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Abstract

Yaba-like disease virus (YLDV) gene encodes a seven-transmembrane G protein-coupled receptor with 53 % amino acid identity to human CC chemokine receptor 8 (CCR8). Initial characterization of 7L showed that this 56 kDa cell-surface glycoprotein binds human CCL1 with high affinity ( =0·6 nM) and induces signal transduction by activation of heterotrimeric G proteins and downstream protein kinases. Further characterization of YLDV 7L is presented here and shows that murine CC chemokines can induce G-protein activation via the 7L receptor, despite having a low binding affinity for this receptor. In addition, when expressed by recombinant vaccinia virus (VACV), YLDV 7L was found on the outer envelope of VACV extracellular enveloped virus. The contribution of 7L to poxvirus pathogenesis was investigated by infection of mice with a recombinant VACV expressing 7L (vΔB8R-7L) and was compared with the outcome of infection by parental and revertant control viruses. In both intranasal and intradermal models, expression of 7L caused attenuation of VACV. The role of this protein in viral virulence is discussed.

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2006-04-01
2019-11-19
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References

  1. Alcami, A. ( 2003; ). Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 3, 36–50.[CrossRef]
    [Google Scholar]
  2. Alcami, A. & Smith, G. L. ( 1992; ). A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71, 153–167.[CrossRef]
    [Google Scholar]
  3. Alcamí, A. & Smith, G. L. ( 1995; ). Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J Virol 69, 4633–4639.
    [Google Scholar]
  4. Arvanitakis, L., Geras-Raaka, E., Varma, A., Gershengorn, M. C. & Cesarman, E. ( 1997; ). Human herpesvirus KSHV encodes a constitutively active G-protein-coupled receptor linked to cell proliferation. Nature 385, 347–350.[CrossRef]
    [Google Scholar]
  5. Bartlett, N. W., Dumoutier, L., Renauld, J.-C., Kotenko, S. V., McVey, C. E., Lee, H.-J. & Smith, G. L. ( 2004; ). A new member of the interleukin 10-related cytokine family encoded by a poxvirus. J Gen Virol 85, 1401–1412.[CrossRef]
    [Google Scholar]
  6. Bennett, A. M., Lescott, T., Phillpotts, R. J., Mackett, M. & Titball, R. W. ( 1999; ). Recombinant vaccinia viruses protect against Clostridium perfringens alpha-toxin. Viral Immunol 12, 97–105.[CrossRef]
    [Google Scholar]
  7. Bodaghi, B., Jones, T. R., Zipeto, D., Vita, C., Sun, L., Laurent, L., Arenzana-Seisdedos, F., Virelizier, J.-L. & Michelson, S. ( 1998; ). Chemokine sequestration by viral chemoreceptors as a novel viral escape strategy: withdrawal of chemokines from the environment of cytomegalovirus-infected cells. J Exp Med 188, 855–866.[CrossRef]
    [Google Scholar]
  8. Buller, R. M., Smith, G. L., Cremer, K., Notkins, A. L. & Moss, B. ( 1985; ). Decreased virulence of recombinant vaccinia virus expression vectors is associated with a thymidine kinase-negative phenotype. Nature 317, 813–815.[CrossRef]
    [Google Scholar]
  9. Burger, M., Burger, J. A., Hoch, R. C., Oades, Z., Takamori, H. & Schraufstatter, I. U. ( 1999; ). Point mutation causing constitutive signaling of CXCR2 leads to transforming activity similar to Kaposi's sarcoma herpesvirus-G protein-coupled receptor. J Immunol 163, 2017–2022.
