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Extracellular Enveloped Vaccinia Virus

Entry, Egress, and Evasion
  • Geoffrey L. Smith
  • Alain Vanderplasschen
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 440)

Abstract

Vaccinia virus is a large and complex virus that produces two types of infectious virus particles, termed intracellular mature virus (IMV) and extracellular enveloped virus (EEV). EEV contains an extra lipid envelope and ten associated proteins that are absent from IMV. Although EEV represents less than 1% of infectious progeny it is very important biologically. First, it mediates virus dissemination and second, it is the virus against which protective immune responses are directed. This article reviews the genes known to encode EEV proteins and their functions, describes recent data showing that the cellular receptors for IMV and EEV are different, and demonstrates that EEV, in contrast to IMV, is resistant to neutralisation by antibody.

Keywords

Vaccinia Virus Variola Virus Vaccinia Virus Strain Vaccinia Virus Infection Comet Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aguado, B., Selmes, I. P., and Smith, G. L., 1992, Nucleotide sequence of 21.8 kbp of variola major virus strain Harvey and comparison with vaccinia virus, J. Gen. Virol. 73: 2887–2902.PubMedCrossRefGoogle Scholar
  2. Alcami, A. and Smith, G. L., 1995, Cytokine receptors encoded by poxviruses: a lesson in cytokine biology, Immunol. Today 16: 474–478.PubMedCrossRefGoogle Scholar
  3. Alcamí, A. and Smith, G. L., 1996, Receptors for gamma-interferon encoded by poxviruses: implications for the unknown origin of vaccinia virus, Trends Microbiol. 4: 321–326.PubMedCrossRefGoogle Scholar
  4. Appleyard, G. and Andrews, C., 1974, Neutralizing activities of antisera to poxvirus soluble antigens, J. Gen. Virol. 23: 197–200.PubMedCrossRefGoogle Scholar
  5. Appleyard, G., Hapel, A. J., and Boulter, E. A., 1971, An antigenic difference between intracellular and extracellular rabbitpox virus, J. Gen. Virol. 13: 9–17.PubMedCrossRefGoogle Scholar
  6. Armstrong, J. A., Metz, D. H., and Young, M. R.,1973, The mode of entry of vaccinia virus into L cells, J. Gen. Virol. 21: 533–537.PubMedCrossRefGoogle Scholar
  7. Baxby, D., 1981, “Jenner’s smallpox vaccine: the riddle of the origin of vaccinia virus.” Heineman Educational Books, London.Google Scholar
  8. Blasco, R. and 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, J. Virol. 65, 5910–5920.PubMedGoogle Scholar
  9. Blasco, R. and Moss, B., 1992, Role of cell-associated enveloped vaccinia virus in cell-to-cell spread, J. Virol. 66: 4170–4179.PubMedGoogle Scholar
  10. Blasco, R., Sisler, J. R., and 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 A34Rgene, J. Virol. 67: 3319–3325.PubMedGoogle Scholar
  11. Boulter, E. A., 1969, Protection against poxviruses, Proc. R. Soc. Med. 62: 295–297.PubMedGoogle Scholar
  12. Boulter, E. A. and Appleyard, G., 1973, Differences between extracellular and intracellular forms of poxviruses and their implications, Prog. Med. Virol. 16: 86–108.PubMedGoogle Scholar
  13. Boulter, E. A., Zwartouw, H. T., Titmuss, D. H. I., and Maber, H. B., 1971, The nature of the immune state produced by inactivated vaccinia virus in rabbits, Am. J. Epidemiol. 94: 612–620.PubMedGoogle Scholar
  14. Brown, C. K., Turner, P. C. and Moyer, R. W., 1991, Molecular characterization of the vaccinia virus hemagglutinin gene, J. Virol. 65: 3598–606.PubMedGoogle Scholar
