Regulation of apoptosis: The ubiquitous way

FASEB Journal

Volumn 17, Issue 8, 2003, Pages 790-799

  Yang, Yili ^a   Yu, Xiaodan ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

Caspase; IAP; Ring finger protein; Ubiquitin protein ligase (E3); Ubiquitination

Indexed keywords

CASPASE; INHIBITOR OF APOPTOSIS PROTEIN; PROTEASOME; PROTEIN BCL 2; PROTEIN P53; UBIQUITIN;

APOPTOSIS; CELL CYCLE; CELL DEATH; CELL TRANSFORMATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; APOPTOSIS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; LIGASES; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 0038375025     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.02-0654rev     Document Type: Review

References (117)

1. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479
2. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H. D., Mayer, T. U., and Jentsch, S. (1999) A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 96, 635-644
3. Almond, J. B., and Cohen, G. M. (2002) The proteasome: a novel target for cancer chemotherapy. Leukemia 16, 433-443
4. Dai, R. M., and Li, C. C. (2001) Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitinproteasome degradation. Nat. Cell Biol. 3, 740-744
5. Weissman, A. M. (2001) Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2, 169-178
6. Yao, T., and Cohen, R. E. (2002) A cryptic protease couples deubiquitination and degradation by the proteasome. Nature (London) 419, 403-407
7. Li, M., Chen, D., Shiloh, A., Luo, J., Nikolaev, A. Y., Qin, J., and Gu, W. (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature (London) 416, 648-653
8. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
9. Scheffner, M., Huibregtse, J. M., Vierstra, R. D., and Howley, P. M. (1993) The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75, 495-505
10. Huibregtse, J. M., Scheffner, M., Beaudenon, S., and Howley, P. M. (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92, 2563-2567
11. Lu, P. J., Zhou, X. Z., Shen, M., and Lu, K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283, 1325-1328
12. Kishino, T., Lalande, M., and Wagstaff, J. (1997) UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15, 70-73
13. Rotin, D., Kanelis, V., and Schild, L. (2001) Trafficking and cell surface stability of ENaC. Am. J. Physiol. 281, F391-F399
14. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature (London) 387, 296-299
15. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997) Regulation of p53 stability by Mdm2. Nature (London) 387, 299-303
16. Joazeiro, C. A., and Weissman, A. M. (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102, 549-552
17. Zheng, N., Wang, P., Jeffrey, P. D., and Pavletich, N. P. (2000) Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102, 533-539
18. Zheng, N., Schulman, B. A., Song, L., Miller, J. J., Jeffrey, P. D., Wang, P., Chu, C., Koepp, D. M., Elledge, S.J., Pagano, M., et al. (2002) Structure of the Cull-Rbxl-Skpl-F boxSkp2 SCF ubiquitin ligase complex. Nature (London) 416, 703-709
19. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K. I. (2001) U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276, 33111-33120
20. Coscoy, L., Sanchez, D.J., and Ganem, D. (2001) A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell Biol. 155, 1265-1273
21. Lu, Z., Xu, S., Joazeiro, C., Cobb, M. H., and Hunter, T. (2002) The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol. Cell 9, 945-956
22. Capili, A. D., Schultz, D. C., Rauscher, I. F., and Borden, K. L. (2001) Solution structure of the PHD domain from the KAP-1 corepressor: structural determinants for PHD, RING and LIM zinc-binding domains. EMBO J. 20, 165-177
23. Aravind, L., and Koonin, E. V. (2000) The U box is a modified RING finger - a common domain in ubiquitination. Curr. Biol. 10, R132-R134
24. Connell, P., Ballinger, C. A., Jiang, J., Wu, Y., Thompson, L. J., Hohfeld, J., and Patterson, C. (2001) The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat. Cell Biol. 3, 93-96
25. Kim, K. I., Baek, S. H., and Chung, C. H. (2002) Versatile protein tag, SUMO: its enzymology and biological function. J. Cell. Physiol. 191, 257-268
