The role of the ubiquitin-proteasome pathway in apoptosis

Cell Death and Differentiation

Volumn 6, Issue 4, 1999, Pages 303-313

  Orlowski, Robert Z ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Apoptosis; Multicatalytic proteinase complex; Programmed cell death; Proteasome; Ubiquitin

Indexed keywords

CASPASE; CELL PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEASOME; PROTEIN P53; UBIQUITIN;

APOPTOSIS; CELL CYCLE; CELL DEATH; HUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

EID: 0032919345     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400505     Document Type: Review

References (115)

1. Baumeister W, Cejka Z, Kania M and Seemuller E (1997) The proteasome: a macromolecular assembly designed to confine proteolysis to a nanocompartment. Biol. Chem. 378: 121-130
2. Ciechanover A and Schwartz AL (1998) The ubiquitin-proteasome pathway: The complexity and myriad functions of proteins death. Proc. Natl. Acad. Sci. USA 95: 2727-2730
3. Goldberg AL, Akopian TN, Kisselev AF, Lee DH and Rohrwild M (1997) New insights into the mechanisms and importance of the proteasome in intracellular protein degradation. Biol. Chem. 378: 131-140
4. Hershko A and Ciechanover A (1992) The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61: 761-807
5. Orlowski M (1990) The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry 29: 10289-10297
6. Rechsteiner M, Hoffman L and Dubiel W (1993) The multicatalytic and 26S proteases. J. Biol. Chem. 268: 6065-6068
7. Tanaka K (1998) Proteasomes: structure and biology. J. Biochem (Tokyo) 123: 195-204
8. Hershko A (1997) Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol. 9: 788-799
9. King RW, Deshaies RJ, Peters J-M and Kirschner MW (1996) How proteolysis drives the cell cycle. Science 274: 1652-1659
10. Oikawa T, Sasaki T, Nakamura M, Shimamura M, Tanahashi N, Omura S and Tanaka K (1998) The proteasome is involved in angiogenesis. Biochem. Biophys. Res. Commun. 246: 243-248
11. Heinemeyer W, Kleinschmidt JA, Saidowsky J, Escher C and Wolf DH (1991) Proteinase yscE, the yeast proteasome/multicatalytic multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 10: 555-562
12. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267: 1456-1462
13. Vaux DL and Strasser A (1996) The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA 93: 2239-2244
14. Wyllie AH (1997) Apoptosis and carcinogenesis. J. Cell Biol. 73: 189-197
15. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW and Yuan J (1996) Human ICE/CED-3 protease nomenclature. Cell 87: 171
