1887

Abstract

Interferon (IFN)- and - are the main cytokines for innate immune responses against viral infections. To replicate efficiently in the hosts, viruses have evolved various countermeasures to the IFN response. The V protein of measles virus (MV) has been shown to block IFN-/ signalling. Here, the wild-type IC-B strain of MV was shown to grow comparably in the presence and absence of IFN-, whereas replication of the Edmonston tag strain recovered from cloned DNA was strongly suppressed in its presence. The V protein of the IC-B strain, but not the Edmonston tag strain, blocked IFN- signalling. The V protein of the Edmonston strain from the ATCC also inhibited IFN- signalling. There were three amino acid differences between the V proteins of the Edmonston ATCC and tag strains, and substitutions of both residues at positions 110 and 272 were required for the Edmonston ATCC V protein to lose IFN-antagonist activity. The P protein of the IC-B strain, which shares the N-terminal 231 aa residues with the V protein, also inhibited IFN- signalling. Indeed, fragments comprising only those 231 residues of the IC-B and Edmonston ATCC V proteins, but not the Edmonston tag V protein, were able to block IFN- signalling. However, the N-terminal region of the Edmonston tag V protein, when attached to the C-terminal region of the Edmonston ATCC V protein, inhibited IFN- signalling. Taken together, our results indicate that both the N- and C-terminal regions contribute to the IFN-antagonist activity of the MV V protein.

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2004-10-01
2020-08-05
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References

  1. Andrejeva J., Poole E., Young D. F., Goodbourn S., Randall R. E. 2002a; The p127 subunit (DDB1) of the UV-DNA damage repair binding protein is essential for the targeted degradation of STAT1 by the V protein of the paramyxovirus simian virus 5. J Virol 76:11379–11386 [CrossRef]
    [Google Scholar]
  2. Andrejeva J., Young D. F., Goodbourn S., Randall R. E. 2002b; Degradation of STAT1 and STAT2 by the V proteins of simian virus 5 and human parainfluenza virus type 2, respectively: consequences for virus replication in the presence of alpha/beta and gamma interferons. J Virol 76:2159–2167 [CrossRef]
    [Google Scholar]
  3. Aversa G., Chang C.-C., Carballido J. M., Cocks B. G., de Vries J. E. 1997; Engagement of the signaling lymphocytic activation molecule (SLAM) on activated T cells results in IL-2-independent, cyclosporin A-sensitive T cell proliferation and IFN-gamma production. J Immunol 158:4036–4044
    [Google Scholar]
  4. Chatziandreou N., Young D., Andrejeva J., Goodbourn S., Randall R. E. 2002; Differences in interferon sensitivity and biological properties of two related isolates of simian virus 5: a model for virus persistence. Virology 293:234–242 [CrossRef]
    [Google Scholar]
  5. Combredet C., Labrousse V., Mollet L. 7 other authors; 2003; A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol 77:11546–11554 [CrossRef]
    [Google Scholar]
  6. Didcock L., Young D. F., Goodbourn S., Randall R. E. 1999; The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J Virol 73:9928–9933
    [Google Scholar]
  7. Emeny J. M., Morgan M. J. 1979; Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. J Gen Virol 43:247–252 [CrossRef]
    [Google Scholar]
  8. Enders J. F., Peebles T. C. 1954; Propagation in tissue cultures of cytopathic agents from patients with measles. Proc Soc Exp Biol Med 86:277–286 [CrossRef]
    [Google Scholar]
  9. Erlenhoefer C., Wurzer W. J., Loffler S., Schneider-Schaulies S., ter Meulen V., Schneider-Schaulies J. 2001; CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J Virol 75:4499–4505 [CrossRef]
    [Google Scholar]
  10. Escoffier C., Manie S., Vincent S., Muller C. P., Billeter M., Gerlier D. 1999; Nonstructural C protein is required for efficient measles virus replication in human peripheral blood cells. J Virol 73:1695–1698
    [Google Scholar]
  11. Garcia-Sastre A. 2001; Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279:375–384 [CrossRef]
    [Google Scholar]
  12. Garcin D., Marq J. B., Strahle L., le Mercier P., Kolakofsky D. 2002; All four Sendai virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295:256–265 [CrossRef]
    [Google Scholar]
  13. Goodbourn S., Didcock L., Randall R. E. 2000; Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341–2364
    [Google Scholar]
  14. Gotoh B., Komatsu T., Takeuchi K., Yokoo J. 2002; Paramyxovirus strategies for evading the interferon response. Rev Med Virol 12:337–357 [CrossRef]
    [Google Scholar]
  15. Griffin D. 2001; Measles virus. In Fields Virology , 4th edn. pp  1401–1441 Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott, Williams & Wilkins;
