Mitochondria: Releasing power for life and unleashing the machineries of death

Cell

Volumn 112, Issue 4, 2003, Pages 481-490

  Newmeyer, Donald D ^a   Ferguson Miller, Shelagh ^b  

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

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CARDIOLIPIN; CYTOTOXIC FACTOR; MEMBRANE LIPID; OXYGEN RADICAL; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL FUNCTION; CELL KINETICS; CELL ORGANELLE; ENDOPLASMIC RETICULUM; ENERGY RESOURCE; HUMAN; INTRACELLULAR SPACE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

EID: 0037459081     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00116-8     Document Type: Review

References (93)

1. Annis M.G., Zamzami N., Zhu W., Penn L.Z., Kroemer G., Leber B., Andrews D.W. Endoplasmic reticulum localized Bcl-2 prevents apoptosis when redistribution of cytochrome c is a late event. Oncogene. 20:2001;1939-1952.
2. Asumendi A., Morales M.C., Alvarez A., Arechaga J., Perez-Yarza G. Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl)retinamide-induced apoptosis. Br. J. Cancer. 86:2002;1951-1956.
3. Baffy G., Miyashita T., Williamson J.R., Reed J.C. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem. 268:1993;6511-6519.
4. Basanez G., Nechushtan A., Drozhinin O., Chanturiya A., Choe E., Tutt S., Wood K.A., Hsu Y., Zimmerberg J., Youle R.J. Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc. Natl. Acad. Sci. USA. 96:1999;5492-5497.
5. Basanez G., Zhang J., Chau B.N., Maksaev G.I., Frolov V.A., Brandt T.A., Burch J., Hardwick J.M., Zimmerberg J. Pro-apoptotic cleavage products of Bcl-xL form cytochrome c-conducting pores in pure lipid membranes. J. Biol. Chem. 276:2001;31083-31091.
6. Basanez G., Sharpe J.C., Galanis J., Brandt T.B., Hardwick J.M., Zimmerberg J. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277:2002;49360-49365.
7. Borner C. The Bcl-2 protein family. sensors and checkpoints for life-or-death decisions Mol. Immunol. 39:2003;615-647.
8. 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.
9. Brenner C., Cadiou H., Vieira H.L., Zamzami N., Marzo I., Xie Z., Leber B., Andrews D., Duclohier H., Reed J.C., Kroemer G. Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene. 19:2000;329-336.
10. Chandra D., Liu J.W., Tang D.G. Early mitochondrial activation and cytochrome c upregulation during apoptosis. J. Biol. Chem. 277:2002;50842-50854.
11. Csordas G., Madesh M., Antonsson B., Hajnoczky G. tcBid promotes Ca(2+) signal propagation to the mitochondria. control of Ca(2+) permeation through the outer mitochondrial membrane EMBO J. 21:2002;2198-2206.
12. D'Herde K., De Prest B., Mussche S., Schotte P., Beyaert R., Coster R.V., Roels F. Ultrastructural localization of cytochrome c in apoptosis demonstrates mitochondrial heterogeneity. Cell Death Differ. 7:2000;331-337.
13. De Giorgi F., Lartigue L., Bauer M.K., Schubert A., Grimm S., Hanson G.T., Remington S.J., Youle R.J., Ichas F. The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J. 16:2002;607-609.
14. Degli Esposti M. Lipids, cardiolipin and apoptosis. a greasy licence to kill Cell Death Differ. 9:2002;234-236. a.
15. Degli Esposti M. Sequence and functional similarities between pro-apoptotic Bid and plant lipid transfer proteins. Biochim. Biophys. Acta. 1553:2002;331-340. b.
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. 144:1999;891-901.
17. Epand R.F., Martinou J.C., Fornallaz-Mulhauser M., Hughes D.W., Epand R.M. The apoptotic protein tBid promotes leakage by altering membrane curvature. J. Biol. Chem. 277:2002;32632-32639. a.
