Skip to main content

Roles of Mitochondria in Apoptosis

  • Chapter
Mitochondrial Diseases
  • 141 Accesses

Abstract

Programmed cell death appears as a very early event in the course of evolution, limiting the size cellular populations and eliminating some undesirable cells (Ellis et al. 1991). This process is fundemental for the development of multicellular organisms, in the course of which many embryonic cells die. Programmed cell death and proliferation helps determine the size and form of organs, as well as the functional maturation of some systems. During the development of limbs, cell profileration and differentiation allow the appearance and the growth of limb buds, while the morphogenesis of fingers and toes invokes the death cells initially located in interdigital positions. During the development of the nervous system, neurons that do not reach their target are eliminated by a process of programmed cell death (Thompson 1995). This death allows the establishment of functions of the nervous system by playing on its plasticity. The functional maturation of the immune system also involves massive programmed cell death. The clones of self-reactive T lymphocytes are eliminated by a process of programmed cell death. In other cases, structures whose physiological role is only transitory are eliminated, for example during the metamorphosis of amphibians (tail of tadpoles) and insects (intersegmental muscles).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akao Y, Otsuki Y, Kataoka S, Ito Y, Tsujimoto Y (1994) Multiple subcellular localization of Bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res 54:2468–2471

    PubMed  CAS  Google Scholar 

  • Ali ST, Coggins JR, Jacobs HT (1997) The study of cell death proteins in the outer mitochondrial membrane chemical cross-linking. Biochem J 325:321–324

    PubMed  CAS  Google Scholar 

  • Ameisen JC, Estaquier J, Idziorek T, De Bels F (1995) The relevance of apoptosis to AIDS pathogenesis. Trends Cell Biol 5:27–32

    Article  PubMed  CAS  Google Scholar 

  • Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R, Martinou JC (1997) Inhibition of Bax channel-forming acitivity by Bcl-2. Science 277:370–372

    Article  PubMed  CAS  Google Scholar 

  • Bernardi P, Vassanelli S, Veronese P, Colonna R, Szabo I, Zoratti M (1992) Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J Biol Chem 267:2934–2939

    PubMed  CAS  Google Scholar 

  • Beutner G, Ruck A, Riede B, Weite W, Brdiczka D (1996) Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett 396:189–195

    Article  PubMed  CAS  Google Scholar 

  • Boyd JM, Malstrom S, Subramanian T, Venkatesh LK, Schaeper U, Elangovan B, D’Sa EC, Chinnadurai G (1994) Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341–351

    Article  PubMed  CAS  Google Scholar 

  • Bursch W, Oberhammer F, Schulte-Hermann R (1992) Cell death by apoptosis and its protective role against disease. Trends Pharmacol Sci 13:245–251

    Article  PubMed  CAS  Google Scholar 

  • Carayon P, Portier M, Dussossoy D, Bord A, Petitpretre G, Canat X, Le Fur G, Casellas P (1996) Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood 87:3170–3178

    PubMed  CAS  Google Scholar 

  • Chinnaiyan AM, Chaudhary D, O’Rourke K, Koonin EV, Dixit VM (1997a) Role of CED-4 in the activation of CED-3. Nature 388:728–729

    Article  PubMed  CAS  Google Scholar 

  • Chinnaiyan AM, O’Rourke K, Lane BR, Dixit VM (1997b) Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 275:1122–1126

    Article  PubMed  CAS  Google Scholar 

  • Clarke PGH (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195–213

    Article  PubMed  CAS  Google Scholar 

  • De Jong D, Prins FA, Mason DY, Reed JC, van Ommen GB, Kluin PM (1994) Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells. Cancer Res 54:256–260

    PubMed  Google Scholar 

  • Decaudin D, Geley S, Hirsch T, Castedo M, Marchetti P, Macho A, Kofler R, Kroemer G (1997) Bcl-2 and Bcl-XL antagonize the mitochondrial dysfunction preceding nuclear apoptosis induced by chemotherapeutic agents. Cancer Res 57:62–67

    PubMed  CAS  Google Scholar 

  • Ellis RE, Yuan JY, Horvitz HR (1991) Mechanisms and functions of cell death. Annu Rev Cell Biol 7:663–698

    Article  PubMed  CAS  Google Scholar 

  • Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Handcock DC (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119–128

    Article  PubMed  CAS  Google Scholar 

  • Fernandez SM, Bischoff JR (1993) Bcl-2 associated with the ras-related protein R-ras p23. Nature 366:274–275

    Article  Google Scholar 

  • France-Lanord V, Brugg B, Michel PP, Agid Y, Ruberg M (1997) Mitochondrial free radical signal in ceramide-dependent apoptosis: a putative mechanism for neuronal death in Parkinson’s disease. J Neurochem 69:1612–1621

