Apoptosis: Checkpoint at the mitochondrial frontier

Mutation Research - DNA Repair

Volumn 434, Issue 3, 1999, Pages 243-251

  Bossy Wetzel, Ella ^a   Green, Douglas R ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Apoptosis; Cytochrome c; Mitochondria

Indexed keywords

CASPASE; CYTOCHROME C; PROTEASOME;

APOPTOSIS; CELL DEATH; HUMAN; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0032806596     PISSN: 09218777     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0921-8777(99)00032-4     Document Type: Article

References (88)

1. Jacobson M.D., Burne J.F., King M.P., Miyashita T., Reed J.C., Raff M.C. Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature. 361:1993;365-369.
2. Newmeyer D.D., Farschon D.M., Reed J.C. Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell. 79:1994;353-364.
3. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:1996;147-157.
4. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP dependent formation of Apaf-1/caspase-9 complex initiate an apoptotic protease cascade. Cell. 91:1997;479-489.
5. Adachi S., Cross A.R., Babior B.M., Gottlieb R.A. Bcl-2 and the outer mitochondrial membrane in the inactivation of cytochrome c during Fas-mediated apoptosis. J. Biol. Chem. 272:1997;21878-21882.
6. Kharbanda S., Pandey P., Schofield L., Israels S., Roncinske R., Yoshida K., Bharti A., Yuan Z.-M., Saxena S., Weichselbaum R., Nalin C., Kufe D. Role for Bcl-xL as an inhibitor of cytosolic cytochrome c accumulation in DNA damage-induced apoptosis. Proc. Natl. Acad. Sci. 94:1997;6939-6942.
7. Kim C.N., Wang X., Huang Y., Ibrado A.M., Liu L., Fang G., Bhalla K. Overexpression of Bcl-xL inhibits Ara-c-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res. 57:1997;3115-3120.
8. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
9. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.-I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1997;1129-1132.
10. Bossy-Wetzel E., Newmeyer D.D., Green D.R. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17:1998;37-49.
11. Petit P.X., Susin S.-A., Zamzami N., Mignotte B., Kroemer G. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396:1996;7-13.
12. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssiere J.L., Petit P.X., Kroemer G. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 374:1995;1661-1672.
13. Zoratti M., Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:1995;139-176.
14. Susin S.A., Zamazami 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. 184:1996;1331-1341.
15. Hockenbery D.M., Oltvai Z.N., Yin X.-M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an anti-oxidant pathway. Cell. 75:1993;241-251.
16. Kane D.J., Sarafin T.A., Anton R., Hahn H., Gralla E.B., Valentine J.S., Örd T., Bredesen D.E. Bcl-2 inhibition of neuronal death: decreased generation of reactive oxygen species. Science. 262:1993;1274-1277.
17. Sarafin T.A., Bredesen D.E. Is apoptosis mediated by reactive oxygen species? Free Radical Res. 21:1994;1-8.
18. Greenlund L.J.S., Deckwerth T.L., Johnson E.M.J. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed cell death. Neuron. 14:1995;303-315.
19. Reed J.C. Cytochrome c: can't live with it - can't live without it. Cell. 91:1997;559-562.
20. Cai J., Jones D.P. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J. Biol. Chem. 273:1998;11401-11404.
21. Hampton M.B., Zhivotovsky B., Slater A.F., Burgess D.H., Orrenius S. Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem. J. 329:1998;95-99.
22. Kluck R.M., Martin S.J., Hoffman B.M., Zhou J.S., Green D.R., Newmeyer D.D. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J. 16:1997;4639-4649.
23. Cyrns V., Yuan J. Proteases to die for. Genes Dev. 12:1998;1551-1570.
24. Zou H., Henzel W.J., 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. 90:1997;405-413.
25. Muzio M., Chinnaiyan A.M., Kischkel F.C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz J.D., Zhang M., Ni Gentz R.J.et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/Apo-1) death-inducing signaling complex. Cell. 85:1996;817-827.
26. Boldin M.P., Goncharov T.M., Goltsev Y.V., Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/Apo-1 and TNF receptor induced cell death. Cell. 85:1996;803-815.
27. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory protein family of WD-repeat proteins. Nature. 371:1994;297-300.
28. Srinivasula S.M., Ahmad M., Fernandes-Alnemri T., Alnemri E.S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell. 1:1998;949-957.
29. Yang X., Chang H.Y., Baltimore D. Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. Science. 281:1998;1355-1357.
30. Hu Y., Ding L., Spencer D.M., Nunez G. WD-40 repeat region regulates Apaf-1 self-association and pro-caspase-9 activation. J. Biol. Chem. 273:1998;33489-33494.
