Inflammasomes and viruses: cellular defence versus viral offence Open Access

Abstract

Pro-inflammatory cytokines are important mediators in immune responses against invading pathogens, including viruses. Precursors of the pro-inflammatory cytokines interleukin (IL)-1β and IL-18 are processed by caspase-1. Caspase-1 is activated through autocleavage, but how this is regulated remained elusive for a long time. In 2002, an intracellular multimeric complex was discovered that facilitated caspase-1 cleavage and was termed ‘inflammasome’. To date, different inflammasomes have been described, which recognize a variety of ligands and pathogens. In this review, we discuss the role of inflammasomes in sensing viral infection as well as the evasion strategies that viruses developed to circumvent inflammasome-dependent effects.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.042978-0
2012-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/10/2063.html?itemId=/content/journal/jgv/10.1099/vir.0.042978-0&mimeType=html&fmt=ahah

References

  1. Aksentijevich I., Masters S. L., Ferguson P. J., Dancey P., Frenkel J., van Royen-Kerkhoff A., Laxer R., Tedgård U., Cowen E. W. other authors 2009; An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N Engl J Med 360:2426–2437 [View Article][PubMed]
    [Google Scholar]
  2. Alcamí A., Smith G. L. 1992; A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71:153–167 [View Article][PubMed]
    [Google Scholar]
  3. Allen I. C., Scull M. A., Moore C. B., Holl E. K., McElvania-TeKippe E., Taxman D. J., Guthrie E. H., Pickles R. J., Ting J. P. 2009; The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30:556–565 [View Article][PubMed]
    [Google Scholar]
  4. Barker B. R., Taxman D. J., Ting J. P. 2011; Cross-regulation between the IL-1β/IL-18 processing inflammasome and other inflammatory cytokines. Curr Opin Immunol 23:591–597 [View Article][PubMed]
    [Google Scholar]
  5. Barlan A. U., Danthi P., Wiethoff C. M. 2011a; Lysosomal localization and mechanism of membrane penetration influence nonenveloped virus activation of the NLRP3 inflammasome. Virology 412:306–314 [View Article][PubMed]
    [Google Scholar]
  6. Barlan A. U., Griffin T. M., McGuire K. A., Wiethoff C. M. 2011b; Adenovirus membrane penetration activates the NLRP3 inflammasome. J Virol 85:146–155 [View Article][PubMed]
    [Google Scholar]
  7. Bauernfeind F. G., Horvath G., Stutz A., Alnemri E. S., MacDonald K., Speert D., Fernandes-Alnemri T., Wu J., Monks B. G. other authors 2009; Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183:787–791 [View Article][PubMed]
    [Google Scholar]
  8. Bauernfeind F., Ablasser A., Bartok E., Kim S., Schmid-Burgk J., Cavlar T., Hornung V. 2011; Inflammasomes: current understanding and open questions. Cell Mol Life Sci 68:765–783 [View Article][PubMed]
    [Google Scholar]
  9. Boyden E. D., Dietrich W. F. 2006; Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat Genet 38:240–244 [View Article][PubMed]
    [Google Scholar]
  10. Boyle J. P., Monie T. P. 2012; Computational analysis predicts the Kaposi’s sarcoma-associated herpesvirus tegument protein ORF63 to be alpha helical. Proteins (in press) [View Article][PubMed]
    [Google Scholar]
  11. Bürckstümmer T., Baumann C., Blüml S., Dixit E., Dürnberger G., Jahn H., Planyavsky M., Bilban M., Colinge J. other authors 2009; An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10:266–272 [View Article][PubMed]
    [Google Scholar]
  12. Burdette D., Haskett A., Presser L., McRae S., Iqbal J., Waris G. 2012; Hepatitis C virus activates interleukin-1β via caspase-1-inflammasome complex. J Gen Virol 93:235–246 [View Article][PubMed]
    [Google Scholar]
