FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex

Cell

Volumn 85, Issue 6, 1996, Pages 817-827

  Muzio, Marta ^a   Chinnaiyan, Arul M ^a   Kischkel, Frank C ^b   O'Rourke, Karen ^a   Shevchenko, Andrej ^c   Ni, Jian ^d   Scaffidi, Carsten ^b   Bretz, James D ^a   Zhang, Mei ^d   Gentz, Reiner ^d   Mann, Matthias ^c   Krammer, Peter H ^b   Peter, Marcus E ^b   Dixit, Vishva M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; PROTEINASE; PROTEINASE FLICE; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; ENZYME ACTIVATION; ENZYME ISOLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 15844412409     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81266-0     Document Type: Article

References (74)

1. Baglioni, C. (1992). Mechanisms of cytotoxicity, cytolysis, and growth stimulation by TNF. In Tumor Necrosis Factors: The Molecules and Their Emerging Role in Medicine, B. Beutler, ed. (New York: Raven Press), pp. 425-438.
2. Berke, G. (1995). Unlocking the secrets of CTL and NK cells, Immunol. Today 16, 343-346.
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. Chinnaiyan, A.M., and Dixit, V.M. (1996). The cell-death machine. Curr. Biol. 6, 555-562.
5. 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.
6. 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.
7. Chinnaiyan, A.M., Orth, K., O'Rourke, K., Duan, H., Poirier, G.G., and Dixit, V.M. (1996b). Molecular ordering of the cell death pathway: bcl-2 and bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271, 4573-4576.
8. Cleveland, J.L., and Ihle, J.N. (1995). Contenders in FasL/TNF Signaling. Cell 81, 479-482.
9. Darmon, A.J., Nicholson, D.W., and Bleackley, R.C. (1995). Activation of the apoptotic protease CPP-32 by cytotoxic T cell-derived granzyme B. Nature 377, 446-448.
10. Duan, H., Chinnaiyan, A.M., Hudson, P.L., Wing, J.P., He, W., and Dixit, V.M. (1996a). ICE-LAP3, a novel mammalian homolog of the Caenorhabditis elegans cell death protein CED-3, is activated during Fas-and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 271, 35013-35035.
11. Duan, H., Orth, K., Chinnaiyan, A., Poirier, G., Froelich, C.J., He, W.-W., and Dixit, V.M. (1996b). ICE-LAP6, a novel member of the ICE/ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem., in press.
12. Enari, M., Hug, H., and Nagata, S. (1995). Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 375, 78-81.
13. Faucheu, C., Diu, A., Chan, A.W.E., Blanchet, A.-M., Miossec, C., Hervé, F., Collard-Dutilleul, V., Gu, Y., Aldape, R.A., Lippke, J.A., Rocher, C., Su, M.S-S., Livingston, D.J., Hercend, T., and Lalanne, J.-L. (1995). A novel human protease similar to the interleukin-1β converting enzyme induces apoptosis in transfected cells. EMBO J. 14, 1914-1922.
14. Fenn, J.B., Mann, M., Meng, C.K., Wong, S.F., and Whitehouse, C.M. (1989). Electrospray ionization for the mass spectrometry of large biomolecules. Science 246, 64-71.
15. Fearnhead, H.O., Dinsdale, D., and Cohen, G.M. (1995). An interleukin-1β-converting enzyme-like protease is a common mediator of apoptosis in thymocytes. FEBS Lett. 375, 283-288.
16. Fernandes-Alnemri, T., Litwack, G., and Alnemri, E.S. (1994). CPP-32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein CED-3 and mammalian interleukin-1β-converting enzyme. J. Biol. Chem. 269, 30761-30764.
17. Fernandes-Alnemri, T., Litwack, G., and Alnemri, E.S. (1995). Mch-2, a new member of the apoptotic CED-3/ICE cysteine protease gene family. Cancer Res. 55, 2737-2742.