18. Epand R.F., Martinou J.C., Fornallaz-Mulhauser M., Hughes D.W., Epand R.M. tBid promotes leakage by altering membrane properties. J. Biol. Chem. 24:2002;24. b.
19. Epand R.F., Martinou J.C., Montessuit S., Epand R.M. Membrane perturbations induced by the apoptotic Bax protein. Biochem. J. 367:2002;849-855. c.
20. Epand R.F., Martinou J.C., Montessuit S., Epand R.M., Yip C.M. Direct evidence for membrane pore formation by the apoptotic protein Bax. Biochem. Biophys. Res. Commun. 298:2002;744-749. d.
21. 2+ ions. J Cell Biol. 143:1998;217-224.
22. Fantin V.R., Berardi M.J., Scorrano L., Korsmeyer S.J., Leder P. A novel mitochondriotoxic small molecule that selectively inhibits tumor cell growth. Cancer Cell. 2:2002;29-42.
23. Fleury C., Mignotte B., Vayssiere J.L. Mitochondrial reactive oxygen species in cell death signaling. Biochimie. 84:2002;131-141.
24. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:2001;515-525.
25. Gao W., Pu Y., Luo K.Q., Chang D.C. Temporal relationship between cytochrome c release and mitochondrial swelling during UV-induced apoptosis in living HeLa cells. J. Cell Sci. 114:2001;2855-2862.
26. Goldstein J.C., Waterhouse N.J., Juin P., Evan G.I., Green D.R. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2:2000;156-162.
27. Green D.R., Evan G.I. A matter of life and death. Cancer Cell. 1:2002;19-30.
28. Hockenbery D., Nuñez G., Milliman C., Schreiber R.D., Korsmeyer S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 348:1990;334.
29. 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.
30. Karbowski M., Lee Y.-J., Gaume B., Jeong S.-Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159:2002;931-938.
31. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature. 419:2002;367-374.
32. 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.
33. Kluck R.M., Esposti M.D., Perkins G., Renken C., Kuwana T., Bossy-Wetzel E., Goldberg M., Allen T., Barber M.J., Green D.R., Newmeyer D.D. The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J. Cell Biol. 147:1999;809-822.
34. Krajewski S., Tanaka S., Takayama S., Schibler M.J., Fenton W., Reed J.C. Investigation of the subcellular distribution of the bcl-2 oncoprotein. residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes Cancer Res. 53:1993;4701-4714.
35. Krysko D.V., Roels F., Leybaert L., D'Herde K. Mitochondrial transmembrane potential changes support the concept of mitochondrial heterogeneity during apoptosis. J. Histochem. Cytochem. 49:2001;1277-1284.
36. 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. 275:2000;22713-22718.
37. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:2002;331-342.
38. Lee S.T., Hoeflich K.P., Wasfy G.W., Woodgett J.R., Leber B., Andrews D.W., Hedley D.W., Penn L.Z. Bcl-2 targeted to the endoplasmic reticulum can inhibit apoptosis induced by Myc but not etoposide in Rat-1 fibroblasts. Oncogene. 18:1999;3520-3528.
39. Lemasters J.J., Qian T., Trost L.C., Herman B., Cascio W.E., Bradham C.A., Brenner D.A., Nieminen A.L. Confocal microscopy of the mitochondrial permeability transition in necrotic and apoptotic cell death. Biochem. Soc. Symp. 66:1999;205-222.
40. Lenaz G., Bovina C., D'Aurelio M., Fato R., Formiggini G., Genova M.L., Giuliano G., Pich M.M., Paolucci U., Castelli G.P., Ventura B. Role of mitochondria in oxidative stress and aging. Ann. N Y Acad. Sci. 959:2002;199-213.
41. Lindsten T., Ross A.J., King A., Zong W.X., Rathmell J.C., Shiels H.A., Ulrich E., Waymire K.G., Mahar P., Frauwirth K.et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell. 6:2000;1389-1399.
42. 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.
43. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80:2002;780-787.
