1887

Abstract

The V proteins of paramyxoviruses are composed of two evolutionarily distinct domains, the N-terminal 75 % being common to the viral P, V and W proteins, and not highly conserved between viruses, whilst the remaining 25 % consists of a cysteine-rich V-specific domain, which is conserved across almost all paramyxoviruses. There is evidence supporting a number of different functions of the V proteins of morbilliviruses in blocking the signalling pathways of type I and II IFNs, but it is not clear which domains of V are responsible for which activities and whether all these activities are required for effective blockade of IFN signalling. We have shown here that the two domains of rinderpest virus V protein have distinct functions: the N-terminal domain acted to bind STAT1, whilst the C-terminal V-specific domain interacted with the IFN receptor-associated kinases Jak1 and Tyk2. Effective blockade of IFN signalling required the intact V protein.

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2014-01-01
2021-03-03
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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-beta promoter. Proc Natl Acad Sci U S A 101:17264–17269 [CrossRef][PubMed]
    [Google Scholar]
  2. Boxer E. L., Nanda S. K., Baron M. D. 2009; The rinderpest virus non-structural C protein blocks the induction of type 1 interferon. Virology 385:134–142 [CrossRef][PubMed]
    [Google Scholar]
  3. Caignard G., Guerbois M., Labernardière J. L., Jacob Y., Jones L. M., Wild F., Tangy F., Vidalain P. O. Infectious Mapping Project I-MAP 2007; Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368:351–362 [CrossRef][PubMed]
    [Google Scholar]
  4. Caignard G., Bouraï M., Jacob Y., Tangy F., Vidalain P. O. Infection-MAPping project I-MAP 2009; Inhibition of IFN-alpha/beta signaling by two discrete peptides within measles virus V protein that specifically bind STAT1 and STAT2. Virology 383:112–120 [CrossRef][PubMed]
    [Google Scholar]
  5. Cattaneo R., Kaelin K., Baczko K., Billeter M. A. 1989; Measles virus editing provides an additional cysteine-rich protein. Cell 56:759–764 [CrossRef][PubMed]
    [Google Scholar]
  6. Chinnakannan S. K., Nanda S. K., Baron M. D. 2013; Morbillivirus V proteins exhibit multiple mechanisms to block type 1 and type 2 interferon signalling pathways. PLoS ONE 8:e57063 [CrossRef][PubMed]
    [Google Scholar]
  7. Conzelmann K.-K. 2005; Transcriptional activation of alpha/beta interferon genes: interference by nonsegmented negative-strand RNA viruses. J Virol 79:5241–5248 [CrossRef][PubMed]
    [Google Scholar]
  8. Demaison C., Parsley K., Brouns G., Scherr M., Battmer K., Kinnon C., Grez M., Thrasher A. J. 2002; High-level transduction and gene expression in hematopoietic repopulating cells using a human imunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13:803–813 [CrossRef][PubMed]
    [Google Scholar]
  9. Devaux P., von Messling V., Songsungthong W., Springfeld C., Cattaneo R. 2007; Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72–83 [CrossRef][PubMed]
    [Google Scholar]
  10. Devaux P., Hodge G., McChesney M. B., Cattaneo R. 2008; Attenuation of V- or C-defective measles viruses: infection control by the inflammatory and interferon responses of rhesus monkeys. J Virol 82:5359–5367 [CrossRef][PubMed]
    [Google Scholar]
  11. Domanski P., Yan H., Witte M. M., Krolewski J., Colamonici O. R. 1995; Homodimerization and intermolecular tyrosine phosphorylation of the Tyk-2 tyrosine kinase. FEBS Lett 374:317–322 [CrossRef][PubMed]
    [Google Scholar]
  12. Eilers A., Kanda K., Klose B., Krolewski J., Decker T. 1996; Constitutive STAT1 tyrosine phosphorylation in U937 monocytes overexpressing the TYK2 protein tyrosine kinase does not induce gene transcription. Cell Growth Differ 7:833–840[PubMed]
