25 to Asp in the 14,000-Mr envelope protein of vaccinia virus induces a size change that leads to the small plaque size phenotype of the virus. Journal of Virology 63:4507–4514
    [Google Scholar]
  15. Gong S. C., Lai C. F., Esteban M. 1990; Vaccinia virus induces cell fusion at acid pH and this activity is mediated by the N-terminus of the 14-kDa virus envelope protein. Virology 178:81–91
    [Google Scholar]
  16. Herzog M., Draeger A., Ehler E., Small V. J. 1994; Immunofluorescence microscopy of the cytoskeleton: double and triple immunofluorescence. In Cell Biology: A Laboratory Manual pp. 355–360 San Diego: Academic Press;
    [Google Scholar]
  17. Hiller G., Weber K. 1985; Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. Journal of Virology 55:651–659
    [Google Scholar]
  18. 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]
  19. Ichihashi Y. 1996; Extracellular enveloped vaccinia virus escapes neutralization. Virology 217:478–485
    [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. Mathew E., Sanderson C. M., Hollinshead M., Smith G. L. 1998; The extracellular domain of vaccinia virus protein B5R affects plaque formation, EEV release and intracellular actin tail formation. Journal of Virology 72:2429–2438
    [Google Scholar]
  25. Morgan C. 1976; Vaccinia virus reexamined: development and release. Virology 73:43–58
    [Google Scholar]
  26. Moss B. 1996; Poxviridae : the viruses and their replication. In Fields Virology pp. 2637–2671 Fields B. N., Knipe D. M., Howley P. M. Edited by Philadelphia: Lippincott-Raven;
    [Google Scholar]
  27. Parkinson J. E., Smith G. L. 1994; Vaccinia virus gene A36R encodes a Mr 43-50 K protein on the surface of extracellular enveloped virus. Virology 204:376–390
    [Google Scholar]
  28. Payne L. G., Kristensson K. 1979; Mechanism of vaccinia virus release and its specific inhibition by N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. Journal of Virology 32:614–622
    [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. Rodriguez J. F., Smith G. L. 1990; IPTG-dependent vaccinia virus : identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Research 18:5347–5351
    [Google Scholar]
  31. Rodriguez J. F., Janezcko R., Esteban M. 1985; Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. Journal of Virology 56:482–488
    [Google Scholar]
  32. 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]
  33. 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]
  34. Sanderson C. M., Way M., Smith G. L. 1998; Virus-induced cell motility. Journal of Virology 72:1235–1243
    [Google Scholar]
  35. Schmelz M., Sodeik B., Ericsson M., Wolffe E. J., Shida H., Hiller G., 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]
  36. Shida H. 1986; Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150:451–462
    [Google Scholar]
  37. Sodeik B., Doms R. W., Ericsson M., Hiller G., Machamer C. E., van’Hof W., van Meer G., Moss B., Griffiths G. 1993; Assembly of vaccinia virus : role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. Journal of Cell Biology 121:521–541
    [Google Scholar]
  38. Tilney L. G., Tilney M. S. 1993; The wily ways of a parasite : induction of actin assembly by Listeria . Trends in Microbiology 1:25–31
    [Google Scholar]
  39. 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]
  40. Tsutsui K. 1983; Release of vaccinia virus from FL cells infected with IHD-W strain. Journal of Electron Microscopy 32:125–140
    [Google Scholar]
  41. Vanderplasschen A., Smith G. L. 1997; A 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]
  42. Vanderplasschen A., Hollinshead M., Smith G. L. 1997; Antibodies against vaccinia virus do not neutralize extracellular enveloped virus but prevent virus release from infected cells and comet formation. Journal of General Virology 78:2041–2048
    [Google Scholar]
  43. Vanderplasschen A., Hollinshead M., Smith G. L. 1998; Vaccinia virus extracellular enveloped virus and intracellular mature virus enter cells by different mechanisms. Journal of General Virology 79:877–887
    [Google Scholar]
  44. Welch M. D., Iwamatsu A., Mitchison T. J. 1997; Actin poly-merization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes . Nature 385:265–269
    [Google Scholar]
  45. 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]
  46. Wolffe E., Katz E., Weisberg A., Moss B. 1997; The A34R glycoprotein gene is required for induction of specialized actin-containing microvilli and efficient cell-to-cell transmission of vaccinia virus. Journal of Virology 71:3905–3915
    [Google Scholar]
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