    [Google Scholar]
  16. He B., Paterson R. G., Stock N., Durbin J. E., Durbin R. K., Goodbourn S., Randall R. E., Lamb R. A. 2002; Recovery of paramyxovirus simian virus 5 with a V protein lacking the conserved cysteine-rich domain: the multifunctional V protein blocks both interferon- β induction and interferon signaling. Virology 303:15–32 [CrossRef]
    [Google Scholar]
  17. Horton R. M., Cai Z. L., Ho S. N., Pease L. R. 1990; Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528–535
    [Google Scholar]
  18. Hsu E., Iorio C., Sarangi F., Khine A., Richardson C. 2001; CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279:9–21 [CrossRef]
    [Google Scholar]
  19. Kato A., Ohnishi Y., Kohase M., Saito S., Tashiro M., Nagai Y. 2001; Y2, the smallest of the Sendai virus C proteins, is fully capable of both counteracting the antiviral action of interferons and inhibiting viral RNA synthesis. J Virol 75:3802–3810 [CrossRef]
    [Google Scholar]
  20. Katze M. G., He Y., Gale M. J. 2002; Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2:675–687 [CrossRef]
    [Google Scholar]
  21. Kobune F., Sakata H., Sugiura A. 1990; Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J Virol 64:700–705
    [Google Scholar]
  22. Kobune F., Takahashi H., Terao K. 7 other authors 1996; Nonhuman primate models of measles. Lab Anim Sci 46:315–320
    [Google Scholar]
  23. Kubota T., Yokosawa N., Yokota S., Fujii N. 2001; C terminal CYS-RICH region of mumps virus structural V protein correlates with block of interferon α and γ signal transduction pathway through decrease of STAT 1- α . Biochem Biophys Res Commun 283:255–259 [CrossRef]
    [Google Scholar]
  24. Manchester M., Eto D. S., Valsamakis A., Liton P. B., Fernandez-Munoz R., Rota P. A., Bellini W. J., Forthal D. N., Oldstone M. B. A. 2000; Clinical isolates of measles virus use CD46 as a cellular receptor. J Virol 74:3967–3974 [CrossRef]
    [Google Scholar]
  25. Naniche D., Yeh A., Eto D., Manchester M., Friedman R. M., Oldstone M. B. 2000; Evasion of host defenses by measles virus: wild-type measles virus infection interferes with induction of alpha/beta interferon production. J Virol 74:7478–7484 [CrossRef]
    [Google Scholar]
  26. Nishio M., Tsurudome M., Ito M., Kawano M., Komada H., Ito Y. 2001; High resistance of human parainfluenza type 2 virus protein-expressing cells to the antiviral and anti-cell proliferative activities of alpha/beta interferons: cysteine-rich V-specific domain is required for high resistance to the interferons. J Virol 75:9165–9176 [CrossRef]
    [Google Scholar]
  27. Nishio M., Garcin D., Simonet V., Kolakofsky D. 2002; The carboxyl segment of the mumps virus V protein associates with Stat proteins in vitro via a tryptophan-rich motif. Virology 300:92–99 [CrossRef]
    [Google Scholar]
  28. Niwa H., Yamamura K., Miyazaki J. 1991; Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199 [CrossRef]
    [Google Scholar]
  29. Ono N., Tatsuo H., Hidaka Y., Aoki T., Minagawa H., Yanagi Y. 2001; Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75:4399–4401 [CrossRef]
    [Google Scholar]
  30. Palosaari H., Parisien J. P., Rodriguez J. J., Ulane C. M., Horvath C. M. 2003; STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J Virol 77:7635–7644 [CrossRef]
    [Google Scholar]
  31. Parisien J. P., Lau J. F., Rodriguez J. J., Sullivan B. M., Moscona A., Parks G. D., Lamb R. A., Horvath C. M. 2001; The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 283:230–239 [CrossRef]
    [Google Scholar]
  32. Park M. S., Shaw M. L., Munoz-Jordan J., Cros J. F., Nakaya T., Bouvier N., Palese P., Garcia-Sastre A., Basler C. F. 2003; Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J Virol 77:1501–1511 [CrossRef]
    [Google Scholar]
  33. Parks C. L., Lerch R. A., Walpita P., Wang H. P., Sidhu M. S., Udem S. A. 2001; Comparison of predicted amino acid sequences of measles virus strains in the Edmonston vaccine lineage. J Virol 75:910–920 [CrossRef]
    [Google Scholar]
  34. Patterson J. B., Thomas D., Lewicki H., Billeter M. A., Oldstone M. B. 2000; V and C proteins of measles virus function as virulence factors in vivo . Virology 267:80–89 [CrossRef]
    [Google Scholar]
  35. Poole E., He B., Lamb R. A., Randall R. E., Goodbourn S. 2002; The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon- β . Virology 303:33–46 [CrossRef]
    [Google Scholar]
  36. Radecke F., Spielhofer P., Schneider H., Kaelin K., Huber M., Dotsch C., Christiansen G., Billeter M. A. 1995; Rescue of measles viruses from cloned DNA. EMBO J 14:5773–5784
    [Google Scholar]
