Dual signaling of the Fas receptor: Initiation of both apoptotic and necrotic cell death pathways

Journal of Experimental Medicine

Volumn 188, Issue 5, 1998, Pages 919-930

  Vercammen, Dominique ^a   Brouckaert, Greet ^a   Denecker, Geertrui ^a   Van De Craen, Marc ^a   Declercq, Wim ^a   Fiers, Walter ^a   Vandenabeele, Peter ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Apoptosis; Caspases; Fas antigen; Necrosis; Oxygen radicals

Indexed keywords

CASPASE INHIBITOR; ENZYME INHIBITOR; FAS ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OXYGEN RADICAL; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; FIBROSARCOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; ANTIGENS, CD95; APOPTOSIS; CASPASE 3; CASPASE 7; CASPASES; CELL DEATH; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; ENZYME ACTIVATION; FIBROSARCOMA; HUMANS; LIGANDS; MICE; NECROSIS; NF-KAPPA B; OLIGOPEPTIDES; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0032494143     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.5.919     Document Type: Article

References (72)

1. Grooten, J., V. Goossens, B. Vanhaesebroeck, and W. Fiers. 1993. Cell membrane permeabilization and cellular collapse, followed by loss of dehydrogenase activity: early events in tumour necrosis factor-induced cytotoxicity. Cytokine. 5: 546-555.
2. Kerr, J.F.R., A.H. Wyllie, and A.R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239-257.
3. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie. 1980. Cell death: the significance ot apoptosis. Int. Rev. Cytol. 68:251-306.
4. Jacobson, M.D., M. Weil, and M.C. Raff. 1997. Programmed cell death in animal development. Cell. 88:347-354.
5. Thompson, C. 1995. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1456-1462.
6. Nicholson, D.W., and N.A. Thornberry. 1997. Caspases: killer proteases. Trends Biochem. Sci. 22:299-306.
7. Villa, P., S.H. Kaufmann, and W.C. Earnshaw. 1997. Caspases and caspase inhibitors. Trends Biochem. Sci. 22:388-393.
8. Porter, A.G., P. Ng, and R.U. Jänicke. 1997. Death substrates come alive. Bioessays. 19:501-507.
9. Nagata, S. 1997. Apoptosis by death factor. Cell. 88:355-365.
10. Itoh, N., and S. Nagata. 1993. A novel protein domain required for apoptosis. Mutational analysis ot human Fas antigen J. Biol. Chem. 268:10932-10937.
11. Tartaglia, L., T. Ayres, G. Wong, and D. Goeddel. 1993. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 74:845-853.
12. Song, H.Y., J.D. Dunbar, and D.B. Donner. 1994. Aggregation of the intracellular domain of the type 1 tumor necrosis factor receptor defined by the two-hybrid system. J. Biol. Chem. 269:22492-22495.
13. Boldin, M.P., E.E. Varfolomeev, Z. Pancer, I.L. Mett, J.H. Camonis, and D. Wallach. 1995. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 270:7795-7798.
14. Vandevoorde, V., G. Haegeman, and W. Fiers. 1997. Induced expression of trimerized intracellular domains of the human tumor necrosis factor (TNF) p55 receptor elicits TNF effects. J. Cell Biol. 137:1627-1638.
15. Hsu, H., J. Xiong, and D.V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell. 81:495-504.
16. Hsu, H., H.B. Shu, M.G. Pan, and D.V. Goeddel. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell. 84:299-308.
17. Chinnaiyan, A.M., K. O'Rourke, M. Tewari, and V.M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 81:505-512.
