c-FLIP protects T lymphocytes from apoptosis in the intrinsic pathway

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3444-3451

  He, Ming Xiao ^a   He, You Wen ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CASPASE 8; CYTOCHROME C; FLICE INHIBITORY PROTEIN; REACTIVE OXYGEN METABOLITE; APOPTOSIS REGULATORY PROTEIN; BCL-2-LIKE PROTEIN 11; MEMBRANE PROTEIN; ONCOPROTEIN; STAUROSPORINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; C FLIP GENE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME RELEASE; GENE DELETION; IN VITRO STUDY; MITOCHONDRION; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; DRUG EFFECTS; GENETICS; INTRACELLULAR SPACE; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL SURVIVAL; CYTOCHROMES C; INTRACELLULAR SPACE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; STAUROSPORINE; T-LYMPHOCYTES;

EID: 84925842808     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400469     Document Type: Article

References (44)

1. Budd, R. C., W. C. Yeh, and J. Tschopp. 2006. cFLIP regulation of lymphocyte activation and development. Nat. Rev. Immunol. 6: 196-204.
2. Golks, A., D. Brenner, C. Fritsch, P. H. Krammer, and I. N. Lavrik. 2005. c-FLIPR, a new regulator of death receptor-induced apoptosis. J. Biol. Chem. 280: 14507-14513.
3. Ueffing, N., E. Keil, C. Freund, R. Kühne, K. Schulze-Osthoff, and I. Schmitz. 2008. Mutational analyses of c-FLIPR, the only murine short FLIP isoform, reveal requirements for DISC recruitment. Cell Death Differ. 15: 773-782.
4. Zhang, N., K. Hopkins, and Y. W. He. 2008. c-FLIP protects mature T lymphocytes from TCR-mediated killing. J. Immunol. 181: 5368-5373.
5. Danial, N. N., and S. J. Korsmeyer. 2004. Cell death: critical control points. Cell 116: 205-219.
6. He, M. X., and Y. W. He. 2013. CFLAR/c-FLIPL: a star in the autophagy, apoptosis and necroptosis alliance. Autophagy 9: 791-793.
7. McLeod, I. X., W. Jia, and Y. W. He. 2012. The contribution of autophagy to lymphocyte survival and homeostasis. Immunol. Rev. 249: 195-204.
8. Pua, H. H., J. Guo, M. Komatsu, and Y. W. He. 2009. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 182: 4046-4055.
9. Stephenson, L. M., B. C. Miller, A. Ng, J. Eisenberg, Z. Zhao, K. Cadwell, D. B. Graham, N. N. Mizushima, R. Xavier, H. W. Virgin, and W. Swat. 2009. Identification of Atg5-dependent transcriptional changes and increases in mitochondrial mass in Atg5-deficient T lymphocytes. Autophagy 5: 625-635.
10. Hubbard, V. M., R. Valdor, B. Patel, R. Singh, A. M. Cuervo, and F. Macian. 2010. Macroautophagy regulates energy metabolism during effector T cell activation. J. Immunol. 185: 7349-7357.
11. Jia, W., and Y. W. He. 2011. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 186: 5313-5322.
12. Pua, H. H., I. Dzhagalov, M. Chuck, N. Mizushima, and Y. W. He. 2007. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204: 25-31.
13. 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.
14. Lee, J. S., Q. Li, J. Y. Lee, S. H. Lee, J. H. Jeong, H. R. Lee, H. Chang, F. C. Zhou, S. J. Gao, C. Liang, and J. U. Jung. 2009. FLIP-mediated autophagy regulation in cell death control. Nat. Cell Biol. 11: 1355-1362.
15. 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.
16. He, M. X., and Y. W. He. 2013. A role for c-FLIP(L) in the regulation of apoptosis, autophagy, and necroptosis in T lymphocytes. Cell Death Differ. 20: 188-197.
17. Zhang, N., and Y. W. He. 2005. An essential role for c-FLIP in the efficient development of mature T lymphocytes. J. Exp. Med. 202: 395-404.
18. Vooijs, M., J. Jonkers, and A. Berns. 2001. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2: 292-297.
19. Zhang, N., K. Hopkins, and Y. W. He. 2008. The long isoform of cellular FLIP is essential for T lymphocyte proliferation through an NF-kappaB-independent pathway. J. Immunol. 180: 5506-5511.
20. Waterhouse, N. J., R. Steel, R. Kluck, and J. A. Trapani. 2004. Assaying cytochrome C translocation during apoptosis. Methods Mol. Biol. 284: 307-313.
21. Piao, X., S. Komazawa-Sakon, T. Nishina, M. Koike, J. H. Piao, H. Ehlken, H. Kurihara, M. Hara, N. Van Rooijen, G. Schütz, et al. 2012. c-FLIP maintains tissue homeostasis by preventing apoptosis and programmed necrosis. Sci. Signal. 5: ra93.
