On the release of cytochrome c from mitochondria during cell death signaling

Journal of Biomedical Science

Volumn 9, Issue 6, 2002, Pages 488-506

  Lim, Maria L R ^a   Lum, May Ghee ^a   Hansen, Tania M ^a   Roucou, Xavier ^a   Nagley, Phillip ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Apoptosis; Bax; Bcl 2; Caspases; Confocal microscopy; Cytochrome c; Green fluorescent protein; Mammalian cells; Membrane potential; Mitochondria; Signaling; Yeast

Indexed keywords

CASPASE; CYTOCHROME C; GREEN FLUORESCENT PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BID;

APOPTOSIS; BIOCHEMISTRY; CELL DEATH; CELL FRACTIONATION; CONFOCAL MICROSCOPY; CYTOPLASM; ENZYME ACTIVATION; IMMUNOCHEMISTRY; MAMMAL CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; YEAST CELL;

MAMMALIA;

EID: 0036423710     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1159/000064722     Document Type: Review

References (103)

1. Adams JM, Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-66;2001.
2. Adrain C, Creagh EM, Martin SJ. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J 20:6627-6636; 2001.
3. Adrain C, Martin SJ. The mitochondrial apoptosome: A killer unleashed by the cytochrome seas. Trends Biochem Sci 26:390-397;2001.
4. Antonsson B, Martinou JC. The Bcl-2 protein family. Exp Cell Res 256:50-57;2000.
5. L, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci USA 96:5492-5497;1999.
6. Bernardi P, Basso E, Colonna R, Costantini P, Di Lisa F, Eriksson O, Fontaine E, Forte M, Ichas F, Massari S, Nicolli A, Petronilli V, Scorrano L. Perspectives on the mitochondrial permeability transition. Biochim Biophys Acta 1365:200-206;1998.
7. Bernardi P, Petronilli V, Lisa FD, Forte M. A mitochondrial perspective on cell death. Trends Biochem Sci 26:112-117;2001.
8. Beutner G, Ruck A, Riede B, Brdiczka D. Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim Biophys Acta 1368:7-18;1998.
9. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17: 37-49;1998.
10. Brustugun OT, Fladmark KE, Doskeland SO, Orrenius S, Zhivotovsky B. Apoptosis induced by microinjection of cytochrome c is caspase-dependent and is inhibited by Bcl-2. Cell Death Differ 5:660-668;1998.
11. Chai J, Du C, Wu J-W, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 406: 855-862;2000.
12. L. Nature 379:554-556;1996.
13. Chinnaiyan AM, O'Rourke K, Lane BR, Dixit VM. Interaction of CED-4 with CED-3 and CED-9: A molecular framework for cell death. Science 275:1122-1126;1997.
14. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233-249;1999.
15. Desagher S, Martinou J-C. Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369-377;2000.
16. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou J-C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144:891-901;1999.
17. Deveraux QL, Reed JC. IAP family of proteins - Suppressors of apoptosis. Genes Dev 12:239-252;1999.
18. Diekert K, de Kroon AIPM, Ahting U, Niggemeyer B, Neupert W, de Kruijff B, Lill R. Apocytochrome c requires the TOM complex for translocation across the mitochondrial outer membrane. EMBO J 20:5626-5635;2001.
19. Downward J. How BAD phosphorylation is good for survival. Nat Cell Biol 1:E33-E35; 1999.
20. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33-42; 2000.
21. Dumont ME, Cardillo TS, Hayes MK, Sherman F. Role of cytochrome c heme lyase in mitochondrial import and accumulation of cytochrome c in Saccharomyces cerevisiae. Mol Cell Biol 11:5487-5496;1991.
22. 2+ ions. J Cell Biol 143:217-224; 1998.
23. Eskes R, Desagher S, Antonsson B, Martinou J-C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20:929-935;2000.
24. Finkel E. The mitochondrion: Is it central to apoptosis? Science 292:624-626;2001.
25. Frey TG, Mannella CA. The internal structure of mitochondria. Trends Biochem Sci 25:319-324;2000.
26. 2+-independent mechanisms that are regulated by Bax. J Biol Chem 276:19066-19071;2001.
27. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2:156-162;2000.
28. Gotow T, Shibata M, Kanamori S, Tokuno O, Ohsawa Y, Sato N, Isahara K, Yayoi Y, Watanabe T, Leterrier JF, Linden M, Kominami E, Uchiyama Y. Selective localization of Bcl-2 to the inner mitochondrial and smooth endoplasmic reticulum membranes in mammalian cells. Cell Death Differ 7:666-674;2000.
29. Graham JM. Homogenization of tissues and cells. In: Graham JM, Rickwood D, eds. Sub-cellular Fractionation: A Practical Approach. New York, Oxford University Press, 1-28; 1997.
30. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 17:3878-3885;1998.
31. Gross A, Pilcher K, Blachly-Dyson E, Basso E, Jockel J, Bassik MC, Korsmeyer SJ, Forte M. Biochemical and genetic analysis of the mitochondrial response of yeast to BAX and BCL-X(L). Mol Cell Biol 20:3125-3126;2000.
32. L prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274:1156-1163;1999.
