1887

Journal of General Virology header logo

Volume 83, Issue 1

Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread Free

Abstract

The roles of vaccinia virus (VV) intracellular mature virus (IMV), intracellular enveloped virus (IEV), cell-associated enveloped virus (CEV) and extracellular enveloped virus (EEV) and their associated proteins in virus spread were investigated. The plaques made by VV mutants lacking individual IEV- or EEV-specific proteins (vΔA33R, vΔA34R, vΔA36R, vΔA56R, vΔB5R, vΔF12L and vΔF13L) were compared in the presence of IMV- or EEV-neutralizing antibodies (Ab). Data presented show that for long-range spread, the comet-shaped plaques of VV were caused by the unidirectional spread of EEV probably by convection currents, and for cell-to-cell spread, VV uses a combination of Ab-resistant and Ab-sensitive pathways. Actin tails play a major role in the Ab-resistant pathway, but mutants such as vΔA34R and vΔA36R that do not make actin tails still spread from cell to cell in the presence of Ab. Most strikingly, the Ab-resistant pathway was abolished when the A33R gene was deleted. This effect was not due to alterations in the efficiency of neutralization of EEV made by this mutant, nor due to a deficiency in IMV wrapping to form IEV, which was indispensable for EEV formation by vΔA33R and vΔA34R. We suggest a role for A33R in promoting Ab-resistant cell-to-cell spread of virus. The roles of the different virus forms in the VV life-cycle are discussed.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society

Erratum

An erratum has been published for this content:
Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-1-209
2002-01-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/1/0830209a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-1-209&mimeType=html&fmt=ahah