    Article  PubMed  CAS  Google Scholar 

  • Gillet G, Brun G (1996) Viral inhibition of apoptosis. Trends Mircobiol 4:312–317

    Article  CAS  Google Scholar 

  • Gonzalez-Garcia M, Perez-Ballestero R, Ding L, Duan L, Boise LH, Thompson CB, Nunez G (1994) bel-XL is the major bcl-x mRNA from expressed during murine development and its product localizes to mitochondria. Development 120:3033–3042

    PubMed  CAS  Google Scholar 

  • Gougeon ML, Montagnier L (1993) Apoptosis in AIDS. Science 260:1269–1270

    Article  PubMed  CAS  Google Scholar 

  • Gudz TI, Tserng KY, Hoppel CL (1997) Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J Biol Chem 272:24154–24158

    Article  PubMed  CAS  Google Scholar 

  • Guénal I, Risler Y, Mignotte B (1997a) Down regulation of actin genes precedes microfilament network disruption and actin cleavage during p53 mediated-apoptosis. J Cell Sci 110:489–495

    PubMed  Google Scholar 

  • Guénal I, Sidoti-de Fraisse C, Gaumer S, Mignotte B (1997b) Bcl-2 and Hsp27 act at different levels to suppress programmed cell death. Oncogene 15:347–360

    Article  PubMed  Google Scholar 

  • Hartley A, Stone JM, Heron C, Cooper JM, Schapira AH (1994) Complex I inhibitors induce dosedependent apoptosis in PC 12 cells: relevance to Parkinson’s disease. J Neurochem 63:1987–1990

    Article  PubMed  CAS  Google Scholar 

  • Hickish T, Robertson D, Clarke P, Hill M, di Stefano F, Clarke C, Cunningham D (1994) Ultrastructural localization of BHRF1: an Epstein-Barr virus gene product which has homology with bcl-2. Cancer Res 54:2808–2811

    PubMed  CAS  Google Scholar 

  • Hockenberg D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ (1990) Bcl-2 is an inner mitochondrial protein that blocks programmed cell death. Nature 348:334–336

    Article  Google Scholar 

  • Ichas F, Jouaville LS, Mazat JP (1997) Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89:1145–1153

    Article  PubMed  CAS  Google Scholar 

  • Irmler M, Hofmann K, Vaux D, Tschopp J (1997) Direct physical interaction between the Caenorhabditis elegans “death proteins” CED-3 and CED-4. FEBS Lett 406:189–190

    Article  PubMed  CAS  Google Scholar 

  • Jacobson MD, Burne JF, King MP, Miyashita T, Reed JC, Raff MC (1993) Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361:365–369

    Article  PubMed  CAS  Google Scholar 

  • Janiak F, Leber B, Andrews DW (1994) Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J Biol Chem 269:9842–9849

    PubMed  CAS  Google Scholar 

  • Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wideranging implications in tissue kinetics. Br J Cancer 26:239–257

    Article  PubMed  CAS  Google Scholar 

  • Kim CN, Wang X, Huang Y, Ibrado AM, Liu L, Fang G, Bhalla K (1997) Overexpression of BclX(L) inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res 57:3115–3120

    PubMed  CAS  Google Scholar 

  • Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132–1136

    Article  PubMed  CAS  Google Scholar 

  • Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC (1993) Investigations 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

    PubMed  CAS  Google Scholar 

  • Krippner Q, Matsuno-Yagi A, Gootlieb RA, Babior BM (1996) Loss of function of cytochrome c in Jurkat cells undergoing Fas-mediated apoptosis. J Biol Chem 271:21629–21636

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3:614–620

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Petit PX, Zamzami N, Vaysière JL, Mignotte B (1995) The biochemistry of programmed cell death. FASEB J 9:1277–1287

    PubMed  CAS  Google Scholar 

  • Kumar S (1995) ICE-like proteases in apoptosis. Trends Biochem Sci 20:198–202

    Article  PubMed  CAS  Google Scholar 

  • Kürschner C, Morgan JI (1995) The cellular prion protein (PrP) selectively binds to Bcl-2 in the yeast two-hybrid system. Mol Brain Res 30:165–168

    Article  PubMed  Google Scholar 

  • Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochromec. Cell 86:147–157

    Article  PubMed  CAS  Google Scholar 

  • Macho A, Castedo M, Marchetti P, Aguilar JJ, Decaudin D, Zamzami N, Girard PM, Uriel J, Kroemer G (1995) Mitochondrial dysfunctions in circulating T lymphocytes from human immunodeficiency virus-1 carriers. Blood 86:2481–2487

    PubMed  CAS  Google Scholar 

  • Macho A, Hirsch T, Marzo I, Marchetti P, Dallaporta B, Susin SA, Zamzami N, Kroemer G (1997) Glutathione depletion in an early and calcium elevation is a late event of thymocyte apoptosis. J Immunol 158:4612–4619