16. Patel T, Gores GJ and Kaufmann SH (1996) The role of proteases during apoptosis. FASEB J. 10: 587-597
17. Solary E Eymin B, Droin N and Haugg M (1998) Proteases, proteolysis, and apoptosis. Cell Biol. Toxicol. 14: 121-132.
18. Zhivotovsky B, Burgess DH, Vanags DM and Orrenius S (1997) Involvement of cellular proteolytic machinery in apoptosis. Biochem. Biophys. Res. Commun. 230: 481-488
19. Schwartz LM, Myer A, Kosz L, Engelstein M and Maier C (1990) Activation of polyubiquitin gene expression during developmentally programmed cell death. Neuron 5: 411-419
20. Roy C, Brown DL, Little JE, Valentine BK, Walker PR, Sikorska M, Leblanc, J and Chaly N (1992) The topoisomerase II inhibitor teniposide (VM-26) induces apoptosis in unstimulated mature murine lymphocytes. Exp. Cell Res. 200: 416-424
21. Lauzon RJ, Patton CW and Weissman IL (1993) A morphological and immunohistochemical study of programmed cell death in Botryllus schlosseri (Tunicata, Ascidiacea). Cell Tissue Res. 272: 115-127
22. Delic J, Morange M and Magdelenat H (1993) Ubiquitin pathway involvement in human lymphocyte γ-irradiation-induced apoptosis. Mol. Cell. Biol. 13:4875-4883
23. Phillips ME and Platt JE (1994) The use of ubiquitin as a marker of thyroxine-induced apoptosis in cultured Rana catesbeiana tail tips. Gen. Comp. Endocrinol. 95: 409-415
24. Sandri M, Carraro U, Podhorska-Okolov M, Rizzi C, Arslan P, Monti D and Franceschi C (1995) Apoptosis, DNA damage and ubiquitin expression in normal and mdx muscle fibers after exercise. FEBS Lett. 373: 291-295
25. Sandri M, Podhorska-Okolow M, Geromel V, Rizzi C, Arslan P, Franceschi C and Carraro U (1997) Exercise induces myonuclear ubiquitination and apoptosis in dystrophin-deficient muscle of mice. J. Neuropathol. Exp. Neurol. 56: 45-57
26. Mampuru LJ, Chen SJ, Kalenik JL, Bradley ME and Lee TC (1996) Analysis of events associated with serum deprivation-induced apoptosis in C3H/Sol8 muscle satellite cells. Exp. Cell Res. 226: 372-380
27. Tanimoto Y, Onishi Y, Hashimoto S and Kizaki H (1997) Peptidyl aldehyde inhibitors of proteasome induce apoptosis rapidly in mouse lymphoma RVC cells. J. Biochem. (Tokyo) 121: 542-549
28. Soldatenkov VA and Dritschilo A (1997) Apoptosis of Ewing's sarcoma cells is accompanied by accumulation of ubiquitinated proteins. Cancer Res. 57: 3881-3885
29. Ferrer I, Pozas E and Planas AM (1997) Ubiquitination of apoptotic cells in the developing cerebellum of the rat following ionizing radiation or methylazoxymethanol injection. Acta Neuropathol. (Berl). 93: 402-407
30. Fahrbach SE and Schwartz LM (1994) Localization of immunoreactive ubiquitin in the nervous system of the Manduca sexta moth. J. Comp. Neurol. 343: 464-482
31. Haas AL, Baboshina O, Williams B and Schwartz LM (1995) Coordinated Induction of the ubiquitin conjugation pathway accompanies the developmentally programmed death of insect skeletal muscle. J. Biol. Chem. 270: 9407-9412
32. Lesche R, Peetz A, van der Hoeven F and Ruther U (1997) Ftl, a novel gene related to ubiquitin-conjugating enzymes, is deleted in the Fused toes mouse mutation. Mamm. Genome 8: 879-883
33. Hauser HP, Bardroff M, Pyrowolakis G and Jentsch S (1998) A giant ubiquitin-conjugating enzyme related to IAP apoptosis inhibitors. J. Cell Biol. 141: 1415-1422
34. Harvey KF, Harvey NL, Michael JM, Parasivam G, Waterhouse N, Alnemri ES, Watters D and Kumar S (1998) Caspase-mediated cleavage of the ubiquitin-protein ligase Nedd4 during apoptosis. J. Biol. Chem. 273: 13524-13530
35. Wolff T and Ready DF (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113: 825-839
36. D'Mello SR and Galli C (1993) SGP2, ubiquitin, 14K lectin and RP8 mRNAs are not induced in neuronal apoptosis. Neuroreport 4: 355-358
37. Martin DP, Ito A, Horigome K, Lampe PA and Johnson EM Jr (1992) Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23: 1205-1220.