  13. Chaix J., Tessmer M. S., Hoebe K., Fuséri N., Ryffel B., Dalod M., Alexopoulou L., Beutler B., Brossay L. other authors 2008; Cutting edge: priming of NK cells by IL-18. J Immunol 181:1627–1631[PubMed] [CrossRef]
    [Google Scholar]
  14. Coscoy L. 2007; Immune evasion by Kaposi’s sarcoma-associated herpesvirus. Nat Rev Immunol 7:391–401 [View Article][PubMed]
    [Google Scholar]
  15. Covarrubias S., Richner J. M., Clyde K., Lee Y. J., Glaunsinger B. A. 2009; Host shutoff is a conserved phenotype of gammaherpesvirus infection and is orchestrated exclusively from the cytoplasm. J Virol 83:9554–9566 [View Article][PubMed]
    [Google Scholar]
  16. Delaloye J., Roger T., Steiner-Tardivel Q. G., Le Roy D., Knaup Reymond M., Akira S., Petrilli V., Gomez C. E., Perdiguero B. other authors 2009; Innate immune sensing of modified vaccinia virus Ankara (MVA) is mediated by TLR2-TLR6, MDA-5 and the NALP3 inflammasome. PLoS Pathog 5:e1000480 [View Article][PubMed]
    [Google Scholar]
  17. Di Paolo N. C., Miao E. A., Iwakura Y., Murali-Krishna K., Aderem A., Flavell R. A., Papayannopoulou T., Shayakhmetov D. M. 2009; Virus binding to a plasma membrane receptor triggers interleukin-1α-mediated proinflammatory macrophage response in vivo. Immunity 31:110–121 [View Article][PubMed]
    [Google Scholar]
  18. Dinarello C. A. 2009; Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27:519–550 [View Article][PubMed]
    [Google Scholar]
  19. Dinarello C. A. 2011; A clinical perspective of IL-1β as the gatekeeper of inflammation. Eur J Immunol 41:1203–1217 [View Article][PubMed]
    [Google Scholar]
  20. Dobbelstein M., Shenk T. 1996; Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J Virol 70:6479–6485[PubMed]
    [Google Scholar]
  21. Dorfleutner A., Talbott S. J., Bryan N. B., Funya K. N., Rellick S. L., Reed J. C., Shi X., Rojanasakul Y., Flynn D. C., Stehlik C. 2007; A Shope fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 35:685–694 [View Article][PubMed]
    [Google Scholar]
  22. Fernandes-Alnemri T., Yu J. W., Datta P., Wu J., Alnemri E. S. 2009; AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509–513 [View Article][PubMed]
    [Google Scholar]
  23. Franchi L., Amer A., Body-Malapel M., Kanneganti T. D., Ozören N., Jagirdar R., Inohara N., Vandenabeele P., Bertin J. other authors 2006; Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages. Nat Immunol 7:576–582 [View Article][PubMed]
    [Google Scholar]
  24. Fujioka N., Akazawa R., Ohashi K., Fujii M., Ikeda M., Kurimoto M. 1999; Interleukin-18 protects mice against acute herpes simplex virus type 1 infection. J Virol 73:2401–2409[PubMed]
    [Google Scholar]
  25. Goldbach-Mansky R., Dailey N. J., Canna S. W., Gelabert A., Jones J., Rubin B. I., Kim H. J., Brewer C., Zalewski C. other authors 2006; Neonatal-onset multisystem inflammatory disease responsive to interleukin-1β inhibition. N Engl J Med 355:581–592 [View Article][PubMed]
    [Google Scholar]
  26. Gregory S. M., Davis B. K., West J. A., Taxman D. J., Matsuzawa S., Reed J. C., Ting J. P., Damania B. 2011; Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331:330–334 [View Article][PubMed]
    [Google Scholar]
  27. Guarda G., So A. 2010; Regulation of inflammasome activity. Immunology 130:329–336 [View Article][PubMed]
    [Google Scholar]
  28. Guarda G., Braun M., Staehli F., Tardivel A., Mattmann C., Förster I., Farlik M., Decker T., Du Pasquier R. A. other authors 2011; Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34:213–223 [View Article][PubMed]
    [Google Scholar]
  29. Hornung V., Ablasser A., Charrel-Dennis M., Bauernfeind F., Horvath G., Caffrey D. R., Latz E., Fitzgerald K. A. 2009; AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514–518 [View Article][PubMed]
    [Google Scholar]
  30. Ichinohe T., Lee H. K., Ogura Y., Flavell R., Iwasaki A. 2009; Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206:79–87 [View Article][PubMed]
