Two CD95 (APO-1/Fas) signaling pathways

EMBO Journal

Volumn 17, Issue 6, 1998, Pages 1675-1687

  Scaffidi, Carsten ^a   Fulda, Simone ^a   Srinivasan, Anu ^b   Friesen, Claudia ^a   Li, Feng ^b   Tomaselli, Kevin J ^b   Debatin, Klaus Michael ^a   Krammer, Peter H ^a   Peter, Marcus E ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b PFIZER INC   (United States)

Author keywords

Apoptosis; Bcl 2; Caspases; Cytochrome c; Mitochondria

Indexed keywords

CYSTEINE PROTEINASE; FAS ANTIGEN; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CELL KINETICS; CELL TYPE; ENZYME ACTIVATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, CD95; APOPTOSIS; B-LYMPHOCYTES; BCL-X PROTEIN; CARRIER PROTEINS; CASPASE 3; CASPASE 8; CASPASE 9; CASPASES; CELL LINE; CYSTEINE ENDOPEPTIDASES; ENZYME ACTIVATION; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GENE EXPRESSION; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0032536771     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.6.1675     Document Type: Article

References (76)

1. Adachi, S., Cross, A.R., Babior, B.M. and Gottlieb, R.A. (1997) Bcl-2 and the outer mitochondrial membrane in the inactivation of cytochrome c during Fas-mediated apoptosis. J. Biol. Chem., 272, 21878-21882.
2. Armstrong, R.C. et al. (1996) Fas-induced activation of the cell death-related protease CPP32 is inhibited by Bcl-2 and by ICE family protease inhibitors. J. Biol. Chem., 271, 16850-16855.
3. Boldin, M.P., Varfolomeev, E.E., Pancer, Z., Mett, I.L., Camonis, J.H. and Wallach, D. (1995) A novel protein that interacts with the death domain of Fas/APO-1 contains a sequence motif related to the death domain. J. Biol. Chem., 270, 7795-7798.
4. Boldin, M.P., Goncharov, T.M., Goltsev, Y.V. and Wallach, D. (1996) Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1-and TNF receptor-induced cell death. Cell, 85, 803-815.
5. L can inhibit apoptosis in cells that have undergone Fas-induced protease activation. Proc. Natl. Acad. Sci. USA, 94, 3759-3764.
6. Cahill, M.A., Peter, M.E., Kischkel, F.C., Chinnaiyan, A.M., Dixit, V.M., Krammer, P.H. and Nordheim, A. (1996) CD95 (APO-1/Fas) induces activation of SAP kinases downstream of ICE-like proteases. Oncogene, 13, 2087-2096.
7. Chinnaiyan, A.M., O'Rourke, K., Tewari, M. and Dixit, V.M. (1995) FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell, 81, 505-512.
8. Chinnaiyan, A.M., Tepper, C.G., Seldin, M.F., O'Rourke, K., Kischkel, F.C., Hellbardt, S., Krammer, P.H., Peter, M.E. and Dixit, V.M. (1996a) FADD/ MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem., 271, 4961-4965.
9. L function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem., 271, 4573-4576.
10. Chinnaiyan, A.M., O'Rourke, K., Lane, B.R. and Dixit, V.M. (1997) Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science, 275, 1122-1126.
11. Chiu, V.K., Walsh, C.M., Liu, C.C., Reed, J.C. and Clark, W.R. (1995) Bcl-2 blocks degranulation but not Fas-based cell-mediated cytotoxicity. J. Immunol., 154, 2023-2032.
12. Cosulich, S.C., Green, S. and Clarke, P.R. (1996) Bcl-2 regulates activation of apoptotic proteases in a cell-free system. Curr. Biol., 6, 997-1005.
13. Enari, M., Hug, H. and Nagata, S. (1995) Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature, 375, 78-81.
14. Enari, M., Talanian, R.V., Wong, W.W. and Nagata, S. (1996) Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature, 380, 723-726.