38. Schwartz LM, Smith SW, Jones MEE and Osborne B (1993) Do all programmed cell deaths occur via apoptosis? Proc. Natl. Acad. Sci. USA 90: 980-984
39. Marushige Y and Marushige K (1995) Disappearance of ubiquitinated histone H2A during chromatin condensation in TGF beta 1-induced apoptosis. Anticancer Res. 15: 267-272
40. Kerr JFR, Wyllie AH and Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239-257
41. Monney L, Otter I, Olivier R, Ozer HL, Haas AL, Omura S and Borner C (1998) Defects in the ubiquitin pathway induce caspase-independent apoptosis blocked by Bcl-2. J. Biol. Chem. 273: 6121-6131
42. Dawson SP, Arnold JE, Mayer NJ, Reynolds SE, Billet MA, Gordon C, Colleaux L, Kloetzel PM, Tanaka K and Mayer RJ (1995) Developmental changes of the 26 S proteasome in abdominal intersegmental muscles of Manduca sexta during programmed cell death. J. Biol. Chem. 270: 1850-1858
43. Takayanagi K, Dawson S, Reynolds SE and Mayer RJ (1996) Specific developmental changes in the regulatory subunits of the 26 S proteasome in intersegmental muscles preceding eclosion in Manduca sexta. Biochem. Biophys. Res. Commun. 228: 517-523
44. Low P, Bussell K, Dawson SP, Billett MA, Mayer RJ and Reynolds SE (1997) Expression of a 26S proteasome ATPase subunit, MS73, in muscles that undergo developmentally programmed cell death, and its control by ecdysteroid hormones in the insect Manduca sexta. FEBS Lett. 400: 345-349
45. Jones ME, Haire MF, Kloetzel PM, Mykles DL and Schwartz LM (1995) Changes in the structure and function of the multicatalytic proteinase (proteasome) during programmed cell death in the intersegmental muscles of the hawkmoth, Manduca sexta. Dev. Biol. 169: 436-447
46. Pitzer F, Dantes A, Fuchs T, Baumeister W and Amsterdam A (1996) Removal of proteasomes from the nucleus and their accumulation in apoptotic blebs during programmed cell death. FEBS Lett. 394: 47-50
47. Machiels BM, Henfling ME, Schutte B, van Engeland M. Broers JL and Ramaekers FC (1996) Subcellular localization of proteasomes in apoptotic lung tumor cells and persistence as compared to intermediate filaments. Eur. J. Cell Biol. 70: 250-259
48. Hashimoto MK, Mykles DL, Schwartz LM and Fahrbach SE (1996) Imaginal cell-specific accumulation of the multicatalytic proteinase complex (proteasome) during post-embryonic development in the tobacco hornworm, Manduca sexta. J. Comp. Neurol. 365: 329-341
49. Grimm LM, Goldberg AL, Poirier GG, Schwartz LM and Osborne BA (1996) Proteasomes play an essential role in thymocyte apoptosis. EMBO J. 15: 3835-3844
50. Beyette J, Mason GG, Murray RZ, CohenGMand RivettAJ (1998) Proteasome activities decrease during dexamethasone-induced apoptosis of thymocytes. Biochem. J. 332: 315-320
51. Hirsch T, Dallaporta B, Zamzami N, Susin SA, 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
52. Kobayashi T, Shinozaki A, Momoi T, Arahata K and Tsukahara T (1996) Identification of an interleukin-1 beta converting enzyme-like activity that increases upon treatment of P19 cells with retinoic acid as the proteasome. J. Biochem. (Tokyo) 120: 699-704
53. Meriin AB, Gabai VL, Yaglom J, Shifrin VI and Sherman MY (1998) Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J. Biol. Chem. 273: 6373-6379
54. Fenteany G and Schreiber SL (1998) Lactacystin, proteasome function, and cell fate. J. Biol. Chem. 273: 8545-8548
55. Imajoh-Ohmi S, Kawaguchi T, Sugiyama S, Tanaka K, Omura S and Kikuchi H (1995) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem. Biophys. Res. Commun. 217: 1070-1077
