Rift Valley fever virus infection induces activation of the NLRP3 inflammasome

Virology

Volumn 449, Issue , 2014, Pages 174-180

  Ermler, Megan E ^a   Traylor, Zachary ^a   Patel, Krupen ^a   Schattgen, Stefan A ^c   Vanaja, Sivapriya K ^c   Fitzgerald, Katherine A ^c   Hise, Amy G ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

ASC; Caspase 1; Dendritic cells; IL 1 ; Inflammasome; Murine; NLRP3; Rift Valley fever virus; Virus

Indexed keywords

APOPTOSIS REPRESSOR WITH CASPASE RECRUITMENT DOMAIN; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DENDRITIC CELL; ENZYME ACTIVATION; ENZYME REPRESSION; IMMUNOCOMPETENT CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RIFT VALLEY FEVER; RIFT VALLEY FEVER BUNYAVIRUS; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

ASC; CASPASE-1; DENDRITIC CELLS; IL-1Β; INFLAMMASOME; MURINE; NLRP3; RIFT VALLEY FEVER VIRUS; VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CASPASE 1; DENDRITIC CELLS; FEMALE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS;

EID: 84896983616     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.11.015     Document Type: Article

References (35)

1. Bae J.Y., Park H.H. Crystal structure of NALP3 protein pyrin domain (PYD) and its implications in inflammasome assembly. J. Biol. Chem. 2011, 286(45):39528-39536.
2. Broz P., Ruby T., Belhocine K., Bouley D.M., Kayagaki N., Dixit V.M., Monack D.M. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 2012, 490(7419):288-291.
3. Burdette D., Haskett A., Presser L., McRae S., Iqbal J., Waris G. Hepatitis C virus activates interleukin-1beta via caspase-1-inflammasome complex. J. Gen. Virol. 2012, 93(Pt 2):235-246.
4. Dao T., Mehal W.Z., Crispe I.N. IL-18 augments perforin-dependent cytotoxicity of liver NK-T cells. J. Immunol. 1998, 161(5):2217-2222.
5. Davidson J., Milton A.S., Rotondo D. A study of the pyrogenic actions of interleukin-1 alpha and interleukin-1 beta: interactions with a steroidal and a non-steroidal anti-inflammatory agent. Br. J. Pharmacol. 1990, 100(3):542-546.
6. Dinarello C.A. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011, 117(14):3720-3732.
7. Ermler M.E., Yerukhim E., Schriewer J., Schattgen S., Traylor Z., Wespiser A.R., Caffrey D.R., Chen Z.J., King C.H., Gale M., Colonna M., Fitzgerald K.A., Buller R.M., Hise A.G. RNA helicase signaling is critical for type I interferon production and protection against Rift Valley fever virus during mucosal challenge. J. Virol. 2013, 87(9):4846-4860.
8. Fernandes-Alnemri T., Yu J.W., Datta P., Wu J., Alnemri E.S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009, 458(7237):509-513.
9. Franchi L., Eigenbrod T., Nunez G. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J. Immunol. 2009, 183(2):792-796.
10. Ghayur T., Banerjee S., Hugunin M., Butler D., Herzog L., Carter A., Quintal L., Sekut L., Talanian R., Paskind M., Wong W., Kamen R., Tracey D., Allen H. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 1997, 386(6625):619-623.
11. Gu Y., Kuida K., Tsutsui H., Ku G., Hsiao K., Fleming M.A., Hayashi N., Higashino K., Okamura H., Nakanishi K., Kurimoto M., Tanimoto T., Flavell R.A., Sato V., Harding M.W., Livingston D.J., Su M.S. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 1997, 275(5297):206-209.
12. Hoffman H.M., Rosengren S., Boyle D.L., Cho J.Y., Nayar J., Mueller J.L., Anderson J.P., Wanderer A.A., Firestein G.S. Prevention of cold-associated acute inflammation in familial cold autoinflammatory syndrome by interleukin-1 receptor antagonist. Lancet 2004, 364(9447):1779-1785.
13. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9(8):847-856.
14. Ichinohe T., Lee H.K., Ogura Y., Flavell R., Iwasaki A. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 2009, 206(1):79-87.
15. Ichinohe T., Pang I.K., Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 2010, 11(5):404-410.