15. Estoppey, S., Rodriguez, I., Sadoul, R. and Martinou, J.-C. (1997) Bcl-2 prevents activation of CPP32 cysteine protease and cleavage of poly (ADP-ribose) polymerase and U1-70 KDa proteins in staurosporine-medialed apoptosis. Cell Death Differ., 4, 34-38.
16. Fernandes-Alnemri, T. et al. (1995) Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res., 55, 6045-6052.
17. Fernandes-Alnemri, T. et al. (1996) In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl Acad. Sci. USA, 93, 7464-7469.
18. Hasegawa, J., Kamada, S., Kamiike, W., Shimizu, S., Imazu, T. Matsuda, H. and Tsujimoto, Y. (1996) Involvement of CPP32/Yama(-like) proteases in Fas-mediated apoptosis. Cancer Res., 56, 1713-1718.
19. L and adenovirus protein E1B19kD are functionally equivalent in their ability to inhibit cell death. Oncogene, 14, 405414.
20. Itoh, N., Tsujimoto, Y. and Nagata, S. (1993) Effect of Bcl-2 on Fas antigen-mediated cell death. J. Immunol., 151, 621-627.
21. Irmler, M. et al. (1997) Inhibition of death receptor signals by cellular FLIP. Nature, 388, 190-195.
22. Jäättelä, M., Benedict, M., Tewari, M., Shayman, J.A. and Dixit, V.M. (1995) Bcl-x and Bcl-2 inhibit TNF and Fas-induced apoptosis and activation of phospholipase A2 in breast carcinoma cells. Oncogene, 10, 2297-2305.
23. Kamada, S., Washida, M., Hasegawa, J., Kusano, H., Funahashi, Y. and Tsujimoto, Y. (1997) Involvement of caspase-4(-like) protease in Fas-mediated apoptotic pathway. Oncogene, 15, 285-290.
24. L inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res., 57, 3115-3120.
25. Kischkel, F.C., Hellbardt, S., Behrmann, I., Germer, M., Pawlita, M., Krammer, P.H. and Peter, M.E. (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J., 14, 5579-5588.
26. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. and Newmeyer, D.D. (1997a) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275, 1132-1136.
27. Kluck, R.M., Martin, S.J., Hoffman, B.M., Zhou, J.S., Green, D.R. and Newmeyer, D.D. (1997b) Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J., 16, 4639-4649.
28. Kuida, K., Zheng, T.S., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P. and Flavell, R.A. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature, 384, 368-372.
29. Krippner, A., Matsuno-Yagi, A., Gottlieb, R.A. and Babior, B.M. (1996) Loss of function of cytochrome c in Jurkat cells undergoing Fas-mediated apoptosis. J. Biol. Chem., 271, 21629-21636.
30. Kroemer, G., Zamzami, N. and Susin, S.A. (1997) Mitochondrial control of apoptosis. Immunol. Today, 18, 44-51.
31. Lacronique, V. et al. (1996) Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nature Med., 2, 80-86.
32. Lee, R.K., Spielman, J. and Podack, E.R. (1996) Bcl-2 protects against Fas-based but not perforin-based T cell-mediated cytolysis. Int. Immunol., 8, 991-1000.
33. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X. (1997a) Cytochrome c and dATP-dependent formation of Apaf-1-caspase-9 complex initiates an apoptotic protease cascade. Cell, 91, 479-489.
34. Li, F., Srinivasan, A., Wang, Y., Armstrong, R.C., Tomaselli, K.J and Fritz, L.C. (1997b) Cell-specific induction of apoptosis by microinjection of cytochrome c. J. Biol. Chem., 272, 30299-30305.
35. Liu, X., Kim, C.N., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-157.
36. Los, M. et al. (1995) Requirement of an ICE/CED-3 protease for Fas/ APO-1-mediated apoptosis. Nature, 375, 81-83.
37. Mandal, M., Maggirwar, S.B., Sharma, N., Kaufmann, S.H., Sun, S.C. and Kumar, R. (1996) Bcl-2 prevents CD95 (Fas/APO-1)-induced degradation of lamin B and poly(ADP-ribose) polymerase and restores the NF-κB signaling pathway. J. Biol. Chem., 271, 30354-30359.
