1887

Abstract

Interferon (IFN) induces an antiviral state in cells that results in alterations of the patterns and levels of parainfluenza virus type 5 (PIV5) transcripts and proteins. This study reports that IFN-stimulated gene 56/IFN-induced protein with tetratricopeptide repeats 1 (ISG56/IFIT1) is primarily responsible for these effects of IFN. It was shown that treating cells with IFN after infection resulted in an increase in virus transcription but an overall decrease in virus protein synthesis. As there was no obvious decrease in the overall levels of cellular protein synthesis in infected cells treated with IFN, these results suggested that ISG56/IFIT1 selectively inhibits the translation of viral mRNAs. This conclusion was supported by translation studies. Previous work has shown that ISG56/IFIT1 can restrict the replication of viruses lacking a 2′--methyltransferase activity, an enzyme that methylates the 2′-hydroxyl group of ribose sugars in the 5′-cap structures of mRNA. However, the data in the current study strongly suggested that PIV5 mRNAs are methylated at the 2′-hydroxyl group and thus that ISG56/IFIT1 selectively inhibits the translation of PIV5 mRNA by some as yet unrecognized mechanism. It was also shown that ISG56/IFIT1 is primarily responsible for the IFN-induced inhibition of PIV5.

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2013-01-01
2019-10-13
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References

  1. Andrejeva J., Childs K. S., Young D. F., Carlos T. S., Stock N., Goodbourn S., Randall R. E.. ( 2004;). The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. . Proc Natl Acad Sci U S A 101:, 17264–17269. [CrossRef][PubMed]
    [Google Scholar]
  2. Carlos T. S., Fearns R., Randall R. E.. ( 2005;). Interferon-induced alterations in the pattern of parainfluenza virus 5 transcription and protein synthesis and the induction of virus inclusion bodies. . J Virol 79:, 14112–14121. [CrossRef][PubMed]
    [Google Scholar]
  3. Carlos T. S., Young D., Stertz S., Kochs G., Randall R. E.. ( 2007;). Interferon-induced inhibition of parainfluenza virus type 5; the roles of MxA, PKR and oligo A synthetase/RNase L. . Virology 363:, 166–173. [CrossRef][PubMed]
    [Google Scholar]
  4. Carlos T. S., Young D. F., Schneider M., Simas J. P., Randall R. E.. ( 2009;). Parainfluenza virus 5 genomes are located in viral cytoplasmic bodies whilst the virus dismantles the interferon-induced antiviral state of cells. . J Gen Virol 90:, 2147–2156. [CrossRef][PubMed]
    [Google Scholar]
  5. Chatziandreou N., Young D., Andrejeva J., Goodbourn S., Randall R. E.. ( 2002a;). 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][PubMed]
    [Google Scholar]
  6. Chatziandreou N., Young D. F., Andrejeva J., Goodbourn S., Randall R. E.. ( 2002b;). 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][PubMed]
    [Google Scholar]
  7. Chen S., Short J. A., Young D. F., Killip M. J., Schneider M., Goodbourn S., Randall R. E.. ( 2010;). Heterocellular induction of interferon by negative-sense RNA viruses. . Virology 407:, 247–255. [CrossRef][PubMed]
    [Google Scholar]
  8. Childs K. S., Andrejeva J., Randall R. E., Goodbourn S.. ( 2009;). Mechanism of mda-5 inhibition by paramyxovirus V proteins. . J Virol 83:, 1465–1473. [CrossRef][PubMed]
    [Google Scholar]
  9. Childs K., Randall R., Goodbourn S.. ( 2012;). Paramyxovirus V proteins interact with the RNA Helicase LGP2 to inhibit RIG-I-dependent interferon induction. . J Virol 86:, 3411–3421. [CrossRef][PubMed]
    [Google Scholar]
  10. Daffis S., Szretter K. J., Schriewer J., Li J., Youn S., Errett J., Lin T. Y., Schneller S., Zust R.. & other authors ( 2010;). 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. . Nature 468:, 452–456. [CrossRef][PubMed]
    [Google Scholar]
  11. 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.[PubMed]
    [Google Scholar]
  12. Everett R. D., Murray J., Orr A., Preston C. M.. ( 2007;). Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. . J Virol 81:, 10991–11004. [CrossRef][PubMed]
    [Google Scholar]
  13. Fearns R., Young D. F., Randall R. E.. ( 1994;). Evidence that the paramyxovirus simian virus 5 can establish quiescent infections by remaining inactive in cytoplasmic inclusion bodies. . J Gen Virol 75:, 3525–3539. [CrossRef][PubMed]
    [Google Scholar]
  14. Fensterl V., Sen G. C.. ( 2011;). The ISG56/IFIT1 gene family. . J Interferon Cytokine Res 31:, 71–78. [CrossRef][PubMed]
    [Google Scholar]
  15. Ferron F., Longhi S., Henrissat B., Canard B.. ( 2002;). Viral RNA-polymerases – a predicted 2′-O-ribose methyltransferase domain shared by all Mononegavirales. . Trends Biochem Sci 27:, 222–224. [CrossRef][PubMed]
    [Google Scholar]
  16. Furuichi Y., Shatkin A. J.. ( 2000;). Viral and cellular mRNA capping: past and prospects. . Adv Virus Res 55:, 135–184. [CrossRef][PubMed]
    [Google Scholar]
  17. Goodbourn S., Randall R. E.. ( 2009;). The regulation of type I interferon production by paramyxoviruses. . J Interferon Cytokine Res 29:, 539–547. [CrossRef][PubMed]
    [Google Scholar]
  18. Guo J., Hui D. J., Merrick W. C., Sen G. C.. ( 2000;). A new pathway of translational regulation mediated by eukaryotic initiation factor 3. . EMBO J 19:, 6891–6899. [CrossRef][PubMed]
    [Google Scholar]
  19. Hilton L., Moganeradj K., Zhang G., Chen Y. H., Randall R. E., McCauley J. W., Goodbourn S.. ( 2006;). The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. . J Virol 80:, 11723–11732. [CrossRef][PubMed]
    [Google Scholar]
  20. Killip M. J., Young D. F., Ross C. S., Chen S., Goodbourn S., Randall R. E.. ( 2011;). Failure to activate the IFN-β promoter by a paramyxovirus lacking an interferon antagonist. . Virology 415:, 39–46. [CrossRef][PubMed]
    [Google Scholar]
  21. Killip M. J., Young D. F., Precious B. L., Goodbourn S., Randall R. E.. ( 2012;). Activation of the beta interferon promoter by paramyxoviruses in the absence of virus protein synthesis. . J Gen Virol 93:, 299–307. [CrossRef][PubMed]
    [Google Scholar]
  22. Kumar H., Kawai T., Akira S.. ( 2011;). Pathogen recognition by the innate immune system. . Int Rev Immunol 30:, 16–34. [CrossRef][PubMed]
    [Google Scholar]
  23. Lamb R. A., Parks G. D.. ( 2007;). Paramyxoviridae: the viruses and their replication. . In Fields Virology, , 5th edn., pp. 1449–1496. Edited by Knipe D. M., Howley P. M., Griffin D. E., Martin M. A., Lamb R. A., Roizman B., Straus S. E... Philadelphia:: Lippincott Williams & Wilkins;.