References

  1. Alcamí A., Smith G. L. 1992; A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71:153–167
     [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. 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]
  5. Blasco R., Moss B. 1992; Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. Journal of Virology 66:4170–4179 erratum 5703–5704
    [Google Scholar]
  6. Blasco R., Sisler J. R., Moss B. 1993; Dissociation of progeny vaccinia virus from the cell membrane is regulated by a viral envelope glycoprotein: effect of a point mutation in the lectin homology domain of the A34R gene. Journal of Virology 67:3319–3325
     [Google Scholar]
  7. Boulanger D., Smith T., Skinner M. A. 2000; Morphogenesis and release of fowlpox virus. Journal of General Virology 81:675–687
     [Google Scholar]
  8. Boulter E. A., Appleyard G. 1973; Differences between extracellular and intracellular forms of poxvirus and their implications. Progress in Medical Virology 16:86–108
     [Google Scholar]
  9. Boulter E. A., Zwartouw H. T., Titmuss D. H., Maber H. B. 1971; The nature of the immune state produced by inactivated vaccinia virus in rabbits. American Journal of Epidemiology 94:612–620
     [Google Scholar]
  10. Dingwell K. S., Johnson D. C. 1998; The herpes simplex virus gE–gI complex facilitates cell-to-cell spread and binds to components of cell junctions. Journal of Virology 72:8933–8942
     [Google Scholar]
  11. Dingwell K. S., Brunetti C. R., Hendricks R. L., Tang Q., Tang M., Rainbow A. J., Johnson D. C. 1994; Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. Journal of Virology 68:834–845
     [Google Scholar]
  12. 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]
  13. Engelstad M., Smith G. L. 1993; The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194:627–637
     [Google Scholar]
  14. 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]
  15. Firsching R., Buchholz C. J., Schneider U., Cattaneo R., ter Meulen V., Schneider-Schaulies J. 1999; Measles virus spread by cell–cell contacts: uncoupling of contact-mediated receptor (CD46) downregulation from virus uptake. Journal of Virology 73:5265–5273 erratum 10556
    [Google Scholar]
  16. Flexner C., Hugin A., Moss B. 1987; Prevention of vaccinia virus infection in immunodeficient mice by vector-directed IL-2 expression. Nature 330:259–262
     [Google Scholar]
  17. Galmiche M. C., Goenaga J., Wittek R., Rindisbacher L. 1999; Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254:71–80
     [Google Scholar]
  18. Herrera E., Lorenzo M. M., Blasco R., Isaacs S. N. 1998; Functional analysis of vaccinia virus B5R protein: essential role in virus envelopment is independent of a large portion of the extracellular domain. Journal of Virology 72:294–302
     [Google Scholar]
  19. 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]
  20. Hiller G., Eibl H., Weber K. 1981; Characterization of intracellular and extracellular vaccinia virus variants: N 1-isonicotinoyl- N 2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release. Journal of Virology 39:903–913
     [Google Scholar]
  21. 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]
  22. Hollinshead M., Rodger G., van Eijl H., Law M., Hollinshead R., Vaux D. J. T., Smith G. L. 2001; Vaccinia virus utilizes microtubules for movement to the cell surface. Journal of Cell Biology 154:389–402
     [Google Scholar]
  23. Hooper J. W., Custer D. M., Schmaljohn C. S., Schmaljohn A. L. 2000; DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge. Virology 266:329–339
     [Google Scholar]
  24. Ichihashi Y. 1996; Extracellular enveloped vaccinia virus escapes neutralization. Virology 217:478–485
     [Google Scholar]
  25. Ichihashi Y., Dales S. 1971; Biogenesis of poxviruses: interrelationship between hemagglutinin production and polykaryocytosis. Virology 46:533–543
     [Google Scholar]
  26. Ichihashi Y., Oie M. 1980; Adsorption and penetration of the trypsinized vaccinia virion. Virology 101:50–60
     [Google Scholar]
  27. Ichihashi Y., Oie M. 1996; Neutralizing epitope on penetration protein of vaccinia virus. Virology 220:491–494
     [Google Scholar]
  28. 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]
  29. Johnson D. C., Frame M. C., Ligas M. W., Cross A. M., Stow N. D. 1988; Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. Journal of Virology 62:1347–1354
     [Google Scholar]
  30. Kato N., Eggers H. J., Rolly H. 1969; Inhibition of release of vaccinia virus by N 1-isonicotinoly- N 2-3-methyl-4-chlorobenzoylhydrazine. Journal of Experimental Medicine 129:795–808
     [Google Scholar]
  31. Krijnse-Locker J., Kuehn A., Schleich S., Rutter G., Hohenberg H., Wepf R., Griffiths G. 2000; Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Molecular Biology of the Cell 11:2497–2511
     [Google Scholar]
  32. Law M., Smith G. L. 2001; Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology 280:132–142
     [Google Scholar]
  33. Lorenzo M. M., Galindo I., Griffiths G., Blasco R. 2000; Intracellular localization of vaccinia virus extracellular enveloped virus envelope proteins individually expressed using a Semliki Forest virus replicon. Journal of Virology 74:10535–10550
     [Google Scholar]
  34. McIntosh A. A., Smith G. L. 1996; Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. Journal of Virology 70:272–281
     [Google Scholar]
  35. Madeley C. R. 1968; The immunogenicity of heat-inactivated vaccinia virus in rabbits. Journal of Hygiene 66:89–107
     [Google Scholar]
  36. Mathew E., Sanderson C. M., Hollinshead M., Smith G. L. 1998; The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation. Journal of Virology 72:2429–2438
     [Google Scholar]
  37. Mathew E. C., Sanderson C. M., Hollinshead R., Smith G. L. 2001; A mutational analysis of the vaccinia virus B5R protein. Journal of General Virology 82:1199–1213
     [Google Scholar]
  38. Mo C., Schneeberger E. E., Arvin A. M. 2000; Glycoprotein E of varicella-zoster virus enhances cell–cell contact in polarized epithelial cells. Journal of Virology 74:11377–11387
     [Google Scholar]
