1887

Abstract

Poxviruses encode up to four different soluble TNF receptors, named cytokine response modifier B (CrmB), CrmC, CrmD and CrmE. These proteins mimic the extracellular domain of the cellular TNF receptors to bind and inhibit the activity of TNF and, in some cases, other TNF superfamily ligands. Most of these ligands are released after the enzymic cleavage of a membrane precursor. However, transmembrane TNF (tmTNF) is not only a precursor of soluble TNF but also exerts specific pro-inflammatory and immunological activities. Here, we report that viral TNF receptors bound and inhibited tmTNF and describe some interesting differences in their activity against the soluble cytokine. Thus, CrmE, which does not inhibit mouse soluble TNF, could block murine tmTNF-induced cytotoxicity. We propose that this anti-tmTNF effect should be taken into consideration when assessing the role of viral TNF decoy receptors in the pathogenesis of poxvirus.

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2015-10-01
2024-04-19
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References

  1. Aggarwal B.B. 2003; Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol 3:745–756 [View Article][PubMed]
    [Google Scholar]
  2. Alcami A. 2003; Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 3:36–50 [View Article][PubMed]
    [Google Scholar]
  3. Alejo A., Ruiz-Argüello M.B., Ho Y., Smith V.P., Saraiva M., Alcami A. 2006; A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Proc Natl Acad Sci U S A 103:5995–6000 [View Article][PubMed]
    [Google Scholar]
  4. Alejo A., Pontejo S.M., Alcami A. 2011; Poxviral TNFRs: properties and role in viral pathogenesis. Adv Exp Med Biol 691:203–210 [View Article][PubMed]
    [Google Scholar]
  5. Allenbach C., Launois P., Mueller C., Tacchini-Cottier F. 2008; An essential role for transmembrane TNF in the resolution of the inflammatory lesion induced by Leishmania major infection. Eur J Immunol 38:720–731 [View Article][PubMed]
    [Google Scholar]
  6. Alzhanova D., Früh K. 2010; Modulation of the host immune response by cowpox virus. Microbes Infect 12:900–909 [View Article][PubMed]
    [Google Scholar]
  7. Black R.A., Rauch C.T., Kozlosky C.J., Peschon J.J., Slack J.L., Wolfson M.F., Castner B.J., Stocking K.L., Reddy P., other authors. 1997; A metalloproteinase disintegrin that releases tumour-necrosis factor-α from cells. Nature 385:729–733 [View Article][PubMed]
    [Google Scholar]
  8. Cabal-Hierro L., Lazo P.S. 2012; Signal transduction by tumor necrosis factor receptors. Cell Signal 24:1297–1305 [View Article][PubMed]
    [Google Scholar]
  9. Crowe P.D., VanArsdale T.L., Walter B.N., Ware C.F., Hession C., Ehrenfels B., Browning J.L., Din W.S., Goodwin R.G., Smith C.A. 1994; A lymphotoxin-β-specific receptor. Science 264:707–710 [View Article][PubMed]
    [Google Scholar]
  10. DeBerge M.P., Ely K.H., Enelow R.I. 2014; Soluble, but not transmembrane, TNF-α is required during influenza infection to limit the magnitude of immune responses and the extent of immunopathology. J Immunol 192:5839–5851 [View Article][PubMed]
    [Google Scholar]
  11. Eissner G., Kolch W., Scheurich P. 2004; Ligands working as receptors: reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Cytokine Growth Factor Rev 15:353–366 [View Article][PubMed]
    [Google Scholar]
  12. Fenner F. 1993; Smallpox: emergence, global spread, and eradication. In Hist Philos Life Sci 15397–420[PubMed]
    [Google Scholar]
  13. Georgopoulos S., Plows D., Kollias G. 1996; Transmembrane TNF is sufficient to induce localized tissue toxicity and chronic inflammatory arthritis in transgenic mice. In J Inflamm 4686–97[PubMed]
    [Google Scholar]
  14. Graham S.C., Bahar M.W., Abrescia N.G., Smith G.L., Stuart D.I., Grimes J.M. 2007; Structure of CrmE, a virus-encoded tumour necrosis factor receptor. J Mol Biol 372:660–671 [View Article][PubMed]
    [Google Scholar]
  15. Grell M., Douni E., Wajant H., Löhden M., Clauss M., Maxeiner B., Georgopoulos S., Lesslauer W., Kollias G., other authors. 1995; The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 83:793–802 [View Article][PubMed]
    [Google Scholar]
  16. Horiuchi T., Mitoma H., Harashima S., Tsukamoto H., Shimoda T. 2010; Transmembrane TNF-α: structure, function and interaction with anti-TNF agents. Rheumatology (Oxford) 49:1215–1228 [View Article][PubMed]
    [Google Scholar]
  17. Hu F.Q., Smith C.A., Pickup D.J. 1994; Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 204:343–356 [View Article][PubMed]
    [Google Scholar]
  18. Ierna M.X., Scales H.E., Mueller C., Lawrence C.E. 2009; Transmembrane tumor necrosis factor alpha is required for enteropathy and is sufficient to promote parasite expulsion in gastrointestinal helminth infection. Infect Immun 77:3879–3885 [View Article][PubMed]
    [Google Scholar]