26. Buchberger, A., Howard, M. J., Proctor, M., and Bycroft, M. (2001) The UBX domain: a widespread ubiquitin-like module. J. Mol. Biol. 307, 17-24
27. Ryu, S. W., and Kim, E. (2001) Apoptosis induced by human Fas-associated factor 1, hFAF1, requires its ubiquitin homologous domain, but not the Fas-binding domain. Biochem. Biophys. Res. Commun. 286, 1027-1032
28. Schwartz, L. M., Myer, A., Kosz, L., Engelstein, M., and Maier, C. (1990) Activation of polyubiquitin gene expression during developmentally programmed cell death. Neuron 5, 411-419
29. Orlowski, R. Z. (1999) The role of the ubiquitin-proteasome pathway in apoptosis. Cell Death Differ. 6, 303-313
30. Delic, J., Morange, M., and Magdelenat, H. (1993) Ubiquitin pathway involvement in human lymphocyte gamma-irradiation-induced apoptosis. Mol. Cell. Biol. 13, 4875-4883
31. Grimm, L. M., Goldberg, A. L., Poirier, G. G., Schwartz, L. M., and Osborne, B. A. (1996) Proteasomes play an essential role in thymocyte apoptosis. EMBO J. 15, 3835-3844
32. Sadoul, R., Fernandez, P. A., Quiquerez, A. L., Martinou, I., Maki, M., Schroter, M., Becherer, J. D., Irmler, M., Tschopp, J., and Martinou, J, C. (1996) Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J. 15, 3845-3852
33. Hirsch, T., Dallaporta, B., Zamzami, N., Susin, S. A., Ravagnan, L., Marzo, I., Brenner, C., and Kroemer, G. (1998) Proteasome activation occurs at an early, premitochondrial step of thymocyte apoptosis. J. Immunol. 161, 35-40
34. Oren, M. (1999) Regulation of the p53 tumor suppressor protein. J. Biol. Chem. 274, 36031-36034
35. Balint, E. E., and Vousden, K. H. (2001) Activation and activities of the p53 tumour suppressor protein. Br. J. Cancer 85, 1813-1823
36. Sherr, C. J. (2001) The INK4a/ARF network in turnout suppression. Nat. Rev. Mol. Cell Biol. 2, 731-737
37. Parant, J., Chavez-Reyes, A., Little, N. A., Yan, W., Reinke, V., Jochemsen, A. G., and Lozano, G. (2001) Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat. Genet. 29, 92-95
38. Finch, R. A., Donoviel, D. B., Potter, D., Shi, M., Fan, A., Freed, D. D., Wang, C. Y., Zambrowicz, B. P., Ramirez-Solis, R., Sands, A. T., et al. (2002) MdmX is a negative regulator of p53 activity in vivo. Cancer Res. 62, 3221-3225
39. Migliorini, D., Denchi, E. L., Danovi, D., Jochemsen, A., Capillo, M., Gobbi, A., Helin, K., Pelicci, P. G., and Marine, J. C. (2002) Mdm4 (Mdmx) regulates p53-induced growth arrest and neuronal cell death during early embryonic mouse development. Mol. Cell. Biol. 22, 5527-5538
40. Gu, J., Kawai, H., Nie, L., Kitao, H., Wiederschain, D., Jochemsen, A. G., Parant, J., Lozano, G., and Yuan, Z. M. (2002) Mutual dependence of MDM2 and MDMX in their functional inactivation of p53. J. Biol. Chem. 277, 19251-19254
41. Riemenschneider, M. J., Buschges, R., Wolter, M., Reifenberger, J., Bostrom, J., Kraus, J. A., Schlegel, U., and Reifenberger, G. (1999) Amplification and overexpression of the MDM4 (MDMX) gene from 1q32 in a subset of malignant gliomas without TP53 mutation or MDM2 amplification. Cancer Res. 59, 6091-6096
42. Ryan, K. M., Phillips, A. C., and Vousden, K. H. (2001) Regulation and function of the p53 tumor suppressor protein. Curr. Opin. Cell Biol. 13, 332-337
43. Cory, S., and Adams, J. M. (2002) The bc12 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656
44. Fesik, S. W. (2000) Insights into programmed cell death through structural biology. Cell 103, 273-282
45. Huang, D. C., and Strasser, A. (2000) BH3-only proteins essential initiators of apoptotic cell death. Cell 103, 839-842
46. Lindsten, T., Ross, A. J., King, A., Zong, W. X., Rathmell, J. C., Shiels, H. A., Ulrich, E., Wayrnire, K. G., Mahar, P., Frauwirth, K., et al. (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 6, 1389-1399
47. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730
48. Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., and Korsmeyer, S. J. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14, 2060-2071
49. Dimmeler, S., Breitschopf, K., Haendeler, J., and Zeiher, A. M. (1999) Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J. Exp. Med. 189, 1815-1822
