1887

Abstract

Vaccinia virus (VV) strain Western Reserve gene B8R encodes a 43 kDa glycoprotein that is secreted from infected cells early in infection as a homodimer. This protein has amino acid similarity with the extracellular domain of cellular IFN-γ receptor (IFN-γR) and binds and inhibits IFN-γ from a wide range of species. Here we demonstrate that the B8R protein also inhibits equine IFN-γ. The 5′ end of the B8R mRNA has been mapped by primer extension analysis and the contribution of IFN-γRs to VV virulence was studied by the construction of a deletion mutant lacking the B8R gene (vΔB8R) and a revertant virus (vB8R-R) in which the B8R gene was re-inserted into the deletion mutant. A recombinant virus that expressed a soluble form of the mouse IFN-γR was also constructed and studied. The virulence of these viruses was tested in rodent models of infection. In mice, the loss of the VV IFN-γR did not affect virulence compared with WT and revertant viruses, consistent with the low affinity of the VV IFN-γR for mouse IFN-γ. However, expression of the mouse soluble IFN-γR increased virus virulence slightly. In rabbit skin, loss of the VV IFN-γR produced lesions with histological differences compared with WT and revertant viruses. Lastly, the affinity constants of the VV IFN-γR for human and mouse IFN-γ were determined by surface plasmon resonance.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-8-1953
2002-08-01
2021-05-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/8/0831953a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-8-1953&mimeType=html&fmt=ahah

