Caspase-8 inactivation in T cells increases necroptosis and suppresses autoimmunity in Bim-/- mice

Journal of Cell Biology

Volumn 195, Issue 2, 2011, Pages 277-291

  Bohgaki, Toshiyuki ^a   Mozo, Julien ^a   Salmena, Leonardo ^b   Matysiak Zablocki, Elzbieta ^a   Bohgaki, Miyuki ^a   Sanchez, Otto ^c   Strasser, Andreas ^d   Hakem, Anne ^a   Hakem, Razqallah ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ONTARIO INSTITUTE OF TECHNOLOGY   (Canada)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CASPASE 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; ENZYME INACTIVATION; IMMUNOSUPPRESSIVE TREATMENT; LIFESPAN; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOIMMUNITY; CASPASE 8; CELL PROLIFERATION; CELL SURVIVAL; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS; T-LYMPHOCYTES;

MUS;

EID: 80155206809     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201103053     Document Type: Article

References (59)

1. Bell, B.D., S. Leverrier, B.M. Weist, R.H. Newton, A.F. Arechiga, K.A. Luhrs, N.S. Morrissette, and C.M. Walsh. 2008. FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc. Natl. Acad. Sci. USA. 105:16677-16682. http://dx.doi.org/10.1073/pnas.0808597105
2. Bidère, N., H.C. Su, and M.J. Lenardo. 2006. Genetic disorders of programmed cell death in the immune system. Annu. Rev. Immunol. 24:321-352. http://dx.doi.org/10.1146/annurev.immunol.24.021605.090513
3. Bouillet, P., and L.A. O'Reilly. 2009. CD95, BIM and T cell homeostasis. Nat. Rev. Immunol. 9:514-519. http://dx.doi.org/10.1038/nri2570
4. Bouillet, P., D. Metcalf, D.C. Huang, D.M. Tarlinton, T.W. Kay, F. Köntgen, J.M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 286:1735-1738. http://dx.doi.org/10.1126/science.286.5445.1735
5. Bouillet, P., J.F. Purton, D.I. Godfrey, L.C. Zhang, L. Coultas, H. Puthalakath, M. Pellegrini, S. Cory, J.M. Adams, and A. Strasser. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature. 415:922-926. http://dx.doi.org/10.1038/415922a
6. Ch'en, I.L., J.S. Tsau, J.D. Molkentin, M. Komatsu, and S.M. Hedrick. 2011. Mechanisms of necroptosis in T cells. J. Exp. Med. 208:633-641. http://dx.doi.org/10.1084/jem.20110251
7. Cho, Y.S., S. Challa, D. Moquin, R. Genga, T.D. Ray, M. Guildford, and F.K. Chan. 2009. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 137:1112-1123. http://dx.doi.org/10.1016/j.cell.2009.05.037
8. Chun, H.J., L. Zheng, M. Ahmad, J. Wang, C.K. Speirs, R.M. Siegel, J.K. Dale, J. Puck, J. Davis, C.G. Hall, et al. 2002. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature. 419:395-399. http://dx.doi.org/10.1038/nature01063
9. Cohen, P.L., and R.A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243-269. http://dx.doi.org/10.1146/annurev.iy.09.040191.001331
10. Davey, G.M., C. Kurts, J.F. Miller, P. Bouillet, A. Strasser, A.G. Brooks, F.R. Carbone, and W.R. Heath. 2002. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J. Exp. Med. 196:947-955. http://dx.doi.org/10.1084/jem.20020827
11. Declercq, W., T. Vanden Berghe, and P. Vandenabeele. 2009. RIP kinases at the crossroads of cell death and survival. Cell. 138:229-232. http://dx.doi.org/10.1016/j.cell.2009.07.006
12. Degterev, A., Z. Huang, M. Boyce, Y. Li, P. Jagtap, N. Mizushima, G.D. Cuny, T.J. Mitchison, M.A. Moskowitz, and J. Yuan. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1:112-119. http://dx.doi.org/10.1038/nchembio711
13. Degterev, A., J. Hitomi, M. Germscheid, I.L. Ch'en, O. Korkina, X. Teng, D. Abbott, G.D. Cuny, C. Yuan, G. Wagner, et al. 2008. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4:313-321. http://dx.doi.org/10.1038/nchembio.83
14. Enders, A., P. Bouillet, H. Puthalakath, Y. Xu, D.M. Tarlinton, and A. Strasser. 2003. Loss of the pro-apoptotic BH3-only Bcl-2 family member Bim inhibits BCR stimulation-induced apoptosis and deletion of autoreactive B cells. J. Exp. Med. 198:1119-1126. http://dx.doi.org/10.1084/jem.20030411
15. Feldmann, M. 2008. Many cytokines are very useful therapeutic targets in disease. J. Clin. Invest. 118:3533-3536. http://dx.doi.org/10.1172/JCI37346
16. Gozuacik, D., and A. Kimchi. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 23:2891-2906. http://dx.doi.org/10.1038/sj.onc.1207521
