Cell death regulation by the Bcl-2 protein family in the mitochondria

Journal of Cellular Physiology

Volumn 195, Issue 2, 2003, Pages 158-167

  Tsujimoto, Yoshihide ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; CASPASE; CYTOCHROME C; ENDONUCLEASE; ENDONUCLEASE G; PROTEIN BCL 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DEATH; CONTROLLED STUDY; CYTOPLASM; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ANIMALS; APOPTOSIS; CELL MEMBRANE PERMEABILITY; EUKARYOTIC CELLS; HUMANS; INTRACELLULAR MEMBRANES; MITOCHONDRIA; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EID: 0037401562     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10254     Document Type: Review

References (99)

1. Adams JM, Cory S. 1998. The Bcl-2 protein family: Arbiters of cell survival. Science 281:1322-1326.
2. Antonsson B, Montessuit S, Lauper S, Eskes R, Martinou JC. 2000. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345(Pt 2):271-278.
3. Antonsson B, Montessuit S, Sanchez B, Martinou JC. 2001. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276:11615-11623.
4. Chen F, Hersh BM, Conradt B, Zhou Z, Riemer D, Gruenbaum Y, Horvitz HR. 2000. Translocation of C. elegans Ced-4 to nuclear membranes during programmed cell death. Science 287:1485-1489.
5. Cheng EH, Levine B, Boise LH, Thompson CB, Hardwick JM. 1996. Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379:554-556.
6. Cheng EH, Nicholas J, Bellows DS, Hayward GS, Guo HG, Reitz MS, Hardwick JM. 1997. A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc Natl Acad Sci USA 94:690-694.
7. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer SJ. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 8:705-711.
8. Chinnaiyan AM, O'Rourke K, Lane BR, Dixit VM. 1997. Interaction of CED-4 with CED-3 and CED-9: A molecular framework for cell death. Science 275:1122-1126.
9. Cuconati A, White E. 2002. Viral homologs of Bcl-2: Role of apoptosis in the regulation of virus infection. Genes Dev 16:2465-2478.
10. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou JC. 1999. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144:891-901.
11. Du C, Fang M, Li Y, Li L, Wang X. 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33-42.
12. Eskes R, Desagher S, Antonsson B, Martinou JC. 2000. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20:929-935.
13. Esposti MD, Erler JT, Hickman JA, Dive C. 2001. Bid, a widely expressed proapoptotic protein of the Bcl-2 family, displays lipid transfer activity. Mol Cell Biol 21:7268-7276.
14. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. 2000. The coordinate release of cytochrome c during apoptosis is rapid, complete, and kinetically invariant. Nat Cell Biol 2:156-162.
15. Goping IS, Gross A, Lavoie JN, Nguyen M, Jemmerson R, Roth K, Korsmeyer SJ, Shore GC. 1998. Regulated targeting of BAX to mitochondria. J Cell Biol 143:207-215.
16. Green D. 2000. Apoptotic pathways: Paper wraps stone blunts scissors. Cell 102:1-4.
17. Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, Corfe BM, Dive C, Hickman JA. 1999. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144:903-914.
18. Grinberg M, Sarig R, Zaltsman Y, Frumkin D, Grammatikakis N, Reuveny E, Gross A. 2002. tBID homooligomerizes in the mitochondrial membrane to induce apoptosis. J Biol Chem 277:12237-12245.
19. He L, Lemasters JJ. 2002. Regulated and unregulated mitochondrial permeability transition pores: A newparadigm of pore structure and function? FEBS Lett 512:1-7.
20. Hegde R, Srinivasula SM, Zhang Z, Wassell R, Mukattash R, Cilenti L, DuBois G, Lazebnik Y, Zervos AS, Fernandes-Alnemri T, Alnemri ES. 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.
21. Heibein JA, Goping IS, Barry M, Pinkoski MJ, Shore GC, Green DR, Bleackley RC. 2000. Granzyme B-mediated cytochrome c release is regulated by the Bel-2 family members bid and Bax. J Exp Med 192:1391-1402.
22. Huang DC, Adams JM, Cory S. 1998. The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J 17:1029-1039.
23. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, Noda T, Kitamura Y, Kondoh H, Tsujimoto Y. 1995. Bcl-2 deficiency in mice leads to pleiotropic abnormalities: Accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res 55:354-359.
24. Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E, Goldberg M, Allen T, Barber MJ, Green DR, Newmeyer DD. 1999. The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147:809-822.
25. Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nature Med 6:513-519.
26. Kudla G, Montessuit S, Eskes R, Berrier C, Martinou JC, Ghazi A, Antonsson B. 2000. The destabilization of lipid membranes induced by the C-terminal fragment of caspase 8-cleaved bid is inhibited by the N-terminalfragment. J Biol Chem 275:22713-22718.
27. Kusano H, Shimizu S, Koya R-C, Fujita H, Kamada S, Kuzumaki N, Tsujimoto Y. 2000. Human gelsolin prevents apoptosis by inhibiting apoptotic mitochondrial changes via closing VDAC. Oncogene 19:4807-4814.
28. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD. 2002. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342.
29. Le Mellay V, Troppmair J, Benz R, Rapp UR. 2002. Negative regulation of mitochondrial VDAC channels by C-Raf kinase. BMC Cell Biol 3:14.
30. Letai A, Bassik M, Walensky L, Sorcinelli M, Weiler S, Korsmeyer S. 2002. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183-192.
31. Li H, Zhu H, Xu CJ, Yuan J. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501.
32. Li LY, Luo X, Wang X. 2001. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95-109.
33. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA, Ulrich E, Waymire KG, Mahar P, Frauwirth K, Chen Y, Wei M, Eng VM, Adelman DM, Simon MC, Ma A, Golden JA, Evan G, Korsmeyer SJ, MacGregor GR, Thompson CB. 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.
34. Liu QA, Hengartner MO. 1999. The molecular mechanism of programmed cell death in C. elegans. Ann NY Acad Sci 887:92-104.
35. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. 1996. Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. 86:147-157.
36. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481-490.
37. Lutter M, Fang M, Luo X, Nishijima M, Xie X, Wang X. 2000. Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol 2:754-761.
38. Madesh M, Hajnoczky G. 2001. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J Cell Biol 155:1003-1015.
39. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G. 1996. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184:1155-1160.
40. Martinou J-C, Green RD. 2001. Breaking the mitochondrial barrier. Nat Rev 2:63-67.
41. Martins LM, Iaccarino I, Tenev T, Gschmeissner S, Totty NF, Lemoine NR, Savopoulos J, Gray CW, Creasy CL, Dingwall C, Downward J. 2002. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J Biol Chem 277:439-444.
42. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G. 1998. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027-2031.
43. Minn AJ, Kettlun CS, Liang H, Kelekar A, Vander Heiden MG, Chang BS, Fesik SW, Fill M, Thompson CB. 1999. Bcl-xL regulates apoptosis by heterodimerization-dependent and -independent mechanisms. EMBO J 18:632-643.
44. Mootha VK, Wei MC, Buttle KF, Scorrano L, Panoutsakopoulou V, Mannella CA, Korsmeyer SJ. 2001. A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J 20:661-671.
45. Nakano K, Vousden KH. 2001. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7:683-694.
46. Nakayama K, Nakayama K, Negishi I, Kuida K, Sawa H, Loh DY. 1994. Targeted disruption of Bcl-2αβ in mice: Occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci USA 91:3700-3704.
47. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ. 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153:1265-1276.
48. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T, Matsuda H, Tsujimoto Y. 2003. 14-3-3 interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 278:2058-2065.
49. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N. 2000. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053-1058.
50. Parrish J, Li L, Klotz K, Ledwich D, Wang X, Xue D. 2001. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature 412:90-94.
51. Pavlov EV, Priault M, Pietkiewicz D, Cheng EH, Antonsson B, Manon S, Korsmeyer SJ, Mannella CA, Kinnally KW. 2001. A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155:725-731.
52. Putcha GV, Harris CA, Moulder KL, Easton RM, Thompson CB, Johnson EM, Jr. 2002. Intrinsic and extrinsic pathway signaling during neuronal apoptosis: Lessons from the analysis of mutant mice. J Cell Biol 157:441-453.
53. Puthalakath H, Strasser A. 2002. Keeping killers on a tight leash: Transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 9:505-512.
54. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A. 1999. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3:287-296.
55. Puthalakath H, Villunger A, O'Reilly LA, Beaumont JG, Coultas L, Cheney RE, Huang DC, Strasser A. 2001. Bmf: A proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 293:1829-1832.
56. Roucou X, Rostovtseva T, Montessuit S, Martinou JC, Antonsson B. 2002a. Bid induces cytochrome c-impermeable Bax channels in liposomes. Biochem J 363(Pt 3):547-552.
57. Roucou X, Montessuit S, Antonsson B, Martinou JC. 2002b. Bax oligomerization in mitochondrial membranes requires tBid and a mitochondrial protein. Biochem J 368(Part 3):915-921.
58. Saito M, Korsmeyer SJ, Schlesinger PH. 2000. Bax-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2:553-555.
59. Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S. 1999. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60, and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO J 18:2040-2048.
60. Samuel T, Weber HO, Rauch P, Verdoodt B, Eppel J-T, McShea A, Hermeking H, Funk JO. 2001. The G2/M regulator 14-3-3 σ prevents apoptosis through sequestration of Bax. J Biol Chem 276:45201-45206.
61. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ. 2002. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2:55-67.
62. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacronique V, Matsuda H, Tsujimoto Y. 1998. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 95:1455-1459.
63. Shimizu S, Narita M, Tsujimoto Y. 1999. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483-487.
64. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. 2000a. BH4 domain of anti-apoptotic Bcl-2 family members closes VDAC, and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci USA 97:3100-3105.
65. L independently regulate apoptotic changes of yeast mitochondria that require VDAC but not adenine nucleotide translocator. Oncogene 19:4309-4318.
66. Shimizu S, Ide T, Yanagida T, Tsujimoto Y. 2000c. Electrophysiological study of a novel large pore formed by Bax and VDAC, which is permeable to cytochrome c. J Biol Chem 275:12321-12325.
67. Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. 2001. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol 152:237-250.
68. Spector MS, Desnoyers S, Hoeppner DJ, Hengartner MO. 1997. Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature 385:653-656.
69. Sugiyama T, Shimizu S, Matsuoka Y, Yoneda Y, Tsujimoto Y. 2002. Activation of mitochondrial voltage-dependent anion channel by a pro-apoptotic BH3-only protein Bim. Oncogene 21:4944-4956.
70. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
71. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. 2001. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8:613-621.
72. Terradillos O, Montessuit S, Huang DC, Martinou JC. 2002. Direct addition of BimL to mitochondria does not lead to cytochrome c release. FEBS Lett 522:29-34.
73. Thornberry NA, Lazebnik Y. 1998. Caspases: Enemies within. Science 281:1312-1316.
74. Tsujimoto Y. 1989. Stress-resistance conferred by high level of bcl-2α protein in humna B lymphoblastoid cell. Oncogene 4:1331-1336.
75. Tsujimoto Y, Croce CM. 1986. Analysis of the structure transcripts and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 83:5214-5218.
76. Tsujimoto Y, Shimizu S. 2000a. Bcl-2: Life-or-death switch. FEBS Lett 466:6-10.
77. Tsujimoto Y, Shimizu S. 2000b. VDAC regulation by the Bcl-2 family of proteins. Cell Death Diff 7:1174-1181.
78. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. 1985. Involvement of the bcl-2 gene in human follicular lymphoma. Science 228:1440-1443.
79. van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri ES, Gevaert K, Vandekerckhove J, Declercq W, Vandenabeele P. 2002. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ 9:20-26.
80. L promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J Biol Chem 276:19414-19419.
81. Vaux DL, Weissman IL, Kim SK. 1992. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258:1955-1957.
82. Vaux DL, Cory S, Adams JM. 1998. bcl-2 gene promotes haematopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442.
83. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229-240.
84. Velazquez JLP, Frantseva MV, Huzar DV, Carlen PL. 2000. Mitochondrial porin required for ischemia-induced mitochondrial dysfunction and neuronal damage. Neuroscience 97:363-369.
85. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL. 2000. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43-53.
86. Verhagen AM, Silke J, Ekert PG, Pakusch M, Kaufmann H, Connolly LM, Day CL, Tikoo A, Burke R, Wrobel C, Moritz RL, Simpson RJ, Vaux DL. 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.
87. Wang X. 2001. The expanding role of mitochondria in apoptosis. Genes Dev 15:2922-2933.
88. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ. 2001a. tBid, a membrane-targeted death ligand, oligomerizes Bak to release cytochorome c. Genes Dev 14:2060-2071.
89. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. 2001b. Pro-apoptotic Bax and Bak are a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
90. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281-1292.
91. Wu D, Wallen HD, Nunez G. 1997. Interaction and regulation of subcellular localization of CED-4 by CED-9. Science 275:1126-1129.
92. Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson DW. 1999. Hsp60 accelerates the maturation of pro-caspases-3 by upstream activator proteases during apoptosis. EMBO J 18:2049-2056.
93. Yamaguchi H, Wang H-G. 2002. Bcl-xL protects BimEL-induced Bax conformational change and cytochrome c release independent of interacting with Bax or BimEL. J Biol Chem 277:41604-41612.
94. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. 2001. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7:673-682.
95. Zamzami N, Kroemer G. 2001. The mitochondrion in apoptosis: How Pandora's box opens. Nat Rev 2:67-71.
96. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. 1996a. Mitochondrial control of nuclear apoptosis. J Exp Med 183:1533-1544.
97. Zamzami N, Marchetti P, Castedo M, Hirsch T, Susin SA, Masse B, Kroemer G. 1996b. Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett 384:53-57.
98. L. Cell 87:619-628.
99. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.