    [Google Scholar]
  31. Ichinohe T., Pang I. K., Iwasaki A. 2010; Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11:404–410 [View Article][PubMed]
    [Google Scholar]
  32. Ichinohe T., Pang I. K., Kumamoto Y., Peaper D. R., Ho J. H., Murray T. S., Iwasaki A. 2011; Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108:5354–5359 [View Article][PubMed]
    [Google Scholar]
  33. Ikegame S., Takeda M., Ohno S., Nakatsu Y., Nakanishi Y., Yanagi Y. 2010; Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/beta interferon in measles virus-infected human cells. J Virol 84:372–379 [View Article][PubMed]
    [Google Scholar]
  34. Johnston J. B., Barrett J. W., Nazarian S. H., Goodwin M., Riciuto D., Wang G., McFadden G. 2005; A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23:587–598 [View Article][PubMed]
    [Google Scholar]
  35. Kanneganti T. D. 2010; Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10:688–698 [View Article][PubMed]
    [Google Scholar]
  36. Kanneganti T. D., Body-Malapel M., Amer A., Park J. H., Whitfield J., Franchi L., Taraporewala Z. F., Miller D., Patton J. T. other authors 2006; Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J Biol Chem 281:36560–36568 [View Article][PubMed]
    [Google Scholar]
  37. Karim R., Meyers C., Backendorf C., Ludigs K., Offringa R., van Ommen G. J., Melief C. J., van der Burg S. H., Boer J. M. 2011; Human papillomavirus deregulates the response of a cellular network comprising of chemotactic and proinflammatory genes. PLoS ONE 6:e17848 [View Article][PubMed]
    [Google Scholar]
  38. Kawai T., Akira S. 2010; The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373–384 [View Article][PubMed]
    [Google Scholar]
  39. Kayagaki N., Warming S., Lamkanfi M., Vande Walle L., Louie S., Dong J., Newton K., Qu Y., Liu J. other authors 2011; Non-canonical inflammasome activation targets caspase-11. Nature 479:117–121 [View Article][PubMed]
    [Google Scholar]
  40. Kersse K., Vanden Berghe T., Lamkanfi M., Vandenabeele P. 2007; A phylogenetic and functional overview of inflammatory caspases and caspase-1-related CARD-only proteins. Biochem Soc Trans 35:1508–1511 [View Article][PubMed]
    [Google Scholar]
  41. Kerur N., Veettil M. V., Sharma-Walia N., Bottero V., Sadagopan S., Otageri P., Chandran B. 2011; IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9:363–375 [View Article][PubMed]
    [Google Scholar]
  42. Kettle S., Blake N. W., Law K. M., Smith G. L. 1995; Vaccinia virus serpins B13R (SPI-2) and B22R (SPI-1) encode M(r) 38.5 and 40K, intracellular polypeptides that do not affect virus virulence in a murine intranasal model. Virology 206:136–147 [View Article][PubMed]
    [Google Scholar]
  43. Kochs G., García-Sastre A., Martínez-Sobrido L. 2007; Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81:7011–7021 [View Article][PubMed]
    [Google Scholar]
  44. Komiyama T., Ray C. A., Pickup D. J., Howard A. D., Thornberry N. A., Peterson E. P., Salvesen G. 1994; Inhibition of interleukin-1β converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J Biol Chem 269:19331–19337[PubMed]
    [Google Scholar]
  45. Komune N., Ichinohe T., Ito M., Yanagi Y. 2011; Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol 85:13019–13026 [View Article][PubMed]
    [Google Scholar]
  46. Lamkanfi M. 2011; Emerging inflammasome effector mechanisms. Nat Rev Immunol 11:213–220 [View Article][PubMed]
    [Google Scholar]
  47. Lamkanfi M., Dixit V. M. 2011; Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 187:597–602 [View Article][PubMed]
    [Google Scholar]
  48. Latz E. 2010; The inflammasomes: mechanisms of activation and function. Curr Opin Immunol 22:28–33 [View Article][PubMed]
    [Google Scholar]