17. Hao, Z., G.S. Duncan, J. Seagal, Y.W. Su, C. Hong, J. Haight, N.J. Chen, A. Elia, A. Wakeham, W.Y. Li, et al. 2008. Fas receptor expression in germinalcenter B cells is essential for T and B lymphocyte homeostasis. Immunity. 29:615-627. http://dx.doi.org/10.1016/j.immuni.2008.07.016
18. He, S., L. Wang, L. Miao, T. Wang, F. Du, L. Zhao, and X. Wang. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 137:1100-1111. http://dx.doi.org/10.1016/j.cell.2009.05.021
19. 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. http://dx.doi.org/10.1016/j.cell.2008.10.044
20. Holler, N., R. Zaru, O. Micheau, M. Thome, A. Attinger, S. Valitutti, J.L. Bodmer, P. Schneider, B. Seed, and J. Tschopp. 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1:489-495. http://dx.doi.org/10.1038/82732
21. Hu, X., and L.B. Ivashkiv. 2009. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity. 31:539-550. http://dx.doi.org/10.1016/j.immuni.2009.09.002
22. Hughes, P.D., G.T. Belz, K.A. Fortner, R.C. Budd, A. Strasser, and P. Bouillet. 2008. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity. 28:197-205. http://dx.doi.org/10.1016/j.immuni.2007.12.017
23. Hutcheson, J., J.C. Scatizzi, A.M. Siddiqui, G.K. Haines III, T. Wu, Q.Z. Li, L.S. Davis, C. Mohan, and H. Perlman. 2008. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity. 28:206-217. http://dx.doi.org/10.1016/j.immuni.2007.12.015
24. Kaiser, W.J., J.W. Upton, A.B. Long, D. Livingston-Rosanoff, L.P. Daley-Bauer, R. Hakem, T. Caspary, and E.S. Mocarski. 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature. 471:368-372. http://dx.doi.org/10.1038/nature09857
25. Kang, T.B., T. Ben-Moshe, E.E. Varfolomeev, Y. Pewzner-Jung, N. Yogev, A. Jurewicz, A. Waisman, O. Brenner, R. Haffner, E. Gustafsson, et al. 2004. Caspase-8 serves both apoptotic and nonapoptotic roles. J. Immunol. 173:2976-2984.
26. Kelley, V.E., and J.B. Roths. 1985. Interaction of mutant lpr gene with background strain influences renal disease. Clin. Immunol. Immunopathol. 37:220-229. http://dx.doi.org/10.1016/0090-1229(85)90153-9
27. Klionsky, D.J., and S.D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721. http://dx.doi.org/10.1126/science.290.5497.1717
28. Krammer, P.H., R. Arnold, and I.N. Lavrik. 2007. Life and death in peripheral T cells. Nat. Rev. Immunol. 7:532-542. http://dx.doi.org/10.1038/nri2115
29. Kunz, M., and S.M. Ibrahim. 2009. Cytokines and cytokine profiles in human autoimmune diseases and animal models of autoimmunity. Mediators Inflamm. 2009:979258. http://dx.doi.org/10.1155/2009/979258
30. Lemmers, B., L. Salmena, N. Bidère, H. Su, E. Matysiak-Zablocki, K. Murakami, P.S. Ohashi, A. Jurisicova, M. Lenardo, R. Hakem, and A. Hakem. 2007. Essential role for caspase-8 in Toll-like receptors and NFkappaB signaling. J. Biol. Chem. 282:7416-7423. http://dx.doi.org/10.1074/jbc.M606721200
31. Lu, B., E. Capan, and C. Li. 2007. Autophagy induction and autophagic cell death in effector T cells. Autophagy. 3:158-159.
32. Ludwinski, M.W., J. Sun, B. Hilliard, S. Gong, F. Xue, R.J. Carmody, J. DeVirgiliis, and Y.H. Chen. 2009. Critical roles of Bim in T cell activation and T cell-mediated autoimmune inflammation in mice. J. Clin. Invest. 119:1706-1713. http://dx.doi.org/10.1172/JCI37619
33. Maelfait, J., and R. Beyaert. 2008. Non-apoptotic functions of caspase-8. Biochem. Pharmacol. 76:1365-1373. http://dx.doi.org/10.1016/j.bcp.2008.07.034
34. Marleau, A.M., and N. Sarvetnick. 2005. T cell homeostasis in tolerance and immunity. J. Leukoc. Biol. 78:575-584. http://dx.doi.org/10.1189/jlb.0105050
35. Nagata, S., and T. Suda. 1995. Fas and Fas ligand: lpr and gld mutations. Immunol. Today. 16:39-43. http://dx.doi.org/10.1016/0167-5699(95)80069-7
36. Newton, K., A.W. Harris, M.L. Bath, K.G. Smith, and A. Strasser. 1998. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J. 17:706-718. http://dx.doi.org/10.1093/emboj/17.3.706
37. Oberst, A., C.P. Dillon, R. Weinlich, L.L. McCormick, P. Fitzgerald, C. Pop, R. Hakem, G.S. Salvesen, and D.R. Green. 2011. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature. 471:363-367. http://dx.doi.org/10.1038/nature09852