33. Heiskanen KM, Bhat MB, Wang H-W, Ma J, Nieminen A-L. Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J Biol Chem 274:5654-5658;1999.
34. L during apoptosis. Proc Natl Acad Sci USA 94: 3668-3672;1997.
35. L interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci USA 95:4386-4391;1998.
36. Ichas F, Mazat J-P. From calcium signaling to cell death: Two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366:33-50;1998.
37. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95:4997-5002;1998.
38. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136; 1997.
39. Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC. Investigation of the subcellular distribution of the bcl-2 oncoprotein: Residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res 53:4701-4714;1993.
40. Kudla G, Montessuit S, Eskes R, Berrier C, Martinou J-C, Ghazi A, Antonsson B. The destabilization of lipid membranes induced by the C-terminal fragment of caspase 8-cleaved Bid is inhibited by the N-terminal fragment. J Biol Chem 275:22713-22718;2000.
41. Kuida K, Haydar TF, Kuan C-Y, Gu Y, Taya C, Karasuyama H, Su MS-S, Rakic P, Flavell RA. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94:325-337;1998.
42. Li K, Li Y, Shelton JM, Richardson JA, Spencer E, Chen ZJ, Wang X, Williams RS. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 101:389-399;2000.
43. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489;1997.
44. Lim MLR, Minamikawa T, Nagley P. The pro-tonophore CCCP induces mitochondrial permeability transition without cytochrome c release in human osteosarcoma cells. FEBS Lett 503:69-74;2001.
45. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86:147-157;1996.
46. Lorenzo HK, Susin SA, Penninger J, Kroemer G. Apoptosis inducing factor (AIF): A phylogenetically old, caspase-independent effector of cell death. Cell Death Differ 6:516-524;1999.
47. Mahajan NP, Linder K, Berry G, Gordon GW, Heim R, Herman B. Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat Biotechnol 16:547-552;1998.
48. L. FEBS Lett 415:29-32;1997.
49. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184:1155-1160; 1996.
50. Martinou J-C, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2:63-67;2001.
51. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HLA, Prevost M-C, Xie Z, Matsuyama S, Reed JC, Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027-2031;1998.
52. Mayer A, Neupert W, Lill R. Translocation of apocytochrome c across the outer membrane of mitochondria. J Biol Chem 270:12390-12397; 1995.
53. Minamikawa T, Sriratana A, Williams DA, Bowser DN, Hill JS, Nagley P. Chloromethyl-X-rosamine (MitoTracker Red) photosensitizes mitochondria and induces apoptosis in intact human cells. J Cell Sci 112:2419-2430; 1999.
54. Minamikawa T, Williams DA, Bowser DN, Nagley P. Mitochondrial permeability transition and swelling can occur reversibly without inducing cell death in intact human cells. Exp Cell Res 246:26-37;1999.
55. L regulates apoptosis by heterodimerization-dependent and -independent mechanisms. EMBO J 18:632-643;1999.
56. L, an inhibitor of programmed cell death. Nature 381:335-341;1996.
57. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H, Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 95:14681-14686;1998.
58. Newmeyer DD, Farschon DM, Reed JC. Cell-free apoptosis inXenopusegg extracts: Inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353-364;1994.
59. Nguyen M, Branton PE, Walton PA, Oltvai ZN, Korsmeyer SJ, Shore GC. Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J Biol Chem 269:16521-16524;1994.
60. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619;1993.
61. Pastorino JG, Chen S-T, Tafani M, Snyder JW, Farber JL. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J Biol Chem 273: 7770-7775;1998.
62. Pastorino JG, Tafani M, Rothman RJ, Marcineviciute A, Hoek JB, Farber JL. Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J Biol Chem 274:31734-31739;1999.
63. Patterson SD, Spahr CS, Daugas E, Susin SA, Irinopoulou T, Koehler C, Kroemer G. Mass spectrometric identification of protein released from mitochondria undergoing permeability transition. Cell Death Differ 7:137-144;2000.
64. Pavlov EV, Priault M, Pietkiewicz D, Cheng EH-Y, Antonsson B, Manon S, Korsmeyer SJ, Mannella CA, Kinnally KW. A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155:725-731;2001.
65. Petit PX, Goubern M, Diolez P, Susin SA, Zamzami N, Kroemer G. Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: The impact of irreversible permeability transition. FEBS Lett 426:111-116;1998.
66. Priault M, Camougrand N, Chaudhuri B, Schaeffer J, Manon S. Comparison of the effects of bax-expression in yeast under fermentative and respiratory conditions: Investigation of the role of adenine nucleotides carrier and cytochrome c. FEBS Lett 456:232-238;1999.
