Mitochondria-dependent apoptosis and cellular pH regulation (original) (raw)
Hatefi Y . 1985 The mitochondrial electron transport and oxidative phosphorylation system. Ann Rev of Biochem54: 1015–1069 ArticleCAS Google Scholar
Konforti B . 1999 Picture story. How proton pumps make ATP. Nature Structural Biology6: 1090 ArticleCASPubMed Google Scholar
Alberts B, Bray D, Lewis J, Raff M, Roberts K and Watson J . 1994 In Molecular Biology of The Cell. (3rd ed.) (New York London: Garland Publishing, Inc.)
Nicholls D and Budd S . 2000 Mitochondria and neuronal survival. Physiol Review80: 315–360 ArticleCAS Google Scholar
Appleby RD, Porteous WK, Hughes G, James AM, Shannon D, Wei Y-H and Murphy MP . 1999 Quantitation and origin of the mitochondrial membrane potential in human cells lacking mitochondrial DNA. Eur. J. Biochem.262: 108–116 ArticleCASPubMed Google Scholar
Numata M, Petrecca K, Lake N and Orlowski J . 1998 Identification of a mitochondrial Na+/H+ exchanger. J. Biol. Chem.273: 6951–6959 ArticleCASPubMed Google Scholar
Halestrap AP . 1989 The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim. Biophys. Acta973: 355–382 ArticleCASPubMed Google Scholar
Garlid KD, Jaburek M and Jezek P . 1998 The mechanism of proton transport mediated by mitochondrial uncoupling proteins. FEBS Lett438: 10–14 ArticleCASPubMed Google Scholar
Garlid KD . 1994 Mitochondrial cation transport: A progress report. J Bioenerg Biomembr26: 537–542 ArticleCASPubMed Google Scholar
Bernardi P . 1999 Mitochondrial transport of cations: channels, exchangers and permeability transition. Physiol Rev.79: 1127–1155 ArticleCASPubMed Google Scholar
Mannella CA, Forte M and Colombini M . 1992 Toward the molecular structure of the mitochondrial channel, VDAC. J. Bioenerg. Biomembr.24: 7–19 ArticleCASPubMed Google Scholar
Loew LM, Carrington W, Tuft RA and Fay FS . 1994 Physiological cytosolic Ca2+ transients evoke concurrent mitochondrial depolarizations. Proc. Natl. Acad. Sci. USA91: 12579–12583 ArticleCASPubMedPubMed Central Google Scholar
Bernardi P, Colonna R, Constantini P, Eriksson O, Fontaine E, Ichas F, Massari S, Nicolli A, Petronnilli V and Scorrano I . 1998 The Mitochondrial permeability transition. Biofactors8: 273–281 ArticleCASPubMed Google Scholar
Vander Heiden MG and Thompson CB . 1999 Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat. Cell. Biol.1: E209–E216 ArticleCASPubMed Google Scholar
Bossy-Wetzel E, Newmeyer D and Green D . 1998 Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J17: 37–49 ArticleCASPubMedPubMed Central Google Scholar
Goldstein J, Waterhouse N, Juin P, Evan G and Green D . 2000 The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell. Biol.2: 156–162 ArticleCASPubMed Google Scholar
Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT and Thompson CB . 1997 Bcl-XL regulates the membrane protential and volume homeostasis of mitochondria. Cell91: 627–637 ArticleCASPubMed Google Scholar
Martinou I, Desagher S, Eskes R, Antonsson B, André E, Fakan S and Martinou J-C . 1999 The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell. Biol.144: 883–889 ArticleCASPubMedPubMed Central Google Scholar
Matsuyama S, Llopi J, Deveraux Q, Tsien R and Reed J . 2000 Changes in intramitochondrial and cytosolic pH: Early events that modulate caspase activation during apoptosis. Nat. Cell. Biol.2: 318–325 ArticleCASPubMed Google Scholar