18. Fernandes-Alnemri, T., Takahashi, A., Armstrong, R., Krebs, J., Fritz, L., Tomaselli, K.J., Wang, L., Yu, Z., Croce, C.M., Salveson, G., Earnshaw, W.C., Litwack, G., and Alnemri, E.S. (1995). Mch-3, a novel human apoptotic cysteine protease highly related to CPP-32. Cancer Res. 55, 6045-6052.
19. Golstein, P., Marguet, D., and Depraetere, V. (1995). Homology between reaper and the cell death domains of Fas and TNFR1. Cell 81, 185-186.
20. Hanna, W.L., Zhang, X., Turbov, J., Winkler, U., Hudig, D., and Froelich, C.J. (1993). Rapid purification of cationic granule proteases: application to human granzymes. Prot. Expr. Purif. 4, 398-404.
21. Hengartner, M.O. (1996). Programmed cell death in invertebrates. Curr. Opin. Genet. Dev. 6, 34-38.
22. Hsu, H., Xiong, J., and Goeddel, D.V. (1995). The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell 81, 495-504.
23. Hsu, H., Shu, H.-B., Pan, M.-P., and Goeddel, D.V. (1996a). TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor-1 signal transduction pathways. Cell 84, 299-308.
24. Hsu, H., Huang, J., Shu, H.-B., Baichwal, V., and Goeddel, D.V. (1996b). TNF dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4, 387-396.
25. Hunt, D.F., Yates, J.R.D., Shabanowitz, J., Winston, S., and Hauer, C.R. (1986). Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 83, 6233-6237.
26. Itoh, N., and Nagata, S. (1993). A novel protein domain required for apoptosis: mutational analysis of human Fas antigen. J. Biol. Chem. 268, 10932-10937.
27. Itoh, N., Yonehara, S., Ishii, A., Yonehara, M., Mizushima, S.-I., Sameshima, M., Hase, A., Seto, Y., and Nagata, S. (1991). The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66, 233-243.
28. Kamens, J., Paskind, M., Hugunin, M., Talanian, R.V., Allen, H., Banach, D., Bump, N., Hackett, M., Johnston, C.G., Li, P., and others. (1995). Identification and characterization of ICH-2, a novel member of the interleukin-1β-converting enzyme family of cysteine proteases. J. Biol. Chem. 270, 15250-15256.
29. Kischkel, F.C., Hellbardt, S., Behrmann, I., Germer, M., Pawlita, M., Krammer, P.H., and Peter, M.E. (1995). Cytoxicity-dependent APO-1 (Fas/CD95)-associated proteins (CAP) form a death-inducing signalling complex (DISC) with the receptor. EMBO J. 14, 5579-5588.
30. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S.-S., and Flavell, R.A. (1995). Altered cytokine export and apoptosis in mice deficient in interleukin-1β converting enzyme. Science 267, 2000-2003.
31. Kumar, S., Kinoshita, M., Noda, M., Copeland, N.G., and Jenkins, N.A. (1994). Induction of apoptosis by the mouse nedd2gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1β-converting enzyme. Genes Dev. 8, 1613-1626.
32. Lazebnik, Y.A., Kaufmann, S.H., Desnoyers, S., Poirier, G.G., and Earnshaw, W.C. (1994). Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371, 346-347.
33. Li, P., Allen, H., Banerjee, S., Franklin, S., Herzog, L., Johnston, C., McDowell, J., Paskind, M., Rodman, L., Salfeld, J., Towne, E., Tracey, D., Wardwell, S., Wei, F.-Y., Wong, W., Kamen, R., and Seshadri, T. (1995). Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock. Cell 80, 401-411.
34. Lippke, J.A., Gu, Y., Sarnecki, C., Caron, P.R., and Su, M.S.-S. (1996). Identification and characterization of CPP-32/Mch-2 homolog 1, a novel cysteine protease similar to CPP-32. J. Biol. Chem. 277, 1825-1828.
35. Los, M., Van de Craen, M., Penning, L.C., Schenk, H., Westendorp, M., Baeuerle, P.A., Droge, W., Krammer, P.H., Fiers, W., and Schulze-Osthoff, K. (1995). Requirement of an ICE/CED-3 protease for Fas/ APO-1-mediated apoptosis. Nature 375, 81-83.
