1887

Journal of General Virology header logo

Volume 99, Issue 4

Human parainfluenza virus type 2 V protein inhibits caspase-1 Free

Abstract

The multifunctional V protein of human parainfluenza virus type 2 (hPIV2) plays important roles in controlling viral genome replication, inhibiting the host interferon response and promoting virus growth. We screened a yeast two-hybrid library using V protein as bait to identify host factors that are important for other functions of V. One of several positive clones isolated from HeLa cell-derived cDNA library encodes caspase-1. We found that the C-terminal region of V interacts with the C-terminal region of caspase-1 in mammalian cells. Moreover, the V protein repressed caspase-1 activity and the formation of interleukin-1β (IL-1β) in a dose-dependent manner. IL-1β secretion induced by wild-type hPIV2 infection in human monocytic THP-1 cells was significantly lower than that induced by recombinant hPIV2 lacking V protein or having a mutant V. These data suggest that hPIV2 V protein inhibits caspase-1-mediated maturation of IL-1β via its interaction with caspase-1.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): caspase-1 , human parainfluenza virus type 2 , interleukin-1β and V protein
© 2018 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001037
2018-04-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/4/501.html?itemId=/content/journal/jgv/10.1099/jgv.0.001037&mimeType=html&fmt=ahah

References

  1. Lamb RA, Parks GD. Paramyxoviridae. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA et al. (editors) Fields Virology, 6th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2013 pp. 957–995
     [Google Scholar]
  2. Ohgimoto S, Bando H, Kawano M, Okamoto K, Kondo K et al. Sequence analysis of P gene of human parainfluenza type 2 virus: P and cysteine-rich proteins are translated by two mRNAs that differ by two nontemplated G residues. Virology 1990; 177:116–123 [View Article][PubMed]
     [Google Scholar]
  3. Paterson RG, Leser GP, Shaughnessy MA, Lamb RA. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 1995; 208:121–131 [View Article][PubMed]
     [Google Scholar]
  4. Li T, Chen X, Garbutt KC, Zhou P, Zheng N. Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 2006; 124:105–117 [View Article][PubMed]
     [Google Scholar]
  5. Watanabe N, Kawano M, Tsurudome M, Nishio M, Ito M et al. Binding of the V proteins to the nucleocapsid proteins of human parainfluenza type 2 virus. Med Microbiol Immunol 1996; 185:89–94 [View Article][PubMed]
     [Google Scholar]
  6. Nishio M, Tsurudome M, Ishihara H, Ito M, Ito Y. The conserved carboxyl terminus of human parainfluenza virus type 2 V protein plays an important role in virus growth. Virology 2007; 362:85–98 [View Article][PubMed]
     [Google Scholar]
  7. Nishio M, Ohtsuka J, Tsurudome M, Nosaka T, Kolakofsky D. Human parainfluenza virus type 2 V protein inhibits genome replication by binding to the L protein: possible role in promoting viral fitness. J Virol 2008; 82:6130–6138 [View Article][PubMed]
     [Google Scholar]
  8. Nishio M, Tsurudome M, Ito M, Kawano M, Kusagawa S et al. Isolation of monoclonal antibodies directed against the V protein of human parainfluenza virus type 2 and localization of the V protein in virus-infected cells. Med Microbiol Immunol 1999; 188:79–82 [View Article][PubMed]
     [Google Scholar]
  9. Nishio M, Tsurudome M, Ito M, Ito Y. Identification of RNA-binding regions on the P and V proteins of human parainfluenza virus type 2. Med Microbiol Immunol 2006; 195:29–36 [View Article][PubMed]
     [Google Scholar]
  10. Nishio M, Tsurudome M, Ito M, Garcin D, Kolakofsky D et al. Identification of paramyxovirus V protein residues essential for STAT protein degradation and promotion of virus replication. J Virol 2005; 79:8591–8601 [View Article][PubMed]
     [Google Scholar]
  11. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N et al. 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 USA 2004; 101:17264–17269 [View Article][PubMed]
     [Google Scholar]
  12. Childs K, Stock N, Ross C, Andrejeva J, Hilton L et al. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 2007; 359:190–200 [View Article][PubMed]
     [Google Scholar]
  13. Childs KS, Andrejeva J, Randall RE, Goodbourn S. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J Virol 2009; 83:1465–1473 [View Article][PubMed]
     [Google Scholar]
  14. Childs K, Randall R, Goodbourn S. Paramyxovirus V proteins interact with the RNA Helicase LGP2 to inhibit RIG-I-dependent interferon induction. J Virol 2012; 86:3411–3421 [View Article][PubMed]
     [Google Scholar]
  15. Kitagawa Y, Yamaguchi M, Zhou M, Nishio M, Itoh M et al. Human parainfluenza virus type 2 V protein inhibits TRAF6-mediated ubiquitination of IRF7 to prevent TLR7- and TLR9-dependent interferon induction. J Virol 2013; 87:7966–7976 [View Article][PubMed]
     [Google Scholar]
  16. Nishio M, Tsurudome M, Ito M, Kawano M, Komada H et al. 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 2001; 75:9165–9176 [View Article][PubMed]
     [Google Scholar]