16. Ikegami T., Won S., Peters C.J., Makino S. Rescue of infectious Rift Valley fever virus entirely from cDNA, analysis of virus lacking the NSs gene, and expression of a foreign gene. J. Virol. 2006, 80(6):2933-2940.
17. Ito M., Yanagi Y., Ichinohe T. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog. 2012, 8(8):e1002857.
18. Kayagaki N., Warming S., Lamkanfi M., Vande Walle L., Louie S., Dong J., Newton K., Qu Y., Liu J., Heldens S., Zhang J., Lee W.P., Roose-Girma M., Dixit V.M. Non-canonical inflammasome activation targets caspase-11. Nature 2011, 479(7371):117-121.
19. Keller M., Ruegg A., Werner S., Beer H.D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008, 132(5):818-831.
20. Lamkanfi M., Dixit V.M. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 2010, 8(1):44-54.
21. Lawrence T.M., Hudacek A.W., de Zoete M.R., Flavell R.A., Schnell M.J. Rabies virus is recognized by the NLRP3 inflammasome and activates interleukin-1beta release in murine dendritic cells. J. Virol. 2013, 87(10):5848-5857.
22. Le May N., Dubaele S., Proietti De Santis L., Billecocq A., Bouloy M., Egly J.M. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 2004, 116(4):541-550.
23. McElroy A.K., Nichol S.T. Rift Valley fever virus inhibits a pro-inflammatory response in experimentally infected human monocyte derived macrophages and a pro-inflammatory cytokine response may be associated with patient survival during natural infection. Virology 2012, 422(1):6-12.
24. Negash A.A., Ramos H.J., Crochet N., Lau D.T., Doehle B., Papic N., Delker D.A., Jo J., Bertoletti A., Hagedorn C.H., Gale M. IL-1beta production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog. 2013, 9(4):e1003330.
25. Nfon C.K., Marszal P., Zhang S., Weingartl H.M. Innate immune response to Rift Valley fever virus in goats. PLoS Negl.Trop. Dis. 2012, 6(4):e1623.
26. Okamura H., Tsutsi H., Komatsu T., Yutsudo M., Hakura A., Tanimoto T., Torigoe K., Okura T., Nukada Y., Hattori K., et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995, 378(6552):88-91.
27. Pascual V., Allantaz F., Arce E., Punaro M., Banchereau J. Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade. J. Exp. Med. 2005, 201(9):1479-1486.
28. Poeck H., Bscheider M., Gross O., Finger K., Roth S., Rebsamen M., Hannesschlager N., Schlee M., Rothenfusser S., Barchet W., Kato H., Akira S., Inoue S., Endres S., Peschel C., Hartmann G., Hornung V., Ruland J. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat. Immunol. 2010, 11(1):63-69.
29. Rajan J.V., Rodriguez D., Miao E.A., Aderem A. The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J. Virol. 2011, 85(9):4167-4172.
30. Rathinam V.A., Jiang Z., Waggoner S.N., Sharma S., Cole L.E., Waggoner L., Vanaja S.K., Monks B.G., Ganesan S., Latz E., Hornung V., Vogel S.N., Szomolanyi-Tsuda E., Fitzgerald K.A. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 2010, 11(5):395-402.
31. Sabbah A., Chang T.H., Harnack R., Frohlich V., Tominaga K., Dube P.H., Xiang Y., Bose S. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 2009, 10(10):1073-1080.
32. Segovia J., Sabbah A., Mgbemena V., Tsai S.Y., Chang T.H., Berton M.T., Morris I.R., Allen I.C., Ting J.P., Bose S. TLR2/MyD88/NF-kappaB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 2012, 7(1):e29695.
33. Stutz A., Golenbock D.T., Latz E. Inflammasomes: too big to miss. J. Clin. Invest. 2009, 119(12):3502-3511.
34. Subramanian N., Natarajan K., Clatworthy M.R., Wang Z., Germain R.N. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 2013, 153(2):348-361.
35. Thornberry N.A., Bull H.G., Calaycay J.R., Chapman K.T., Howard A.D., Kostura M.J., Miller D.K., Molineaux S.M., Weidner J.R., Aunins J., et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 1992, 356(6372):768-774.