The Caspase 8 Inhibitor c-FLIP_L Modulates T-Cell Receptor-Induced Proliferation but Not Activation-Induced Cell Death of Lymphocytes

REFERENCES

• Alderson, M. R., T. W. Tough, T. Davis-Smith, S. Braddy, B. Falk, K. A. Schooley, R. G. Goodwin, C. A. Smith, F. Ramsdell, and D. H. Lynch. 1995. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 181: 71–77.
   PubMed Web of Science ®Google Scholar
• Algeciras-Schimnich, A., T. S. Griffith, D. H. Lynch, and C. V. Paya. 1999. Cell cycle-dependent regulation of FLIP levels and susceptibility to Fas-mediated apoptosis. J. Immunol. 162: 5205–5211.
   PubMedGoogle Scholar
• Ashkenazi, A., and V. M. Dixit. 1998. Death receptors: signaling and modulation. Science 281: 1305–1308.
   PubMed Web of Science ®Google Scholar
• Beg, A. A., W. C. Sha, R. T. Bronson, and D. Baltimore. 1995. Constitutive NF-κB activation, enhanced granulopoiesis, and neonatal lethality in IκBα-deficient mice. Genes Dev. 9: 2736–2746.
   PubMed Web of Science ®Google Scholar
• Bertin, J., R. C. Armstrong, S. Ottilie, D. A. Martin, Y. Wang, S. Banks, G. H. Wang, T. G. Senkevich, E. S. Alnemri, B. Moss, M. J. Lenardo, K. J. Tomaselli, and J. I. Cohen. 1997. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. USA 94: 1172–1176.
   PubMed Web of Science ®Google Scholar
• Brunner, T., R. J. Mogil, D. LaFace, N. J. Yoo, A. Mahboubi, F. Echeverri, S. J. Martin, W. R. Force, D. H. Lynch, C. F. Ware, et al. 1995. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373: 441–444.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Darzynkiewicz, Z., X. Li, and J. Gong. 1994. Assays of cell viability: discrimination of cells dying by apoptosis. Methods Cell Biol. 41: 15–38.
   PubMed Web of Science ®Google Scholar
• Dhein, J., H. Walczak, C. Baumler, K. M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373: 438–441.
   PubMed Web of Science ®Google Scholar
• Earnshaw, W. C., L. M. Martins, and S. H. Kaufmann. 1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68: 383–424.
   PubMed Web of Science ®Google Scholar
• Esslinger, C. W., A. Wilson, B. Sordat, F. Beermann, and C. V. Jongeneel. 1997. Abnormal T lymphocyte development induced by targeted overexpression of IκBα. J. Immunol. 158: 5075–5078.
   PubMedGoogle Scholar
• Fisher, G. H., F. J. Rosenberg, S. E. Straus, J. K. Dale, L. A. Middleton, A. Y. Lin, W. Strober, M. J. Lenardo, and J. M. Puck. 1995. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 81: 935–946.
   PubMed Web of Science ®Google Scholar
• French, L. E., A. Wilson, M. Hahne, I. Viard, J. Tschopp, and H. R. MacDonald. 1997. Fas ligand expression is restricted to nonlymphoid thymic components in situ. J. Immunol. 159: 2196–2202.
   PubMedGoogle Scholar
• Gillette-Ferguson, I., and C. L. Sidman. 1994. A specific intercellular pathway of apoptotic cell death is defective in the mature peripheral T cells of autoimmune lpr and gld mice. Eur. J. Immunol. 24: 1181–1185.
   PubMedGoogle Scholar
• Goltsev, Y. V., A. V. Kovalenko, E. Arnold, E. E. Varfolomeev, V. M. Brodianskii, and D. Wallach. 1997. CASH, a novel caspase homologue with death effector domains. J. Biol. Chem. 272: 19641–19644.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10: 735–744.
   PubMed Web of Science ®Google Scholar
• Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17–27.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hu, S., C. Vincenz, J. Ni, R. Gentz, and V. M. Dixit. 1997. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1- and CD-95-induced apoptosis. J. Biol. Chem. 272: 17255–17257.
   PubMed Web of Science ®Google Scholar
• Inohara, N., T. Koseki, Y. Hu, S. Chen, and G. Nunez. 1997. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis. Proc. Natl. Acad. Sci. USA 94: 10717–10722.
   PubMedGoogle Scholar
• Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schroter, K. Burns, C. Mattmann, D. Rimoldi, L. E. French, and J. Tschopp. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190–195.
   PubMed Web of Science ®Google Scholar
• Ju, S. T., D. J. Panka, H. Cui, R. Ettinger, M. el-Khatib, D. H. Sherr, B. Z. Stanger, and A. Marshak-Rothstein. 1995. Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373: 444–448.
   PubMed Web of Science ®Google Scholar
• Kataoka, T., R. C. Budd, N. Holler, M. Thome, F. Martinon, M. Irmler, K. Burns, M. Hahne, N. Kennedy, M. Kovacsovics, and J. Tschopp. 2000. The caspase-8 inhibitor FLIP promotes activation of NF-κB and Erk signaling pathways. Curr. Biol. 10: 640–648.