67. Priault M, Chaudhuri B, Clow A, Camougrand N, Manon S. Investigation of bax-induced release of cytochrome c from yeast mitochondria: Permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur J Biochem 260:684-691;1999.
68. Puthalakath H, Huang DCS, O'Reilly LA, King SM, Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3:287-296;1999.
69. Rosse T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B, Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391:496-498;1998.
70. Roucou X, Prescott M, Devenish RJ, Nagley P. A cytochrome c-GFP fusion is not released from mitochondria into the cytoplasm upon expression of Bax in yeast cells. FEBS Lett 471: 235-239;2000.
71. Saito M, Korsmeyer SJ, Schlesinger PH. Bax-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2:553-555;2000.
72. Saleh A, Srinivasula SM, Acharya S, Fishel R, Alnemri ES. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J Biol Chem 274:17941-17945;1999.
73. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature 407:784-788; 2000.
74. Scarlett JL, Murphy MP. Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett 418:282-286; 1997.
75. Schendel SL, Montal M, Reed JC. Bcl-2 family proteins as ion-channels. Cell Death Differ 5: 372-380;1998.
76. Schlesinger PH, Gross A, Yin X-M, Yamamoto K, Saito M, Waksman G, Korsmeyer SJ. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA 94:11357-11362; 1997.
77. Scorrano L, Petronilli V, Di Lisa F, Bernardi P. Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J Biol Chem 274: 22581-22585;1999.
78. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacronique V, Matsuda H, Tsujimoto Y. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 95:1455-1459;1998.
79. Shimizu S, Ide T, Yanagida Y, Tsujimoto Y. Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J Biol Chem 275:12321-12325;2000.
80. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483-487;1999
81. Srinivasula SM, Hedge R, Saleh A, Pinaki D, Shiozaki E, Chai J, Lee R-A, Robbins PD, Fernandes-Alnemri T, Shi Y, Alnemri ES. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410:112-116;2001.
82. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem 69:217-245; 2000.
83. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Brenner C, Larochette N, Prevost MC, Alzari PM, Kroemer G. Mitochondrial release of cas-pase-2 and -9 during the apoptotic process. J Exp Med 189:381-393;1999.
84. 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. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446;1999.
85. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184:1331-1341;1996.
86. Tanaka S, Saito K, Reed JC. Structure-function analysis of the Bcl-2 oncoprotein. Addition of a heterologous transmembrane domain to portions of the Bcl-2 beta protein restores function as a regulator of cell survival. J Biol Chem 268: 10920-10926;1996.
87. Unkila M, McColl KS, Thomenius MJ, Heis-kanen K, Distelhorst CW. Unreliability of the cytochrome c-enhanced green fluorescent fusion protein as a marker of cytochrome c release in cells that overexpress Bcl-2. J Biol Chem 276:39132-39137;2001.
88. L prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell 3:159-167;1999.
89. L regulates the membrane potential and volume homeostasis of mitochondria. Cell 91:627-637;1997.
90. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43-53;2000.
91. Waterhouse NJ, Goldstein JC, von Ahsen O, Schuler M, Newmeyer DD, Green DR. Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J Cell Biol 153: 319-328;2001.
92. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060-2071;2000.
93. Wei MC, Zong W-X, Cheng EH-Y, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 292:727-730;2001.
94. Wolter KG, Hsu Y-T, Smith CL, Nechushtan A, Xi X-G, Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281-1292;1997.
95. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T-I, Jones DP, Wang X. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 275: 1129-1132;1997.
96. Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, Mak TW. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750;1998.
97. Zamzami N, Kroemer G. The mitochondrion in apoptosis: How Pandora's box opens. Nat Rev Mol Cell Biol 2:67-71;2001.
98. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med 183:1293-1295;1996.
99. Zha H, Aime-Sempe C, Sato T, Reed JC. Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J Biol Chem 271:7440-7444;1996.
100. Zhang C, Sriratana A, Minamikawa T, Nagley P. Photosensitisation properties of mitochondrially localised green fluorescent protein. Biochem Biophys Res Commun 242: 390-395;1998
101. Zhivotovsky B, Orrenius S, Brustugun OT, Doskeland SO. Injected cytochrome c induces apoptosis. Nature 391:449-450;1998.
102. Zhu W, Cowie A, Wasfy GW, Penn LZ, Leber B, Andrews DW. Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J 15:4130-4141;1996.
103. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413;1997.