  15. Buller, R. M. L., Chakrabarti, S., Cooper, J. A., Twardzik, D. R., and Moss, B., 1988, Deletion of the vaccinia virus growth factor gene reduces virus virulence, J. Virol. 62: 866–874.PubMedGoogle Scholar
  16. Chang, A. and Metz, D. H., 1976, Further investigations on the mode of entry of vaccinia virus into cells, J. Gen. Virol. 32: 275–282.PubMedCrossRefGoogle Scholar
  17. Chang, W., Hsiao, J.-C, Chung, C.-S., and Bair, C.-H., 1995, Isolation of a monoclonal antibody which blocks vaccinia virus infection, J. Virol. 69: 517–522.PubMedGoogle Scholar
  18. Cudmore, S., Cossart, P., Griffiths, G., and Way, M., 1995, Actin-based motility of vaccinia virus, Nature 378: 636–638.PubMedCrossRefGoogle Scholar
  19. Cudmore, S., Reckmann, I., Griffiths, G., and Way, M., 1996, Vaccinia virus: a model system for actin-membrane interactions, J. Cell Sci. 109: 1739–1747.PubMedGoogle Scholar
  20. Czerny, C. P. and Mahnel, H., 1990, Structural and functional analysis of orthopoxvirus epitopes with neutralizing monoclonal antibodies, J. Gen. Virol. 71: 2341–2352.PubMedCrossRefGoogle Scholar
  21. Dales, S. and Kajioka, R., 1964, The cycle of multiplication of vaccinia virus in Earles strain L cells. I. Uptake and penetration, Virology 24: 278–294.PubMedCrossRefGoogle Scholar
  22. Doms, R. W., Blumenthal, R., and Moss, B., 1990, Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane, J. Virol. 64: 4884–4892.PubMedGoogle Scholar
  23. Duncan, S. A., 1992, D. Phil. Analysis of three vaccinia virus genes, one of which is essential for plaque formation. University of Oxford, Oxford.Google Scholar
  24. Duncan, S. A. and Smith, G. L., 1992, Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress, J. Virol. 66: 1610–1621.PubMedGoogle Scholar
  25. Engelstad, M., Howard, S. T. and 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.PubMedCrossRefGoogle Scholar
  26. Engelstad, M. and 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.PubMedCrossRefGoogle Scholar
  27. Eppstein, D. A., Marsh, Y. V., Schreiber, A. B., Newman, S. R., Todaro, G. J. and Nestor, J. J., 1985, Epidermal growth factor receptor occupancy inhibits vaccinia virus infection, Nature 318: 663–665.PubMedCrossRefGoogle Scholar
  28. Fenner, F., Anderson, D. A., Arita, I., Jezek, Z. and Ladnyi, I. D., 1988, “Smallpox and Its Eradication.” World Health Organisation, Geneva.Google Scholar
  29. Flexner, C., Hugin, A. and Moss, B., 1987, Prevention of vaccinia virus infection in immunodeficient mice by vector-directed IL-2 expression, Nature 330: 259–262.PubMedCrossRefGoogle Scholar
  30. Goebel, S. J., Johnson, G. P., Perkus, M. E., Davis, S. W., Winslow, J. P. and Paoletti, E., 1990, The complete DNA sequence of vaccinia virus, Virology 179: 247–266.PubMedCrossRefGoogle Scholar
  31. Grosenbach, D. W., Ulaeto, D. O. and Hruby, D. E., 1997, Palmitylation of the vaccinia virus 37-kDa major envelope antigen. Identification of a conserved acceptor motif and biological relevance, J. Biol. Chem. 272: 1956–1964.PubMedCrossRefGoogle Scholar
  32. Hiller, G. and Weber, K., 1985, Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment, J. Virol. 55: 651–659.PubMedGoogle Scholar
  33. Hirt, P., Hiller, G. and Wittek, R., 1986, Localization and fine structure of a vaccinia virus gene encoding an envelope antigen, J. Virol. 58: 757–764.PubMedGoogle Scholar