  49. Leslie K. S., Lachmann H. J., Bruning E., McGrath J. A., Bybee A., Gallimore J. R., Roberts P. F., Woo P., Grattan C. E., Hawkins P. N. 2006; Phenotype, genotype, and sustained response to anakinra in 22 patients with autoinflammatory disease associated with CIAS-1/NALP3 mutations. Arch Dermatol 142:1591–1597 [View Article][PubMed]
    [Google Scholar]
  50. Liu B., Mori I., Hossain M. J., Dong L., Takeda K., Kimura Y. 2004; Interleukin-18 improves the early defence system against influenza virus infection by augmenting natural killer cell-mediated cytotoxicity. J Gen Virol 85:423–428 [View Article][PubMed]
    [Google Scholar]
  51. MacNeill A. L., Moldawer L. L., Moyer R. W. 2009; The role of the cowpox virus crmA gene during intratracheal and intradermal infection of C57BL/6 mice. Virology 384:151–160 [View Article][PubMed]
    [Google Scholar]
  52. Martinon F., Tschopp J. 2007; Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14:10–22 [View Article][PubMed]
    [Google Scholar]
  53. Martinon F., Burns K., Tschopp J. 2002; The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol Cell 10:417–426 [View Article][PubMed]
    [Google Scholar]
  54. Martinon F., Mayor A., Tschopp J. 2009; The inflammasomes: guardians of the body. Annu Rev Immunol 27:229–265 [View Article][PubMed]
    [Google Scholar]
  55. Mason D. R., Beck P. L., Muruve D. A. 2012; Nucleotide-binding oligomerization domain-like receptors and inflammasomes in the pathogenesis of non-microbial inflammation and diseases. J Innate Immun 4:16–30 [View Article][PubMed]
    [Google Scholar]
  56. Miao E. A., Leaf I. A., Treuting P. M., Mao D. P., Dors M., Sarkar A., Warren S. E., Wewers M. D., Aderem A. 2010; Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11:1136–1142 [View Article][PubMed]
    [Google Scholar]
  57. Muruve D. A., Pétrilli V., Zaiss A. K., White L. R., Clark S. A., Ross P. J., Parks R. J., Tschopp J. 2008; The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452:103–107 [View Article][PubMed]
    [Google Scholar]
  58. Nazarian S. H., Rahman M. M., Werden S. J., Villeneuve D., Meng X., Brunetti C., Valeriano C., Wong C., Singh R. other authors 2008; Yaba monkey tumor virus encodes a functional inhibitor of interleukin-18. J Virol 82:522–528 [View Article][PubMed]
    [Google Scholar]
  59. Nour A. M., Reichelt M., Ku C. C., Ho M. Y., Heineman T. C., Arvin A. M. 2011; Varicella-zoster virus infection triggers formation of an interleukin-1β (IL-1β)-processing inflammasome complex. J Biol Chem 286:17921–17933 [View Article][PubMed]
    [Google Scholar]
  60. Onoguchi K., Yoneyama M., Fujita T. 2011; Retinoic acid-inducible gene-I-like receptors. J Interferon Cytokine Res 31:27–31 [View Article][PubMed]
    [Google Scholar]
  61. Owen D. M., Gale M. Jr 2009; Fighting the flu with inflammasome signaling. Immunity 30:476–478 [View Article][PubMed]
    [Google Scholar]
  62. Pang I. K., Iwasaki A. 2011; Inflammasomes as mediators of immunity against influenza virus. Trends Immunol 32:34–41 [View Article][PubMed]
    [Google Scholar]
  63. Pien G. C., Satoskar A. R., Takeda K., Akira S., Biron C. A. 2000; Cutting edge: selective IL-18 requirements for induction of compartmental IFN-γ responses during viral infection. J Immunol 165:4787–4791[PubMed] [CrossRef]
    [Google Scholar]
  64. Poeck H., Ruland J. 2012; From virus to inflammation: mechanisms of RIG-I-induced IL-1β production. Eur J Cell Biol 91:59–64 [View Article][PubMed]
    [Google Scholar]
  65. Poeck H., Bscheider M., Gross O., Finger K., Roth S., Rebsamen M., Hannesschläger N., Schlee M., Rothenfusser S. other authors 2010; Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production. Nat Immunol 11:63–69 [View Article][PubMed]
    [Google Scholar]