    PubMed  CAS  Google Scholar 

  • Marchetti P, Susin SS, Decaudin D, Gamen S, Castedo M, Hirsch T, Zamzami N, Naval J, Senik A, Kroemer G (1996) Apoptosis-associated derangement of mitochondrial function in cellslacking mitochondrial DNA. Cancer Res 56:2033–2038

    PubMed  CAS  Google Scholar 

  • Martin SJ (1993) Programmed cell death and AIDS. Science 262:1355–1356

    PubMed  CAS  Google Scholar 

  • Mignotte B, Vayssière JL (1998) Mitochondria and apoptosis. Eur J Biochem 252:1–15

    Article  PubMed  CAS  Google Scholar 

  • Mignotte B, Larcher JC, Zheng DQ, Esnault C, Couland D, Feunteun J (1990) SV40-induced cellular immortalization: phenotypic changes associated with the loss of proliferative capacity in a conditionally immortalized cell line. Oncogene 5:1529–1533

    PubMed  CAS  Google Scholar 

  • Minn AJ, Velez P, Schendel SL, Liang H, Muchmore SW, Fesik SW, Fill M, Thompson CB (1997) Bcl-xL forms an ion channel in synthetic lipid membranes. Nature 385:353–357

    Article  PubMed  CAS  Google Scholar 

  • Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SI, Ng SC, Fesik SW (1996) X-ray and NMR structure of human Bcl-XL, an inhibitor of programmed cell death. Nature 381:335–341

    Article  PubMed  CAS  Google Scholar 

  • Nakai M, Takeda A, Cleary ML, Endo T (1993) The bcl-2 protein is inserted into the outer membrane but not into the inner membrane of rat liver mitochondria in vitro. Biochem Biophys Res Commun 196:233–239

    Article  PubMed  CAS  Google Scholar 

  • Naumovski L, Cleary ML (1996) The p53-binding protein 53BP2 also interacts with Bcl-2 and impedes cell cycle progression at G2/M. Mol Cell Biol 16:3884–3892

    PubMed  CAS  Google Scholar 

  • Newmeyer DD, Farschon DM, Reed JC (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79:353–364

    Article  PubMed  CAS  Google Scholar 

  • Nguyen M, Millar DG, Yong VW, Korsmeyer SJ, Shore GC (1993) Targeting of bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J Biol Chem 268:25265–25268

    PubMed  CAS  Google Scholar 

  • Nguyen M, Branton PE, Walton PA, Oltvai ZN, Korsmeyer SJ, Shore GC (1994) Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J Biol Chem 269:16521–16524

    PubMed  CAS  Google Scholar 

  • Pastorino JG, Chen ST, Tafani M, Snyder JW, Farber JL (1998) The overexpression of bax produces cell death upon induction of the mitochondrial permeability transition. J Biol Chem 273:7770–7775

    Article  PubMed  CAS  Google Scholar 

  • Paumen MB, Ishida Y, Han H, Muramatsu M, Eguchi Y, Tsujimoto Y, Honjo T (1997) Direct interaction of the mitochondrial membrane protein carnitine palmitoyltransferase I with Bcl-2. Biochem Biophys Res Commun 231:523–525

    Article  PubMed  CAS  Google Scholar 

  • Petit PX, Lecoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML (1995) Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocytes apoptosis. J Cell Biol 130:157–167

    Article  PubMed  CAS  Google Scholar 

  • Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G (1996) Mitochondria and programmed cell death: back to the future. FEBS Lett 396:7–13

    Article  PubMed  CAS  Google Scholar 

  • Petronilli V, Nicolli A, Costantini P, Colonna R, Bernardi P (1994) Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim Biophys Acta 1187:255–259

    Article  PubMed  CAS  Google Scholar 

  • Quillet-Mary A, Jaffrezou JP, Mansat V, Bordier C, Naval J, Laurent G (1997) Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J Biol Chem 272:21388–21395

    Article  PubMed  CAS  Google Scholar 

  • Reed JC (1997) Double identity for proteins of the Bcl-2 family. Nature 387:773–776

    Article  PubMed  CAS  Google Scholar 

  • Scarlett JL, Murphy MP (1997) Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett 418:282–286

    Article  PubMed  CAS  Google Scholar 

  • Schendel SL, Xie Z, Montai MO, Matsuyama S, Montai M, Reed JC (1997) Channel formation by antiapoptotic protein Bcl-2. Proc Natl Acad Sci USA 94:5113–5118

    Article  PubMed  CAS  Google Scholar 

  • Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W (1992) Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 267:5317–5323

    PubMed  CAS  Google Scholar 

  • Schwartz LM, Smith SW, Jones MEE, Osborne BA (1993) Do all programmed cell deaths occur via apoptosis? Proc Natl Acad Sci USA 90:980–984