Minamikawa T, Williams DA, Bowser DN and Nagley P . 1999 Mitochondrial permeability transition and swelling can occur reversibly without inducing cell death in intact human cells. Exp. Cell. Res.246: 26–37 ArticleCASPubMed Google Scholar
Minn J, Kettlun C, Liang H, Kelekar A, Vander Heiden M, Chang B, Fesik S, FIll M and Thompson C . 1999 BcI-xL regulates apoptosis by heterodimerization-dependent and -independent mechanisms. EMBO J18: 632–643 ArticleCASPubMedPubMed Central Google Scholar
Krohn AJ, Wahlbrink T and Prehn JH . 1999 Mitochondrial depolarization is not required for neuronal apoptosis. J. Neurosci.19: 7394–7404 ArticleCASPubMedPubMed Central Google Scholar
Budd SL, Tenneti L, Lishnak T and Lipton SA . 2000 Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc. Natl. Acad. Sci. USA97: 6161–6166 ArticleCASPubMedPubMed Central Google Scholar
Petronilli V, Miotto G, Canton M, Colonna R, Bernardi P and Di Lisa F . 1998 Imaging the mitochondrial permeability transition pore in intact cells. Biofactors8: 263–272 ArticleCASPubMed Google Scholar
Rottenberg H and Wu S . 1998 Quantitative assay by flow cytometry of the mitochondrial membrane potential in intact cells. Biochimica et Biophysica Acta1404: 393–404 ArticleCASPubMed Google Scholar
Llopis J, McCaffery JM, Miyawaki A, Farquhar MG and Tsien RY . 1998 Measurement of cytosolic, mitochondrial and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA95: 6803–6808 ArticleCASPubMedPubMed Central Google Scholar
Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacroniqe V, Matsuda H and Tsujimoto Y . 1998 Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc. Natl. Acad. Sci. USA95: 1455–1459 ArticleCASPubMedPubMed Central Google Scholar
Gross A, McDonnell J and Korsmeyer S . 1999 BCL-2 family members and the mitochondria in apoptosis. Genes Dev.13: 1899–1911 ArticleCASPubMed Google Scholar
Vaux DL, Haecker G and Strasser A . 1994 An evolutionary perspective on apoptosis. Cell76: 777–779 ArticleCASPubMed Google Scholar
Matsuyama S, Nouraini S and Reed J . 1999 Yeast as a tool for apoptosis research. Curr. Opin. Microbiol.2: 618–623 ArticleCASPubMed Google Scholar
Zha H, Fisk HA, Yaffe MP, Mahajan N, Herman B and Reed JC . 1996 Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. Biol.16: 6494–6508 ArticleCASPubMedPubMed Central Google Scholar
Manon S, Chaudhuri B and BuÈrin M . 1997 Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells and prevention of these effects by coexpression of Bcl-XL. FEBS Lett.415: 29–32 ArticleCASPubMed Google Scholar
Gross A, Pilcher K, Blachly-Dyson E, Basso E, Jockel J, Bassik MC, Korsmeyer SJ and Forte M . 2000 Biochemical and genetic analysis of the mitochondrial response of yeast to BAX and BCL-XL . Mol. Cell. Biol.20: 3125–3136 ArticleCASPubMedPubMed Central Google Scholar
Harris MH, Vander Heiden MG, Kron SJ and Thompson CB . 2000 Role of oxidative phosphorylation in bax toxicity. Mol. Cell. Biol.20: 3590–3596 ArticleCASPubMedPubMed Central Google Scholar
Asoh S, Nishimaki K, Nanbu-Wakao R and Ohta S . 1998 A trace amount of the human pro-apoptotic factor Bax induces bacterial death accompanied by damage of DNA. J. Biol. Chem.273: 11384–11391 ArticleCASPubMed Google Scholar
Nouraini S, Six E, Matsuyama S, Krajewski S and Reed J . 2000 The putative pore forming-domain of bax regulates mitochondrial localization and interaction with bcl-xL. Mol. Cell. Biol.20: 1604–1615 ArticleCASPubMedPubMed Central Google Scholar