    [Google Scholar]
  10. Casarosa, P., Waldhoer, M., LiWang, P. J., Vischer, H. F., Kledal, T., Timmerman, H., Schwartz, T. W., Smit, M. J. & Leurs, R. ( 2005; ). CC and CX3C chemokines differentially interact with the N terminus of the human cytomegalovirus-encoded US28 receptor. J Biol Chem 280, 3275–3285.[CrossRef]
    [Google Scholar]
  11. Colantonio, L., Iellem, A., Sinigaglia, F. & D'Ambrosio, D. ( 2002; ). Skin-homing CLA+ T cells and regulatory CD25+ T cells represent major subsets of human peripheral blood memory T cells migrating in response to CCL1/I-309. Eur J Immunol 32, 3506–3514.[CrossRef]
    [Google Scholar]
  12. Coupar, B. E. H., Oke, P. G. & Andrew, M. E. ( 2000; ). Insertion sites for recombinant vaccinia virus construction: effects on expression of a foreign protein. J Gen Virol 81, 431–439.
    [Google Scholar]
  13. Dairaghi, D. J., Fan, R. A., McMaster, B. E., Hanley, M. R. & Schall, T. J. ( 1999; ). HHV8-encoded vMIP-I selectively engages chemokine receptor CCR8. Agonist and antagonist profiles of viral chemokines. J Biol Chem 274, 21569–21574.[CrossRef]
    [Google Scholar]
  14. D'Ambrosio, D., Iellem, A., Bonecchi, R., Mazzeo, D., Sozzani, S., Mantovani, A. & Sinigaglia, F. ( 1998; ). Selective up-regulation of chemokine receptors CCR4 and CCR8 upon activation of polarized human type 2 Th cells. J Immunol 161, 5111–5115.
    [Google Scholar]
  15. Falkner, F. G. & Moss, B. ( 1990; ). Transient dominant selection of recombinant vaccinia viruses. J Virol 64, 3108–3111.
    [Google Scholar]
  16. Fraile-Ramos, A., Pelchen-Matthews, A., Kledal, T. N., Browne, H., Schwartz, T. W. & Marsh, M. ( 2002; ). Localization of HCMV UL33 and US27 in endocytic compartments and viral membranes. Traffic 3, 218–232.[CrossRef]
    [Google Scholar]
  17. Gombert, M., Dieu-Nosjean, M.-C., Winterberg, F. & 21 other authors ( 2005; ). CCL1-CCR8 interactions: an axis mediating the recruitment of T cells and Langerhans-type dendritic cells to sites of atopic skin inflammation. J Immunol 174, 5082–5091.[CrossRef]
    [Google Scholar]
  18. Gutiérrez, J., Kremer, L., Zaballos, Á., Goya, Í., Mártinez-A., C. & Márquez, G. ( 2004; ). Analysis of post-translational CCR8 modifications and their influence on receptor activity. J Biol Chem 279, 14726–14733.[CrossRef]
    [Google Scholar]
  19. Haeberle, H. A., Kuziel, W. A., Dieterich, H.-J., Casola, A., Gatalica, Z. & Garofalo, R. P. ( 2001; ). Inducible expression of inflammatory chemokines in respiratory syncytial virus-infected mice: role of MIP-1α in lung pathology. J Virol 75, 878–890.[CrossRef]
    [Google Scholar]
  20. 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]
  21. Krauss, O., Hollinshead, R., Hollinshead, M. & Smith, G. L. ( 2002; ). An investigation of incorporation of cellular antigens into vaccinia virus particles. J Gen Virol 83, 2347–2359.
    [Google Scholar]
  22. Kremer, L., Carramolino, L., Goya, Í., Zaballos, Á., Gutiérrez, J., Moreno-Ortiz, M. del C., Mártinez-A., C. & Márquez, G. ( 2001; ). The transient expression of C-C chemokine receptor 8 in thymus identifies a thymocyte subset committed to become CD4+ single-positive T cells. J Immunol 166, 218–225.[CrossRef]
    [Google Scholar]
  23. Law, M., Hollinshead, M., Lee, H.-J. & Smith, G. L. ( 2004; ). Yaba-like disease virus protein Y144R, a member of the complement control protein family, is present on enveloped virions that are associated with virus-induced actin tails. J Gen Virol 85, 1279–1290.[CrossRef]
    [Google Scholar]
  24. Lee, M. S., Roos, J. M., McGuigan, L. C., Smith, K. A., Cormier, N., Cohen, L. K., Roberts, B. E. & Payne, L. G. ( 1992; ). Molecular attenuation of vaccinia virus: mutant generation and animal characterization. J Virol 66, 2617–2630.