22. Schattenberg, J. M., T. Zimmermann, M. Wörns, M. F. Sprinzl, A. Kreft, T. Kohl, M. Nagel, J. Siebler, H. Schulze Bergkamen, Y. W. He, et al. 2011. Ablation of c-FLIP in hepatocytes enhances death-receptor mediated apoptosis and toxic liver injury in vivo. J. Hepatol. 55: 1272-1280.
23. Shimizu, T., T. Numata, and Y. Okada. 2004. A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl(-) channel. Proc. Natl. Acad. Sci. USA 101: 6770-6773.
24. Tenev, T., K. Bianchi, M. Darding, M. Broemer, C. Langlais, F. Wallberg, A. Zachariou, J. Lopez, M. MacFarlane, K. Cain, and P. Meier. 2011. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43: 432-448.
25. 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.
26. Simbulan-Rosenthal, C. M., D. S. Rosenthal, S. Iyer, A. H. Boulares, and M. E. Smulson. 1998. Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J. Biol. Chem. 273: 13703-13712.
27. Krohn, A. J., E. Preis, and J. H. Prehn. 1998. Staurosporine-induced apoptosis of cultured rat hippocampal neurons involves caspase-1-like proteases as upstream initiators and increased production of superoxide as a main downstream effector. J. Neurosci. 18: 8186-8197.
28. Chae, H. J., J. S. Kang, J. O. Byun, K. S. Han, D. U. Kim, S. M. Oh, H. M. Kim, S. W. Chae, and H. R. Kim. 2000. Molecular mechanism of staurosporine-induced apoptosis in osteoblasts. Pharmacol. Res. 42: 373-381.
29. Zhang, N., H. Hartig, I. Dzhagalov, D. Draper, and Y. W. He. 2005. The role of apoptosis in the development and function of T lymphocytes. Cell Res. 15: 749-769.
30. Mikhailov, V., M. Mikhailova, K. Degenhardt, M. A. Venkatachalam, E. White, and P. Saikumar. 2003. Association of Bax and Bak homo-oligomers in mitochondria. Bax requirement for Bak reorganization and cytochrome c release. J. Biol. Chem. 278: 5367-5376.
31. Dejean, L. M., S. Martinez-Caballero, L. Guo, C. Hughes, O. Teijido, T. Ducret, F. Ichas, S. J. Korsmeyer, B. Antonsson, E. A. Jonas, and K. W. Kinnally. 2005. Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol. Biol. Cell 16: 2424-2432.
32. Wei, M. C., W. X. Zong, E. H. Cheng, T. Lindsten, V. Panoutsakopoulou, A. J. Ross, K. A. Roth, G. R. MacGregor, C. B. Thompson, and S. J. Korsmeyer. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
33. 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.
34. Han, D. K., P. M. Chaudhary, M. E. Wright, C. Friedman, B. J. Trask, R. T. Riedel, D. G. Baskin, S. M. Schwartz, and L. Hood. 1997. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death. Proc. Natl. Acad. Sci. USA 94: 11333-11338.
35. McLeod, I. X., X. Zhou, Q. J. Li, F. Wang, and Y. W. He. 2011. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Rα surface expression. J. Immunol. 187: 5051-5061.
36. Ploner, C., R. Kofler, and A. Villunger. 2008. Noxa: at the tip of the balance between life and death. Oncogene 27(Suppl. 1): S84-S92.
37. Erlacher, M., E. M. Michalak, P. N. Kelly, V. Labi, H. Niederegger, L. Coultas, J. M. Adams, A. Strasser, and A. Villunger. 2005. BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 106: 4131-4138.
38. Li, W. Q., T. Guszczynski, J. A. Hixon, and S. K. Durum. 2010. Interleukin-7 regulates Bim proapoptotic activity in peripheral T-cell survival. Mol. Cell. Biol. 30: 590-600.
39. Li, H., H. Zhu, C. J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501.
40. Riedl, S. J., and Y. Shi. 2004. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5: 897-907.
41. Wang, X., J. Zhao, S. Tang, S. Lee, R. I. Glazer, and I. Hewlett. 2009. c-FLIPL regulates PKC via AP-2 to inhibit Bax-mediated apoptosis induced by HIV-1 gp120 in Jurkat cells. Mol. Cell. Biochem. 330: 23-29.
42. Lu, J. V., B. M. Weist, B. J. van Raam, B. S. Marro, L. V. Nguyen, P. Srinivas, B. D. Bell, K. A. Luhrs, T. E. Lane, G. S. Salvesen, and C. M. Walsh. 2011. Complementary roles of Fas-associated death domain (FADD) and receptor interacting protein kinase-3 (RIPK3) in T-cell homeostasis and antiviral immunity. Proc. Natl. Acad. Sci. USA 108: 15312-15317.
43. 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.
44. 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.