References

  1. Aguet M., Dembic Z., Merlin G. 1988; Molecular cloning and expression of the human interferon-γ receptor. Cell 55:273–280
    [Google Scholar]
  2. 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]
  3. Alcamí A., Smith G. L. 1995; Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. Journal of Virology 69:4633–4639
    [Google Scholar]
  4. Alcamí A., Smith G. L. 1996; A mechanism for the inhibition of fever by a virus. Proceedings of the National Academy of Sciences, USA 93:11029–11034
    [Google Scholar]
  5. Alcamí A., Smith G. L. 2002; The vaccinia virus soluble interferon-γ receptor is a homodimer. Journal of General Virology 83:545–549
    [Google Scholar]
  6. Alcamí A., Symons J. A., Collins P. D., Williams T. J., Smith G. L. 1998; Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. Journal of Immunology 160:624–633
    [Google Scholar]
  7. Alcamí A., Symons J. A., Smith G. L. 2000; The vaccinia soluble IFN-α/β receptor binds to the cell surface and protects cells from the anti-viral effects of IFN. Journal of Virology 74:11230–11239
    [Google Scholar]
  8. Antoine G., Scheiflinger F., Dorner F., Falkner F. G. 1998; The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365–396
    [Google Scholar]
  9. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1990 Current Protocols in Molecular Biology, Unit 4.2.1 New York: John Wiley and Sons;
    [Google Scholar]
  10. Baxby D. 1981 Jenner’s Smallpox Vaccine London: Heinemann;
    [Google Scholar]
  11. Blanchard T. J., Alcamí A., Andrea P., Smith G. L. 1998; Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. Journal of General Virology 79:1159–1167
    [Google Scholar]
  12. Colamonici O. R., Domanski P., Sweitzer S. M., Larner A., Buller R. M. L. 1995; Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon α transmembrane signaling. Journal of Biological Chemistry 270:15974–15978
    [Google Scholar]
  13. 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]
  14. Davison A. J., Moss B. 1989; Structure of vaccinia virus early promoters. Journal of Molecular Biology 210:749–769
    [Google Scholar]
  15. Ealick S. E., Cook W. J., Vijay-Kumar S., Carson M., Nagabhushan T. L., Trotta P. P., Bugg C. E. 1991; Three-dimensional structure of recombinant human interferon-gamma. Science 252:698–702
    [Google Scholar]
  16. 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]
  17. Falkner F. G., Moss B. 1990; Transient dominant selection of recombinant vaccinia viruses. Journal of Virology 64:3108–3111
    [Google Scholar]
  18. Farrar M. A., Schreiber R. D. 1993; The molecular cell biology of interferon-γ and its receptor. Annual Review of Immunology 11:571–611
    [Google Scholar]
  19. Fountoulakis M., Schlaeger E.-J., Gentz R., Juranville J.-F., Manneberg M., Ozmen L., Garotta G. 1991; Purification and biochemical characterization of a soluble mouse interferon-γ receptor produced in insect cells. European Journal of Biochemistry 198:441–450
    [Google Scholar]
  20. Fountoulakis M., Zulauf M., Lustig A., Garotta G. 1992; Stoichiometry of interaction between interferon γ and its receptor. European Journal of Biochemistry 208:781–787
    [Google Scholar]
  21. Goebel S. J., Johnson G. P., Perkus M. E., Davis S. W., Winslow J. P., Paoletti E. 1990; The complete DNA sequence of vaccinia virus. Virology 179:247–266
    [Google Scholar]
  22. Greenlund A. C., Schreiber R. D., Goeddel D. V., Pennica D. 1993; Interferon-γ induces receptor dimerization in solution and on cells. Journal of Biological Chemistry 268:18103–18110
    [Google Scholar]
  23. Hemmi S., Peghini P., Metzler M., Merlin G., Dembic Z., Aguet M. 1989; Cloning of murine interferon gamma receptor cDNA: expression in human cells mediates high-affinity binding but is not sufficient to confer sensitivity to murine interferon gamma. Proceedings of the National Academy of Sciences, USA 86:9901–9905
    [Google Scholar]
  24. Horton R. M., Hunt H. D., Ho S. N., Pullen J. K., Pease L. R. 1989; Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61–68
    [Google Scholar]
  25. Howard S. T., Chan Y. S., Smith G. L. 1991; Vaccinia virus homologues of the Shope fibroma virus inverted terminal repeat proteins and a discontinuous ORF related to the tumor necrosis factor receptor family. Virology 180:633–647
    [Google Scholar]
  26. Huang S., Hendriks W., Althage A., Hemmi S., Bluethmann H., Kamijo R., Vilcek J., Zinkernagel R. M., Aguet M. 1993; Immune response in mice that lack the interferon-gamma receptor. Science 259:1742–1745
    [Google Scholar]
  27. Hughes S. J., Johnston L. H., de Carlos A., Smith G. L. 1991; Vaccinia virus encodes an active thymidylate kinase that complements a cdc8 mutant of Saccharomyces cerevisiae . Journal of Biological Chemistry 266:20103–20109
    [Google Scholar]
  28. Karupiah G., Fredrickson T. N., Holmes K. L., Khairallah L. H., Buller R. M. L. 1993; Importance of interferons in recovery from mousepox. Journal of Virology 67:4214–4226
    [Google Scholar]
  29. Kerr S. M., Smith G. L. 1991; Vaccinia virus DNA ligase is nonessential for virus replication: recovery of plasmids from virus-infected cells. Virology 180:625–632
    [Google Scholar]
  30. 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]
  31. 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 Glover D. M. Oxford: IRL Press;
    [Google Scholar]
  32. Moore J. B., Smith G. L. 1992; Steroid hormone synthesis by a vaccinia enzyme: a new type of virus virulence factor. EMBO Journal 11:1973–1980 [Erratum 11, 3490.]
    [Google Scholar]
  33. Moss B. 2001; Poxviridae : the viruses and their replication. In Fields Virology pp 2849–2883 Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams & Wilkins;
    [Google Scholar]
  34. Mossman K., Upton C., Buller R. M., McFadden G. 1995; Species specificity of ectromelia virus and vaccinia virus interferon-gamma binding proteins. Virology 208:762–769
    [Google Scholar]
  35. Ng A., Tscharke D. C., Reading P. C., Smith G. L. 2001; The vaccinia virus A41L protein is a soluble 30 kDa glycoprotein that affects virus virulence. Journal of General Virology 82:2095–2105
    [Google Scholar]
  36. Nicholson M. W., Barclay A. N., Singer M. S., Rosen S. D., van der Merwe P. A. 1998; Affinity and kinetic analysis of L-selectin (CD62L) binding to glycosylation-dependent cell-adhesion molecule-1. Journal of Biological Chemistry 273:763–770
    [Google Scholar]
  37. 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]
  38. Perkus M. E., Goebel S. J., Davis S. W., Johnson G. P., Norton E. K., Paoletti E. 1991; Deletion of 55 open reading frames from the termini of vaccinia virus. Virology 180:406–410
    [Google Scholar]
  39. Puehler F., Weining K. C., Symons J. A., Smith G. L., Staeheli P. 1998; Vaccinia virus-encoded cytokine receptor binds and neutralizes chicken interferon-gamma. Virology 248:231–240
    [Google Scholar]
  40. Samudzi C. T., Burton L. E., Rubin J. R. 1991; Crystal structure of recombinant rabbit interferon-gamma at 2·7-Å resolution. Journal of Biological Chemistry 266:21791–21797
    [Google Scholar]
  41. Smith G. L., Chan Y. S., Howard S. T. 1991; Nucleotide sequence of 42 kbp of vaccinia virus strain WR from near the right inverted terminal repeat. Journal of General Virology 72:1349–1376
    [Google Scholar]
  42. Spriggs M., Hruby D. E., Maliszewski C. R., Pickup D. J., Sims J. E., Buller R. M. L., Vanslyke J. 1992; Vaccinia and cowpox viruses encode a novel secreted interleukin-1 binding protein. Cell 71:145–152
    [Google Scholar]
  43. Symons J. A., Alcamí A., Smith G. L. 1995; Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81:551–560
    [Google Scholar]
  44. Tscharke D. C., Smith G. L. 1999; A model for vaccinia virus pathogenesis and immunity based on intradermal injection of mouse ear pinnae. Journal of General Virology 80:2751–2755
    [Google Scholar]
  45. Upton C., Mossman K., McFadden G. 1992; Encoding of a homolog of IFN-γ receptor by myxoma virus. Science 258:1369–1372
    [Google Scholar]
  46. van den Broek M. F., Muller U., Huang S., Aguet M., Zinkernagel R. M. 1995; Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. Journal of Virology 69:4792–4796
    [Google Scholar]
  47. Verardi P. H., Jones L. A., Aziz F. H., Ahmad S., Yilma T. D. 2001; Vaccinia virus vectors with an inactivated gamma interferon receptor homolog gene (B8R) are attenuated in vivo without a concomitant reduction in immunogenicity. Journal of Virology 75:11–18
    [Google Scholar]
  48. Walter M. R., Windsor W. T., Nagabhushan T. L., Lundell D. J., Lunn C. A., Zauodny P. J., Narula S. K. 1995; Crystal structure of a complex between interferon-gamma and its soluble high-affinity receptor. Nature 376:230–235
    [Google Scholar]
  49. Zhang W.-H., Wilcock D., Smith G. L. 2000; The vaccinia virus F12L protein is required for actin tail formation, normal plaque size and virulence. Journal of Virology 74:11663–11670
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-8-1953
Loading
/content/journal/jgv/10.1099/0022-1317-83-8-1953
Loading

Data & Media loading...

Most cited this month 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