Canonical Inflammasomes Drive IFN-γ to Prime Caspase-11 in Defense against a Cytosol-Invasive Bacterium

Cell Host and Microbe

Volumn 18, Issue 3, 2015, Pages 320-332

  Aachoui, Youssef ^a,b   Kajiwara, Yuji ^c   Leaf, Irina A ^d   Mao, Dat ^a,b   Ting, Jenny P Y ^a,b   Coers, Jörn ^e   Aderem, Alan ^d   Buxbaum, Joseph D ^c   Miao, Edward A ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CASPASE 4; CASPASE 5; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 18; CASP11 PROTEIN, MOUSE; CASP4 PROTEIN, HUMAN; CASPASE; INITIATOR CASPASE; INTERLEUKIN 1BETA CONVERTING ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BURKHOLDERIA THAILANDENSIS; CANONICAL ANALYSIS; CONTROLLED STUDY; CYTOSOL; DEFENSE MECHANISM; ENZYME ACTIVITY; FEMALE; GENE ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK; TRANSGENE; ANIMAL; BURKHOLDERIA; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; BURKHOLDERIA; CASPASE 1; CASPASES; CASPASES, INITIATOR; CYTOSOL; HUMANS; INFLAMMASOMES; INTERFERON-GAMMA; INTERLEUKIN-18; MICE; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 84941317034     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.07.016     Document Type: Article

References (49)