Priault M, Chaudhuri B, Clow A, Camougrand N and Manon S . 1999 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 ArticleCASPubMed Google Scholar
Schendel S, Montal M and Reed JC . 1998 Bcl-2 family proteins as ion-channels. Cell Death Differ.5: 372–380 ArticleCASPubMed Google Scholar
Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG and Youle RJ . 1997 Movement of bax from the cytosol to mitochondria during apoptosis. J. Cell Biol.139: 1281–1292 ArticleCASPubMedPubMed Central Google Scholar
Goping I, Gross A, Lavoie J, Nguyen M, Jemmerson R, Roth K, Korsmeyer S and Shore G . 1998 Regulated targeting of BAX to mitochodria. J. Cell Bio.143: 207–215 ArticleCAS Google Scholar
Gross T, Jockel J, Wei MC and Korsmeyer SJ . 1998 Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J.17: 3878–3885 ArticleCASPubMedPubMed Central Google Scholar
Jrgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D and Reed JC . 1998 Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. U S A95: 4997–5002 Article Google Scholar
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 and Martinou J-C . 1997 Inhibition of Bax channel-forming activity by Bcl-2. Science277: 370–372 ArticleCASPubMed Google Scholar
Schlesinger P, Gross A, Yin X-M, Yamamoto K, Saito M, Waksman G and Korsmeyer S . 1997 Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA94: 11357–11362 ArticleCASPubMedPubMed Central Google Scholar
Shimizu S, Narita M and Tsujimoto Y . 1999 Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature399: 483–487 ArticleCASPubMed Google Scholar
Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HLA, Preevost M-C, Xie Z, Matsuyama S, Reed JC and Kroemer G . 1998 Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science281: 2027–2031 ArticleCASPubMed Google Scholar
Priault M, Camougrand N, Chaudhuri B, Schaeffer J and Manon S . 1999 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 ArticleCASPubMed Google Scholar
Greenhalf W, Stephan C and Chaudhuri B . 1996 Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett.380: 169–175 ArticleCASPubMed Google Scholar
Clow A, Greenhalf W and Chaudhuri B . 1998 Under respiratory growth conditions, Bcl-X(L) and Bcl-2 are unable to overcome yeast cell death triggered by a mutant BAX protein lacking the membrane anchor. Eur. J. Biochem.258: 19–28 ArticleCASPubMed Google Scholar
Kissova I, Polcic P, Kempna P, Zeman I, Sabova L and Kolarov J . 2000 The cytotoxic action of Bax on yeast cells does not require mitochondrial ADP/ATP carrier but may be related to its import to the mitochondria. FEBS Lett.471: 113–118 ArticleCASPubMed Google Scholar
Matsuyama S, Xu Q, Velours J and Reed JC . 1998 Mitochondrial F0F1-ATPase proton-pump is required for function of pro-apoptotic protein bax in yeast and mammalian cells. Mol. Cell1: 327–336 ArticleCASPubMed Google Scholar
Velours J, Arselin G, Paul MF, Galante M, Durrens P, Aigle M and Guerin B . 1989 The yeast ATP synthase subunit 4: structure and function. Biochimie.71: 903–915 ArticleCASPubMed Google Scholar
Walker JE, Lutter R, Dupuis A and Runswick MJ . 1991 Identification of the subunits of F1F0-ATPase from bovine heart mitochondria. Biochemistry30: 5369–5378 ArticleCASPubMed Google Scholar
Narita M, Shimizu S, Ito T, Chittenden T, Lutz R, Matsuda H and Tsujimoto Y . 1998 Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA95: 14681–14686 ArticleCASPubMedPubMed Central Google Scholar