    Article  PubMed  CAS  Google Scholar 

  • Sentman CL, Shutter JR, Hockenbery D, Kanagawa O, Korsmeyer SJ (1991) Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67:879–888

    Article  PubMed  CAS  Google Scholar 

  • Shaw P, Bovey R, Tardy S, Sahli R, Sordat B, Costa J (1992) Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc Natl Acad Sci USA 89:4495–4499

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Glynn JM, Guilbert LJ, Cotter TG, Bissonnette RD, Green DR (1992) Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science 257:212–214

    Article  PubMed  CAS  Google Scholar 

  • Shibasaki F, Kondo E, Akagi T, McKeon F (1997) Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386:728–731

    Article  PubMed  CAS  Google Scholar 

  • Shimizu S, Eguchi Y (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13:21–29

    PubMed  CAS  Google Scholar 

  • Sidoti-de Fraisse C, Rincheval V, Risler Y, Mignotte B, Vayssière JL (1998) TNF-a activates at least two apoptotic signaling cascades. Oncogene 17:1639–1651

    Article  Google Scholar 

  • Skowronek P, Haferkamp O, Rodel G (1992) A fluorescence-microscopic and flow cytometric study of HeLa cells with an experimentally induced respiratory deficiency. Biochem Biophys Res Commun 187:991–998

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Strasser A, Harris AW, Cory S (1991) Bcl-2 transgene inhibits T-cell death and perturbs thymic self-censorship. Cell 67:889–899 Susin SA, Zamzami N, Castedo M, Hirsh T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184:1–111

    Google Scholar 

  • Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA, Reed JC (1995) Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279–284

    Article  PubMed  CAS  Google Scholar 

  • Tan EM (1994) Autoimmunity and apoptosis. J Exp Med 179:1083–1086

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Saito K, Reed JC (1993) 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

    PubMed  CAS  Google Scholar 

  • Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267:1456–1462

    Article  PubMed  CAS  Google Scholar 

  • Van der Heiden MG, Chandel NS, Williamson EK, Schumaker PT, Thompson CB (1997) Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91:627–637

    Article  Google Scholar 

  • Vayssière JL, Petit PX, Risler Y, Mignotte B (1994) Commitment to apoptosis is associated with changes in mitochondrial biogenesis and acitvity in cell lines conditionally immortalized with simian virus 40. Proc Natl Acad Sci USA 91:11752–11756

    Article  PubMed  Google Scholar 

  • Wang HG, Miyashita T, Takayama S, Sato T, Torigoe T, Krajewski S, Tanaka S, Hovey LR, Troppmair J, Rapp UR, Reed JC (1994) Apoptosis regulation by interaction of Bcl-2 protein and Raf-1 kinase. Oncogene 9:2751–2756

    PubMed  CAS  Google Scholar 

  • Williams GT (1991) Programmed cell death: apoptosis and oncogenesis. Cell 65:1097–1098 Wolvetang EJ, Johnson KL, Krauer K, Ralph SJ, Limnane AW (1994) Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett 339:40–44

    Google Scholar 

  • Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132

    Article  PubMed  CAS  Google Scholar 

  • Yang T, Kozopas KM, Craig RW (1995) The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J Cell Biol 128:1173–1184

    Article  PubMed  CAS  Google Scholar 

  • Yonish-Rouach E, Resnitzky D, Lotem J, Sachs L, Kimchi A, Oren M (1991) Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 352:345–347

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Petit PX, Mignotte B, Kroemer G (1995a) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367–377

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssière JL, Petit PX, Kroemer G (1995b) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 181:1661–1672

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Marchetti P, Castedo M, Hirsch T, Susin SA, Masse B, Kroemer G (1996a) Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett 384:53–57

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G (1996b) Mitochondrial control of nuclear apoptosis. J Exp Med 183:1533–1544

    Article  PubMed  CAS  Google Scholar 

  • Zheng DQ, Vayssière JL, Lecoeur H, Petit PX, Spatz A, Mignotte B, Feunteun J (1994) Apoptosis is antogonized by large T antigens in the pathway to immortalization by polyomaviruses. Oncogene 9:3345–3351

    PubMed  CAS  Google Scholar 

  • Zhu W, Cowie A, Wasfy GW, Penn LZ, Leber B, Andrews DW (1996) Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J 15:4130–4141

    PubMed  CAS  Google Scholar 

  • Zou H, Henzel WJ, Liu X, Lutschg A, Wang X (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspases-3. Cell 90:405–413

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Mignotte, B., Kroemer, G. (1999). Roles of Mitochondria in Apoptosis. In: Lestienne, P. (eds) Mitochondrial Diseases. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59884-5_18

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-59884-5_18

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64166-4

  • Online ISBN: 978-3-642-59884-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics