1887

Abstract

(YLDV) is a yatapoxvirus, a group of slow-growing poxviruses from primates. Analysis of the growth cycle of YLDV in tissue culture showed that maximum virus titres were reached 3 days post-infection and at this time only 3·3 % of infectious progeny was extracellular. The intracellular and extracellular virions have different buoyant densities and are separable on CsCl density gradients. They are also distinguishable by electron microscopy with the extracellular virions having an additional lipid envelope. In YLDV-infected cells, thick actin bundles with virions at their tips were seen protruding from the cell surface, despite the fact that YLDV lacks a protein comparable to A36R, which is required for VV-induced actin tail formation. In addition to these observations, the YLDV gene was characterized. This gene is predicted to encode a transmembrane protein containing three short consensus repeat (SCR) motifs common to members of the complement control protein family. Antibody generated against recombinant Y144R recognized products of 36, 41 and 48–55 kDa in YLDV-infected cells and purified extracellular enveloped virus (EEV) but not intracellular mature virus (IMV). Y144R protein is a glycoprotein with type I membrane topology that is synthesized early and late during infection. By immunoblot, indirect immunofluorescence and immuno-cryoelectron microscopy the Y144R protein was detected on the intracellular enveloped virus (IEV), cell-associated enveloped virus (CEV) and EEV. This represents the first study of a YLDV IEV, CEV and EEV protein at the molecular level.

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2004-05-01
2019-11-12
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References

  1. Adams, E. M., Brown, M. C., Nunge, M., Krych, M. & Atkinson, J. P. ( 1991; ). Contribution of the repeating domains of membrane cofactor protein (CD46) of the complement system to ligand binding and cofactor activity. J Immunol 147, 3005–3011.
    [Google Scholar]
  2. Afonso, C. L., Tulman, E. R., Lu, Z., Zsak, L., Kutish, G. F. & Rock, D. L. ( 2000; ). The genome of fowlpox virus. J Virol 74, 3815–3831.[CrossRef]
    [Google Scholar]
  3. Afonso, C. L., Tulman, E. R., Lu, Z., Zsak, L., Osorio, F. A., Balinsky, C., Kutish, G. F. & Rock, D. L. ( 2002; ). The genome of swinepox virus. J Virol 76, 783–790.[CrossRef]
    [Google Scholar]
  4. Appleyard, G., Hapel, A. J. & Boulter, E. A. ( 1971; ). An antigenic difference between intracellular and extracellular rabbitpox virus. J Gen Virol 13, 9–17.[CrossRef]
    [Google Scholar]
  5. Boulter, E. A. & Appleyard, G. ( 1973; ). Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol 16, 86–108.
    [Google Scholar]
  6. Cameron, C., Hota-Mitchell, S., Chen, L., Barrett, J., Cao, J. X., Macaulay, C., Willer, D., Evans, D. & McFadden, G. ( 1999; ). The complete DNA sequence of myxoma virus. Virology 264, 298–318.[CrossRef]
    [Google Scholar]
  7. Chakrabarti, S., Sisler, J. R. & Moss, B. ( 1997; ). Compact, synthetic, vaccinia virus early/late promoter for protein expression. Biotechniques 23, 1094–1097.
    [Google Scholar]
  8. Davison, A. J. & Moss, B. ( 1989; ). Structure of vaccinia virus late promoters. J Mol Biol 210, 771–784.[CrossRef]
    [Google Scholar]
  9. 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.[CrossRef]
    [Google Scholar]
  10. 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.[CrossRef]
    [Google Scholar]
  11. España, C. ( 1971; ). A pox disease of monkeys transmissible to man. In 2nd Conference of Experimental Medicine and Surgery in Primates, pp. 694–708. Basel: Karger.
  12. Frischknecht, F., Moreau, V., Rottger, S., Gonfloni, S., Reckmann, I., Superti-Furga, G. & Way, M. ( 1999; ). Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926–929.[CrossRef]
    [Google Scholar]
  13. Galmiche, M. C., Goenaga, J., Wittek, R. & Rindisbacher, L. ( 1999; ). Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254, 71–80.[CrossRef]
    [Google Scholar]
  14. 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. J Virol 72, 294–302.
    [Google Scholar]
  15. Hollinshead, M., Vanderplasschen, A., Smith, G. L. & Vaux, D. J. ( 1999; ). Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73, 1503–1517.
    [Google Scholar]
  16. Hourcade, D., Holers, V. M. & Atkinson, J. P. ( 1989; ). The regulators of complement activation (RCA) gene cluster. Adv Immunol 45, 381–416.
    [Google Scholar]
  17. Hu, Y., Lee, J., McCart, J. A., Xu, H., Moss, B., Alexander, H. R. & Bartlett, D. L. ( 2001; ). Yaba-like disease virus: an alternative replicating poxvirus vector for cancer gene therapy. J Virol 75, 10300–10308.[CrossRef]
    [Google Scholar]
  18. 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. J Virol 66, 7217–7224.
    [Google Scholar]
  19. Knight, J. C., Novembre, F. J., Brown, D. R., Goldsmith, C. S. & Esposito, J. J. ( 1989; ). Studies on Tanapox virus. Virology 172, 116–124.[CrossRef]
    [Google Scholar]
  20. Kotwal, G. J. & Moss, B. ( 1988; ). Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 335, 176–178.[CrossRef]
    [Google Scholar]
  21. Law, M. & Smith, G. L. ( 2001; ). Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology 280, 132–142.[CrossRef]
    [Google Scholar]
  22. Law, M., Hollinshead, R. & Smith, G. L. ( 2002; ). 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, 209–222.
    [Google Scholar]
  23. Lee, H. J., Essani, K. & Smith, G. L. ( 2001; ). The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281, 170–192.[CrossRef]
    [Google Scholar]
  24. 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. Edited by D. M. Glover. Oxford: IRL Press.
  25. Martinez-Pomares, L., Stern, R. J. & Moyer, R. W. ( 1993; ). The ps/hr gene (B5R open reading frame homolog) of rabbitpox virus controls pock color, is a component of extracellular enveloped virus, and is secreted into the medium. J Virol 67, 5450–5462.
    [Google Scholar]
  26. 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. J Virol 72, 2429–2438.
    [Google Scholar]
  27. Payne, L. G. ( 1978; ). Polypeptide composition of extracellular enveloped vaccinia virus. J Virol 27, 28–37.
    [Google Scholar]
  28. 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. J Virol 70, 905–914.
    [Google Scholar]
  29. Sanderson, C. M., Frischknecht, F., Way, M., Hollinshead, M. & Smith, G. L. ( 1998; ). Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell-cell fusion. J Gen Virol 79, 1415–1425.
    [Google Scholar]
  30. 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. J Virol 68, 130–147.
    [Google Scholar]
  31. Senkevich, T. G., Bugert, J. J., Sisler, J. R., Koonin, E. V., Darai, G. & Moss, B. ( 1996; ). Genome sequence of a human tumorigenic poxvirus: prediction of specific host response-evasion genes. Science 273, 813–816.[CrossRef]
    [Google Scholar]
  32. Smith, G. L., Vanderplasschen, A. & Law, M. ( 2002; ). The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83, 2915–2931.
    [Google Scholar]
  33. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  34. Tulman, E. R., Afonso, C. L., Lu, Z., Zsak, L., Kutish, G. F. & Rock, D. L. ( 2001; ). Genome of lumpy skin disease virus. J Virol 75, 7122–7130.[CrossRef]
    [Google Scholar]
  35. Tulman, E. R., Afonso, C. L., Lu, Z. & 7 other authors ( 2002; ). The genomes of sheeppox and goatpox viruses. J Virol 76, 6054–6061.[CrossRef]
    [Google Scholar]
  36. 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.[CrossRef]
    [Google Scholar]
  37. van Eijl, H., Hollinshead, M., Rodger, G., 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. J Gen Virol 83, 195–207.
    [Google Scholar]
  38. Willer, D. O., McFadden, G. & Evans, D. H. ( 1999; ). The complete genome sequence of shope (rabbit) fibroma virus. Virology 264, 319–343.[CrossRef]
    [Google Scholar]
  39. 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.[CrossRef]
    [Google Scholar]
  40. Zhang, W. H., Wilcock, D. & Smith, G. L. ( 2000; ). Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J Virol 74, 11654–11662.[CrossRef]
    [Google Scholar]
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