  34. Ichihashi, Y., 1996, Extracellular enveloped vaccinia virus escapes neutralization, Virology 217: 478–485.PubMedCrossRefGoogle Scholar
  35. Ichihashi, Y. and Dales, S., 1971, Biogenesis of poxviruses: interrelationship between hemagglutinin production and polykaryocytosis, Virology 46: 533–543.PubMedCrossRefGoogle Scholar
  36. Isaacs, S. N., Wolffe, E. J., Payne, L. G. and Moss, B., 1992, Characterization of a vaccinia virus-encoded 42-kilo-dalton class I membrane glycoprotein component of the extracellular virus envelope, J. Virol. 66: 7217–7224.PubMedGoogle Scholar
  37. Janeczko, R. A., Rodriguez, J. F. and Esteban, M., 1987, Studies on the mechanism of entry of vaccinia virus in animal cells, Arch. Virol. 92: 135–150.PubMedCrossRefGoogle Scholar
  38. Jensen, O. N., Houthaeve, T., Shevchenko, A., Cudmore, S., Ashford, T., Mann, M., Griffiths, G. and Krijnse Locker, J., 1996, Identification of the major membrane and core proteins of vaccinia virus by two-dimensional electrophoresis, J. Virol. 70: 7485–7497.PubMedGoogle Scholar
  39. Jin, D., Li, Z., Jin, Q., Yuwen, H. and Hou, Y., 1989, Vaccinia virus hemagglutinin. A novel member of the immunoglobulin superfamily, J. Exp. Med. 170: 571–576.PubMedCrossRefGoogle Scholar
  40. Joklik, W. K., 1962, The purification of four strains of poxvirus, Virology 18: 9–18.PubMedCrossRefGoogle Scholar
  41. Katz, E., Wolffe, E. J. and Moss, B., 1997, The cytoplasmic domains of the vaccinia viru B5R protein target a chimeric human immunodeficiency virus type 1 glycoprotein to the outer envelope of nascent vaccinia virions, J. Virol. 71: 3178–3187.PubMedGoogle Scholar
  42. Koonin, E. V, 1996, A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins, Trends Biochem. Sci. 21: 242–243.PubMedGoogle Scholar
  43. Maa, J. S., Rodriguez, J. F. and Esteban, M., 1990, Structural and functional characterization of a cell surface binding protein of vaccinia virus, J. Biol. Chem. 265: 1569–77.PubMedGoogle Scholar
  44. Martinez-Pomares, L., Stern, R. J. and Moyer, R. W., 1993, The ps/hr gene (B5R open reading frame homolog) of rabbitpox virus controls pock colour, is a component of extracellular enveloped virus, and is secreted into the medium, J. Virol. 67: 5450–5462.PubMedGoogle Scholar
  45. Massung, R. F., Esposito, J. J., Liu, L.-i., Qi, J., Utterback, T. R., Knight, J. C., Aubin, L., Yuran, T. E., Parsons, J. M., Loparev, V. N., Selivanov, N. A., Cavallaro, K. F., Kerlavage, A. R., Mahy, B. W. J. and Venter, A. J., 1993, Potential virulence determinants in terminal regions of variola smallpox virus genome; Nature 366: 748–751.PubMedCrossRefGoogle Scholar
  46. McIntosh, A. A. G. and Smith, G. L., 1996, Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus, J. Virol. 70: 272–281.PubMedGoogle Scholar
  47. Moss, B., 1996, Poxviridae: the viruses and their replication, in “Fields Virology” (B. N. Fields, D. M. Knipe, and P. M. Howley, Eds.), Vol. 2, pp. 2637–2671. 2 vols. Lippincott Raven Press, New York.Google Scholar
  48. Moss, B., Rosenblum, E. N., Katz, E. and Grimley, P. M., 1969, Rifampicin: a specific inhibitor of vaccinia virus assembly, Nature 224: 1280–1284.PubMedCrossRefGoogle Scholar
  49. Niles, E. G. and Seto, J., 1988, Vaccinia virus gene D8 encodes a virion transmembrane protein, J. Virol. 62: 3772–3778.PubMedGoogle Scholar
  50. Oie, M., Shida, H. and Ichihashi, Y, 1990, The function of the vaccinia hemagglutinin in the proteolytic activation of infectivity, Virology 176: 494–504.PubMedCrossRefGoogle Scholar