36. Mann, M., and Wilm, M. (1994). Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem. 66, 4390-4399.
37. Mann, M., and Wilm, M. (1995). Electrospray mass spectrometry for protein characterization. Trends Biochem. Sci. 20, 219-224.
38. Miura, M., Zhu, H., Rotello, R., Hartwieg, E.A., and Yuan, J. (1993). Induction of apoptosis in fibroblasts by IL-β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75, 653-660.
39. Munday, N.A., Vaillancourt, J.P., Ali, A., Casano, F.J., Miller, D. K., Molineaux, S.M., Yamin, T.T., Yu, V.L., and Nicholson, D.W. (1995). Molecular cloning and proapoptotic activity of ICE rel-II and ICE rel-III, members of the ICE/CED-3 family of cysteine proteases. J. Biol. Chem. 270, 15870-15876.
40. Nagata, S., and Golstein, P. (1995). The Fas death factor. Science 267, 1449-1456.
41. Nicholson, D.W. (1996). ICE/CED-3-like proteases as therapeutic targets for the control of inappropriate apoptosis. Nature Biotechnology 14, 297-301.
42. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., Munday, N.A., Raju, S.M., Smulson, M.E., Yamin, T.-T., Yu, V.L., and Miller, D.K. (1995). Identification and inhibition of the ICE/ CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
43. O'Rourke, K., Laherty, C.D., and Dixit, V.M. (1992). Thrombospondin 1 and thrombospondin 2 are expressed as both homo-and heterotrimers. J. Biol. Chem. 267, 24921-24924.
44. Oehm, A., Behrmann, I., Falk, W., Pawlita, M., Maier, G., Klas, C., Li-Weber, M., Richards, S., Dhein, J., Trauth, B.C., and others. (1992). Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily: sequence identity with the Fas antigen. J. Biol. Chem. 267, 10709-10715.
45. Peter, M.E., Hellbardt, S., Schwartz-Albiez, R., Westendorp, M.O., Moldenhauer, G., Grell, M., and Krammer, P.M. (1995). Cell surface sialylation plays a role in modulating sensitivity towards APO-1-mediated apoptotic cell death. Cell Death Differ. 2, 163-171.
46. Peter, M.E., Kischkel, F.C., Hellbardt, S., Chinnaiyan, A.M., Krammer, P.H., and Dixit, V.M. (1996). CD95(APO-1/Fas)-associating signaling proteins. Cell Death Differ. 3, 161-170.
47. Prank, G.J., Ramer, K., Amiri, P., and Williams, L.T. (1996). Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science 277, 808-810.
48. Quan, L.T., Tewari, M., O'Rourke, K., Dixit, V.M., Snipas, S.J., Poirier, G.G., Ray, C., Pickup, D.J., and Salvesen, G.S. (1996). Proteolytic activation of the cell death protease Yama/CPP-32 gyranzyme B. Proc. Natl. Acad. Sci. USA 93, in press.
49. Raff, M.C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
50. Ray, C.A., Black, R.A., Kronheim, S.R., Greenstreet, T.A., Sleath, P.R., Salvesen, G.S., and Pickup, D.J. (1992). Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β-converting enzyme. Cell 69, 597-604.
51. Roepstorff, P., and Fohlman, J. (1984). Proposal for a common nomenclature for sequence ions in mass spectra. Biomed. Mass. Spectram. 11, 601.
52. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
53. Schlegel, J., Peters, I., Orrenius, S., Miller, D.K., Thornberry, N.A., Yamin, T.-T., and Nicholson, D.W. (1996). CPP-32/Apopain is the key interleukin-1β-converting enzyme-like protease involved in Fasmediated apoptosis. J. Biol. Chem. 277, 1841-1844.
54. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometry sequencing of silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
55. Smith, C.A., Davis, T., Anderson, D., Solam, L., Beckmann, M.P., Jerzy, R., Dower, S.K., Cosman, D., and Goodwin, R.G. (1990). A receptorfor tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248, 1019-1023.
