The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection

Cell Host and Microbe

Volumn 13, Issue 5, 2013, Pages 570-583

  Kobayashi, Taira ^a   Ogawa, Michinaga ^a   Sanada, Takahito ^a   Mimuro, Hitomi ^a   Kim, Minsoo ^a   Ashida, Hiroshi ^a   Akakura, Reiko ^a   Yoshida, Mitsutaka ^b   Kawalec, Magdalena ^c   Reichhart, Jean Marc ^c   Mizushima, Tsunehiro ^d   Sasakawa, Chihiro ^a,e,f  

^a UNIVERSITY OF TOKYO   (Japan)

^b JUNTENDO UNIVERSITY   (Japan)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF HYOGO   (Japan)

^e NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

^f CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN OSPC3; CASPASE 4; CASPASE 4 P19; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CELL DEATH; CONTROLLED STUDY; DIMERIZATION; EFFECTOR CELL; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; ENZYME ACTIVE SITE; ENZYME INHIBITION; EPITHELIUM CELL; EXPERIMENTAL GUINEA PIG; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MOTIF; SALMONELLA TYPHIMURIUM; SHIGELLA FLEXNERI; SHIGELLOSIS;

EID: 84877844771     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.04.012     Document Type: Article

References (61)

1. A. Akhter, K. Caution, A. Abu Khweek, M. Tazi, B.A. Abdulrahman, D.H. Abdelaziz, O.H. Voss, A.I. Doseff, H. Hassan, and A.K. Azad Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization Immunity 37 2012 35 47
2. S. Al-Khodor, C.T. Price, A. Kalia, and Y. Abu Kwaik Functional diversity of ankyrin repeats in microbial proteins Trends Microbiol. 18 2010 132 139
3. D. Arnoult, L. Carneiro, I. Tattoli, and S.E. Girardin The role of mitochondria in cellular defense against microbial infection Semin. Immunol. 21 2009 223 232
4. H. Ashida, M. Kim, M. Schmidt-Supprian, A. Ma, M. Ogawa, and C. Sasakawa A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response Nat. Cell Biol. 12 2010 66 73 1-9
5. H. Ashida, H. Mimuro, M. Ogawa, T. Kobayashi, T. Sanada, M. Kim, and C. Sasakawa Cell death and infection: a double-edged sword for host and pathogen survival J. Cell Biol. 195 2011 931 942
6. H. Ashida, M. Ogawa, H. Mimuro, T. Kobayashi, T. Sanada, and C. Sasakawa Shigella are versatile mucosal pathogens that circumvent the host innate immune system Curr. Opin. Immunol. 23 2011 448 455
7. H. Ashida, M. Ogawa, M. Kim, H. Mimuro, and C. Sasakawa Bacteria and host interactions in the gut epithelial barrier Nat. Chem. Biol. 8 2012 36 45
8. K. Baruch, L. Gur-Arie, C. Nadler, S. Koby, G. Yerushalmi, Y. Ben-Neriah, O. Yogev, E. Shaulian, C. Guttman, R. Zarivach, and I. Rosenshine Metalloprotease type III effectors that specifically cleave JNK and NF-κB EMBO J. 30 2011 221 231
9. J. Bergounioux, R. Elisee, A.L. Prunier, F. Donnadieu, B. Sperandio, P. Sansonetti, and L. Arbibe Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche Cell Host Microbe 11 2012 240 252
10. T. Bergsbaken, S.L. Fink, and B.T. Cookson Pyroptosis: host cell death and inflammation Nat. Rev. Microbiol. 7 2009 99 109
11. S.M. Best Viral subversion of apoptotic enzymes: escape from death row Annu. Rev. Microbiol. 62 2008 171 192
12. 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
13. A.T. Brunger Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2 2007 2728 2733
14. B.A. Callus, and D.L. Vaux Caspase inhibitors: viral, cellular and chemical Cell Death Differ. 14 2007 73 78
15. L.A. Carneiro, L.H. Travassos, F. Soares, I. Tattoli, J.G. Magalhaes, M.T. Bozza, M.C. Plotkowski, P.J. Sansonetti, J.D. Molkentin, D.J. Philpott, and S.E. Girardin Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells Cell Host Microbe 5 2009 123 136