31. Li F., Srinivasan A., Wang Y., Armstrong R.C., Tomaselli K.J., Fritz L.C. Cell-specific induction of apoptosis by microinjection of cytochrome c. J. Biol. Chem. 272:1997;30299-30305.
32. Zhivotovsky B., Orrenius S., Brustugun O.T., Doskeland S.O. Injected cytochrome c induces apoptosis. Nature. 391:1998;449-450.
33. Neame S.J., Rubin L.L., Philpott K.L. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 142:1998;1583-1593.
34. Cecconi F., Alvarez-Bolado G., Meyer B.-I., Roth K.A., Gruss P. Apaf-1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 94:1998;727-737.
35. Yoshida H., Kong Y.Y., Yoshida R., Elia A.J., Hakem A., Hakem R., Penninger J.M., Mak T.W. Apaf-1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 94:1998;739-750.
36. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
37. Yang J.C., Cortopassi G.A. Induction of the mitochondrial permeability transition causes release of the apoptogenic factor cytochrome c. Free Radical Biol. Med. 24:1998;624-631.
38. Zhuang J., Dinsdale D., Cohen G.M. Apoptosis, in human monocytic THP.1 cells, results in the release of cytochrome c from mitochondria prior to their ultracondensation, formation of outer membrane discontinuities and reduction in inner membrane potential. Cell Death Differ. 5:1998;953-962.
39. Martinou I., Desagher S., Eskes R., Antonsson B., Andre E., Fakan S., Martinou J.-C. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Biol. Chem. 144:1999;883-889.
40. Marzo I., Susin S.A., Petit P.X., Ravagnan L., Brenner C., Larochette N., Zamzami N., Kroemer G. Caspases disrupt mitochondrial membrane barrier function. FEBS Lett. 427:1998;198-202.
41. Vander Heiden M.G., Chandel N.S., Williamson E.K., Schumacker P.T., Thompson C.B. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:1997;627-637.
42. Wyllie A.H., Kerr J.F.R., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:1980;251-306.
43. Antonsson B., Conti F., Ciavatta A., Montessuit S., Lewis S., Martinou I., Bernasconi L., Bernard A., Mermod J.-J., Mazzei G., Maundrell K., Gambale F., Sadoul R., Martinou J.-C. Inhibition of Bax channel-forming activity by Bcl-2. Science. 277:1997;370-372.
44. Schlesinger P.H., Gross A., Yin X.-M., Yamamoto K., Saito M., Waksman G., Korsmeyer S.J. Comparison of the ion channel characteristics of proapoptotic Bax and antiapoptotic Bcl-2. Proc. Natl. Acad. Sci. U.S.A. 94:1997;11357-11362.
45. 2+ ions. J. Cell Biol. 143:1998;217-224.
46. Jürgensmeier J.M., Xie Z., Deveraux Q., Ellerby L., Bredesen D., Reed J.C. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. U.S.A. 95:1998;4997-5002.
47. Finucance D.M., Bossy-Wetzel E., Waterhouse N.J., Cotter T.G., Green D.R. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol. Chem. 274:1999;2225-2233.
48. Marzo I., Brenner C., Zamzami N., Jürgensmeier J.M., Susin S.A., Vieira H.L.A., Prévost M.-C., Xie Z., Matsuyama S., Reed J.C., Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:1998;2027-2031.
49. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R.J., 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. U.S.A. 95:1999;14681-14686.
50. Kelekar A., Thompson C.B. Bcl-2 family proteins: the role of the BH-3 domain in apoptosis. Trends Cell Biol. 8:1998;324-330.
51. Knudsen C.M., Korsmeyer S.J. Bcl-2 and Bax function independently to regulate cell death. Nat. Genet. 16:1997;358-363.
52. Zha H., Reed J.C. Heterodimerization-independent functions of cell death regulatory proteins Bax and Bcl-2 in yeast and mammalian cells. J. Biol. Chem. 272:1997;31482-31488.
53. Cheng E.H.Y., Levine B., Boise L.H., Thompson C.B., Hardwick J.M. Bax-independent inhibition of apoptosis by Bcl-xL. Nature. 379:1996;554-556.
54. Mahajam N.P., Linder K., Berry G., Gordon G.W., Heim R., Herman B. Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat. Biotechnol. 16:1998;547-552.
55. T. Rossé, R. Olivier, L. Monney, M. Rager, S. Conus, I. Fellay, B. Janson, C. Borner, Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c, Nature (1998) 496-499.
56. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139:1997;1281-1292.
57. Hsu Y.T., Wolter K.G., Youle R.J. Cytosol-to-membrane redistribution of Bax and Bcl-xL during apoptosis. Proc. Natl. Acad. Sci. U.S.A. 94:1997;3668-3672.
58. Gross A., Jockel J., Wei M.C., Korsmeyer S.J. Enforced dimerization of Bax results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17:1998;3878-3885.
59. 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 mitochonrial cytochrome c release during apoptosis. J. Biol. Chem. 144:1999;891-901.
60. Schendel S.L., Xie Z., Montal M.O., Matsuyama S., Montal M., Reed J.C. Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. U.S.A. 94:1997;5113-5118.