  51. Parkinson, J. E. and 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.PubMedCrossRefGoogle Scholar
  52. Payne, L., 1978, Polypeptide composition of extracellular enveloped vaccinia virus, J. Virol. 27: 28–37.PubMedGoogle Scholar
  53. Payne, L. G., 1979, Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus, J. Virol. 31: 147–155.PubMedGoogle Scholar
  54. Payne, L. G., 1980, Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia virus, J. Gen.Virol. 50: 89–100.PubMedCrossRefGoogle Scholar
  55. Payne, L. G., 1992, Characterization of vaccinia virus glycoproteins by monoclonal antibody preparations, Virology 187: 251–260.PubMedCrossRefGoogle Scholar
  56. Payne, L. G. and Kristensson, K., 1985, Extracellular release of enveloped vaccinia virus from mouse nasal epithelial cells in vivo, J. Gen. Virol. 66: 643–646.PubMedCrossRefGoogle Scholar
  57. Payne, L. G. and Norrby, E., 1976, Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles, J. Gen. Virol. 32: 63–72.PubMedCrossRefGoogle Scholar
  58. Payne, L. G. and Norrby, E., 1978, Adsorption and penetration of enveloped and naked vaccinia virus particles, J. Virol. 11: 19–27.Google Scholar
  59. Ponting, C. P. and Kerr, I. D., 1996, A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues, Protein Sci. 5:914–922.PubMedCrossRefGoogle Scholar
  60. Rodriguez, J. F. and Esteban, M., 1987, Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein, J. Virol. 61: 3550–3554.PubMedGoogle Scholar
  61. Rodriguez, J. F., Janezcko, R. and Esteban, M., 1985, Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus, J. Virol. 56: 482–488.PubMedGoogle Scholar
  62. Rodriguez, J. F., Paez, E. and Esteban, M., 1987, A 14,000-Mr envelope protein of vaccinia virus is involved in cell fusion and forms covalently linked trimers, J. Virol. 61: 395–404.PubMedGoogle Scholar
  63. Rodriguez, J. F. and Smith, G. L., 1990, IPTG-dependent vaccinia virus : identification of a virus protein enabling virion envelopment by Golgi membrane and egress, Nucl. Acids Res. 18: 5347–5351.PubMedCrossRefGoogle Scholar
  64. Roper, R. L., Payne, L. G. and Moss, B., 1996, Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene,J. Virol. 70: 3753–3762.PubMedGoogle Scholar
  65. Schmelz, M., Sodeik, B., Ericsson, M., Wolffe, E. J., Shida, H., G., H. and Griffiths, G., 1994, Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans golgi network, J. Virol. 68: 130–147.PubMedGoogle Scholar
  66. Schmutz, C., Payne, L. G., Gubser, J. and 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, J. Virol. 65: 3435–3442.PubMedGoogle Scholar
  67. Schmutz, C., Rindisbacher, L., Galmiche, M. C. and Wittek, R., 1995, Biochemical analysis of the major vaccinia virus envelope antigen, Virology 213: 19–27.PubMedCrossRefGoogle Scholar
  68. Seki, M., Oie, M., Ichihashi, Y. and Shida, H., 1990, Hemadsorption and fusion inhibition activities of hemagglutinin analyzed by vaccinia virus mutants, Virology 175: 372–384.PubMedCrossRefGoogle Scholar
  69. Shchelkunov, S. N., Massung, R. F. and Esposito, J. J., 1995, Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses, Virus Res. 36: 107–118.PubMedCrossRefGoogle Scholar
  70. Shida, H., 1986, Nucleotide sequence of the vaccinia virus hemagglutinin gene, Virology 150: 451–462.PubMedCrossRefGoogle Scholar
  71. Shida, H. and Dales, S., 1981, Biogenesis of vaccinia: carbohydrate of the hemagglutinin molecule, Virology 111: 56–72.PubMedCrossRefGoogle Scholar