56. Shinohara K, Tomioka M, Nakano H, Tone S, Ito H and Kawashima S (1996) Apoptosis induction resulting from proteasome inhibition. Biochem. J. 317: 385-388
57. Lopes UG, Erhardt P, Yao R and Cooper GM (1997) p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 272: 12893-12896
58. Drexler HC (1997) Activation of the cell death program by inhibition of proteasome function. Proc. Natl. Acad. Sci. USA 94: 855-860
59. Cui H, Matsui K, Omura S, Schauer SL, Matulka RA, Sonenshein GE and Ju ST (1997) Proteasome regulation of activation-induced T cell death. Proc. Natl. Acad. Sci. USA 94: 7515-7520
60. Bellas RE, FitzGerald MJ, Fausto N and Sonenshein GE (1997) Inhibition of NF-kappa B activity induces apoptosis in murine hepatocytes. Am. J. Pathol. 151: 891-896
61. Delic J, Masdehors P, Omura S, Cosset JM, Dumont J, Binet JL and Magdelenat H (1998) The proteasome inhibitor lactacystin induces apoptosis and sensitizes chemo-and radioresistant human chronic lymphocytic leukaemia lymphocytes to TNF-alpha-initiated apoptosis. Br. J. Cancer 77: 1103-1107
62. Bertrand F, Atfi A, Cadoret A, L'Allemain G, Robin H, Lascols O, Capeau J and Cherqui G (1998) A role for nuclear factor kappaB in the antiapoptotic function of insulin. J. Biol. Chem. 273: 2931-2938
63. Ruckdeschel K, Harb S, Roggenkamp A, Hornef M, Zumbihl R, Kohler S, Heesemann J and Rouot B (1998) Yersinia enterocolitica impairs activation of transcription factor NF-kappaB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor alpha production. J. Exp. Med. 187: 1069-1079
64. Wang X, Luo H, Chen H, Duguid W and Wu J (1998) Role of proteasomes in T cell activation and proliferation. J. Immunol. 160: 788-801
65. Orlowski RZ, Eswara JR, Lafond-Walker A, Grever MR, Orlowski M and Dang CV (1998) Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor. Cancer Res. 58: 4342-4348
66. Stefaneli C, Bonavita F, Stanic I, Pignatti C, Farruggia G, Masotti L, Guarnieri C and Caldarera CM (1998) Inhibition of etoposide-induced apoptosis with peptide aldehyde inhibitors of proteasome. Biochem. J. 332: 661-665
67. Sadoul R, Fernandez PA, Quiquerez AL, Martinou I, Maki M, Schroter M, Becherer JD, Irmler M, Tschopp J and Matinou JC (1996) Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J. 15: 3845-3852
68. Martinou I, Missotten M, Fernandez PA, Sadoul R and Martinou JC (1998) Bax and Bak proteins require caspase activity to trigger apoptosis in sympathetic neurons. Neuroreport 9: 15-19
69. Shimizu T and Pommier Y (1996) DNA fragmentation induced by protease activation in p53-null human leukemia HL60 cells undergoing apoptosis following treatment with the topoisomerase I inhibitor camptothecin: cell-free system studies. Exp. Cell Res. 226: 292-301
70. Vinitsky A, Cardozo C, Sepp-Lorenzino L, Michaud C and Orlowski M (1994) Inhibition of the proteolytic activity of the multicatalytic proteinase complex (proteasome) by substrate related peptidyl aldehydes. J. Biol. Chem. 269: 29860-29866
71. Vinitsky A, Michaud C, Powers JC and Orlowski M (1992) Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex. Biochemistry 31: 9421-9428
72. Figueiredo-Pereira ME, Banik N and Wilk S (1994) Comparison of the effect of calpain inhibitors on two extralysosomal proteinases: the multicatalytic proteinase complex and m-calpain. J. Neurochem. 62: 1989-1994
73. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D and Goldberg AL (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761-771
