Cell death triggered by yersinia enterocolitica identifies processing of the proinflammatory signal adapter myd88 as a general event in the execution of apoptosis

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1209-1219

  Novikova, Lena ^a   Czymmeck, Nicole ^a   Deuretzbacher, Anne ^a,b   Buck, Friedrich ^a   Richter, Kathleen ^c,d   Weber, Alexander N R ^e   Aepfelbacher, Martin ^a   Ruckdeschel, Klaus ^a,c  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d GLAXOSMITHKLINE   (United States)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CASPASE 3; CYTOKINE RESPONSE MODIFIER A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; MYELOID DIFFERENTIATION FACTOR 88; STAUROSPORINE; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

APOPTOSIS; ARTICLE; BACTERIAL LOAD; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEEDBACK SYSTEM; FRAGMENTATION REACTION; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR BINDING; SIGNAL TRANSDUCTION; YERSINIA ENTEROCOLITICA; YERSINIOSIS;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CASPASE 3; EPITHELIAL CELLS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-BETA; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MACROPHAGES; MAP KINASE KINASE KINASES; MEMBRANE GLYCOPROTEINS; MICE; MOLECULAR SEQUENCE DATA; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-1; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TOLL-LIKE RECEPTORS; YERSINIA ENTEROCOLITICA;

EID: 84893391042     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203464     Document Type: Article

References (48)

1. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
2. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
3. O'Neill, L. A., and A. G. Bowie. 2007. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7: 353-364.
4. Janssens, S., and R. Beyaert. 2002. A universal role for MyD88 in TLR/IL-1Rmediated signaling. Trends Biochem. Sci. 27: 474-482.
5. Salaun, B., P. Romero, and S. Lebecque. 2007. Toll-like receptors' two-edged sword: when immunity meets apoptosis. Eur. J. Immunol. 37: 3311-3318.
6. Vanlangenakker, N., T. Vanden Berghe, and P. Vandenabeele. 2012. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 19: 75-86.
7. Brodsky, I. E., and R. Medzhitov. 2009. Targeting of immune signalling networks by bacterial pathogens. Nat. Cell Biol. 11: 521-526.
8. Finlay, B. B., and G. McFadden. 2006. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124: 767-782.
9. Aepfelbacher, M., C. Trasak, and K. Ruckdeschel. 2007. Effector functions of pathogenic Yersinia species. Thromb. Haemost. 98: 521-529.
10. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59: 69-89.
11. Mittal, R., S. Y. Peak-Chew, and H. T. McMahon. 2006. Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl. Acad. Sci. USA 103: 18574-18579.
12. Mukherjee, S., G. Keitany, Y. Li, Y. Wang, H. L. Ball, E. J. Goldsmith, and K. Orth. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
13. Ruckdeschel, K., O. Mannel, K. Richter, C. A. Jacobi, K. Trulzsch, B. Rouot, and J. Heesemann. 2001. Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J. Immunol. 166: 1823-1831.
14. Zhang, Y., A. T. Ting, K. B. Marcu, and J. B. Bliska. 2005. Inhibition of MAPK and NF-kappa B pathways is necessary for rapid apoptosis in macrophages infected with Yersinia. J. Immunol. 174: 7939-7949.
15. Haase, R., C. J. Kirschning, A. Sing, P. Schrottner, K. Fukase, S. Kusumoto, H. Wagner, J. Heesemann, and K. Ruckdeschel. 2003. A dominant role of Tolllike receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J. Immunol. 171: 4294-4303.
16. Ruckdeschel, K., G. Pfaffinger, R. Haase, A. Sing, H. Weighardt, G. Hacker, B. Holzmann, and J. Heesemann. 2004. Signaling of apoptosis through TLRs critically involves toll/IL-1 receptor domain-containing adapter inducing IFNbeta, but not MyD88, in bacteria-infected murine macrophages. J. Immunol. 173: 3320-3328.
17. Han, K. J., X. Su, L. G. Xu, L. H. Bin, J. Zhang, and H. B. Shu. 2004. Mechanisms of the TRIF-induced interferon-stimulated response element and NFkappaB activation and apoptosis pathways. J. Biol. Chem. 279: 15652-15661.
18. Kaiser, W. J., and M. K. Offermann. 2005. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174: 4942-4952.
19. Fischer, U., R. U. Janicke, and K. Schulze-Osthoff. 2003. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 10: 76-100.
20. Frelin, C., V. Imbert, V. Bottero, N. Gonthier, A. K. Samraj, K. Schulze-Osthoff, P. Auberger, G. Courtois, and J. F. Peyron. 2008. Inhibition of the NF-kappaB survival pathway via caspase-dependent cleavage of the IKK complex scaffold protein and NF-kappaB essential modulator NEMO. Cell Death Differ. 15: 152-160.
21. Rebsamen, M., E. Meylan, J. Curran, and J. Tschopp. 2008. The antiviral adaptor proteins Cardif and Trif are processed and inactivated by caspases. Cell Death Differ. 15: 1804-1811.
22. Tang, G., J. Yang, Y. Minemoto, and A. Lin. 2001. Blocking caspase-3-mediated proteolysis of IKKbeta suppresses TNF-Alpha-induced apoptosis. Mol. Cell 8: 1005-1016.
23. Youn, H. S., J. Y. Lee, K. A. Fitzgerald, H. A. Young, S. Akira, and D. H. Hwang. 2005. Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: molecular targets are TBK1 and RIP1 in TRIF complex. J. Immunol. 175: 3339-3346.
24. Wesche, H., W. J. Henzel, W. Shillinglaw, S. Li, and Z. Cao. 1997. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
25. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672.
26. Uren, A. G., M. Pakusch, C. J. Hawkins, K. L. Puls, and D. L. Vaux. 1996. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-Associated factors. Proc. Natl. Acad. Sci. USA 93: 4974-4978.
27. Li, S., A. Strelow, E. J. Fontana, and H. Wesche. 2002. IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. USA 99: 5567-5572.
28. Kirschning, C. J., H. Wesche, T. Merrill Ayres, and M. Rothe. 1998. Human tolllike receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 188: 2091-2097.
29. Nagai, Y., S. Akashi, M. Nagafuku, M. Ogata, Y. Iwakura, S. Akira, T. Kitamura, A. Kosugi, M. Kimoto, and K. Miyake. 2002. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3: 667-672.
30. Crawford, E. D., and J. A. Wells. 2011. Caspase substrates and cellular remodeling. Annu. Rev. Biochem. 80: 1055-1087.
31. Mahrus, S., J. C. Trinidad, D. T. Barkan, A. Sali, A. L. Burlingame, and J. A.Wells. 2008. Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134: 866-876.
32. Gay, N. J., M. Gangloff, and L. A. O'Neill. 2011. What the Myddosome structure tells us about the initiation of innate immunity. Trends Immunol. 32: 104-109.
33. Cheng, H., T. Addona, H. Keshishian, E. Dahlstrand, C. Lu, M. Dorsch, Z. Li, A. Wang, T. D. Ocain, P. Li, et al. 2007. Regulation of IRAK-4 kinase activity via autophosphorylation within its activation loop. Biochem. Biophys. Res. Commun. 352: 609-616.
34. Ruckdeschel, K., A. Roggenkamp, V. Lafont, P. Mangeat, J. Heesemann, and B. Rouot. 1997. Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect. Immun. 65: 4813-4821.
35. Sakurai, H., H. Miyoshi, J. Mizukami, and T. Sugita. 2000. Phosphorylationdependent activation of TAK1 mitogen-Activated protein kinase kinase kinase by TAB1. FEBS Lett. 474: 141-145.
36. He, B., N. Lu, and Z. Zhou. 2009. Cellular and nuclear degradation during apoptosis. Curr. Opin. Cell Biol. 21: 900-912.
37. Labbé, K., and M. Saleh. 2008. Cell death in the host response to infection. Cell Death Differ. 15: 1339-1349.
38. Lamkanfi, M., and V. M. Dixit. 2010. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8: 44-54.
39. Hitomi, J., D. E. Christofferson, A. Ng, J. Yao, A. Degterev, R. J. Xavier, and J. Yuan. 2008. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135: 1311-1323.
40. Mocarski, E. S., J. W. Upton, and W. J. Kaiser. 2012. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12: 79-88.
41. De Trez, C., B. Pajak, M. Brait, N. Glaichenhaus, J. Urbain, M. Moser, G. Lauvau, and E. Muraille. 2005. TLR4 and Toll-IL-1 receptor domaincontaining adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J. Immunol. 175: 839-846.
42. Johnson, C. E., and S. Kornbluth. 2008. Caspase cleavage is not for everyone. Cell 134: 720-721.
43. Dix, M. M., G. M. Simon, and B. F. Cravatt. 2008. Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 134: 679-691.
44. Piatkov, K. I., C. S. Brower, and A. Varshavsky. 2012. The N-end rule pathway counteracts cell death by destroying proapoptotic protein fragments. Proc. Natl. Acad. Sci. USA 109: E1839-E1847.
45. Avbelj, M., S. Horvat, and R. Jerala. 2011. The role of intermediary domain of MyD88 in cell activation and therapeutic inhibition of TLRs. J. Immunol. 187: 2394-2404.
46. Schrader, K., J. Huai, L. Jockel, C. Oberle, and C. Borner. 2010. Non-caspase proteases: triggers or amplifiers of apoptosis? Cell. Mol. Life Sci. 67: 1607-1618.
47. Cataisson, C., R. Salcedo, S. Hakim, B. A. Moffitt, L. Wright, M. Yi, R. Stephens, R. M. Dai, L. Lyakh, D. Schenten, et al. 2012. IL-1R-MyD88 signaling in keratinocyte transformation and carcinogenesis. J. Exp. Med. 209: 1689-1702.
48. Coste, I., K. Le Corf, A. Kfoury, I. Hmitou, S. Druillennec, P. Hainaut, A. Eychene, S. Lebecque, and T. Renno. 2010. Dual function of MyD88 in RAS signaling and inflammation, leading to mouse and human cell transformation. J. Clin. Invest. 120: 3663-3667.