    [Google Scholar]
  13. Fontana J. M., Bankamp B., Rota P. A. 2008; Inhibition of interferon induction and signaling by paramyxoviruses. Immunol Rev 225:46–67 [CrossRef][PubMed]
    [Google Scholar]
  14. Goodbourn S., Randall R. E. 2009; The regulation of type I interferon production by paramyxoviruses. J Interferon Cytokine Res 29:539–548 [CrossRef][PubMed]
    [Google Scholar]
  15. Gotoh B., Komatsu T., Takeuchi K., Yokoo J. 2002; Paramyxovirus strategies for evading the interferon response. Rev Med Virol 12:337–357 [CrossRef][PubMed]
    [Google Scholar]
  16. Hahm B. 2009; Hostile communication of measles virus with host innate immunity and dendritic cells. Curr Top Microbiol Immunol 330:271–287 [CrossRef][PubMed]
    [Google Scholar]
  17. Hale B. G., Jackson D., Chen Y. H., Lamb R. A., Randall R. E. 2006; Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. Proc Natl Acad Sci U S A 103:14194–14199 [CrossRef][PubMed]
    [Google Scholar]
  18. Haller O., Kochs G., Weber F. 2006; The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119–130 [CrossRef][PubMed]
    [Google Scholar]
  19. Horvath C. M. 2004; Silencing STATs: lessons from paramyxovirus interferon evasion. Cytokine Growth Factor Rev 15:117–127 [CrossRef][PubMed]
    [Google Scholar]
  20. Nanda S. K., Baron M. D. 2006; Rinderpest virus blocks type I and type II interferon action: role of structural and nonstructural proteins. J Virol 80:7555–7568 [CrossRef][PubMed]
    [Google Scholar]
  21. Ohno S., Ono N., Takeda M., Takeuchi K., Yanagi Y. 2004; Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J Gen Virol 85:2991–2999 [CrossRef][PubMed]
    [Google Scholar]
  22. Pfaller C. K., Conzelmann K. K. 2008; Measles virus V protein is a decoy substrate for IkappaB kinase alpha and prevents Toll-like receptor 7/9-mediated interferon induction. J Virol 82:12365–12373 [CrossRef][PubMed]
    [Google Scholar]
  23. Quelle F. W., Thierfelder W., Witthuhn B. A., Tang B., Cohen S., Ihle J. N. 1995; Phosphorylation and activation of the DNA binding activity of purified Stat1 by the Janus protein-tyrosine kinases and the epidermal growth factor receptor. J Biol Chem 270:20775–20780 [CrossRef][PubMed]
    [Google Scholar]
  24. Ramachandran A., Parisien J. P., Horvath C. M. 2008; STAT2 is a primary target for measles virus V protein-mediated alpha/beta interferon signaling inhibition. J Virol 82:8330–8338 [CrossRef][PubMed]
    [Google Scholar]
  25. 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]
  26. Rodriguez J. J., Horvath C. M. 2004; Host evasion by emerging paramyxoviruses: Hendra virus and Nipah virus v proteins inhibit interferon signaling. Viral Immunol 17:210–219 [CrossRef][PubMed]
    [Google Scholar]
  27. Rothlisberger A., Wiener D., Schweizer M., Peterhans E., Zurbriggen A., Plattet P. 2010; Two domains of the V protein of virulent canine distemper virus selectively inhibit STAT1 and STAT2 nuclear import. J Virol 84:6328–6343 [CrossRef][PubMed]
    [Google Scholar]
  28. Usacheva A., Tian X., Sandoval R., Salvi D., Levy D., Colamonici O. R. 2003; The WD motif-containing protein RACK-1 functions as a scaffold protein within the type I IFN receptor-signaling complex. J Immunol 171:2989–2994[PubMed] [CrossRef]
    [Google Scholar]
  29. Valmas C., Grosch M. N., Schümann M., Olejnik J., Martinez O., Best S. M., Krähling V., Basler C. F., Mühlberger E. 2010; Marburg virus evades interferon responses by a mechanism distinct from Ebola virus. PLoS Pathog 6:e1000721 [CrossRef][PubMed]
    [Google Scholar]
  30. Versteeg G. A., García-Sastre A. 2010; Viral tricks to grid-lock the type I interferon system. Curr Opin Microbiol 13:508–516 [CrossRef][PubMed]
    [Google Scholar]
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