   PubMed Web of Science ®Google Scholar
• Kataoka, T., M. Schroter, M. Hahne, P. Schneider, M. Irmler, M. Thome, C. J. Froelich, and J. Tschopp. 1998. FLIP prevents apoptosis induced by death receptors but not by perforin/granzyme B, chemotherapeutic drugs, and gamma irradiation. J. Immunol. 161: 3936–3942.
   PubMed Web of Science ®Google Scholar
• Kennedy, N. J., T. Kataoka, J. Tschopp, and R. C. Budd. 1999. Caspase activation is required for T cell proliferation. J. Exp. Med. 190: 1891–1896.
   PubMed Web of Science ®Google Scholar
• Kishimoto, H., C. D. Surh, and J. Sprent. 1998. A role for Fas in negative selection of thymocytes in vivo. J. Exp. Med. 187: 1427–1438.
   PubMed Web of Science ®Google Scholar
• Klas, C., K. M. Debatin, R. R. Jonker, and P. H. Krammer. 1993. Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5: 625–630.
   PubMed Web of Science ®Google Scholar
• Lee, E. G., D. L. Boone, S. Chai, S. L. Libby, M. Chien, J. P. Lodolce, and A. Ma. 2000. Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289: 2350–2354.
   PubMed Web of Science ®Google Scholar
• Lenardo, M., K. M. Chan, F. Hornung, H. McFarland, R. Siegel, J. Wang, and L. Zheng. 1999. Mature T lymphocyte apoptosis—immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17: 221–253.
   PubMed Web of Science ®Google Scholar
• Luther, S. A., and H. Acha-Orbea. 1997. Mouse mammary tumor virus: immunological interplays between virus and host. Adv. Immunol. 65: 139–243.
   PubMedGoogle Scholar
• Mariathasan, S., S. S. Ho, A. Zakarian, and P. S. Ohashi. 2000. Degree of ERK activation influences both positive and negative thymocyte selection. Eur. J. Immunol. 30: 1060–1068.
   PubMedGoogle Scholar
• Medema, J. P., J. de Jong, T. van Hall, C. J. Melief, and R. Offringa. 1999. Immune escape of tumors in vivo by expression of cellular FLICE-inhibitory protein. J. Exp. Med. 190: 1033–1038.
   PubMed Web of Science ®Google Scholar
• Muzio, M., B. R. Stockwell, H. R. Stennicke, G. S. Salvesen, and V. M. Dixit. 1998. An induced proximity model for caspase-8 activation. J. Biol. Chem. 273: 2926–2930.
   PubMed Web of Science ®Google Scholar
• Nagata, S. 1997. Apoptosis by death factor. Cell 88: 355–365.
   PubMed Web of Science ®Google Scholar
• Newton, K., A. W. Harris, M. L. Bath, K. G. C. 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.
   PubMed Web of Science ®Google Scholar
• Radvanyi, L. G., G. B. Mills, and R. G. Miller. 1993. Religation of the T cell receptor after primary activation of mature T cells inhibits proliferation and induces apoptotic cell death. J. Immunol. 150: 5704–5715.
   PubMed Web of Science ®Google Scholar
• Rasper, D. M., J. P. Vaillancourt, S. Hadano, V. M. Houtzager, I. Seiden, S. L. Keen, P. Tawa, S. Xanthoudakis, J. Nasir, D. Martindale, B. F. Koop, E. P. Peterson, N. A. Thornberry, J. Huang, D. P. MacPherson, S. C. Black, F. Hornung, M. J. Lenardo, M. R. Hayden, S. Roy, and D. W. Nicholson. 1998. Cell death attenuation by "Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 5: 271–288.
   PubMed Web of Science ®Google Scholar
• Refaeli, Y., L. Van Parijs, C. A. London, J. Tschopp, and A. K. Abbas. 1998. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8: 615–623.
   PubMed Web of Science ®Google Scholar
• Rieux-Laucat, F., F. Le Deist, C. Hivroz, I. A. Roberts, K. M. Debatin, A. Fischer, and J. P. de Villartay. 1995. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 268: 1347–1349.
   PubMed Web of Science ®Google Scholar
• Russell, J. Q., T. Mooney, P. L. Cohen, B. MacPherson, R. J. Noelle, and R. C. Budd. 1998. Anti-CD40L accelerates renal disease and adenopathy in MRL-lpr mice in parallel with decreased thymocyte apoptosis. J. Immunol. 161: 729–739.
   PubMedGoogle Scholar
• Scaffidi, C., S. Kirchhoff, P. H. Krammer, and M. E. Peter. 1999. Apoptosis signaling in lymphocytes. Curr. Opin. Immunol. 11: 277–285.
   PubMed Web of Science ®Google Scholar
• Scaffidi, C., I. Schmitz, P. H. Krammer, and M. E. Peter. 1999. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274: 1541–1548.