61. Minn A.J., Velez P., Schendel S.L., Liang H., Muchmore S.W., Fesik S.W., Fill M., Thompson C.B. Bcl-xL forms an ion channel in synthetic lipid membranes. Nature. 381:1997;335-341.
62. Baffy G., Miyashita T., Williamson J.R., Reed J.R. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoetic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncogene production. J. Biol. Chem. 268:1993;6511-6519.
63. Shimizu S., Eguchi Y., Kamiike W., Funahashi J., Mignon A., Lacronique V., Matsuda H., Tsujimoto Y. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc. Natl. Acad. Sci. U.S.A. 95:1998;1455-1459.
64. Matsuyama S., Xu Q., Velours J., C Reed J. Mitochondrial Fo/F1-ATPase proton pump is required for function of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. 1:1998;327-336.
65. Deshmukh M., Johnson E.M. Jr. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytosolic cytochrome c. Neuron. 21:1998;695-705.
66. M.H. Cardone, N. Roy, H.R. Stennicke, G.S. Salvesen, T.F. Franke, E. Stanbridge, S. Frisch, J.C. Reed, Regulation of cell death protease caspase-9 by phosphorylation, Science (1998) 1318-1321.
67. Deveraux Q., Takahashi R., Salvesen G.S., Reed J.C. X-linked IAP is a direct inhibitor of cell death proteases. Nature. 388:1997;300-303.
68. Deveraux Q.L., Roy N., Stennicke H.R., Van Arsdale T., Zhou Q., Srinivasula S.M., Alnemri E.S., Salvesen G.S., Reed J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17:1998;2215-2223.
69. Tamm I., Wang Y., Sausville E., Scudiero D.A., Vigna N., Oltersdorf T., Reed J.C. IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res. 58:1998;5315-5320.
70. Pan G., O'Rourke K., Dixit V.M. Caspase-9, Bcl-xL, and Apaf-1 form a ternary complex. J. Biol. Chem. 273:1998;5841-5845.
71. Hu Y., Benedict M.A., Wu D., Inohara N., Nunez G. Bcl-xL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Nat. Acad. Sci. U.S.A. 95:1998;4386-4391.
72. Duckett C.S., Li F., Wang Y., Tomaselli K.J., Thompson C.B., Armstrong R.C. Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol. Cell. Biol. 18:1998;608-615.
73. Medema J.P., Scaffidi C., Kischkel F.C., Shevchenko A., Mann M., Krammer P.H., Peter M.E. FLICE is activated by association with CD95 death-inducing signaling complex (DISC). EMBO J. 16:1997;2794-2804.
74. Stennicke H.R., Jürgensmeier J.M., Shin H., Deveraux Q., Wolf B.B., Xaing X., Zhou Q., Ellerby H.M., Ellerby L.M., Bredesen D., Green D.R., Reed J.C., Froelich C.J., Salvesen G.S. Pro-caspase-3 is a major physiologic target of caspase-8. J. Biol. Chem. 273:1998;27084-27090.
75. Kuwana T., Smith J.J., Muzio M., Dixit V., Newmeyer D.D., Kornbluth S. Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome c. J. Biol. Chem. 273:1998;16589-16594.
76. Steemans M., Goossens V., Van de Craen M., Van Herreweghe F., Vancompernolle K., De Vos K., Vandenabeele P., Grooten J. A caspase-activated factor (CAF) induces mitochondrial membrane depolarization and cytochrome c release by a nonproteolytic mechanism. J. Exp. Med. 188:1998;2193-2198.
77. E. Bossy-Wetzel, D.R. Green, Caspase-8 induces cytochrome c release from mitochondria by activating a cytosolic factor, J. Biol. Chem. (1999) (in press).
78. Li H., Zhu H., Xu C., Yuan J. Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
79. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
80. Gross A., Yin X.-M., Wang K., Wei M.C., Jockel J., Milliman C., Erdjument-Bromage H., Tempst P., Korsmeyer S.T. Caspase cleaved Bid targets mitochondria and is required for cytochrome c release, while Bcl-xL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274:1999;1156-1163.
81. Wang K., Yin X.M., Chao D.T., Milliman C.L., Korsmeyer S.J. BID: a novel BH3 domain-only death agonist. Genes Dev. 10:1996;2859-2869.
82. Cheng E.H., Kirsch D.G., Clem R.J., Ravi R., Kastan M.B., Bedi A., Ueno K., Hardwick J.M. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1997;1966-1968.
83. Clem R.J., Cheng E.H., Karp C.L., Kirsch D.G., Ueno K., Takahashi A., Kastan M.B., Griffin D.E., Earnshaw W.C., Veliuona M.A., Hardwick J.M. Modulation of cell death by Bcl-xL through caspase interaction. Proc. Natl. Acad. Sci. 95:1998;554-559.
84. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1998;1675-1687.
85. Longthorne V.L., Williams G.T. Caspase activity is required for commitment to Fas-mediated apoptosis. EMBO J. 16:1997;3805-3807.
86. Sun X.M., MacFarlane M., Zhuang J., Wolf B.B., Green D.G., Cohen G.M. Distinct caspase cascades are initiated in receptor-mediated and chemical-induced apoptosis. J. Biol. Chem. 274:1999;5053-5060.
87. McCarthy N.J., Whyte M.K., Gilbert C.S., Evan G.I. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136:1997;215-227.
88. Xiang J., Chao D.T., Korsmeyer S.J. Bax-induced cell death may not require interleukin 1 converting enzyme-like proteases. Proc. Natl. Acad. Sci. 93:1996;14559-14563.