74. Tsubuki S, Saito Y, Tomioka M, Ito H and Kawashima S (1996) Differential inhibition of calpain and proteasome activities by peptidyl aldehydes of dileucine and tri-leucine. J. Biochem. 119: 572-576
75. Squier MKT and Cohen JJ (1997) Calpain, an upstream regulator of thymocyte apoptosis. J. Immunol. 158: 3690-3697
76. Ostrowska H, Wojcik C, Omura S and Worowski K (1997) Lactacystin, a specific inhibitor of the proteasome, inhibits human platelet lysosomal cathepsin A-like enzyme. Biochem. Biophys. Res. Commun. 234: 729-732
77. Lin K-I, Baraban JM and Ratan RR (1998) Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ. 5: 577-583
78. Fujita E, Mukasa T, Tsukahara T, Arahata K, Omura S and Momoi T (1996) Enhancement of CPP32-like activity in the TNF-treated U937 cells by the proteasome inhibitors. Biochem. Biophys. Res. Commun. 224: 74-79
79. He H, Qi X-M, Grossmann J and DistelhorstCW (1998) c-Fos degradation by the proteasome. J. Biol. Chem. 273: 25015-25019
80. Kulka RG, Raboy B, Schuster R, Parag HA, Diamond G, Ciechanover A and Marcus M (1988) A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature-sensitive ubiquitin-activating enzyme, E1. J. Biol. Chem. 263: 15726-15731
81. Finley D, Sadis S, Monia BP, Boucher P, Ecker DJ, Crooke ST and Chau V (1994) Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell. Biol. 14: 5501-5509
82. Sherwood SW, Kung AL, Ritelman J, Simoni RD and Schimke RT (1993) In vivo inhibition of cyclin B degradation and induction of cell-cycle arrest in mammalian cells by the neutral cysteine protease inhibitor N-acetylleucylleucylnorleucinal. Proc. Natl. Acad. Sci. USA 90: 3353-3357
83. Fenteany G, Standaert RF, Reichard GA, Corey EJ and Schreiber SL (1994) A beta-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc. Natl. Acad. Sci. USA 91: 3358-3362
84. 2-phase and metaphase in HeLa cells. Eur. J. Cell Biol. 70: 172-178
85. 2 phases in neuro 2a cells. J. Antibiotics 48: 344-346
86. Agarwal ML, Taylor WR, Chernov MV, Chernova OB and Stark GR (1998) The p53 network. J. Biol. Chem. 273: 1-4
87. Canman CE and Kastan MB (1997) Role of p53 in apoptosis. Adv. Pharmacol. 41: 429-460
88. Morgan SE and Kastan MB (1997) p53 and ATM: cell cycle, cell death, and cancer. Adv. Cancer Res. 71: 1-25
89. Maki CG, Huibregtse JM and Howley PM (1996) In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56: 2649-2654
90. Rolfe M, Chiu MI and Pagano M (1997) The ubiquitin-mediated proteolytic pathway as a therapeutic area. J. Mol. Med. 75: 5-17
91. Chang YC, Lee YS, Tejima T, Tanaka K, Omura S, Heintz NH, Mitsui Y and Magae J (1998) mdm2 and bax, downstream mediators of the p53 response, are degraded by the ubiquitin-proteasome pathway. Cell Growth Differ. 9: 79-84
92. de Stanchina E, McCurrach ME, Zindy F, Shieh SY, Ferbeyre G, Samuelson AV, Prives C, Roussel MF, Sherr CJ and Lowe SW (1998) E1A signaling to p53 involves the p19(ARF) tumor suppressor. Genes Dev. 12: 2434-2442
93. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ and Roussel MF (1998) Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12: 2424-2433
94. Katayose Y, Kim M, RakkarANS, Li Z, Cowan KH andSeth P (1997) Promoting apoptosis: a novel activity associated with the cyclin-dependent kinase inhibitor p27. Cancer Res. 57: 5441-5445
95. Wang X, Gorsope M, Huang Y and Holbrook NJ (1997) p27Kip1 overexpression causes apoptotic death of mammalian cells. Oncogene 15: 2991-2997