18. Kischkel, F.C., S. Hellbardt, I. Behrmann, M. Germer, M. Pawlita, P.H. Krammer, and M.E. Peter. 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO (Eur. Mol. Biol. Organ.) J. 14:5579-5588.
19. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/ FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell. 85:803-815.
20. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz, 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. Cell. 85:817-827.
21. Medema, J.P., C. Scaffidi, F.C. Kischkel, A. Shevchenko, M. Mann, P.H. Krammer, and M.E. Peter. 1997. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO (Eur. Mol. Biol. Organ.) J. 16:2794-2804.
22. Srinivasula, S.M., M. Ahmad, T. Fernandes-Alnemri, G. Litwack, and E.S. Alnemri. 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. Prof. Natl. Acad. Sci. USA. 93: 14486-14491.
23. Muzio, M., G.S. Salvesen, and V.M. Dixit. 1997. FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem. 272:2952-2956.
24. Wallach, D., M. Boldin, E. Varfblomeev, R. Beyaert, P. Vandenabeele, and W. Fiers. 1997. Cell death induction by receptors of the TNF family: towards a molecular understanding. FEBS Lett. 410:96-106.
25. Laster, S.M., J.G. Wood, and L.R. Gooding. 1988. Tumor necrosis factor can induce both apoptotic and necrotic forms of cell lysis. J. Immunol. 141:2629-2635.
26. Fiers, W., R. Beyaert, E. Boone, S. Cornelis, W. Declercq, E. Decoster, G. Denecker, B. Depuydt, D. De Valck, G. De Wilde, et al. 1995. TNF-induced intracellular signaling leading to gene induction or to cytotoxicity by necrosis or by apoptosis. J. Inflamm. 47:67-75.
27. Vercammen, D., R. Beyaert, G. Denecker, V. Goossens, G. Van Loo, W. Declercq, J. Grooten, W. Fiers, and P. Vandenabeele. 1998. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187:1477-1485.
28. Goossens, V., J. Grooten, K. De Vos, and W. Fiers. 1995. Direct evidence tor tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. USA. 92:8115-8119.
29. Vanhaesebroeck, B., S. Van Bladel, A. Lenaerts, P. Suffys, R. Beyaert, R. Lucas, F. Van Roy, and W. Fiers. 1991. Two discrete types ot tumor necrosis factor-resistant cells derived from the same cell line. Cancer Res. 51:2469-2477.
30. Fransen, L., R. Müller, A. Marmenout, J. Tavernier, J. Van der Heyden, E. Kawashima, E. Chollet, R. Tizard, H. Van Heuverswyn, A. Van Vliet, et al. 1985. Molecular cloning of mouse tumour necrosis factor cDNA and its eukaryotic expression. Nucleic Acids Res. 13:4417-4429.
31. Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:5322.
32. Tada, H., O. Shiho, K. Kuroshima, M. Koyama, and K. Tsukamoto. 1986. An improved colorimetric assay for interleukin 2. J. Immunol. Methods. 93:157-165.
33. b promoter: enhancer-like sequences and their role in the regulation of class I gene expression. Cell. 44:261-272.
34. Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S. Mizushima, M. Sameshima, A. Hase, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell. 66:233-243.
35. Opipari, A.W., H.M. Hu, Jr., R. Yabkowitz, and V.M. Dixit. 1992. The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J. Biol. Chern. 267:12424-12427.
36. Jäättelä, M., H. Mouritzen, F. Elling, and L. Bastholm. 1996. A20 zinc finger protein inhibits TNF and IL-1 signaling. J. Immunol. 156:1166-1173.
37. Kirstein, M., W. Fiers, and C. Baglioni. 1986. Growth inhibition and cytotoxicity of tumor necrosis factor in L929 cells is enhanced by high cell density and inhibition of mRNA synthesis. J. Immunol. 137:2277-2280.
