Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens

Cell Host and Microbe

Volumn 16, Issue 2, 2014, Pages 249-256

  Knodler, Leigh A ^a,b   Crowley, Shauna M ^c   Sham, Ho Pan ^c   Yang, Hyungjun ^c   Wrande, Marie ^a   Ma, Caixia ^c   Ernst, Robert K ^d   Steele Mortimer, Olivia ^b   Celli, Jean ^a,b   Vallance, Bruce A ^c  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CASPASE 11; CASPASE 4; INFLAMMASOME; INTERLEUKIN 18; SMALL INTERFERING RNA; CASP11 PROTEIN, MOUSE; CASP4 PROTEIN, HUMAN; CASPASE; INITIATOR CASPASE; INTERLEUKIN 18 PROTEIN, HUMAN; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTERITIS; ENTEROBACTERIACEAE; ENTEROPATHOGENIC ESCHERICHIA COLI; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTRACELLULAR SPACE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PYROPTOSIS; RNA INTERFERENCE; SALMONELLA TYPHIMURIUM; ANIMAL; C57BL MOUSE; ENZYME ACTIVATION; ENZYMOLOGY; ESCHERICHIA COLI INFECTION; GASTROENTERITIS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SALMONELLA ENTERICA; SALMONELLOSIS; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; CASPASES; CASPASES, INITIATOR; CELL LINE, TUMOR; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME ACTIVATION; ESCHERICHIA COLI INFECTIONS; GASTROENTERITIS; HUMANS; INFLAMMASOMES; INTERLEUKIN-18; INTESTINAL MUCOSA; LIPOPOLYSACCHARIDES; MICE, INBRED C57BL; MICE, KNOCKOUT; SALMONELLA ENTERICA; SALMONELLA INFECTIONS;

EID: 84911992879     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.07.002     Document Type: Article

References (41)