  39. Moss B. 1996; Poxviridae: the viruses and their replication. In Fields Virology pp 2637–2671 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
     [Google Scholar]
  40. Palese P., Tobita K., Ueda M., Compans R. W. 1974; Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61:397–410
     [Google Scholar]
  41. 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]
  42. Payne L. G. 1978; Polypeptide composition of extracellular enveloped vaccinia virus. Journal of Virology 27:28–37
     [Google Scholar]
  43. Payne L. G. 1980; Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. Journal of General Virology 50:89–100
     [Google Scholar]
  44. Payne L. G. 1992; Characterization of vaccinia virus glycoproteins by monoclonal antibody precipitation. Virology 187:251–260
     [Google Scholar]
  45. Payne L. G., Norrby E. 1978; Adsorption and penetration of enveloped and naked vaccinia virus particles. Journal of Virology 27:19–27
     [Google Scholar]
  46. Payne L. G., Kristenson K. 1979; Mechanism of vaccinia virus release and its specific inhibition by N 1-isonicotinoyl- N 2-3-methyl-4-chlorobenzoylhydrazine. Journal of Virology 32:614–622
     [Google Scholar]
  47. Piguet V., Schwartz O., Le Gall S., Trono D. 1999; The downregulation of CD4 and MHC-I by primate lentiviruses: a paradigm for the modulation of cell surface receptors. Immunological Reviews 168:51–63
     [Google Scholar]
  48. 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]
  49. Roper R. L., Wolffe E. J., Weisberg A., Moss B. 1998; The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus. Journal of Virology 72:4192–4204
     [Google Scholar]
  50. Röttger S., Frischknecht F., Reckmann I., Smith G. L., Way M. 1999; Interactions between vaccinia virus IEV membrane proteins and their roles in IEV assembly and actin tail formation. Journal of Virology 73:2863–2875
     [Google Scholar]
  51. Sanderson C. S., Smith G. L. 1999; Cell motility and morphology: viruses in control. Expert Reviews in Molecular Medicine http://www-ermm.cbcu.cam.ac.uk/99000629h.htm
     [Google Scholar]
  52. Sanderson C. M., Frischknecht F., Way M., Hollinshead M., Smith G. L. 1998a; Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell–cell fusion. Journal of General Virology 79:1415–1425
     [Google Scholar]
  53. Sanderson C. M., Way M., Smith G. L. 1998b; Virus-induced cell motility. Journal of Virology 72:1235–1243
     [Google Scholar]
  54. Sanderson C. M., Hollinshead M., Smith G. L. 2000; The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. Journal of General Virology 81:47–58
     [Google Scholar]
  55. 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]
  56. Schmutz C., Payne L. G., Gubser J., Wittek R. 1991; A mutation in the gene encoding the vaccinia virus 37,000-Mr protein confers resistance to an inhibitor of virus envelopment and release. Journal of Virology 65:3435–3442
     [Google Scholar]
  57. Shida H. 1986; Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150:451–462
     [Google Scholar]
  58. Shida H., Dales S. 1981; Biogenesis of vaccinia: carbohydrate of the hemagglutinin molecules. Virology 111:56–72
     [Google Scholar]
  59. Shinkai K. 1975; Plaque morphology of herpes simplex virus in various cells under liquid overlay as a marker for its type differentiation. Japanese Journal of Microbiology 19:459–462
     [Google Scholar]
  60. Tooze J., Hollinshead M., Reis B., Radsak K., Kern H. 1993; Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. European Journal of Cell Biology 60:163–178
     [Google Scholar]
  61. Tsutsui K. 1983; Release of vaccinia virus from FL cells infected with the IHD-W strain. Journal of Electron Microscopy 32:125–140
     [Google Scholar]
  62. 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]
  63. Ulaeto D., Grosenbach D., Hruby D. E. 1995; Brefeldin A inhibits vaccinia virus envelopment but does not prevent normal processing and localization of the putative envelopment receptor P37. Journal of General Virology 76:103–111
     [Google Scholar]
  64. 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]
  65. 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]
  66. Vanderplasschen A., Hollinshead M., Smith G. L. 1998a; Intracellular and extracellular vaccinia virions enter cells by different mechanisms. Journal of General Virology 79:877–887
     [Google Scholar]
  67. Vanderplasschen A., Mathew E., Hollinshead M., Sim R. B., Smith G. L. 1998b; Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proceedings of the National Academy of Sciences, USA 95:7544–7549
     [Google Scholar]
  68. van Eijl H., Hollinshead M., Smith G. L. 2000; The vaccinia virus A36R protein is a type Ib membrane protein present on intracellular but not extracellular enveloped virus particles. Virology 271:26–36
     [Google Scholar]
  69. van Eijl H., Hollinshead M., Zhang W.-H., Smith G. L. 2002; The vaccinia virus F12L protein is associated with intracellular enveloped virus particles and is required for their egress to the cell surface. Journal of General Virology 83:195–207
     [Google Scholar]
  70. Ward B. M., Moss B. 2001; Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein–B5R membrane protein chimera. Journal of Virology 75:4802–4813
     [Google Scholar]
  71. 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 erratum 5709–5711
    [Google Scholar]
  72. Wolffe E. J., 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 71:3904–3915
     [Google Scholar]
  73. Wolffe E. J., Weisberg A. S., Moss B. 1998; Role for the vaccinia virus A36R outer envelope protein in the formation of virus-tipped actin-containing microvilli and cell-to-cell virus spread. Virology 244:20–26
     [Google Scholar]
  74. Zhang W. H., Wilcock D., Smith G. L. 2000; Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. Journal of Virology 74:11654–11662
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-1-209
Loading
Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread
J. Gen. Virol. 83, 209 (2002); https://doi.org/10.1099/0022-1317-83-1-209
/content/journal/jgv/10.1099/0022-1317-83-1-209
/content/journal/jgv/10.1099/0022-1317-83-1-209
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error