38. Vercammen, D., P. Vandenabeele, R. Beyaert, W. Declercq, and W. Fiers. 1997. Tumour necrosis factor-induced necrosis versus anti-Fas-induced apoptosis in L929 cells. Cytokine. 9: 801-808.
39. Fernandes-Alnemri, T., R.C. Armstrong, J. Krebs, S.M. Srinivasula, L. Wang, F. Bullrich, L.C. Fritz, J.A. Trapani, K.J. Tomaselli, G. Litwack, and E.S. Alnemri. 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.
40. Fernandes-Alnemri, T., A. Takahashi, R. Armstrong, J. Krebs, L. Fritz, K.J. Tomaselli, L. Wang, Z. Yu, C.M. Croce, G. Salveson, et al. 1995. Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res. 55:6045-6052.
41. Nicholson, D.W., A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, Y.A. Lazebnik, et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:37-43.
42. Sarin, A., M.L. Wu, and P.A. Henkart. 1996. Diflerent interleukin-1β converting enzyme (ICE) family protease requirements for the apoptotic death of T lymphocytes triggered by diverse stimuli. J. Exp. Med. 184:2445-2450.
43. Margolin, N., S.A. Raybuck, K.P. Wilson, W. Chen, T. Fox, Y. Gu, and D.J. Livingston. 1997. Substrate and inhibitor specificity of interleukin-1β-converting enzyme and related caspases. J. Biol. Chem. 272:7223-7228.
44. Odake, S., C.M. Kam, L. Narasimhan, M. Poe, J.T. Blake, O. Krahenbuhl, J. Tschopp, and J.G. Powers. 1991. Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins. Biochemistry. 30:2217-2227.
45. Shi, L., C.M. Kam, J.C. Powers, R. Aebersold, and A.H. Greenberg. 1992. Purification ot three cytotoxic lymphocyte granule serine proteases that induce apoptosis through distinct substrate and target cell interactions. J. Exp. Med. 176:1521-1529.
46. Schulze-Osthoff, K., A.C. Bakker, B. Vanhaesebroeck, R. Beyaert, W.A. Jacob, and W. Fiers. 1992. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. J. Biol. Chem. 267:5317-5323.
47. Schulze-Osthoff, K., P.H. Krammer, and W. Dröge. 1994. Divergent signalling via APO-1/Fas and the TNF receptor, two homologous molecules involved in physiological cell death. EMBO (Eur. Mol. Biol. Organ.) J. 13:4587-4596.
48. Patestos, N.P., G. Haegeman, V. Vandevoorde, and W. Fiers. 1993. Activation of the nuclear factor KB is not sufficient for regulation of tumor necrosis factor-induced interleukin-6 gene expression. Biochimie (Paris). 75:1007-1018.
49. Müller, J.M., R.A. Rupee, and P.A. Baeuerle. 1997. Study of gene regulation by NF-κB and AP-1 in response to reactive oxygen intermediates. Methods. 11:301-312.
50. Yonehara, S., A. Ishii, and M. Yonehara. 1989. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169:1747-1756.
51. Los, M., M. Van de Craen, L.C. Penning, H. Schenk, M. Westendorp, P.A. Baeuerle, W. Dröge, P.H. Krammer, W. Fiers, and K. Schulze-Osthoff 1995. Requirement ot an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature. 375:81-83.
52. Enari, M., H. Hug, and S. Nagata. 1995. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature. 375:78-81.
53. Enari, M., R.V. Talanian, W.W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature. 380:723-726.
54. Tewari, M., L.T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D.R. Beidler, G.G. Poirier, G.S. Salvesen, and V.M. Dixit. 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:801-809.
55. Kamada, S., M. Washida, J. Hasegawa, H. Kusano, Y. Funahashi, and Y. Tsujimoto. 1997. Involvement of caspase-4(-like) protease in Fas-mediated apoptotic pathway. Oncogene. 15:285-290.