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. A. Akhter, K. Caution, A. Abu Khweek, M. Tazi, B.A. Abdulrahman, D.H.A. Abdelaziz, O.H. Voss, A.I. Doseff, H. Hassan, and A.K. Azad et al. Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization Immunity 37 2012 35 47
3. D. Artis Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut Nat. Rev. Immunol. 8 2008 411 420
4. M. Barthel, S. Hapfelmeier, L. Quintanilla-Martínez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Rüssmann, and W.-D. Hardt Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host Infect. Immun. 71 2003 2839 2858
5. M. Bielaszewska, C. Rüter, L. Kunsmann, L. Greune, A. Bauwens, W. Zhang, T. Kuczius, K.S. Kim, A. Mellmann, M.A. Schmidt, and H. Karch Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis PLoS Pathog. 9 2013 e1003797
6. 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
7. S. Crépin, J. Harel, and C.M. Dozois Chromosomal complementation using Tn7 transposon vectors in Enterobacteriaceae Appl. Environ. Microbiol. 78 2012 6001 6008
8. D. Demon, A. Kuchmiy, A. Fossoul, Q. Zhu, T.-D. Kanneganti, and M. Lamkanfi Caspase-11 is expressed in the colonic mucosa and protects against dextran sodium sulfate-induced colitis Mucosal Immunol. 2014 10.1038/mi.2014.36
9. D. Drecktrah, S. Levine-Wilkinson, T. Dam, S. Winfree, L.A. Knodler, T.A. Schroer, and O. Steele-Mortimer Dynamic behavior of Salmonella-induced membrane tubules in epithelial cells Traffic 9 2008 2117 2129
10. F. Fassy, O. Krebs, H. Rey, B. Komara, C. Gillard, C. Capdevila, C. Yea, C. Faucheu, A.M. Blanchet, C. Miossec, and A. Diu-Hercend Enzymatic activity of two caspases related to interleukin-1beta-converting enzyme Eur. J. Biochem. 253 1998 76 83
11. G. Gonzalez-Escobedo, and J.S. Gunn Gallbladder epithelium as a niche for chronic Salmonella carriage Infect. Immun. 81 2013 2920 2930
12. Y. Gu, and J. Rosenblatt New emerging roles for epithelial cell extrusion Curr. Opin. Cell Biol. 24 2012 865 870
13. Y. Gu, K. Kuida, H. Tsutsui, G. Ku, K. Hsiao, M.A. Fleming, N. Hayashi, K. Higashino, H. Okamura, and K. Nakanishi et al. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme Science 275 1997 206 209
14. 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
15. S.K. Hoiseth, and B.A. Stocker Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines Nature 291 1981 238 239
16. H.C. Jung, L. Eckmann, S.K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M.F. Kagnoff A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion J. Clin. Invest. 95 1995 55 65
17. G. Kang, A.B. Pulimood, R. Koshi, A. Hull, D. Acheson, P. Rajan, G.T. Keusch, V.I. Mathan, and M.M. Mathan A monkey model for enterohemorrhagic Escherichia coli infection J. Infect. Dis. 184 2001 206 210
18. S.J. Kang, R. Popat, C. Bragdon, K. Odonnell, S. Phelan, J. Yuan, and S.T. Sonis Caspase-11 is not necessary for chemotherapy-induced intestinal mucositis DNA Cell Biol. 23 2004 490 495
19. N. Kayagaki, S. Warming, M. Lamkanfi, L. Vande Walle, S. Louie, J. Dong, K. Newton, Y. Qu, J. Liu, and S. Heldens et al. Non-canonical inflammasome activation targets caspase-11 Nature 479 2011 117 121
20. N. Kayagaki, M.T. Wong, I.B. Stowe, S.R. Ramani, L.C. Gonzalez, S. Akashi-Takamura, K. Miyake, J. Zhang, W.P. Lee, and A. Muszyński et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4 Science 341 2013 1246 1249
21. L.A. Knodler, V. Nair, and O. Steele-Mortimer Quantitative assessment of cytosolic Salmonella in epithelial cells PLoS ONE 9 2014 e84681
22. L.A. Knodler, B.A. Vallance, J. Celli, S. Winfree, B. Hansen, M. Montero, and O. Steele-Mortimer Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia Proc. Natl. Acad. Sci. USA 107 2010 17733 17738
23. T. Kobayashi, M. Ogawa, T. Sanada, H. Mimuro, M. Kim, H. Ashida, R. Akakura, M. Yoshida, M. Kawalec, and J.-M. Reichhart et al. The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection Cell Host Microbe 13 2013 570 583
24. M. Lamkanfi Emerging inflammasome effector mechanisms Nat. Rev. Immunol. 11 2011 213 220
25. R.C. Laughlin, L.A. Knodler, R. Barhoumi, H.R. Payne, J. Wu, G. Gomez, R. Pugh, S.D. Lawhon, A.J. Bäumler, O. Steele-Mortimer, and L.G. Adams Spatial segregation of virulence gene expression during acute enteric infection with Salmonella enterica serovar Typhimurium MBio 5 2014 e00946-e13
26. M.M. Levine, E.J. Bergquist, D.R. Nalin, D.H. Waterman, R.B. Hornick, C.R. Young, and S. Sotman Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive Lancet 1 1978 1119 1122
27. 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
28. P. Malik-Kale, S. Winfree, and O. Steele-Mortimer The bimodal lifestyle of intracellular Salmonella in epithelial cells: replication in the cytosol obscures defects in vacuolar replication PLoS ONE 7 2012 e38732
29. L.E. Månsson, M. Montero, M. Zarepour, K.S. Bergstrom, C. Ma, T. Huang, C. Man, G.A. Grassl, and B.A. Vallance MyD88 signaling promotes both mucosal homeostatic and fibrotic responses during Salmonella-induced colitis Am. J. Physiol. Gastrointest. Liver Physiol. 303 2012 G311 G323
30. F. Martinon, K. Burns, and J. Tschopp The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta Mol. Cell 10 2002 417 426
31. A. Menendez, E.T. Arena, J.A. Guttman, L. Thorson, B.A. Vallance, W. Vogl, and B.B. Finlay Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever J. Infect. Dis. 200 2009 1703 1713
32. C.P. Miller, M. Bohnhoff, and D. Rifkind The effect of an antibiotic on the susceptibility of the mouse's intestinal tract to Salmonella infection Trans. Am. Clin. Climatol. Assoc. 68 1956-1957 51 55 discussion 55-58
33. S. Myeni, R. Child, T.W. Ng, J.J. Kupko 3rd, T.D. Wehrly, S.F. Porcella, L.A. Knodler, and J. Celli Brucella modulates secretory trafficking via multiple type IV secretion effector proteins PLoS Pathog. 9 2013 e1003556
34. T.M. Ng, and D.M. Monack Revisiting caspase-11 function in host defense Cell Host Microbe 14 2013 9 14
35. J.M. Ritchie, H. Rui, X. Zhou, T. Iida, T. Kodoma, S. Ito, B.M. Davis, R.T. Bronson, and M.K. Waldor Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea PLoS Pathog. 8 2012 e1002593
36. R.L. Santos, S. Zhang, R.M. Tsolis, R.A. Kingsley, L.G. Adams, and A.J. Bäumler Animal models of Salmonella infections: enteritis versus typhoid fever Microbes Infect. 3 2001 1335 1344
37. G. Sollberger, G.E. Strittmatter, M. Kistowska, L.E. French, and H.-D. Beer Caspase-4 is required for activation of inflammasomes J. Immunol. 188 2012 1992 2000
38. R.H. Valdivia, and S. Falkow Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction Mol. Microbiol. 22 1996 367 378
39. F.L. van de Veerdonk, M.G. Netea, C.A. Dinarello, and L.A.B. Joosten Inflammasome activation and IL-1β and IL-18 processing during infection Trends Immunol. 32 2011 110 116
40. T.S. Wallis, W.G. Starkey, J. Stephen, S.J. Haddon, M.P. Osborne, and D.C. Candy The nature and role of mucosal damage in relation to Salmonella typhimurium-induced fluid secretion in the rabbit ileum J. Med. Microbiol. 22 1986 39 49
41. Y. Yin, Y. Yan, X. Jiang, J. Mai, N.C. Chen, H. Wang, and X.-F. Yang Inflammasomes are differentially expressed in cardiovascular and other tissues Int. J. Immunopathol. Pharmacol. 22 2009 311 322