  19. Lazdins J.K., Grell M., Walker M.R., Woods-Cook K., Scheurich P., Pfizenmaier K. 1997; Membrane tumor necrosis factor (TNF) induced cooperative signaling of TNFR60 and TNFR80 favors induction of cell death rather than virus production in HIV-infected T cells. J Exp Med 185:81–90 [View Article][PubMed]
    [Google Scholar]
  20. Loparev V.N., Parsons J.M., Knight J.C., Panus J.F., Ray C.A., Buller R.M., Pickup D.J., Esposito J.J. 1998; A third distinct tumor necrosis factor receptor of orthopoxviruses. Proc Natl Acad Sci U S A 95:3786–3791 [View Article][PubMed]
    [Google Scholar]
  21. Lu F., Fang J., Chen C.Q. 2001; TNF receptor-associated factor-2 binding site is involved in TNFR75-dependent enhancement of TNFR55-induced cell death. Cell Res 11:217–222 [View Article][PubMed]
    [Google Scholar]
  22. Mavian C., López-Bueno A., Bryant N.A., Seeger K., Quail M.A., Harris D., Barrell B., Alcami A. 2014; The genome sequence of ectromelia virus Naval and Cornell isolates from outbreaks in North America. Virology 462-463:218–226 [View Article][PubMed]
    [Google Scholar]
  23. Monastra G., Cabrelle A., Zambon A., Rosato A., Macino B., Collavo D., Zanovello P. 1996; Membrane form of TNF-α induces both cell lysis and apoptosis in susceptible target cells. Cell Immunol 171:102–110 [View Article][PubMed]
    [Google Scholar]
  24. Mueller C., Corazza N., Trachsel-Løseth S., Eugster H.P., Bühler-Jungo M., Brunner T., Imboden M.A. 1999; Noncleavable transmembrane mouse tumor necrosis factor-α (TNFα) mediates effects distinct from those of wild-type TNFα in vitro and in vivo . J Biol Chem 274:38112–38118 [View Article][PubMed]
    [Google Scholar]
  25. Olleros M.L., Guler R., Corazza N., Vesin D., Eugster H.P., Marchal G., Chavarot P., Mueller C., Garcia I. 2002; Transmembrane TNF induces an efficient cell-mediated immunity and resistance to Mycobacterium bovis bacillus Calmette-Guérin infection in the absence of secreted TNF and lymphotoxin-α. J Immunol 168:3394–3401 [View Article][PubMed]
    [Google Scholar]
  26. Olleros M.L., Guler R., Vesin D., Parapanov R., Marchal G., Martinez-Soria E., Corazza N., Pache J.C., Mueller C., Garcia I. 2005; Contribution of transmembrane tumor necrosis factor to host defense against Mycobacterium bovis bacillus Calmette-Guerin and Mycobacterium tuberculosis infections. Am J Pathol 166:1109–1120 [View Article][PubMed]
    [Google Scholar]
  27. Palumbo G.J., Buller R.M., Glasgow W.C. 1994; Multigenic evasion of inflammation by poxviruses. J Virol 68:1737–1749[PubMed]
    [Google Scholar]
  28. Perez C., Albert I., DeFay K., Zachariades N., Gooding L., Kriegler M. 1990; A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell 63:251–258 [View Article][PubMed]
    [Google Scholar]
  29. Pontejo S.M., Alejo A., Alcami A. 2015; Comparative biochemical and functional analysis of viral and human secreted TNF decoy receptors. J Biol Chem 290:15973–15984 [View Article][PubMed]
    [Google Scholar]
  30. Reading P.C., Khanna A., Smith G.L. 2002; Vaccinia virus CrmE encodes a soluble and cell surface tumor necrosis factor receptor that contributes to virus virulence. Virology 292:285–298 [View Article][PubMed]
    [Google Scholar]
  31. Ribas G., Rivera J., Saraiva M., Campbell R.D., Alcami A. 2003; Genetic variability of immunomodulatory genes in ectromelia virus isolates detected by denaturing high-performance liquid chromatography. J Virol 77:10139–10146 [View Article][PubMed]
    [Google Scholar]
  32. Saraiva M., Alcami A. 2001; CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. J Virol 75:226–233 [View Article][PubMed]
    [Google Scholar]
  33. Smith C.A., Hu F.Q., Smith T.D., Richards C.L., Smolak P., Goodwin R.G., Pickup D.J. 1996; Cowpox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LTα. Virology 223:132–147 [View Article][PubMed]
    [Google Scholar]
  34. Torres D., Janot L., Quesniaux V.F., Grivennikov S.I., Maillet I., Sedgwick J.D., Ryffel B., Erard F. 2005; Membrane tumor necrosis factor confers partial protection to Listeria infection. Am J Pathol 167:1677–1687 [View Article][PubMed]
    [Google Scholar]
  35. Upton C., Macen J.L., Schreiber M., McFadden G. 1991; Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence. Virology 184:370–382 [View Article][PubMed]
    [Google Scholar]
  36. Zhang X.M., Weber I., Chen M.J. 1992; Site-directed mutational analysis of human tumor necrosis factor-α receptor binding site and structure–functional relationship. J Biol Chem 267:24069–24075[PubMed]
    [Google Scholar]
  37. Zheng F., Liu N., Chen Q., Yang L., Liu L., Xiong P., Feng W., Jiang X., Gong F., Li Z. 2009; Leader sequence is required for activity of transmembrane tumor necrosis factor-α. Mol Immunol 46:3336–3344 [View Article][PubMed]
    [Google Scholar]
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