38. Marchetti, P. et al. (1996) Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med., 184, 1155-1160.
39. Medema, J.P., Scaffidi, C., Kischkel, F.C., Shevchenko, A., Mann, M., Krammer, P.H. and Peter, M.E. (1997) FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J., 16, 2794-2804.
40. L acts downstream of caspase-8 activation by the death-inducing signaling complex. J. Biol. Chem., 273, 3388-3393.
41. Memon, S.A., Moreno, M.B., Petrak, D. and Zacharchuk, C.M. (1995) Bcl-2 blocks glucocorticoid-but not Fas-or activation-induced apoptosis in a T cell hybridoma. J. Immunol., 155, 4644-4652.
42. Monney, L., Otter, I., Olivier, R., Ravn, U., Mirzasaleh, H., Fellay, I., Poirier, G.G. and Borner, C. (1996) Bcl-2 overexpression blocks activation of the death protease CPP32/Yama/apopain. Biochem. Biophys. Res. Commun., 221, 340-345.
43. Moreno, M.B., Memon, S.A. and Zacharchuk, C.M. (1996) Apoptosis signaling pathways in normal T cells: differential activity of Bcl-2 and IL-β-converting enzyme family protease inhibitors on glucocorticoid-and Fas-mediated cytotoxicity. J. Immunol., 157, 3845-3849.
44. Muzio, M. et al. (1996) FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex (DISC). Cell, 85, 817-827.
45. Muzio, M., Salvesen, G.S. and Dixit, V.M. (1997) FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem., 272, 2952-2956.
46. Newmeyer, D.D., Farschon, D.M. and Reed, J.C. (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell, 79, 353-364.
47. Nicholson, D.W. and Thornberry, N.A. (1997) Caspases: killer proteases. Trends Biochem. Sci., 22, 299-306.
48. Perry, D.K., Smyth, M.J., Wang, H.-G., Reed, J.C., Duriez, P., Poirier, G.G., Obeid, L.M. and Hannun, Y. (1997) Bcl-2 acts upstream of the PARP protease and prevents its activation. Cell Death Differ., 4, 29-33.
49. Peter, M.E., Hellbardt, S., Schwartz-Albiez, R., Westendorp, M.O., Moldenhauer, G., Grell, M. and Krammer, P.H. (1995) Cell surface sialylation plays a role in modulating sensitivity towards APO-1-mediated apoptotic cell death. Cell Death Differ., 2, 163-171.
50. Peter, M.E., Heufelder, A. and Hengartner, M.O. (1997a) Advances in apoptosis research. Proc. Natl Acad. Sci. USA, 94, 12736-12737.
51. Peter, M.E., Kischkel, F.C., Scheuerpflug, C., Medema, J.P., Debatin, K.-M. and Krammer, P.H. (1997b) Resistance of cultured peripheral T cells towards activation induced cell death involves a lack of recuitment of FLICE to the death-inducing signaling complex (DISC). Eur. J. Immunol., 27, 1207-1212.
52. Peter, M.E., Scaffidi, C., Medema, J.P., Kischkel, F. and Krammer, P.H. (1998) The death receptors. In Kumar, S., (ed.), Apoptosis, Problems and Diseases. Springer, Heidelberg, in press.
53. Rodriguez, I., Matsuura, K., Khatib, K., Reed, J.C., Nagata, S. and Vassalli, P. (1996) A Bcl-2 transgene expressed in hepatocytes protects mice from fulminant liver destruction but not from rapid death induced by anti-Fas antibody injection. J. Exp. Med., 183, 1031-1036.
54. Scaffidi, C., Medema, J.P., Krammer, P.H. and Peter, M.E. (1997) Two FLICE isoforms, caspase-8/a and caspase-8/b, are recruited and activated by the CD95 death-inducing signaling complex (DISC). J. Biol. Chem., 272, 26953-26958.
55. Schlegel, J., Peters, I., Orrenius, S., Miller, D.K., Thornberry, N.A., Yamin, T.T. and Nicholson, D.W. (1996) CPP32/apopain is a key interleukin 1 beta converting enzyme-like protease involved in Fas-mediated apoptosis. J. Biol. Chem., 271, 1841-1844.