56. Kitson, J., T. Raven, Y.P. Jiang, D.V. Goeddel, K.M. Giles, K.T. Pun, C.J. Grinham, R. Brown, and S.N. Farrow. 1996. A death-domain-containing receptor that mediates apoptosis. Nature. 384:372-375.
57. Chinnaiyan, A.M., K. O'Rourke, G.L. Yu, R.H. Lyons, M. Garg, D.R. Duan, L. Xing, R. Gentz, J. Ni, and V.M. Dixit. 1996. Signal transduction by DR3, a death domain-containing receptor related to TNFR-1 and CD95. Science. 274: 990-992.
58. Marsters, S.A., J.P. Sheridan, C.J. Donahue, R.M. Pitti, C.L. Gray, A.D. Goddard, K.D. Bauer, and A. Ashkenazi. 1996. Apo-3, a new member of the tumor necrosis factor receptor family, contains a death domain and activates apoptosis and NF-κB. Curr. Biol. 6:1669-1676.
59. Pan, G., K. O'Rourke, A.M. Chinnaiyan, R. Gentz, R. Ebner, J. Ni, and V.M. Dixit. 1997. The receptor tor the cytotoxic ligand TRAIL. Science. 276:111-113.
60. Walczak, H., M.A. Degli-Espoti, R.S. Johnson, P.J. Smolak, J.Y. Waugh, N. Boiani, M.S. Timour, M.J. Gerhart, K.A. Schooley, C.A. Smith, et al. 1997. TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO (Eur. Mol. Biol. Organ.) J. 16:5386-5397.
61. Pan, G., J. Ni, Y.F. Wei, G. Yu, R. Gentz, and V.M. Dixit. 1997. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science. 277:815-818.
62. Sheridan, J.P., S.A. Marsters, R.M. Pitti, A. Gurney, M. Skubatch, D. Baldwin, L. Ramakrishnan, C.L. Gray, K. Baker, W.I. Wood, et al. 1997. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science. 277: 818-821.
63. Lippke, J.A., Y. Gu, C. Sarnecki, P.R. Caron, and M.S. Su. 1996. Identification and characterization of CPP32/Mch2 homolog 1, a novel cysteine protease similar to CPP32. J. Biol. Chem. 271:1825-1828.
64. Stancovski, I., and D. Baltimore. 1997. NF-κB activation: the IκB kinase revealed? Cell. 91:299-302.
65. Leist, M., and P. Nicotera. 1997. The shape of cell death. Biochem. Biophys. Res. Commun. 236:1-9.
66. Scaffidi, C., S. Fulda, A. Srinivasan, C. Friesen, F. Li, K.J. Tomaselli, K.-M. Debatin, P.H. Krammer, and M.E. Peter. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO (Eur. Mol. Biol. Organ.) J. 17:1675-1687.
67. Friedlander, R.M., R.H. Brown, V. Gagliardini, J. Wang, and J. Yuan. 1997. Inhibition of ICE slows ALS in mice. Nature. 388:31.
68. Kim, T.-W., W.H. Pettingell, Y.-K. Jung, D.M. Kovacs, and R.E. Tanzi. 1997. Alternative cleavage of Alzheimer-associated presenilins during apoptosis by a caspase-3 family protease. Science. 277:373-376.
69. Goldberg, Y.P., D.W. Nicholson, D.M. Rasper, M.A. Kalchman, H.B. Koide, R.K. Graham, M. Bromm, P. Kazemi-Esfarjani, N.A. Thornberry, J.P. Vaillancourt, and M.R. Hayden. 1996. Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nat. Genet. 13:442-449.
70. Scherzinger, E., R. Lurz, M. Turmaine, L. Mangiarini, B. Hollenbach, R. Hasenbank, G.P. Bates, S.W. Davies, H. Lehrach, and E.E. Wanker. 1997. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell. 90:549-558.
71. Hara, H., R.M. Friedlander, V. Gagliardini, C. Ayata, K. Fink, Z. Huang, M. Shimizu-Sasamata, J. Yuan, and M.A. Moskowitz. 1997. Inhibition of interleukin 1β converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. USA. 94:2007-2012.
72. Rodriguez, I., K. Matsuura, C. Ody, S. Nagata, and P. Vassalli. 1996. Systemic injection of a tripeptide inhibits the intracellular activation of CPP32-like proteases in vivo and fully protects mice against Fas-mediated fulminant liver destruction and death. J. Exp. Med. 184:2067-2072.