    [Google Scholar]
  25. 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]
  26. Mackett, M., Smith, G. L. & Moss, B. ( 1984; ). General method for production and selection of infectious vaccinia virus recombinants expressing foreign genes. J Virol 49, 857–864.
    [Google Scholar]
  27. Moser, B. & Willimann, K. ( 2004; ). Chemokines: role in inflammation and immune surveillance. Ann Rheum Dis 63 (Suppl. 2), ii84–ii89.[CrossRef]
    [Google Scholar]
  28. Najarro, P., Lee, H.-J., Fox, J., Pease, J. & Smith, G. L. ( 2003; ). Yaba-like disease virus protein 7L is a cell-surface receptor for chemokine CCL1. J Gen Virol 84, 3325–3336.[CrossRef]
    [Google Scholar]
  29. Petkovic, V., Moghini, C., Paoletti, S., Uguccioni, M. & Gerber, B. ( 2004; ). Eotaxin-3/CCL26 is a natural antagonist for CC chemokine receptors 1 and 5. A human chemokine with a regulatory role. J Biol Chem 279, 23357–23363.[CrossRef]
    [Google Scholar]
  30. Qu, C., Edwards, E. W., Tacke, F. & 13 other authors ( 2004; ). Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J Exp Med 200, 1231–1241.[CrossRef]
    [Google Scholar]
  31. Reading, P. C. & Smith, G. L. ( 2003; ). A kinetic analysis of immune mediators in the lungs of mice infected with vaccinia virus and comparison with intradermal infection. J Gen Virol 84, 1973–1983.[CrossRef]
    [Google Scholar]
  32. Reading, P. C., Symons, J. A. & Smith, G. L. ( 2003; ). A soluble chemokine-binding protein from vaccinia virus reduces virus virulence and the inflammatory response to infection. J Immunol 170, 1435–1442.[CrossRef]
    [Google Scholar]
  33. Rosenkilde, M. M., Kledal, T. N. & Schwartz, T. W. ( 2005; ). High constitutive activity of a virus-encoded 7TM receptor in the absence of the conserved DRY motif (Asp-Arg-Tyr) in transmembrane helix 3. Mol Pharmacol 68, 11–19.
    [Google Scholar]
  34. Schaerli, P., Ebert, L., Willimann, K., Blaser, A., Roos, R. S., Loetscher, P. & Moser, B. ( 2004; ). A skin-selective homing mechanism for human immune surveillance T cells. J Exp Med 199, 1265–1275.[CrossRef]
    [Google Scholar]
  35. Seifert, R. & Wenzel-Seifert, K. ( 2002; ). Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366, 381–416.[CrossRef]
    [Google Scholar]
  36. 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]
  37. Symons, J. A., Tscharke, D. C., Price, N. & Smith, G. L. ( 2002; ). A study of the vaccinia virus interferon-γ receptor and its contribution to virus virulence. J Gen Virol 83, 1953–1964.
    [Google Scholar]
  38. Tiffany, H. L., Lautens, L. L., Gao, J.-L., Pease, J., Locati, M., Combadiere, C., Modi, W., Bonner, T. I. & Murphy, P. M. ( 1997; ). Identification of CCR8: a human monocyte and thymus receptor for the CC chemokine I-309. J Exp Med 186, 165–170.[CrossRef]
    [Google Scholar]
  39. Tscharke, D. C. & Smith, G. L. ( 1999; ). A model for vaccinia virus pathogenesis and immunity based on intradermal injection of mouse ear pinnae. J Gen Virol 80, 2751–2755.
    [Google Scholar]
  40. Tscharke, D. C., Reading, P. C. & Smith, G. L. ( 2002; ). Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. J Gen Virol 83, 1977–1986.
    [Google Scholar]
  41. Vanderplasschen, A., Mathew, E., Hollinshead, M., Sim, R. B. & Smith, G. L. ( 1998; ). Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc Natl Acad Sci U S A 95, 7544–7549.[CrossRef]
    [Google Scholar]
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