50. Breitschopf, K., Haendeler, J., Malchow, P., Zeiher, A. M., and Dimmeler, S. (2000) Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway. Mol. Cell. Biol. 20, 1886-1896
51. Li, B., and Dou, Q. P. (2000) Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc. Natl. Acad. Sci. USA 97, 3850-3855
52. Marshansky, V., Wang, X., Bertrand, R., Luo, H., Duguid, W., Chinnadurai, G., Kanaan, N., Vu, M. D., and Wu, J. (2001) Proteasomes modulate balance among proapoptotic and antiapoptotic Bcl-2 family members and compromise functioning of the electron transport chain in leukemic cells. J. Immunol. 166, 3130-3142
53. Breitschopf, K., Zeiher, A. M., and Dimmeler, S. (2000) Ubiquitin-mediated degradation of the proapoptotic active form of bid. A functional consequence on apoptosis induction. J. Biol. Chem. 275, 21648-21652
54. Okura, T., Gong, L., Kamitani, T., Wada, T., Okura, I., Wei, C. F., Chang, H. M., and Yeh, E. T. (1996) Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J. Immunol. 157, 4277-4281
55. Becker, K., Schneider, P., Hofmann, K., Mattmann, C., and Tschopp, J. (1997) Interaction of Fas (Apo-1/CD95) with proteins implicated in the ubiquitination pathway. FEBS Lett. 412, 102-106
56. Ryu, S. W., Chae, S. K., and Kim, E. (2000) Interaction of Daxx, a Fas binding protein, with sentrin and Ubc9. Biochem. Biophys. Res. Commun. 279, 6-10
57. Lalioti, V. S., Vergarajauregui, S., Pulido, D., and Sandoval, I. V. (2002) The insulin-sensitive glucose transporter, GLUT4, interacts physically with Daxx. Two proteins with capacity to bind Ubc9 and conjugated to SUMO1. J. Biol. Chem. 277, 19783-19791
58. Thome, M., and Tschopp, J. (2001) Regulation of lymphocyte proliferation and death by FLIP. Nat Rev Immunol 1, 50-58
59. Yeh, W. C., Itie, A., Elia, A.J., Ng, M., Shu, H. B., Wakeham, A., Mirtsos, C., Suzuki, N., Bonnard, M., Goeddel, D. V., et al. (2000) Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12, 633-642
60. Griffith, T. S., Chin, W. A., Jackson, G. C., Lynch, D. H., and Kubin, M. Z. (1998) Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J. Immunol. 161, 2833-2840
61. Kim, Y., Suh, N., Sporn, M., and Reed, J. C. (2002) An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J. Biol. Chem. 277, 22320-22329
62. Bonavida, B., Ng, C. P., Jazirehi, A., Schiller, G., and Mizutani, Y. (1999) Selectivity of TRAIL-mediated apoptosis of cancer cells and synergy with drugs: the trail to non-toxic cancer therapeutics (review). Int. J. Oncol. 15, 793-802
63. Krebs, D. L., and Hilton, D. J. (2001) SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19, 378-387
64. Kamura, T., Sato, S., Haque, D., Liu, L., Kaelin, W. G., Jr., Conaway, R. C., and Conaway, J. W. (1998) The Elongin BC complex interacts Aith the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev. 12, 3872-3881
65. Zhang, J. G., Farley, A., Nicholson, S. E., Willson, T. A., Zugaro, L. M., Simpson, R. J., Moritz, R. L., Cary, D., Richardson, R., Hausmann, G., et al. (1999) The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc, Natl. Acad. Sci. USA 96, 2071-2076
66. Frantsve, J., Schwaller, J., Sternberg, D. W., Kutok, J., and Gilliland, D. G. (2001) Socs-1 inhibits TEL-JAK2-mediated transformation of hematopoietic cells through inhibition of JAK2 kinase activity and induction of proteasome-mediated degradation. Mol. Cell. Biol. 21, 3547-3557
67. Kamizono, S., Hanada, T., Yasukawa, H., Minoguchi, S., Kato, R., Minoguchi, M., Hattori, K., Hatakeyama, S., Yada, M., Morita, S., et al. (2001) The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2. J. Biol. Chem. 276, 12530-12538
68. De Sepulveda, P., Ilangumaran, S., and Rottapel, R. (2000) Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation. J. Biol. Chem. 275, 14005-14008
69. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J., Slaughter, C., Pickart, C., and Chen, Z.J. (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361
70. Wang, C., Deng, L., Hong, M., Akkaraju, G. R., Inoue, J., and Chen, Z. J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature (London) 412, 346-351
71. Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NFκB activity. Annu. Rev. Immunol. 18, 621-663
72. Crook, N. E., Clem, R. J., and Miller, L. K. (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67, 2168-2174
73. Deveraux, Q. L., and Reed, J. C. (1999) IAP family proteins suppressors of apoptosis. Genes Dev. 13, 239-252
74. Richter, B. W., Mir, S. S., Eiben, L. J., Lewis, J., Reffey, S. B., Frattini, A., Tian, L., Frank, S., Youle, R. J., Nelson, D. L., et al. (2001) Molecular cloning of ILP-2, a novel member of the inhibitor of apoptosis protein family. Mol. Cell. Biol. 21, 4292-4301
75. Vucic, D., Stennicke, H. R., Pisabarro, M. T., Salvesen, G. S., and Dixit, V. M. (2000) ML-IAP, a novel inhibitor of apoptosis that is preferentially expressed in human melanomas. Curr. Biol. 10, 1359-1366
76. Goyal, L. (2001) Cell death inhibition: keeping caspases in check. Cell 104, 805-808
77. Yang, Y. L., and Li, X. M. (2000) The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res. 10, 169-177
78. Li, F., Ambrosini, G., Chu, E. Y., Plescia, J., Tognin, S., Marchisio, P. C., and Altieri, D. C. (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature (London) 396, 580-584
79. Fraser, A. G., James, C., Evan, G. I., and Hengartner, M. O. (1999) Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr. Biol. 9, 292-301
80. Uren, A. G., Beilharz, T., O'Connell, M. J., Bugg, S. J., van Driel, R., Vaux, D. L., and Lithgow, T. (1999) Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc. Natl. Acad. Sci. USA 96, 10170-10175
81. Verhagen, A. M., Coulson, E. J., and Vaux, D. L. (2001) Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol. 2, REVIEWS3009
82. Yang, Y., Fang, S., Jensen, J. P., Weissman, A. M., and Ashwell, J. D. (2000) Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 288, 874-877
83. Clem, R. J., Sheu, T. T., Richter, B. W., He, W. W., Thornberry, N. A., Duckett, C. S., and Hardwick, J. M. (2001) c-IAP1 is cleaved by caspases to produce a proapoptotic C-terminal fragment. J. Biol. Chem. 276, 7602-7608
84. Huang, H., Joazeiro, C. A., Bonfoco, E., Kamada, S., Leverson, J. D., and Hunter, T. (2000) The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J. Biol. Chem. 275, 26661-26664
85. Suzuki, Y., Nakabayashi, Y., and Takahashi, R. (2001) Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc. Natl. Acad. Sci. USA 98, 8662-8667
86. Harlin, H., Reffey, S. B., Duckett, C. S., Lindsten, T., and Thompson, C. B. (2001) Characterization of XIAP-deficient mice. Mol. Cell. Biol. 21, 3604-3608
87. Hay, B. A., Wassarman, D. A., and Rubin, G. M. (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262
88. Vucic, D., Kaiser, W. J., and Miller, L. K. (1998) Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol. Cell. Biol. 18, 3300-3309
89. Wang, S. L., Hawkins, C. J., Yoo, S. J., Muller, H. A., and Hay, B. A. (1999) The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98, 453-463
90. Goyal, L., McCall, K., Agapite, J., Hartwieg, E., and Steller, H. (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 19, 589-597
91. Palaga, T., and Osborne, B. (2002) The 3D's of apoptosis: death, degradation and DIAPs. Nat. Cell Biol. 4, E149-E151
92. Hays, R., Wickline, L., and Cagan, R. (2002) Morgue mediates apoptosis in the Drosophila melanogaster retina by promoting degradation of DIAP1. Nat. Cell Biol. 4, 425-431
93. Ryoo, H. D., Bergmann, A., Gonen, H., Ciechanover, A., and Steller, H. (2002) Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 4, 432-438
94. Holley, C. L., Olson, M. R., Colon-Ramos, D. A., and Kornbluth, S. (2002) Reaper eliminates IAP proteins through stimulated IAP degradation and generalized translational inhibition. Nat. Cell Biol. 4, 439-444
95. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M., Clem, R. J., Muller, H. A., and Hay, B. A. (2002) Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4, 416-424
96. Wilson, R., Goyal, L., Ditzel, M., Zachariou, A., Baker, D. A., Agapite, J., Steller, H., and Meier, P. (2002) The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 4, 445-450