  17. Parisien JP, Lau JF, Rodriguez JJ, Sullivan BM, Moscona A et al. The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 2001; 283:230–239 [View Article][PubMed]
     [Google Scholar]
  18. Ohta K, Goto H, Yumine N, Nishio M. Human parainfluenza virus type 2 V protein inhibits and antagonizes tetherin. J Gen Virol 2016; 97:561–570 [View Article][PubMed]
     [Google Scholar]
  19. Lu LL, Puri M, Horvath CM, Sen GC. Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of κB kinase ε(IKKe)/TBK1. J Biol Chem 2008; 283:14269–14276 [View Article][PubMed]
     [Google Scholar]
  20. Cerretti DP, Kozlosky CJ, Mosley B, Nelson N, van Ness K et al. Molecular cloning of the interleukin-1 beta converting enzyme. Science 1992; 256:97–100 [View Article][PubMed]
     [Google Scholar]
  21. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 1992; 356:768–774 [View Article][PubMed]
     [Google Scholar]
  22. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 1995; 267:2000–2003 [View Article][PubMed]
     [Google Scholar]
  23. Tatsuta T, Shiraishi A, Mountz JD. The prodomain of caspase-1 enhances Fas-mediated apoptosis through facilitation of caspase-8 activation. J Biol Chem 2000; 275:14248–14254 [View Article][PubMed]
     [Google Scholar]
  24. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of pro IL-1β. Mol Cell 2002; 10:417–426[PubMed] [Crossref]
     [Google Scholar]
  25. Dinarello CA. Interleukin-1β, interleukin-18, and the interleukin-1β converting enzyme. Ann N Y Acad Sci 1998; 856:1–11 [View Article]
     [Google Scholar]
  26. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010; 327:291–295 [View Article][PubMed]
     [Google Scholar]
  27. Kanneganti TD. Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 2010; 10:688–698 [View Article][PubMed]
     [Google Scholar]
  28. Chen IY, Ichinohe T. Response of host inflammasomes to viral infection. Trends Microbiol 2015; 23:55–63 [View Article][PubMed]
     [Google Scholar]
  29. Stasakova J, Ferko B, Kittel C, Sereinig S, Romanova J et al. Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1β and 18. J Gen Virol 2005; 86:185–195 [View Article][PubMed]
     [Google Scholar]
  30. Moriyama M, Chen IY, Kawaguchi A, Koshiba T, Nagata K et al. The RNA- and TRIM25-binding domains of influenza virus NS1 protein are essential for suppression of NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol 2016; 90:4105–4114 [View Article][PubMed]
     [Google Scholar]
  31. Yoshizumi T, Ichinohe T, Sasaki O, Otera H, Kawabata S et al. Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat Commun 2014; 5:4713 [View Article][PubMed]
     [Google Scholar]
  32. Gerlic M, Faustin B, Postigo A, Yu EC, Proell M et al. Vaccinia virus F1L protein promotes virulence by inhibiting inflammasome activation. Proc Natl Acad Sci USA 2013; 110:7808–7813 [View Article][PubMed]
     [Google Scholar]
  33. Gregory SM, Davis BK, West JA, Taxman DJ, Matsuzawa S et al. Discovery of a viral NLR homolog that inhibits the inflammasome. Science 2011; 331:330–334 [View Article][PubMed]
     [Google Scholar]
  34. Dorfleutner A, Talbott SJ, Bryan NB, Funya KN, Rellick SL et al. A Shope Fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 2007; 35:685–694 [View Article][PubMed]
     [Google Scholar]
  35. Johnston JB, Barrett JW, Nazarian SH, Goodwin M, Ricciuto D et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 2005; 23:587–598 [View Article][PubMed]
     [Google Scholar]
  36. Komune N, Ichinohe T, Ito M, Yanagi Y. Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol 2011; 85:13019–13026 [View Article][PubMed]
     [Google Scholar]
  37. Kitagawa Y, Yamaguchi M, Zhou M, Komatsu T, Nishio M et al. A tryptophan-rich motif in the human parainfluenza virus type 2 V protein is critical for the blockade of toll-like receptor 7 (TLR7)- and TLR9-dependent signaling. J Virol 2011; 85:4606–4611 [View Article][PubMed]
     [Google Scholar]
  38. Nishio M, Garcin D, Simonet V, Kolakofsky D. The carboxyl segment of the mumps virus V protein associates with Stat proteins in vitro via a tryptophan-rich motif. Virology 2002; 300:92–99 [View Article][PubMed]
     [Google Scholar]
  39. Nishio M, Tsurudome M, Kawano M, Watanabe N, Ohgimoto S et al. Interaction between nucleocapsid protein (NP) and phosphoprotein (P) of human parainfluenza virus type 2: one of the two NP binding sites on P is essential for granule formation. J Gen Virol 1996; 77:2457–2463 [View Article][PubMed]
     [Google Scholar]
  40. Nishio M, Tsurudome M, Ito M, Watanabe N, Kawano M et al. Human parainfluenza virus type 2 phosphoprotein: mapping of monoclonal antibody epitopes and location of the multimerization domain. J Gen Virol 1997; 78:1303–1308 [View Article][PubMed]
     [Google Scholar]
  41. Wang Y, Hasegawa M, Imamura R, Kinoshita T, Kondo C et al. PYNOD, a novel Apaf-1/CED4-like protein is an inhibitor of ASC and caspase-1. Int Immunol 2004; 16:777–786 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001037
Loading
Human parainfluenza virus type 2 V protein inhibits caspase-1
J. Gen. Virol. 99, 501 (2018); https://doi.org/10.1099/jgv.0.001037
/content/journal/jgv/10.1099/jgv.0.001037
/content/journal/jgv/10.1099/jgv.0.001037
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error