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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.

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2002-08-01
2019-10-21
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References

  1. Aguet, M., Dembic, Z. & Merlin, G. ( 1988; ). Molecular cloning and expression of the human interferon-γ receptor. Cell 55, 273-280.[CrossRef]
    [Google Scholar]
  2. Alcamı́, 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.[CrossRef]
    [Google Scholar]
  3. Alcamı́, 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. Alcamı́, 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.[CrossRef]
    [Google Scholar]
  5. Alcamı́, 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. Alcamı́, 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. Alcamı́, 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.[CrossRef]
    [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.[CrossRef]
    [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.
  10. Baxby, D. (1981). Jenner’s Smallpox Vaccine. London: Heinemann.
  11. Blanchard, T. J., Alcamı́, 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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  14. Davison, A. J. & Moss, B. ( 1989; ). Structure of vaccinia virus early promoters. Journal of Molecular Biology 210, 749-769.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 D. M. Glover. Oxford:IRL Press.
  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 D. M. Knipe & P. M. Howley. Philadelphia:Lippincott Williams & Wilkins.
  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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  43. Symons, J. A., Alcamı́, 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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
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