  37. Rodriguez J. J., Parisien J. P., Horvath C. M. 2002; Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J Virol 76:11476–11483 [CrossRef]
    [Google Scholar]
  38. Rodriguez J. J., Wang L. F., Horvath C. M. 2003; Hendra virus V protein inhibits interferon signaling by preventing STAT1 and STAT2 nuclear accumulation. J Virol 77:11842–11845 [CrossRef]
    [Google Scholar]
  39. Saito S., Ogino T., Miyajima N., Kato A., Kohase M. 2002; Dephosphorylation failure of tyrosine-phosphorylated STAT1 in IFN-stimulated Sendai virus C protein-expressing cells. Virology 293:205–209 [CrossRef]
    [Google Scholar]
  40. Schneider H., Kaelin K., Billeter M. A. 1997; Recombinant measles viruses defective for RNA editing and V protein synthesis are viable in cultured cells. Virology 227:314–322 [CrossRef]
    [Google Scholar]
  41. Schneider U., von Messling V., Devaux P., Cattaneo R. 2002; Efficiency of measles virus entry and dissemination through different receptors. J Virol 76:7460–7467 [CrossRef]
    [Google Scholar]
  42. Shaffer J. A., Bellini W. J., Rota P. A. 2003; The C protein of measles virus inhibits the type I interferon response. Virology 315:389–397 [CrossRef]
    [Google Scholar]
  43. Takeda M., Kato A., Kobune F., Sakata H., Li Y., Shioda T., Sakai Y., Asakawa M., Nagai Y. 1998; Measles virus attenuation associated with transcriptional impediment and a few amino acid changes in the polymerase and accessory proteins. J Virol 72:8690–8696
    [Google Scholar]
  44. Takeda M., Takeuchi K., Miyajima N., Kobune F., Ami Y., Nagata N., Suzaki Y., Nagai Y., Tashiro M. 2000; Recovery of pathogenic measles virus from cloned cDNA. J Virol 74:6643–6647 [CrossRef]
    [Google Scholar]
  45. Takeuchi K., Miyajima N., Kobune F., Tashiro M. 2000; Comparative nucleotide sequence analyses of the entire genomes of B95a cell-isolated and Vero cell-isolated measles viruses from the same patient. Virus Genes 20:253–257 [CrossRef]
    [Google Scholar]
  46. Takeuchi K., Kadota S. I., Takeda M., Miyajima N., Nagata K. 2003; Measles virus V protein blocks interferon (IFN)- α / β but not IFN- γ signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett 545:177–182 [CrossRef]
    [Google Scholar]
  47. Tatsuo H., Okuma K., Tanaka K., Ono N., Minagawa H., Takade A., Matsuura Y., Yanagi Y. 2000a; Virus entry is a major determinant of cell tropism of Edmonston and wild-type strains of measles virus as revealed by vesicular stomatitis virus pseudotypes bearing their envelope proteins. J Virol 74:4139–4145 [CrossRef]
    [Google Scholar]
  48. Tatsuo H., Ono N., Tanaka K., Yanagi Y. 2000b; SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893–897 [CrossRef]
    [Google Scholar]
  49. Tober C., Seufert M., Schneider H., Billeter M. A., Johnston I. C., Niewiesk S., ter Meulen V., Schneider-Schaulies S. 1998; Expression of measles virus V protein is associated with pathogenicity and control of viral RNA synthesis. J Virol 72:8124–8132
    [Google Scholar]
  50. Valsamakis A., Schneider H., Auwaerter P. G., Kaneshima H., Billeter M. A., Griffin D. E. 1998; Recombinant measles viruses with mutations in the C, V, or F gene have altered growth phenotypes in vivo. J Virol 72:7754–7761
    [Google Scholar]
  51. Wang I. M., Blanco J. C., Tsai S. Y., Tsai M. J., Ozato K. 1996; Interferon regulatory factors and TFIIB cooperatively regulate interferon-responsive promoter activity in vivo and in vitro. Mol Cell Biol 16:6313–6324
    [Google Scholar]
  52. Wansley E. K., Parks G. D. 2002; Naturally occurring substitutions in the P/V gene convert the noncytopathic paramyxovirus simian virus 5 into a virus that induces alpha/beta interferon synthesis and cell death. J Virol 76:10109–10121 [CrossRef]
    [Google Scholar]
  53. Yanagi Y., Cubitt B. A., Oldstone M. B. A. 1992; Measles virus inhibits mitogen-induced T cell proliferation but does not directly perturb the T cell activation process inside the cell. Virology 187:280–289 [CrossRef]
    [Google Scholar]
  54. Yanagi Y., Ono N., Tatsuo H., Hashimoto K., Minagawa H. 2002; Measles virus receptor SLAM (CD150). Virology 299:155–161 [CrossRef]
    [Google Scholar]
  55. Yokota S., Saito H., Kubota T., Yokosawa N., Amano K., Fujii N. 2003; Measles virus suppresses interferon- α signaling pathway: suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon- α receptor complex. Virology 306:135–146 [CrossRef]
    [Google Scholar]
  56. Young D. F., Chatziandreou N., He B., Goodbourn S., Lamb R. A., Randall R. E. 2001; Single amino acid substitution in the V protein of simian virus 5 differentiates its ability to block interferon signaling in human and murine cells. J Virol 75:3363–3370 [CrossRef]
    [Google Scholar]
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