   PubMed Web of Science ®Google Scholar
• Schulze-Osthoff, K., D. Ferrari, M. Los, S. Wesselborg, and M. E. Peter. 1998. Apoptosis signaling by death receptors. Eur. J. Biochem. 254: 439–459.
   PubMedGoogle Scholar
• Scott, D. E., W. J. Kisch, and A. D. Steinberg. 1993. Studies of T cell deletion and T cell anergy following in vivo administration of SEB to normal and lupus-prone mice. J. Immunol. 150: 664–672.
   PubMed Web of Science ®Google Scholar
• Sgonc, R., G. Boeck, H. Dietrich, J. Gruber, H. Recheis, and G. Wick. 1994. Simultaneous determination of cell surface antigens and apoptosis. Trends Genet. 10: 41–42.
   PubMed Web of Science ®Google Scholar
• Shu, H. B., D. R. Halpin, and D. V. Goeddel. 1997. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity 6: 751–763.
   PubMed Web of Science ®Google Scholar
• Smith, K. G., A. Strasser, and D. L. Vaux. 1996. CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO-1)-transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. EMBO J. 15: 5167–5176.
   PubMedGoogle Scholar
• Srinivasula, S. M., M. Ahmad, S. Ottilie, F. Bullrich, S. Banks, Y. Wang, T. Fernandes-Alnemri, C. M. Croce, G. Litwack, K. J. Tomaselli, R. C. Armstrong, and E. S. Alnemri. 1997. FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J. Biol. Chem. 272: 18542–18545.
   PubMed Web of Science ®Google Scholar
• Stanciu, M., Y. Wang, R. Kentor, N. Burke, S. Watkins, G. Kress, I. Reynolds, E. Klann, M. R. Angiolieri, J. W. Johnson, and D. B. DeFranco. 2000. Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem. 275: 12200–12206.
   PubMed Web of Science ®Google Scholar
• Strasser, A., A. W. Harris, D. C. Huang, P. H. Krammer, and S. Cory. 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14: 6136–6147.
   PubMed Web of Science ®Google Scholar
• Takahashi, T., M. Tanaka, C. I. Brannan, N. A. Jenkins, N. G. Copeland, T. Suda, and S. Nagata. 1994. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76: 969–976.
   PubMed Web of Science ®Google Scholar
• Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517–521.
   PubMed Web of Science ®Google Scholar
• Tough, D. F., and J. Sprent. 1994. Turnover of naive- and memory-phenotype T cells. J. Exp. Med. 179: 1127–1135.
   PubMed Web of Science ®Google Scholar
• Tschopp, J., M. Irmler, and M. Thome. 1998. Inhibition of fas death signals by FLIPs. Curr. Opin. Immunol. 10: 552–558.
   PubMed Web of Science ®Google Scholar
• Tschopp, J., M. Thome, K. Hofmann, and E. Meinl. 1998. The fight of viruses against apoptosis. Curr. Opin. Genet. Dev. 8: 82–87.
   PubMed Web of Science ®Google Scholar
• Van Parijs, L., Y. Refaeli, A. K. Abbas, and D. Baltimore. 1999. Autoimmunity as a consequence of retrovirus-mediated expression of C-FLIP in lymphocytes. Immunity 11: 763–770.
   PubMed Web of Science ®Google Scholar
• Walsh, C. M., B. G. Wen, A. M. Chinnaiyan, K. O'Rourke, V. M. Dixit, and S. M. Hedrick. 1998. A role for FADD in T cell activation and development. Immunity 8: 439–449.
   PubMed Web of Science ®Google Scholar
• Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356: 314–317.
   PubMed Web of Science ®Google Scholar
• Willems, F., Z. Amraoui, N. Vanderheyde, V. Verhasselt, E. Aksoy, C. Scaffidi, M. E. Peter, P. H. Krammer, and M. Goldman. 2000. Expression of c-FLIP(L) and resistance to CD95-mediated apoptosis of monocyte-derived dendritic cells: inhibition by bisindolylmaleimide. Blood 95: 3478–3482.
   PubMed Web of Science ®Google Scholar
• Yeh, W. C., A. Itie, A. J. Elia, M. Ng, H. B. Shu, A. Wakeham, C. Mirtsos, N. Suzuki, M. Bonnard, D. V. Goeddel, and T. W. Mak. 2000. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12: 633–642.
   PubMed Web of Science ®Google Scholar
• Zhang, J., D. Cado, A. Chen, N. H. Kabra, and A. Winoto. 1998. Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 392: 296–300.
   PubMed Web of Science ®Google Scholar
• Zheng, L., G. Fisher, R. E. Miller, J. Peschon, D. H. Lynch, and M. J. Lenardo. 1995. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377: 348–351.
   PubMed Web of Science ®Google Scholar
• Zhou, Q., S. Snipas, K. Orth, M. Muzio, V. M. Dixit, and G. S. Salvesen. 1997. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 272: 7797–7800.
   PubMed Web of Science ®Google Scholar