96. Alessanorini A, Chiaur DS and Pagano M (1997) Regulation of the cyclin-dependent kinase inhibitor p27 by degradation and phosphorylation. Leukemia 11: 342-345
97. Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH and Ballard DW (1997) Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis C-IAP2 is under NF-kappaB control. Proc. Natl. Acad. Sci. USA 94: 10057-10062
98. You M, Ku PT, Hrdlickova R and Bose HR Jr (1997) ch-IAP1, a member of the inhibitor-of-apoptosis protein family, is a mediator of the antiapoptotic activity of the v-Rel oncoprotein. Mol. Cell. Biol. 17: 7328-7341
99. Karin M (1998) The NF-kappa B activation pathway: its regulation and role in inflammation and cell survival. Cancer J. Sci. Am. 4 Suppl 1: S92-S99
100. Schmitz ML and Baeuerle PA (1995) Multi-step activation of NF-kappa B/Rel transcription factors. Immunobiology 193: 116-127
101. Sonenshein GE (1997) Rel/NF-kappa B transcription factors and the control of apoptosis. Semin. Cancer Biol. 8: 113-119
102. Schulze-Osthoff K, Ferrari D, Los M, Wesselborg S and Peter ME (1998) Apoptosis signaling by death receptors. Eur. J. Biochem. 254: 439-459
103. Arsura M, Wu M and Sonenshein GE (1996) TGF beta 1 inhibits NF-kappa B/ Rel activity inducing apoptosis of B cells: transcriptional activation of I kappa B alpha. Immunity 5: 31-34
104. Wu M, Lee H, Bellas RE, Schauer SL, Arsura M, Katz D, FitzGerald MJ, Rothstein TL, Sherr DH and Sonenshein GE (1996) Inhibition of NF-kappaB/ Rel induces apoptosis of murine B cells. EMBO J. 15: 4682-4690
105. Taglialatela G, Kaufmann JA, Trevino A and Perez-Polo JR (1998) Central nervous system DNA fragmentation induced by the inhibition of nuclear factor kappa B. Neuroreport 9: 489-493
106. Jeremias I, Kuppatt C, Baumann B, Herr I, Wirth T and Debatin KM (1998) Inhibition of nuclear factor kappaB activation attenuates apoptosis resistance in lymphoid cells. Blood 91: 4624-4631
107. Boldin MP, Mett IL and Wallach D (1995) A protein related to a proteasomal subunit binds to the intracellular domain of the p55 TNF receptor upstream to its 'death domain'. FEBS Lett. 367: 39-44
108. Okura T, Gong L, Kamitani T, Wada T, Okura I, Wei CF, Chang HM and Yeh ET (1996) Protection against Fas/APO-1-and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J. Immunol. 157: 4277-4281
109. Wright DA, Futcher B, Ghosh P and Geha RS (1996) Association of human fas (CD95) with a ubiquitin-conjugating enzyme (UBC-FAP). J. Biol. Chem. 271: 31037-31043
110. 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
111. Wang CY, Mayo MW and Baldwin AS Jr (1996) TNF-and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274: 784-787
112. Nakajima T, Kimura M, Kuroda K, Tanaka M, Kikuchi A, Seino H, Yamao F and Oda K (1997) Induction of ubiquitin conjugating enzyme activity for degradation of topoisomerase II alpha during adenovirus E1A-induced apoptosis. Biochem. Biophys. Res. Commun. 239: 823-829
113. Nakajima T, Morita K, Ohi N, Arai T, Nozaki N, Kikuchi A, Osaka F, Yamao F and Oda K (1996) Degradation of topoisomerase IIalpha during adenovirus E1A-induced apoptosis is mediated by the activation of the ubicuitin proteolysis system. J. Biol. Chem. 271: 24842-24849
114. McPherson JP and Goldenberg GJ (1998) Induction of apoptosis by deregulated expression of DNA topoisomerase IIa. Cancer Res. 58: 4529-4524
115. Kamitani T, Nguyen HP and Yeh ETH (1997) Activation-induied aggregation and processing of the human Fas antigen. Detection with cytoolasmic domain-specific antibodies. J. Biol. Chem. 272: 22307-22314