1. Y. Aachoui, I.A. Leaf, J.A. Hagar, M.F. Fontana, C.G. Campos, D.E. Zak, M.H. Tan, P.A. Cotter, R.E. Vance, A. Aderem, and E.A. Miao Caspase-11 protects against bacteria that escape the vacuole Science 339 2013 975 978
2. Y. Aachoui, V. Sagulenko, E.A. Miao, and K.J. Stacey Inflammasome-mediated pyroptotic and apoptotic cell death, and defense against infection Curr. Opin. Microbiol. 16 2013 319 326
3. I.C. Allen, M.A. Scull, C.B. Moore, E.K. Holl, E. McElvania-TeKippe, D.J. Taxman, E.H. Guthrie, R.J. Pickles, and J.P.Y. Ting The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA Immunity 30 2009 556 565
4. I.C. Allen, C.B. Moore, M. Schneider, Y. Lei, B.K. Davis, M.A. Scull, D. Gris, K.E. Roney, A.G. Zimmermann, J.B. Bowzard, and et al. NLRX1 protein attenuates inflammatory responses to infection by interfering with the RIG-I-MAVS and TRAF6-NF-κB signaling pathways Immunity 34 2011 854 865
5. P. Broz, T. Ruby, K. Belhocine, D.M. Bouley, N. Kayagaki, V.M. Dixit, and D.M. Monack Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1 Nature 490 2012 288 291
6. C.L. Case, L.J. Kohler, J.B. Lima, T. Strowig, M.R. de Zoete, R.A. Flavell, D.S. Zamboni, and C.R. Roy Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila Proc. Natl. Acad. Sci. USA 110 2013 1851 1856
7. I. Ceballos-Olvera, M. Sahoo, M.A. Miller, L. Del Barrio, and F. Re Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1β is deleterious PLoS Pathog. 7 2011 e1002452
8. C.A. Dinarello IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family J. Allergy Clin. Immunol. 103 1999 11 24
9. T. Fernandes-Alnemri, J.-W. Yu, C. Juliana, L. Solorzano, S. Kang, J. Wu, P. Datta, M. McCormick, L. Huang, E. McDermott, and et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis Nat. Immunol. 11 2010 385 393
10. L. Franchi, R. Muñoz-Planillo, and G. Núñez Sensing and reacting to microbes through the inflammasomes Nat. Immunol. 13 2012 325 332
11. O. Gross, H. Poeck, M. Bscheider, C. Dostert, N. Hannesschläger, S. Endres, G. Hartmann, A. Tardivel, E. Schweighoffer, V. Tybulewicz, and et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence Nature 459 2009 433 436
12. P. Gurung, R.K.S. Malireddi, P.K. Anand, D. Demon, L. Vande Walle, Z. Liu, P. Vogel, M. Lamkanfi, and T.-D. Kanneganti Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-β (TRIF)-mediated caspase-11 protease production integrates Toll-like receptor 4 (TLR4) protein- and Nlrp3 inflammasome-mediated host defense against enteropathogens J. Biol. Chem. 287 2012 34474 34483
13. J.A. Hagar, D.A. Powell, Y. Aachoui, R.K. Ernst, and E.A. Miao Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock Science 341 2013 1250 1253
14. J.C. Kagan, T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta Nat. Immunol. 9 2008 361 368
15. Y. Kajiwara, T. Schiff, G. Voloudakis, M.A. Gama Sosa, G. Elder, O. Bozdagi, and J.D. Buxbaum A critical role for human caspase-4 in endotoxin sensitivity J. Immunol. 193 2014 335 343
16. N. Kayagaki, S. Warming, M. Lamkanfi, L. Vande Walle, S. Louie, J. Dong, K. Newton, Y. Qu, J. Liu, S. Heldens, and et al. Non-canonical inflammasome activation targets caspase-11 Nature 479 2011 117 121
17. N. Kayagaki, M.T. Wong, I.B. Stowe, S.R. Ramani, L.C. Gonzalez, S. Akashi-Takamura, K. Miyake, J. Zhang, W.P. Lee, A. Muszyński, and et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4 Science 341 2013 1246 1249
18. B.-H. Kim, A.R. Shenoy, P. Kumar, C.J. Bradfield, and J.D. MacMicking IFN-inducible GTPases in host cell defense Cell Host Microbe 12 2012 432 444
19. T.G. Kimbrough, and S.I. Miller Contribution of Salmonella typhimurium type III secretion components to needle complex formation Proc. Natl. Acad. Sci. USA 97 2000 11008 11013
20. E.M. Kofoed, and R.E. Vance Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity Nature 477 2011 592 595
21. M. Lara-Tejero, F.S. Sutterwala, Y. Ogura, E.P. Grant, J. Bertin, A.J. Coyle, R.A. Flavell, and J.E. Galán Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis J. Exp. Med. 203 2006 1407 1412
22. C.N. LaRock, and B.T. Cookson The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing Cell Host Microbe 12 2012 799 805
23. X.Y. Lin, M.S. Choi, and A.G. Porter Expression analysis of the human caspase-1 subfamily reveals specific regulation of the CASP5 gene by lipopolysaccharide and interferon-gamma J. Biol. Chem. 275 2000 39920 39926
24. S. Mariathasan, K. Newton, D.M. Monack, D. Vucic, D.M. French, W.P. Lee, M. Roose-Girma, S. Erickson, and V.M. Dixit Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf Nature 430 2004 213 218
25. S. Mariathasan, D.S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W.P. Lee, Y. Weinrauch, D.M. Monack, and V.M. Dixit Cryopyrin activates the inflammasome in response to toxins and ATP Nature 440 2006 228 232