97. Wing, J. P., Schreader, B. A., Yokokura, T., Wang, Y., Andrews, P. S., Huseinovic, N., Dong, C. K., Ogdahl, J. L., Schwartz, L. M., White, K., et al. (2002) Drosophila morgue is an F box/ubiquitin conjugase domain protein important for grimreaper mediated apoptosis. Nat. Cell Biol. 4, 451-456
98. Tenev, T., Zachariou, A., Wilson, R., Paul, A., and Meier, P. (2002) Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J. 21, 5118-5129
99. Du, C., Fang, M., Li, Y., Li, L., and Wang, X. (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42
100. Verhagen, A. M., Ekert, P. G., Pakusch, M., Silke, J., Connolly, L. M., Reid, G. E., Moritz, R. L., Simpson, R. J., and Vaux, D. L. (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102, 43-53
101. Chai, J., Du, C., Wu, J. W., Kyin, S., Wang, X., and Shi, Y. (2000) Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature (London) 406, 855-862
102. Liu, Z., Sun, C., Olejniczak, E. T., Meadows, R. P., Betz, S. F., Oost, T., Herrmann, J., Wu, J. C., and Fesik, S. W. (2000) Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature (London) 408, 1004-1008
103. Wu, G., Chai, J., Suber, T. L., Wu, J. W., Du, C., Wang, X., and Shi, Y. (2000) Structural basis of IAP recognition by Smac/DIABLO. Nature (London) 408, 1008-1012
104. Srinivasula, S. M., Hegde, R., Saleh, A., Datta, P., Shiozaki, E., Chai, J., Lee, R. A., Robbins, P. D., Fernandes-Alnemri, T., Shi, Y., et al. (2001) A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature (London) 410, 112-116
105. MacFarlane, M., Merrison, W., Bratton, S. B., and Cohen, G. M. (2002) Proteasome-mediated Degradation of Smac during apoptosis: XIAP promotes smac ubiquitination in vitro. J. Biol. Chem. 277, 36611-36616
106. Deng, Y., Lin, Y., and Wu, X. (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev. 16, 33-45
107. Sun, X. M., Bratton, S. B., Butterworth, M., MacFarlane, M., and Cohen, G. M. (2002) Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J. Biol. Chem. 277, 11345-11351
108. Li, S., Zhao, Y., He, X., Kim, T. H., Kuharsky, D. K., Rabinowich, H., Chen, J., Du, C., and Yin, X. M. (2002) Relief of extrinsic pathway inhibition by the Bid-dependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis. J. Biol. Chem. 277, 26912-26920
109. Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., and Takahashi, R. (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell 8, 613-621
110. Hegde, R., Srinivasula, S. S. M., Zhang, Z., Wassell, R., Mukattash, R., Cilenti, L., DuBois, G., Lazebnik, Y., Zervos, A. S., Fernandes-Alnemri, T., et al. (2002) Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 277, 432-438
111. Martins, L. M., Iaccarino, I., Tenev, T., Gschmeissner, S., Totty, N. F., Lemoine, N. R., Savopoulos, J., Gray, C. W., Creasy, C. L., Dingwall, C., et al. (2002) The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J. Biol. Chem. 277, 439-444
112. Verhagen, A. M., Silke, J., Ekert, P. G., Pakusch, M., Kaufmann, H., Connolly, L. M., Day, C. L., Tikoo, A., Burke, R., Wrobel, C., et al. (2002) HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 277, 445-454
113. Nguyen, L. T., Duncan, G. S., Mirtsos, C., Ng, M., Speiser, D. E., Shahinian, A., Marino, M. W., Mak, T. W., Ohashi, P. S., and Yeh, W. C. (1999) TRAF2 deficiency results in hyperactivity of certain TNFRI signals and impairment of CD40-mediated responses. Immunity 11, 379-389
114. Rothe, M., Pan, M. G., Henzel, W. J., Ayres, T. M., and Goeddel, D. V. (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83, 1243-1252
115. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H., and Lenardo, M. J. (1995) Induction of apoptosis in mature T cells by tumour necrosis factor. Nature (London) 377, 348-351
116. Weiss, T., Grell, M., Siemienski, K., Muhlenbeck, F., Durkop, H., Pfizenmaier, K., Scheurich, P., and Wajant, H. (1998) TNFR80-dependent enhancement of TNFR60-induced cell death is mediated by TNFR-associated factor 2 and is specific for TNFR60. J. Immunol. 161, 3136-3142
117. Li, X., Yang, Y., and Ashwell, J. D. (2002) TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature (London) 416, 345-347