56. Shimizu, S., Eguchi, Y., Kamiike, W., Waguri, S., Uchiyama, Y., Matsuda, H. and Tsujimoto, Y. (1996a) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene. 13, 21-29.
57. Shimizu, S., Eguchi, Y., Kamiike, W., Matsuda, H. and Tsujimoto, Y. (1996b) Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene, 12, 2251-2257.
58. Spector, M.S., Desnoyers, S., Hoeppner, D.J. and Hengartner, M.O. (1997) Interaction between the C.elegans cell-death regulators CED-9 and CED-4. Nature, 385, 653-656.
59. L functions downstream of caspase-8 to inhibit Fas-and TNFR1-induced apoptosis in MCF7 breast carcinoma cells. J. Biol. Chem., 273, 4523-4529.
60. Srinivasula, S.M., Ahmad, M., Fernandes-Alnemri, T., Litwack, G. and Alnemri, E.S. (1996) Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple CED-3/ICE-like cysteine proteases. Proc. Natl Acad. Sci. USA, 93, 14486-14491.
61. Strasser, A., Harris, A.W., Huang, D.C., Krammer, P.H. and Cory, S. (1995) Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J., 14, 6136-6147.
62. Susin, S.A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M. and Kroemer, G. (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med., 184, 1331-1341.
63. Susin, S.A., Zamzami, N., Castedo, M., Daugas, E., Wang, H.G., Geley, S., Fassy, F., Reed, J.C., and Kroemer, G. (1997) The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95-and ceramide-induced apoptosis. J. Exp. Med., 186, 25-37.
64. Takahashi, A. et al. (1997) Affinity labeling displays the stepwise activation of ICE-related proteases by Fas, staurosporine, and CrmA-sensitive caspase-8. Oncogene, 14, 2741-2752.
65. Takayama, S., Sato, T., Krajewski, S., Kochel, K., Irie, S., Millan, J.A. and Reed, J.C. (1995) Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell, 80, 279-284.
66. Trauth, B.C., Klas, C., Peters, A.M., Matzku, S., Möller, P., Falk, W., Debatin, K.-M. and Krammer, P.H. (1989) Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science, 245, 301-305.
67. L regulates the membrane potential and volume homeostasis of mitochondria. Cell, 91, 627-637.
68. Vaux, D.L., Weissman, I.L. and Kim, S.K. (1992) Prevention of programmed cell death in Caenorhabditis elegans by human Bcl-2. Science, 258, 1955-1957.
69. Vincenz, C. and Dixit, V.M. (1997) Fas-associated death domain protein interleukin-1β-converting enzyme 2 (FLICE2), an ICE/CED-3 homolog, is proximally involved in CD95-and p55-mediated death signaling. J. Biol. Chem., 272, 6578-6583.
70. Wu, D., Wallen, H.D. and Nuñez, G. (1997) Interaction and regulation of subcellular localization of CED-4 by CED-9. Science, 275, 1126-1129.
71. Xue, D., Shaham, S. and Horvitz, H.R. (1996) The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev., 10, 1073-1083.
72. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng, T.I., Jones, D.P. and Wang, X. (1997a) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science, 275, 1129-1132.
73. Yang, X., Koshravi-Far, R., Chang, H.Y. and Baltimore, D. (1997b) Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell, 89, 1067-1076.
74. Yuan, J.Y. and Horvitz, H.R. (1990) The Caenorhabditis elegans genes CED-3 and CED-4 act cell autonomously to cause programmed cell death. Dev. Biol., 138, 33-41.
75. Zamzami, N., Susin, S.A., Marchetti, P., Hirsch, T., Gomez-Monterrey, I., Castedo, M. and Kroemer, G. (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med., 183, 1533-1544.
76. Zou, H., Henzel, W.J., Liu, X., Lutschg, A. and Wang, X. (1997) Apaf-1, a human protein homologous to C.elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell, 90, 405-413.