16. J.K. Crane, S. Majumdar, and D.F. Pickhardt 3rd Host cell death due to enteropathogenic Escherichia coli has features of apoptosis Infect. Immun. 67 1999 2575 2584
17. J.K. Crane, B.P. McNamara, and M.S. Donnenberg Role of EspF in host cell death induced by enteropathogenic Escherichia coli Cell. Microbiol. 3 2001 197 211
18. R. Dewoody, P.M. Merritt, A.S. Houppert, and M.M. Marketon YopK regulates the Yersinia pestis type III secretion system from within host cells Mol. Microbiol. 79 2011 1445 1461
19. L. Diacovich, and J.P. Gorvel Bacterial manipulation of innate immunity to promote infection Nat. Rev. Microbiol. 8 2010 117 128
20. W.C. Earnshaw, L.M. Martins, and S.H. Kaufmann Mammalian caspases: structure, activation, substrates, and functions during apoptosis Annu. Rev. Biochem. 68 1999 383 424
21. S. Elmore Apoptosis: a review of programmed cell death Toxicol. Pathol. 35 2007 495 516
22. S.L. Fink, and B.T. Cookson Pyroptosis and host cell death responses during Salmonella infection Cell. Microbiol. 9 2007 2562 2570
23. M. Garcia-Calvo, E.P. Peterson, B. Leiting, R. Ruel, D.W. Nicholson, and N.A. Thornberry Inhibition of human caspases by peptide-based and macromolecular inhibitors J. Biol. Chem. 273 1998 32608 32613
24. P. Golstein, and G. Kroemer Cell death by necrosis: towards a molecular definition Trends Biochem. Sci. 32 2007 37 43
25. C. Hemrajani, C.N. Berger, K.S. Robinson, O. Marchès, A. Mousnier, and G. Frankel NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection Proc. Natl. Acad. Sci. USA 107 2010 3129 3134
26. J. Hitomi, T. Katayama, Y. Eguchi, T. Kudo, M. Taniguchi, Y. Koyama, T. Manabe, S. Yamagishi, Y. Bando, and K. Imaizumi Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death J. Cell Biol. 165 2004 347 356
27. R.M. Jones, H. Wu, C. Wentworth, L. Luo, L. Collier-Hyams, and A.S. Neish Salmonella AvrA Coordinates Suppression of Host Immune and Apoptotic Defenses via JNK Pathway Blockade Cell Host Microbe 3 2008 233 244
28. S. Kamada, Y. Funahashi, and Y. Tsujimoto Caspase-4 and caspase-5, members of the ICE/CED-3 family of cysteine proteases, are CrmA-inhibitable proteases Cell Death Differ. 4 1997 473 478
29. P. Karki, G.R. Dahal, and I.S. Park Both dimerization and interdomain processing are essential for caspase-4 activation Biochem. Biophys. Res. Commun. 356 2007 1056 1061
30. N. Kayagaki, S. Warming, M. Lamkanfi, L. Vande Walle, S. Louie, J. Dong, K. Newton, Y. Qu, J. Liu, and S. Heldens Non-canonical inflammasome activation targets caspase-11 Nature 479 2011 117 121
31. M. Kim, M. Ogawa, Y. Fujita, Y. Yoshikawa, T. Nagai, T. Koyama, S. Nagai, A. Lange, R. Fässler, and C. Sasakawa Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment Nature 459 2009 578 582
32. M. Kim, H. Ashida, M. Ogawa, Y. Yoshikawa, H. Mimuro, and C. Sasakawa Bacterial interactions with the host epithelium Cell Host Microbe 8 2010 20 35
33. L.A. Knodler, B.B. Finlay, and O. Steele-Mortimer The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt J. Biol. Chem. 280 2005 9058 9064
34. T. Komiyama, C.A. Ray, D.J. Pickup, A.D. Howard, N.A. Thornberry, E.P. Peterson, and G. Salvesen Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition J. Biol. Chem. 269 1994 19331 19337
35. W.W. Kum, B.C. Lo, H.B. Yu, and B.B. Finlay Protective role of Akt2 in Salmonella enterica serovar typhimurium-induced gastroenterocolitis Infect. Immun. 79 2011 2554 2566
36. S. Kumar, C.R. Hanning, M.R. Brigham-Burke, D.J. Rieman, R. Lehr, S. Khandekar, R.B. Kirkpatrick, G.F. Scott, J.C. Lee, and F.J. Lynch Interleukin-1F7B (IL-1H4/IL-1F7) is processed by caspase-1 and mature IL-1F7B binds to the IL-18 receptor but does not induce IFN-gamma production Cytokine 18 2002 61 71