26. K.D. Mayer-Barber, D.L. Barber, K. Shenderov, S.D. White, M.S. Wilson, A. Cheever, D. Kugler, S. Hieny, P. Caspar, G. Núñez, and et al. Caspase-1 independent IL-1β production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo J. Immunol. 184 2010 3326 3330
27. E. Meunier, M.S. Dick, R.F. Dreier, N. Schürmann, D. Kenzelmann Broz, S. Warming, M. Roose-Girma, D. Bumann, N. Kayagaki, K. Takeda, and et al. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases Nature 509 2014 366 370
28. E.A. Miao, I.A. Leaf, P.M. Treuting, D.P. Mao, M. Dors, A. Sarkar, S.E. Warren, M.D. Wewers, and A. Aderem Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria Nat. Immunol. 11 2010 1136 1142
29. E.A. Miao, D.P. Mao, N. Yudkovsky, R. Bonneau, C.G. Lorang, S.E. Warren, I.A. Leaf, and A. Aderem Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome Proc. Natl. Acad. Sci. USA 107 2010 3076 3080
30. V. Novem, G. Shui, D. Wang, A.K. Bendt, S.H. Sim, Y. Liu, T.W. Thong, S.P. Sivalingam, E.E. Ooi, M.R. Wenk, and G. Tan Structural and biological diversity of lipopolysaccharides from Burkholderia pseudomallei and Burkholderia thailandensis Clin. Vaccine Immunol. 16 2009 1420 1428
31. D.M. Pilla, J.A. Hagar, A.K. Haldar, A.K. Mason, D. Degrandi, K. Pfeffer, R.K. Ernst, M. Yamamoto, E.A. Miao, and J. Coers Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS Proc. Natl. Acad. Sci. USA 111 2014 6046 6051
32. V.A. Rathinam, S.K. Vanaja, L. Waggoner, A. Sokolovska, C. Becker, L.M. Stuart, J.M. Leong, and K.A. Fitzgerald TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria Cell 150 2012 606 619
33. B. Raupach, S.-K. Peuschel, D.M. Monack, and A. Zychlinsky Caspase-1-mediated activation of interleukin-1β (IL-1β) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection Infect. Immun. 74 2006 4922 4926
34. M. Rayamajhi, D.E. Zak, J. Chavarria-Smith, R.E. Vance, and E.A. Miao Cutting edge: Mouse NAIP1 detects the type III secretion system needle protein J. Immunol. 191 2013 3986 3989
35. M. Rayamajhi, Y. Zhang, and E. Miao Detection of Pyroptosis by Measuring Released Lactate Dehydrogenase Activity C.M. De Nardo, E. Latz, The Inflammasome 2013 Humana Press 85 90
36. G.R. Robbins, A.D. Truax, B.K. Davis, L. Zhang, W.J. Brickey, and J.P.-Y. Ting Regulation of class I major histocompatibility complex (MHC) by nucleotide-binding domain, leucine-rich repeat-containing (NLR) proteins J. Biol. Chem. 287 2012 24294 24303
37. R. Schauvliege, J. Vanrobaeys, P. Schotte, and R. Beyaert Caspase-11 gene expression in response to lipopolysaccharide and interferon-γ requires nuclear factor-κ B and signal transducer and activator of transcription (STAT) 1 J. Biol. Chem. 277 2002 41624 41630
38. M. Schneider, A.G. Zimmermann, R.A. Roberts, L. Zhang, K.V. Swanson, H. Wen, B.K. Davis, I.C. Allen, E.K. Holl, Z. Ye, and et al. The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-κB Nat. Immunol. 13 2012 823 831
39. J. Shi, Y. Zhao, Y. Wang, W. Gao, J. Ding, P. Li, L. Hu, and F. Shao Inflammatory caspases are innate immune receptors for intracellular LPS Nature 514 2014 187 192
40. L.P. Shornick, P. De Togni, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R.W. Karr, T.A. Ferguson, and D.D. Chaplin Mice deficient in IL-1beta manifest impaired contact hypersensitivity to trinitrochlorobenzone J. Exp. Med. 183 1996 1427 1436
41. F. Souza-Fonseca-Guimaraes, M. Adib-Conquy, and J.-M. Cavaillon Natural killer (NK) cells in antibacterial innate immunity: angels or devils? Mol. Med. 18 2012 270 285
42. K. Takeda, H. Tsutsui, T. Yoshimoto, O. Adachi, N. Yoshida, T. Kishimoto, H. Okamura, K. Nakanishi, and S. Akira Defective NK cell activity and Th1 response in IL-18-deficient mice Immunity 8 1998 383 390
43. P.G. Thomas, P. Dash, J.R. Aldridge Jr., A.H. Ellebedy, C. Reynolds, A.J. Funk, W.J. Martin, M. Lamkanfi, R.J. Webby, K.L. Boyd, and et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1 Immunity 30 2009 566 575
44. N.M. Tsuji, H. Tsutsui, E. Seki, K. Kuida, H. Okamura, K. Nakanishi, and R.A. Flavell Roles of caspase-1 in Listeria infection in mice Int. Immunol. 16 2004 335 343
45. P. Utaisincharoen, N. Anuntagool, K. Limposuwan, P. Chaisuriya, and S. Sirisinha Involvement of beta interferon in enhancing inducible nitric oxide synthase production and antimicrobial activity of Burkholderia pseudomallei-infected macrophages Infect. Immun. 71 2003 3053 3057
46. W.J. Wiersinga, B.J. Currie, and S.J. Peacock Melioidosis N. Engl. J. Med. 367 2012 1035 1044
47. J. Wu, S. Huang, X. Zhao, M. Chen, Y. Lin, Y. Xia, C. Sun, X. Yang, J. Wang, Y. Guo, and et al. Poly(I:C) treatment leads to interferon-dependent clearance of hepatitis B virus in a hydrodynamic injection mouse model J. Virol. 88 2014 10421 10431
48. J. Yang, Y. Zhao, J. Shi, and F. Shao Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation Proc. Natl. Acad. Sci. USA 110 2013 14408 14413
49. Y. Zhao, J. Yang, J. Shi, Y.-N. Gong, Q. Lu, H. Xu, L. Liu, and F. Shao The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus Nature 477 2011 596 600