44. Lutter M., Fang M., Luo X., Nishijima M., Xie X.-s., Wang X. Cardiolipin provides specificity for targeting of tBID to mitochondria. Nat. Cell Biol. 2:2000;754-756.
45. Lutter M., Perkins G.A., Wang X. The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites. BMC Cell Biol. 2:2001;22.
46. Magalhaes P.J., Rizzuto R. Mitochondria and calcium homeostasis. a tale of three luminescent proteins Luminescence. 16:2001;67-71.
47. Marchetti P., Castedo M., Susin S.A., Zamzami N., Hirsch F., Geuskens M., Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184:1996;1155-1160. a.
48. Marchetti P., Susin S.A., Decaudin D., Gamen S., Castedo M., Hirsch T., Zamzami N., Naval J., Senik A., Kroemer G. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res. 56:1996;2033-2038. b.
49. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost 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.
50. McClintock D.S., Santore M.T., Lee V.Y., Brunelle J., Budinger G.R., Zong W.X., Thompson C.B., Hay N., Chandel N.S. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol. Cell. Biol. 22:2002;94-104.
51. Melov S., Coskun P., Patel M., Tuinstra R., Cottrell B., Jun A.S., Zastawny T.H., Dizdaroglu M., Goodman S.I., Huang T.T.et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. USA. 96:1999;846-851.
52. Moncada S., Erusalimsky J.D. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3:2002;214-220.
53. Mootha V.K., Wei M.C., Buttle K.F., Scorrano L., Panoutsakopoulou V., Mannella C.A., Korsmeyer S.J. A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J. 20:2001;661-671.
54. 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. USA. 95:1998;14681-14686.
55. Nechushtan A., Smith C.L., Lamensdorf I., Yoon S.H., Youle R.J. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol. 153:2001;1265-1276.
56. 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.
57. Nomura K., Imai H., Koumura T., Kobayashi T., Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351:2000;183-193.
58. 2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 277:2002;20301-20308. a.
59. 2+ stores. J. Biol. Chem. 277:2002;9219-9225. b.
60. Osteryoung K.W. Organelle fission in eukaryotes. Curr. Opin. Microbiol. 4:2001;639-646.
61. Pastorino J.G., Chen S.T., Tafani M., Snyder J.W., Farber J.L. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273:1998;7770-7775.
62. Pastorino J.G., Tafani M., Rothman R.J., Marcinkeviciute A., Hoek J.B., Farber J.L., Marcineviciute A. Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J. Biol. Chem. 274:1999;31734-31739.
63. Petit P.X., Lecoeur H., Zorn E., Dauguet C., Mignotte B., Gougeon M.L. Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell Biol. 130:1995;157-167.
64. Pozzan T., Magalhaes P., Rizzuto R. The comeback of mitochondria to calcium signalling. Cell Calcium. 28:2000;279-283.
65. Pu Y., Chang D.C. Cytosolic Ca(2+) signal is involved in regulating UV-induced apoptosis in hela cells. Biochem. Biophys. Res. Commun. 282:2001;84-89.
66. 2+ microdomains to mitochondria. J. Cell Biol. 159:2002;613-624.
67. Ricci J.E., Gottlieb R.A., Green D.R. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J. Cell Biol. 160:2003;65-75.
68. Rizzuto R., Pinton P., Brini M., Chiesa A., Filippin L., Pozzan T. Mitochondria as biosensors of calcium microdomains. Cell Calcium. 26:1999;193-199.
69. Rizzuto R., Bernardi P., Pozzan T. Mitochondria as all-round players of the calcium game. J. Physiol. 529:2000;37-47.
70. Roucou, X., Montessuit, S., Antonsson, B., and Martinou, J.C. (2002a). Bax oligomerization in mitochondrial membranes requires tBid and a mitochondrial protein. Biochem. J. Pt.