37. K. Labbé, and M. Saleh Cell death in the host response to infection Cell Death Differ. 15 2008 1339 1349
38. M. Lamkanfi, and V.M. Dixit Manipulation of host cell death pathways during microbial infections Cell Host Microbe 8 2010 44 54
39. 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
40. T. Le Gall, M. Mavris, M.C. Martino, M.L. Bernardini, E. Denamur, and C. Parsot Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri Microbiology 151 2005 951 962
41. J. Li, A. Mahajan, and M.D. Tsai Ankyrin repeat: a unique motif mediating protein-protein interactions Biochemistry 45 2006 15168 15178
42. F. Martinon, and J. Tschopp Inflammatory caspases and inflammasomes: master switches of inflammation Cell Death Differ. 14 2007 10 22
43. S. Matsuzaki, T. Hiratsuka, R. Kuwahara, T. Katayama, and M. Tohyama Caspase-4 is partially cleaved by calpain via the impairment of Ca2+ homeostasis under the ER stress Neurochem. Int. 56 2010 352 356
44. E.A. Miao, J.V. Rajan, and A. Aderem Caspase-1-induced pyroptotic cell death Immunol. Rev. 243 2011 206 214
45. M. Miura, H. Zhu, R. Rotello, E.A. Hartwieg, and J. Yuan Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3 Cell 75 1993 653 660
46. T. Nagai, A. Abe, and C. Sasakawa Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: critical role of the 16th leucine residue in EspF J. Biol. Chem. 280 2005 2998 3011
47. J.P. Nougayrède, and M.S. Donnenberg Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway Cell. Microbiol. 6 2004 1097 1111
48. A. Phalipon, and P.J. Sansonetti Shigella's ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? Immunol. Cell Biol. 85 2007 119 129
49. 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
50. C.A. Ray, R.A. Black, S.R. Kronheim, T.A. Greenstreet, P.R. Sleath, G.S. Salvesen, and D.J. Pickup Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme Cell 69 1992 597 604
51. K. Ray, B. Marteyn, P.J. Sansonetti, and C.M. Tang Life on the inside: the intracellular lifestyle of cytosolic bacteria Nat. Rev. Microbiol. 7 2009 333 340
52. T. Rudel, O. Kepp, and V. Kozjak-Pavlovic Interactions between bacterial pathogens and mitochondrial cell death pathways Nat. Rev. Microbiol. 8 2010 693 705
53. Y. Shi Mechanisms of caspase activation and inhibition during apoptosis Mol. Cell 9 2002 459 470
54. D.H. Shim, T. Suzuki, S.Y. Chang, S.M. Park, P.J. Sansonetti, C. Sasakawa, and M.N. Kweon New animal model of shigellosis in the Guinea pig: its usefulness for protective efficacy studies J. Immunol. 178 2007 2476 2482
55. 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
56. S.W. Tait, and D.R. Green Mitochondria and cell death: outer membrane permeabilization and beyond Nat. Rev. Mol. Cell Biol. 11 2010 621 632
57. J. Tschopp, and K. Schroder NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10 2010 210 215
58. P. Vandenabeele, L. Galluzzi, T. Vanden Berghe, and G. Kroemer Molecular mechanisms of necroptosis: an ordered cellular explosion Nat. Rev. Mol. Cell Biol. 11 2010 700 714
59. N.S. Wilson, V. Dixit, and A. Ashkenazi Death receptor signal transducers: nodes of coordination in immune signaling networks Nat. Immunol. 10 2009 348 355
60. S.E. Winter, and A.J. Bäumler Salmonella exploits suicidal behavior of epithelial cells Front. Microbiol. 2 2011 48
61. Q. Zhou, S. Snipas, K. Orth, M. Muzio, V.M. Dixit, and G.S. Salvesen Target protease specificity of the viral serpin CrmA. Analysis of five caspases J. Biol. Chem. 272 1997 7797 7800