    [Google Scholar]
  24. Li Y., Li C., Xue P., Zhong B., Mao A. P., Ran Y., Chen H., Wang Y. Y., Yang F., Shu H. B.. ( 2009;). ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. . Proc Natl Acad Sci U S A 106:, 7945–7950. [CrossRef][PubMed]
    [Google Scholar]
  25. Lin Y., Horvath F., Aligo J. A., Wilson R., He B.. ( 2005;). The role of simian virus 5 V protein on viral RNA synthesis. . Virology 338:, 270–280. [CrossRef][PubMed]
    [Google Scholar]
  26. Lu L. L., Puri M., Horvath C. M., Sen G. C.. ( 2008;). Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of kappaB kinase ϵ (IKKe)/TBK1. . J Biol Chem 283:, 14269–14276. [CrossRef][PubMed]
    [Google Scholar]
  27. Murphy A. M., Moerdyk-Schauwecker M., Mushegian A., Grdzelishvili V. Z.. ( 2010;). Sequence-function analysis of the Sendai virus L protein domain VI. . Virology 405:, 370–382. [CrossRef][PubMed]
    [Google Scholar]
  28. Parisien J. P., Lau J. F., Rodriguez J. J., Ulane C. M., Horvath C. M.. ( 2002;). Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. . J Virol 76:, 4190–4198. [CrossRef][PubMed]
    [Google Scholar]
  29. Parks G. D., Manuse M. J., Johnson J. B.. ( 2011;). The parainfluenza virus simian virus 5. . In The Biology of Paramyxoviruses, pp. 37–68. Edited by Samal S. K... Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  30. Pichlmair A., Lassnig C., Eberle C. A., Górna M. W., Baumann C. L., Burkard T. R., Bürckstümmer T., Stefanovic A., Krieger S.. & other authors ( 2011;). IFIT1 is an antiviral protein that recognizes 5′-triphosphate RNA. . Nat Immunol 12:, 624–630. [CrossRef][PubMed]
    [Google Scholar]
  31. Precious B., Young D. F., Bermingham A., Fearns R., Ryan M., Randall R. E.. ( 1995;). Inducible expression of the P, V, and NP genes of the paramyxovirus simian virus 5 in cell lines and an examination of NP-P and NP-V interactions. . J Virol 69:, 8001–8010.[PubMed]
    [Google Scholar]
  32. Precious B., Childs K., Fitzpatrick-Swallow V., Goodbourn S., Randall R. E.. ( 2005;). Simian virus 5 V protein acts as an adaptor, linking DDB1 to STAT2, to facilitate the ubiquitination of STAT1. . J Virol 79:, 13434–13441. [CrossRef][PubMed]
    [Google Scholar]
  33. Precious B. L., Carlos T. S., Goodbourn S., Randall R. E.. ( 2007;). Catalytic turnover of STAT1 allows PIV5 to dismantle the interferon-induced anti-viral state of cells. . Virology 368:, 114–121. [CrossRef][PubMed]
    [Google Scholar]
  34. Ramachandran A., Horvath C. M.. ( 2009;). Paramyxovirus disruption of interferon signal transduction: STATus report. . J Interferon Cytokine Res 29:, 531–537. [CrossRef][PubMed]
    [Google Scholar]
  35. Randall R. E., Goodbourn S.. ( 2008;). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. . J Gen Virol 89:, 1–47. [CrossRef][PubMed]
    [Google Scholar]
  36. Randall R. E., Young D. F., Goswami K. K., Russell W. C.. ( 1987;). Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. . J Gen Virol 68:, 2769–2780. [CrossRef][PubMed]
    [Google Scholar]
  37. Schmidt A., Endres S., Rothenfusser S.. ( 2011;). Pattern recognition of viral nucleic acids by RIG-I-like helicases. . J Mol Med (Berl) 89:, 5–12. [CrossRef][PubMed]
    [Google Scholar]
  38. Schnierle B. S., Gershon P. D., Moss B.. ( 1992;). Cap-specific mRNA (nucleoside-O2′-)-methyltransferase and poly(A) polymerase stimulatory activities of vaccinia virus are mediated by a single protein. . Proc Natl Acad Sci U S A 89:, 2897–2901. [CrossRef][PubMed]
    [Google Scholar]
  39. Terenzi F., Pal S., Sen G. C.. ( 2005;). Induction and mode of action of the viral stress-inducible murine proteins, P56 and P54. . Virology 340:, 116–124. [CrossRef][PubMed]
    [Google Scholar]
  40. Terenzi F., Saikia P., Sen G. C.. ( 2008;). Interferon-inducible protein, P56, inhibits HPV DNA replication by binding to the viral protein E1. . EMBO J 27:, 3311–3321. [CrossRef][PubMed]
    [Google Scholar]
  41. Young D. F., Andrejeva L., Livingstone A., Goodbourn S., Lamb R. A., Collins P. L., Elliott R. M., Randall R. E.. ( 2003;). Virus replication in engineered human cells that do not respond to interferons. . J Virol 77:, 2174–2181. [CrossRef][PubMed]
    [Google Scholar]
  42. Züst R., Cervantes-Barragan L., Habjan M., Maier R., Neuman B. W., Ziebuhr J., Szretter K. J., Baker S. C., Barchet W.. & other authors ( 2011;). Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. . Nat Immunol 12:, 137–143. [CrossRef][PubMed]
    [Google Scholar]
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