71. Roucou X., Rostovtseva T., Montessuit S., Martinou J.C., Antonsson B. Bid induces cytochrome c-impermeable Bax channels in liposomes. Biochem. J. 363:2002;547-552. b.
72. Saito M., Korsmeyer S.J., Schlesinger P.H. BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat. Cell Biol. 2:2000;553-555.
73. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell. 2:2002;55-67.
74. Shchepina L.A., Pletjushkina O.Y., Avetisyan A.V., Bakeeva L.E., Fetisova E.K., Izyumov D.S., Saprunova V.B., Vyssokikh M.Y., Chernyak B.V., Skulachev V.P. Oligomycin, inhibitor of the F(0) part of H(+)-ATP-synthase, suppresses the TNF-induced apoptosis. Oncogene. 21:2002;8149-8157.
75. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:1999;483-487.
76. Staniek K., Gille L., Kozlov A.V., Nohl H. Mitochondrial superoxide radical formation is controlled by electron bifurcation to the high and low potential pathways. Free Radic. Res. 36:2002;381-387.
77. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M.et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-446.
78. Szalai G., Krishnamurthy R., Hajnoczky G. Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J. 18:1999;6349-6361.
79. Tanaka T., Hosoi F., Yamaguchi-Iwai Y., Nakamura H., Masutani H., Ueda S., Nishiyama A., Takeda S., Wada H., Spyrou G., Yodoi J. Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis. EMBO J. 21:2002;1695-1703.
80. Tang D.G., Li L., Zhu Z., Joshi B., Johnson C.R., Marnett L.J., Honn K.V., Crissman J.D., Krajewski S., Reed J.C.et al. BMD188, A novel hydroxamic acid compound, demonstrates potent anti-prostate cancer effects in vitro and in vivo by inducing apoptosis. requirements for mitochondria, reactive oxygen species, and proteases Pathol. Oncol. Res. 4:1998;179-190.
81. Ueda S., Masutani H., Nakamura H., Tanaka T., Ueno M., Yodoi J. Redox control of cell death. Antioxid. Redox. Signal. 4:2002;405-414.
82. Vanden Abeele F., Skryma R., Shuba Y., Van Coppenolle F., Slomianny C., Roudbaraki M., Mauroy B., Wuytack F., Prevarskaya N. Bcl-2-dependent modulation of Ca(2+) homeostasis and store-operated channels in prostate cancer cells. Cancer Cell. 1:2002;169-179.
83. von Ahsen O., Renken C., Perkins G., Kluck R.M., Bossy-Wetzel E., Newmeyer D.D. Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J. Cell Biol. 150:2000;1027-1036.
84. Wallace, D.C. (1999a). Aging and degenerative diseases: A mitochondrial paradigm. In Frontiers of Cellular Bioenergetics. (New York, Kluwer Academic/Plenum), pp. 751-772.
85. Wallace D.C. Mitochondrial diseases in man and mouse. Science. 283:1999;1482-1488. b.
86. Waterhouse N.J., Goldstein J.C., von Ahsen O., Schuler M., Newmeyer D.D., Green D.R. Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J. Cell Biol. 153:2001;319-328.
87. 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., Korsmeyer S.J. Proapoptotic BAX and BAK. a requisite gateway to mitochondrial dysfunction and death Science. 292:2001;727-730.
88. Westermann B. Merging mitochondria matters. cellular role and molecular machinery of mitochondrial fusion EMBO Rep. 3:2002;527-531.
89. 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.
90. Zamzami N., Kroemer G. The mitochondrion in apoptosis. how Pandora's box opens Nat. Rev. Mol. Cell Biol. 2:2001;67-71.
91. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:1995;367-377.
92. Zhu W., Cowie A., Wasfy G.W., Penn L.Z., Leber B., Andrews D.W. Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J. 15:1996;4130-4141.
93. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson C.B. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15:2001;1481-1486.