56. Stanger, B.Z., Leder, P., Lee, T.H., Kim, E., and Seed, B. (1995). RIP: a novel protein containing a death domain that interacts with Fas/ APO-1 (CD95) in yeast and causes cell death. Cell 81, 513-523.
57. Steller, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445-1449.
58. Tartaglia, L.A., and Goeddel, D.V. (1992).Two TNF receptors. Immunol. Today 73, 151-153.
59. Tartaglia, L.A., Ayres, T.M., Wong, G.H.W., and Goeddel, D.V. (1993). A novel domain within the 55 kDa TNF receptor signals cell death. Cell 74, 845-853.
60. Tewari, M., and Dixit, V.M. (1995a). Signalling through members of the tumor necrosis receptor family. In Modular Texts in Molecular and Cell Biology, M. Purton and C. Heldin, eds. (London:Chapman and Hall), pp. 107-159.
61. Tewari, M., and Dixit, V.M. (1995b). Fas-and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus CrmA gene product. J. Biol. Chem. 270, 3255-3260.
62. Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R., Poirier, G.G., Salvesen, G.S., and Dixit, V.M. (1995). Yama/CPP-32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809.
63. Thornberry, N.A., Bull, H.G., Calaycay, J.R., Chapman, K.T., Howard, A.D., Kostura, M.J., Miller, D.K., Molineaux, S.M., Weidner, J.R., Aunins, J., Elliston, K.O., Ayala, J.M., Casano, F.J., Chin, J., Ding, G.J.-F., Egger, L.A., Gaffney, E.P., Limjuco, G., Palyha, O.G., Raju, S.M., Rolando, A.M., Salley, J.P., Yamin, T.-T., Lee, T.D., Shively, J.E., MacCross, M., Mumford, R.A., Schmidt, J.A., and Tocci, M.J. (1992). A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356, 768-774.
64. Trauth, B.C., Klas, C., Peters, A.M.J., Matzku, S., Moller, P., Falk, W., Debatin, K.-M., and Krammer, P.H. (1989). Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245, 301-305.
65. Vaux, D.L., Haecker, G., and Strasser, A. (1994). An evolutionary perspective on apoptosis. Cell 76, 777-779.
66. Walker, N.P.C., Talanian, R.V., Brady, K.D., Dang, L.C., Bump, N.J., Ferenz, C.R., Franklin, S., Ghayur, T., Hackett, M.C., Hammill, L.D., Herzog, L., Hugunin, M., Houy, W., Mankovich, J.A., McGuiness, L., Orlewicz, E., Paskind, M., Pratt, C.A., Reis, P., Summani, A., Terranova, M., Welch, J.P., Xiong, L., Moller, A., Tracey, D.E., Kamen, R., and Wong, W.W. (1994). Crystal structure of the cysteine protease interleukin-1β-converting enzyme: a (p20/p10)2 homodimer. Cell 78, 343-352.
67. Wang, L., Miura, M., Bergeron, L., Zhu, H., and Yuan, J. (1994). Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78, 739-750.
68. White, K., Grether, M.E., Abrams, J.M., Young, L., Farrell, K., and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
69. White, K., Tahaoglu, E., and Steller, H. (1996). Cell killing the Drosophila gene reaper. Science 271, 805-807.
70. Williams, M.S., and Henkart, P.A. (1994). Apoptotic cell death induced by intracellular proteolysis. J. Immunol. 1994, 4247-4255.
71. Wilm, M., and Mann, M. (1996). Analytical properties of the nano-electrospray ion source. Anal. Chem. 66, 1-8.
72. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., and Mann, M. (1996). Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469.
73. Wilson, K.P., Black, J.-A.F., Thomson, J.A., Kim, E.E., Griffith, J.P., Navia, M.A., Murcko, M.A., Chambers, S.P., Aldape, R.A., Raybuck, S.A., and Livingston, D.J. (1994). Structure and mechanism of interleukin-1β-converting enzyme. Nature 370, 270-275.
74. Yuan, J., Shaham, S., Ledoux, S., Ellis, H.M., and Horvitz, H.R. (1993). The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75, 641-652.