Ikemoto H, Tani E, Ozaki I, Kitagawa H and Arita N . 2000 Calphostin C-mediated translocation and integration of bax into mitochondria induces cytochrome c release before mitochondrial dysfunction. Cell Death Differ.7: 511–520 ArticleCASPubMed Google Scholar
Arato-Oshima T, Matsui H, Wakizaka A and Homareda H . 1996 Mechanism responsible for oligomycin-induced occlusion of Na+ within Na/K-ATPase. J. Biol. Chem.271: 25604–25610 ArticleCASPubMed Google Scholar
Jacobson M, Burne J, King M, Miyashita T, Reed J and Raff M . 1995 Apoptosis and Bcl-2 protein in cells without mitochondrial DNA. Nature361: 365–368 Article Google Scholar
Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H and Tsujimoto Y . 1995 Prevention of hypoxia-induced cell death by Bcl-2 and BclxL. Nature374: 811–813 ArticleCASPubMed Google Scholar
Buchet K and Godinot C . 1998 Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted ρ° cells. J. Biol. Chem.273: 22983–22989 ArticleCASPubMed Google Scholar
Ishaque A and Al-Rubeai M . 1998 Use of intracellular pH and annexin-V flow cytometric assays to monitor apoptosis and its suppression by bcl-2 over-expression in hybridoma cell culture. J. Immunol. Methods221: 43–57 ArticleCASPubMed Google Scholar
Barry MA, Reynolds JE and Eastman A . 1993 Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res.53: 2349–2357 CASPubMed Google Scholar
Gottlieb R, Nordberg J, Skowronski E and Babior B . 1996 Apoptosis induced in Jurkat cells by agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA93: 654–658 ArticleCASPubMedPubMed Central Google Scholar
Furlong IJ, Ascaso R, Lopez Rivas A and Collins MK . 1997 Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J. Cell. Sci.110: 653–661 CASPubMed Google Scholar
Chen Q, Benson RS, Whetton AD, Brant SR, Donowitz M, Montrose MH, Dive C and Watson AJ . 1997 Role of acid/base homeostasis in the suppression of apoptosis in haemopoietic cells by v-Abl protein tyrosine kinase. J. Cell. Sci.110: 379–387 CASPubMed Google Scholar
Li J and Eastman A . 1995 Apoptosis in an interleukin-2-dependent cytotoxic T lymphocyte cell line is associated with intracellular acidification. Role of the Na(+)/H(+)-antiport. J. Biol. Chem.270: 3203–3211 ArticleCASPubMed Google Scholar
Rebollo A, Gomez J, Martinez de Aragon A, Lasters P, Silva A and Perez-Sala D . 1995 Apoptosis induced by IL-2 withdrawal is associated with an intracellular acidification. Exp. Cell. Res.218: 581–585 ArticleCASPubMed Google Scholar
Thangaraju M, Sharma K, Leber B Andrews DW, Shen S-H and Srikant CB . 1999 Regulation of acidification and apoptosis by SHP-1 and Bcl-2. J. Biol. Chem.274: 29549–29557 ArticleCASPubMed Google Scholar
Niessen H, Meisenholder GW and Li HL, et al. 1997 Granulocyte colony-stimulating factor upregulates the vacuolar proton ATPase in human neutrophils. Blood90: 4598–4601 CASPubMed Google Scholar
Pèrez-Sala D, Collado-Escobar D and Mollinedo F . 1995 Intracellular alkalinization suppresses Lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem.270: 6235–6242 ArticlePubMed Google Scholar
Wolf CM and Eastman A . 1999 Intracellular acidification during apoptosis can occur in the absence of a nucleus. Biochem. Biophys. Res. Commun.254: 821–827 ArticleCASPubMed Google Scholar
Meisenholder GW, Martin SJ, Green DR, Nordberg J, Babior BM and Gottlieb RA . 1996 Events in apoptosis: Acidification is downstream of protease activation and bcl-2 protection. J. Biol. Chem.271: 16260–16262 ArticleCASPubMed Google Scholar