38. Ohashi, P.S. 2002. T-cell signalling and autoimmunity: molecular mechanisms of disease. Nat. Rev. Immunol. 2:427-438.
39. Osborn, S.L., G. Diehl, S.J. Han, L. Xue, N. Kurd, K. Hsieh, D. Cado, E.A. Robey, and A. Winoto. 2010. Fas-associated death domain (FADD) is a negative regulator of T-cell receptor-mediated necroptosis. Proc. Natl. Acad. Sci. USA. 107:13034-13039. http://dx.doi.org/10.1073/pnas.1005997107
40. O'Shea, J.J., and W.E. Paul. 2010. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science. 327:1098-1102. http://dx.doi.org/10.1126/science.1178334
41. O'Shea, J.J., A. Ma, and P. Lipsky. 2002. Cytokines and autoimmunity. Nat. Rev. Immunol. 2:37-45. http://dx.doi.org/10.1038/nri702
42. Rébé, C., S. Cathelin, S. Launay, R. Filomenko, L. Prévotat, C. L'Ollivier, E. Gyan, O. Micheau, S. Grant, A. Dubart-Kupperschmitt, et al. 2007. Caspase-8 prevents sustained activation of NF-kappaB in monocytes undergoing macrophagic differentiation. Blood. 109:1442-1450. http://dx.doi.org/10.1182/blood-2006-03-011585
43. Salmena, L., and R. Hakem. 2005. Caspase-8 deficiency in T cells leads to a lethal lymphoinfiltrative immune disorder. J. Exp. Med. 202:727-732. http://dx.doi.org/10.1084/jem.20050683
44. Salmena, L., B. Lemmers, A. Hakem, E. Matysiak-Zablocki, K. Murakami, P.Y. Au, D.M. Berry, L. Tamblyn, A. Shehabeldin, E. Migon, et al. 2003. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17:883-895. http://dx.doi.org/10.1101/gad.1063703
45. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10:170-181. http://dx.doi.org/10.1038/nri2711
46. Sebzda, E., S. Mariathasan, T. Ohteki, R. Jones, M.F. Bachmann, and P.S. Ohashi. 1999. Selection of the T cell repertoire. Annu. Rev. Immunol. 17: 829-874. http://dx.doi.org/10.1146/annurev.immunol.17.1.829
47. Sehra, S., D. Patel, S. Kusam, Z.Y. Wang, C.H. Chang, and A.L. Dent. 2005. A role for caspases in controlling IL-4 expression in T cells. J. Immunol. 174:3440-3446.
48. Siegel, R.M. 2006. Caspases at the crossroads of immune-cell life and death. Nat. Rev. Immunol. 6:308-317. http://dx.doi.org/10.1038/nri1809
49. Strasser, A., P.J. Jost, and S. Nagata. 2009. The many roles of FAS receptor signaling in the immune system. Immunity. 30:180-192. http://dx.doi.org/10.1016/j.immuni.2009.01.001
50. Su, H., N. Bidère, L. Zheng, A. Cubre, K. Sakai, J. Dale, L. Salmena, R. Hakem, S. Straus, and M. Lenardo. 2005. Requirement for caspase-8 in NFkappaB activation by antigen receptor. Science. 307:1465-1468. http://dx.doi.org/10.1126/science.1104765
51. Theofilopoulos, A.N., W. Dummer, and D.H. Kono. 2001. T cell homeostasis and systemic autoimmunity. J. Clin. Invest. 108:335-340.
52. Vandenabeele, P., L. Galluzzi, T. Vanden Berghe, and G. Kroemer. 2010. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11:700-714. http://dx.doi.org/10.1038/nrm2970
53. Weant, A.E., R.D. Michalek, I.U. Khan, B.C. Holbrook, M.C. Willingham, and J.M. Grayson. 2008. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ T cell contraction. Immunity. 28:218-230. http://dx.doi.org/10.1016/j.immuni.2007.12.014
54. Wilson, N.S., V. Dixit, and A. Ashkenazi. 2009. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat. Immunol. 10:348-355. http://dx.doi.org/10.1038/ni.1714
55. Youle, R.J., and A. Strasser. 2008. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9:47-59. http://dx.doi.org/10.1038/nrm2308
56. Zhang, J., D. Cado, A. Chen, N.H. Kabra, and A. Winoto. 1998. Fasmediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature. 392:296-300. http://dx.doi.org/10.1038/32681
57. Zhang, D.W., J. Shao, J. Lin, N. Zhang, B.J. Lu, S.C. Lin, M.Q. Dong, and J. Han. 2009. RIP3, an energy metabolism regulator that switches TNFinduced cell death from apoptosis to necrosis. Science. 325:332-336. http://dx.doi.org/10.1126/science.1172308
58. Zhang, H., X. Zhou, T. McQuade, J. Li, F.K. Chan, and J. Zhang. 2011. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature. 471:373-376. http://dx.doi.org/10.1038/nature09878
59. Zhu, J., H. Yamane, and W.E. Paul. 2010. Differentiation of effector CD4 T cell populations (*). Annu. Rev. Immunol. 28:445-489. http://dx.doi.org/10.1146/annurev-immunol-030409-101212