  66. Pontillo A., Brandão L. A., Guimarães R. L., Segat L., Athanasakis E., Crovella S. 2010; A 3’ UTR SNP in NLRP3 gene is associated with susceptibility to HIV-1 infection. J Acquir Immune Defic Syndr 54:236–240 [View Article][PubMed]
    [Google Scholar]
  67. Puren A. J., Fantuzzi G., Dinarello C. A. 1999; Gene expression, synthesis, and secretion of interleukin 18 and interleukin 1β are differentially regulated in human blood mononuclear cells and mouse spleen cells. Proc Natl Acad Sci U S A 96:2256–2261 [View Article][PubMed]
    [Google Scholar]
  68. Rahman M. M., McFadden G. 2011; Myxoma virus lacking the pyrin-like protein M013 is sensed in human myeloid cells by both NLRP3 and multiple Toll-like receptors, which independently activate the inflammasome and NF-κB innate response pathways. J Virol 85:12505–12517 [View Article][PubMed]
    [Google Scholar]
  69. Rajan J. V., Rodriguez D., Miao E. A., Aderem A. 2011; The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J Virol 85:4167–4172 [View Article][PubMed]
    [Google Scholar]
  70. Rathinam V. A., Fitzgerald K. A. 2010; Inflammasomes and anti-viral immunity. J Clin Immunol 30:632–637 [View Article][PubMed]
    [Google Scholar]
  71. Rathinam V. A., Jiang Z., Waggoner S. N., Sharma S., Cole L. E., Waggoner L., Vanaja S. K., Monks B. G., Ganesan S. other authors 2010; The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11:395–402 [View Article][PubMed]
    [Google Scholar]
  72. Ray C. A., Black R. A., Kronheim S. R., Greenstreet T. A., Sleath P. R., Salvesen G. S., Pickup D. J. 1992; Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β converting enzyme. Cell 69:597–604 [View Article][PubMed]
    [Google Scholar]
  73. Reading P. C., Smith G. L. 2003; Vaccinia virus interleukin-18-binding protein promotes virulence by reducing gamma interferon production and natural killer and T-cell activity. J Virol 77:9960–9968 [View Article][PubMed]
    [Google Scholar]
  74. Reddy S., Jia S., Geoffrey R., Lorier R., Suchi M., Broeckel U., Hessner M. J., Verbsky J. 2009; An autoinflammatory disease due to homozygous deletion of the IL1RN locus. N Engl J Med 360:2438–2444 [View Article][PubMed]
    [Google Scholar]
  75. Roberts T. L., Idris A., Dunn J. A., Kelly G. M., Burnton C. M., Hodgson S., Hardy L. L., Garceau V., Sweet M. J. other authors 2009; HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323:1057–1060 [View Article][PubMed]
    [Google Scholar]
  76. Ross J. B., Finlayson L. A., Klotz P. J., Langley R. G., Gaudet R., Thompson K., Churchman S. M., McDermott M. F., Hawkins P. N. 2008; Use of anakinra (Kineret) in the treatment of familial cold autoinflammatory syndrome with a 16-month follow-up. J Cutan Med Surg 12:8–16[PubMed]
    [Google Scholar]
  77. Rowe M., Glaunsinger B., van Leeuwen D., Zuo J., Sweetman D., Ganem D., Middeldorp J., Wiertz E. J., Ressing M. E. 2007; Host shutoff during productive Epstein–Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc Natl Acad Sci U S A 104:3366–3371 [View Article][PubMed]
    [Google Scholar]
  78. Sauer J. D., Witte C. E., Zemansky J., Hanson B., Lauer P., Portnoy D. A. 2010; Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7:412–419 [View Article][PubMed]
    [Google Scholar]
  79. Schattgen S. A., Fitzgerald K. A. 2011; The PYHIN protein family as mediators of host defenses. Immunol Rev 243:109–118 [View Article][PubMed]
    [Google Scholar]
  80. Schlender J., Hornung V., Finke S., Günthner-Biller M., Marozin S., Brzózka K., Moghim S., Endres S., Hartmann G., Conzelmann K. K. 2005; Inhibition of Toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J Virol 79:5507–5515 [View Article][PubMed]
    [Google Scholar]
  81. Schmitz N., Kurrer M., Bachmann M. F., Kopf M. 2005; Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 79:6441–6448 [View Article][PubMed]