Zanke BW, Lee C, Arab S and Tannock IF . 1998 Death of tumor cells after intracellular acidification is dependent on stress-activated protein kinases (SAPK/JNK) pathway activation and cannot be inhibited by Bcl-2 expression or interleukin 1beta-converting enzyme inhibition. Cancer Res.58: 2801–2808 CASPubMed Google Scholar
Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV and Boldin MP . 1999 Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol.17: 331–367 ArticleCASPubMed Google Scholar
Ashkenazi A and Dixit V . 1998 Death receptors: signaling and modulation. Science281: 1305–1308 ArticleCASPubMed Google Scholar
Chen Q, Takeyama N, Brady G, Watson AJM and Dive C . 1998 Blood cells with reduced mitochondrial membrane potential and cytosolic cytochrome c can survive and maintain clonogenicity given appropriate signals to suppress apoptosis. Blood92: 4545–4553 CASPubMed Google Scholar
Perez-Sala D, Collado-Escobar D and Mollinedo F . 1995 Intracellular alkalinization suppresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem.270: 6235–6242 ArticleCASPubMed Google Scholar
Moolenaar WH, Tsien RY, van der Saag PT and de Laat SW . 1983 Na+/H+ exchange and cytoplasmic pH in the action of growth factors in human fibroblasts. Nature304: 645–648 ArticleCASPubMed Google Scholar
Deveraux QL, Takahashi R, Salvesen GS and Reed JC . 1997 X-linked IAP is a direct inhibitor of cell death proteases. Nature388: 300–304 ArticleCASPubMed Google Scholar
Deveraux Q and Reed J . 1999 IAP family proteins: Suppressors of apoptosis. Genes Dev.13: 239–252 ArticleCASPubMed Google Scholar
Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson R and Vaux DL . 2000 Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell102: 43–53 ArticleCASPubMed Google Scholar
Du C and Fang M . 2000 Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell102: 33–42 ArticleCASPubMed Google Scholar
Zou H, Henzel WJ, Liu X, Lutschg A and Wang X . 1997 Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell90: 405–413 ArticleCASPubMed Google Scholar
Garcia-Calvo M, Peterson EP, Rasper DM, Vaillancourt JP, Zamboni R, Nicholson DW and Thornberry NA . 1999 Purification and catalytic properties of human caspase family members. Cell Death Differ.6: 362–369 ArticleCASPubMed Google Scholar
Stennicke HR, Jurgensmeier JM, Shin H, Deveraux Q, Wolf BB, Yang X, Zhou Q, Ellerby LM, Bredesen D, Green DR, Reed JC, Froelich CJ and Salvesen GS . 1998 Pro-caspase-3 is a major physiologic target of caspase-8. J. Biol. Chem.273: 27084–27090 ArticleCASPubMed Google Scholar
Stennicke HR and Salvesen GS . 1997 Biochemical characteristics of caspase-3, -6, -7 and -8. J. Biol. Chem.272: 25719–25723 ArticleCASPubMed Google Scholar
Deshmukh M and Johnson JE . 1998 Evidence of a Novel Event during Neuronal Death: Development of Competence-to-Die in Response to Cytoplasmic Cytochrome c. Neuron21: 695–705 ArticleCASPubMed Google Scholar
Garland J and Rudin C . 1998 Cytochrome c induces caspase-dependent apoptosis in intact hematopoietic cells and overrides apoptosis suppression mediated by bcl-2, growth factor signaling, MAP-kinase-kinase and malignant change. Blood92: 1235–1246 CASPubMed Google Scholar
Burgess D, Svensson M, Dandrea T, Gröulund K, Hammarquist F, Orrenius S and Cotgreave I . 1999 Human skeletal muscle cytosols are refractory to cytochrome c-dependent activation of type-II caspases and lack APAF-1. Cell Death Differ.6: 256–261 ArticleCASPubMed Google Scholar
Reed J and Paternostro G . 1999 Post-mitochondrial regulation of apoptosis during heart failure. Proc. Natl. Acad. Sci. USA96: 7614–7616 ArticleCASPubMedPubMed Central Google Scholar
Yellon D, Alkhulaifi A and Pugsley W . 1993 Preconditioning the human myocardium. Lancet.342: 276–277 ArticleCASPubMed Google Scholar
Steenbergen C, Perlman ME, London RE and Murphy E . 1993 Mechanism of preconditioning. Ionic alterations. Circulation Research72: 112–125 ArticleCASPubMed Google Scholar
Asimakis GK, Inners-McBride K, Medellin G and Conti VR . 1992 Ischemic preconditioning attenuates acidosis and postischemic dysfunction in isolated rat heart. American Journal of Physiology263: H887–H894 CASPubMed Google Scholar
deAlbuquerque CP, Gerstenblith G and Weiss RG . 1994 Importance of metabolic inhibition and cellular pH in mediating preconditioning comtractile and metabolic effects in rat hearts. Circ. Res.74: 139–150 ArticleCAS Google Scholar
Gottlieb RA, Gruol DL, Zhu JY and Engler RL . 1996 Preconditioning in Rabbit Cardiomyocytes Role of pH, vacuolar proton ATPase and apoptosis. J. Clin. Invest.97: 2391–2398 ArticleCASPubMedPubMed Central Google Scholar
Lemasters J, Nieminen A-L, Qian T, Trost L, Elmore S, Nishimura Y, Crowe R, Cascio W, Bradham C, Brenner D and Herman B . 1998 The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta1366: 177–195 ArticleCASPubMed Google Scholar
Xie Z, Schendel S, Matsuyama S and Reed JC . 1998 Acidic pH promotes dimerization of Bcl-2 family proteins. Biochemistry37: 6410–6418 ArticleCASPubMed Google Scholar
Schendel SL, Xie Z, Montal MO, Matsuyama S, Montal M and Reed JC . 1997 Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA94: 5113–5118 ArticleCASPubMedPubMed Central Google Scholar
Matsuyama S, Schendel S, Xie Z and Reed J . 1998 Cytoprotection by Bcl-2 requires the pore-forming α5 and α6 helices. J. Biol. Chem.273: 30995–31001 ArticleCASPubMed Google Scholar
Schendel S, Azimov R, Pawlowski K, Godzik A, Kagan B and Reed J . 1999 Ion channel activity of the BH3 only Bcl-2 family member, BID. J Biol. Chem.274: 21932–21936 ArticleCASPubMed Google Scholar
Minn AJ, Velez P, Schendel SL, Liang H, Muchmore SW, Fesik S-W, FIll M and Thompson CB . 1997 Bcl-xL forms an ion channel in synthetic lipid membranes. Nature385: 353–357 ArticleCASPubMed Google Scholar
Nechushtan A, Smith C, Hsu Y-T and Youle R . 1999 conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J18: 2330–2341 ArticleCASPubMedPubMed Central Google Scholar
Khaled AR, Kim K, Hofmeister R, Muegge K and Durum SK . 1999 Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proc. Nat. Acad. Sci. USA96: 14476–14481 ArticleCASPubMedPubMed Central Google Scholar
Scarletta JL, Sheardb PW, Hughesa G, Ledgerwooda EC, Kuc H and Murphya MP . 2000 Changes in mitochondrial membrane potential during staurosporine-induced apoptosis in jurkat cells. FEBS Lett.475: 267–272 Article Google Scholar
Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E, Goldberg M, Allen T, Barber MJ, Green DR and 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 ArticleCASPubMedPubMed Central Google Scholar
Alberts B, Bray D, Lewis J, Raff M, Roberts K and Watson JD . 1994 Energy Conversion: Mitochondria and Chloroplasts. In: Molecular Biology of the Cell. Third Edition ed. Robertson M, ed. (New York, NY: Garland Publishing, Inc.) pp. 653–720.vol 14).