  72. Shida, H. and Dales, S., 1982, Biogenesis of vaccinia: molecular basis for the hemagglutinin-negative phenotype of the IHD-W strain, Virology 117: 219–237.PubMedCrossRefGoogle Scholar
  73. Shida, H. and Matsumoto, S., 1983, Analysis of the hemagglutinin glycoprotein from mutants of vaccinia virus that accumulates on the nuclear envelope, Cell 33: 423–434.PubMedCrossRefGoogle Scholar
  74. Smith, G. L., 1996, Virus proteins that bind cytokines, chemokines and interferons, Curr. Opin. Immunol. 8: 467-471.PubMedCrossRefGoogle Scholar
  75. Sodeik, B., Doms, R. W., Ericsson, M., Hiller, G., Machamer, C. E., van ‘t Hof, W., van Meer, G., Moss, B. and Griffiths, G., 1993, Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks, J. Cell Biol. 121: 521–541.PubMedCrossRefGoogle Scholar
  76. Spriggs, M. K., 1996, One step ahead of the game: viral immunomodulatory molecules, Ann. Rev. Immunol, 14: 110–130.CrossRefGoogle Scholar
  77. Stroobant, P., Rice, A. P., Gullick, W. J., Cheng, D. J., Kerr, I. M. and Waterfield, M. D., 1985, Purification and characterization of vaccinia virus growth factor.,Cell 42: 383–393.PubMedCrossRefGoogle Scholar
  78. Takahashi-Nishimaki, F., Funahashi, S., Miki, K., Hashizume, S. and Sugimoto, M., 1991, Regulation of plaque size and host range by a vaccinia virus gene related to complement system proteins, Virology 181: 158–164.PubMedCrossRefGoogle Scholar
  79. Tilney, L. G. and Portnoy, D. A., 1989, Actin filaments and the growth, movement and spread of the intracellular bacterial parasite, Listeria monocytogenes, J. Cell Biol. 109: 1597–1608.PubMedCrossRefGoogle Scholar
  80. Tooze, J., Hollinshead, M., Reis, B., Radsak, K. and Kern, H., 1993, Progeny vaccinia viruses and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes; Eur. J. Cell Biol. 60: 163–178.PubMedGoogle Scholar
  81. Ulaeto, D., Grosenbach, D. and Hruby, D. E., 1995, Brefeldin A inhibits vaccinia virus envelopment but does not prevent normal processing and localization of the putative envelopment receptor P37, J. Gen. Virol. 76: 103–111.PubMedCrossRefGoogle Scholar
  82. Ulaeto, D., Grosenbach, D. and Hruby, D. E., 1996, The vaccinia virus 4c and A-type inclusion proteins are specific markers for the intracellular mature virus particle, J. Virol. 70: 3372–3377.PubMedGoogle Scholar
  83. Vanderplasschen, A., Hollinshead, M. and Smith, G. L., 1997, Antibodies against vaccinia virus do not neutralise extracellular enveloped virus but prevent virus release from infected cells and comet formation, J. Gen. Virol. 78: In press.Google Scholar
  84. Vanderplasschen, A. and 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, J. Virol. 71: 4032–4041.PubMedGoogle Scholar
  85. VanSlyke, J. K. and Hruby, D. E., 1990, Posttranslational modification of vaccinia virus proteins,Curr. Top. Microbiol. Immunol. 163: 185–206.PubMedCrossRefGoogle Scholar
  86. Wolffe, E., Katz, E., Weisberg, A. and 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, J. Virol. 71: 3905–3915.Google Scholar
  87. Wolffe, E. J., Isaacs, S. N. and Moss, B., 1993, Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination, J. Virol. 67: 4732–4741.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  • Geoffrey L. Smith
    • 1
  • Alain Vanderplasschen
    • 1
  1. 1.Sir William Dunn School of PathologyUniversity of OxfordOxfordUK

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