    [Google Scholar]
  82. Seet B. T., Johnston J. B., Brunetti C. R., Barrett J. W., Everett H., Cameron C., Sypula J., Nazarian S. H., Lucas A., McFadden G. 2003; Poxviruses and immune evasion. Annu Rev Immunol 21:377–423 [View Article][PubMed]
    [Google Scholar]
  83. Sergerie Y., Rivest S., Boivin G. 2007; Tumor necrosis factor-alpha and interleukin-1β play a critical role in the resistance against lethal herpes simplex virus encephalitis. J Infect Dis 196:853–860 [View Article][PubMed]
    [Google Scholar]
  84. Sharma R., Raychaudhuri S., Dasgupta A. 2004; Nuclear entry of poliovirus protease-polymerase precursor 3CD: implications for host cell transcription shut-off. Virology 320:195–205 [View Article][PubMed]
    [Google Scholar]
  85. Sims J. E., Smith D. E. 2010; The IL-1 family: regulators of immunity. Nat Rev Immunol 10:89–102 [View Article][PubMed]
    [Google Scholar]
  86. Smith V. P., Alcami A. 2000; Expression of secreted cytokine and chemokine inhibitors by ectromelia virus. J Virol 74:8460–8471 [View Article][PubMed]
    [Google Scholar]
  87. Smith V. P., Bryant N. A., Alcamí A. 2000; Ectromelia, vaccinia and cowpox viruses encode secreted interleukin-18-binding proteins. J Gen Virol 81:1223–1230[PubMed]
    [Google Scholar]
  88. Stasakova J., Ferko B., Kittel C., Sereinig S., Romanova J., Katinger H., Egorov A. 2005; 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 86:185–195 [View Article][PubMed]
    [Google Scholar]
  89. Stehlik C., Dorfleutner A. 2007; COPs and POPs: modulators of inflammasome activity. J Immunol 179:7993–7998[PubMed] [CrossRef]
    [Google Scholar]
  90. Tanaka-Kataoka M., Kunikata T., Takayama S., Iwaki K., Ohashi K., Ikeda M., Kurimoto M. 1999; In vivo antiviral effect of interleukin 18 in a mouse model of vaccinia virus infection. Cytokine 11:593–599 [View Article][PubMed]
    [Google Scholar]
  91. Thomas P. G., Dash P., Aldridge J. R. Jr, Ellebedy A. H., Reynolds C., Funk A. J., Martin W. J., Lamkanfi M., Webby R. J. other authors 2009; The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30:566–575 [View Article][PubMed]
    [Google Scholar]
  92. Thompson J. P., Turner P. C., Ali A. N., Crenshaw B. C., Moyer R. W. 1993; The effects of serpin gene mutations on the distinctive pathobiology of cowpox and rabbitpox virus following intranasal inoculation of Balb/c mice. Virology 197:328–338 [View Article][PubMed]
    [Google Scholar]
  93. Ting J. P., Lovering R. C., Alnemri E. S., Bertin J., Boss J. M., Davis B. K., Flavell R. A., Girardin S. E., Godzik A. other authors 2008; The NLR gene family: a standard nomenclature. Immunity 28:285–287 [View Article][PubMed]
    [Google Scholar]
  94. Turner S. J., Silke J., Kenshole B., Ruby J. 2000; Characterization of the ectromelia virus serpin, SPI-2. J Gen Virol 81:2425–2430[PubMed]
    [Google Scholar]
  95. Unterholzner L., Keating S. E., Baran M., Horan K. A., Jensen S. B., Sharma S., Sirois C. M., Jin T., Latz E. other authors 2010; IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997–1004 [View Article][PubMed]
    [Google Scholar]
  96. Veeranki S., Choubey D. 2012; Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear double-stranded DNA: regulation of subcellular localization. Mol Immunol 49:567–571 [View Article][PubMed]
    [Google Scholar]
  97. Vreede F. T., Fodor E. 2010; The role of the influenza virus RNA polymerase in host shut-off. Virulence 1:436–439 [View Article][PubMed]
    [Google Scholar]
  98. Yazdi A. S., Guarda G., D’Ombrain M. C., Drexler S. K. 2010; Inflammatory caspases in innate immunity and inflammation. J Innate Immun 2:228–237 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.042978-0
Loading
/content/journal/jgv/10.1099/vir.0.042978-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed