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Science 25 September 1998:
Vol. 281. no. 5385, pp. 2027 - 2031
DOI: 10.1126/science.281.5385.2027
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Reports

Bax and Adenine Nucleotide Translocator Cooperate in the Mitochondrial Control of Apoptosis

Isabel Marzo, * Catherine Brenner, * Naoufal Zamzami, Juliane M. Jürgensmeier, Santos A. Susin, Helena L. A. Vieira, Marie-Christine Prévost, Zhihua Xie, Shigemi Matsuyama, John C. Reed, Guido Kroemer dagger

The proapoptotic Bax protein induces cell death by acting on mitochondria. Bax binds to the permeability transition pore complex (PTPC), a composite proteaceous channel that is involved in the regulation of mitochondrial membrane permeability. Immunodepletion of Bax from PTPC or purification of PTPC from Bax-deficient mice yielded a PTPC that could not permeabilize membranes in response to atractyloside, a proapoptotic ligand of the adenine nucleotide translocator (ANT). Bax and ANT coimmunoprecipitated and interacted in the yeast two-hybrid system. Ectopic expression of Bax induced cell death in wild-type but not in ANT-deficient yeast. Recombinant Bax and purified ANT, but neither of them alone, efficiently formed atractyloside-responsive channels in artificial membranes. Hence, the proapoptotic molecule Bax and the constitutive mitochondrial protein ANT cooperate within the PTPC to increase mitochondrial membrane permeability and to trigger cell death.

I. Marzo, N. Zamzami, S. A. Susin, H. L. A. Vieira, G. Kroemer, CNRS, UPR 420, 19 rue Guy Môquet, F-94801 Villejuif, France. C. Brenner, CNRS, UPR 420, 19 rue Guy Môquet, F-94801 Villejuif, France, and CNRS, UPRES-A6022, Université de Technologie de Compiègne, F-60200 Compiègne, France. J. M. Jürgensmeier, Z. Xie, S. Matsuyama, J. C. Reed, Burnham Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA. M.-C. Prévost, Unité d'Oncologie Virale, Institut Pasteur, 28 rue du Docteur Roux, F-75724 Paris Cedex 15, France.
*   These authors contributed equally to this report.

dagger    To whom correspondence should be addressed. E-mail: kroemer{at}infobiogen.fr

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P. Juin, A. Hunt, T. Littlewood, B. Griffiths, L. B. Swigart, S. Korsmeyer, and G. Evan (2002)
Mol. Cell. Biol. 22, 6158-6169
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The antiapoptotic protein Bcl-xL prevents the cytotoxic effect of Bax, but not Bax-induced formation of reactive oxygen species, in Kluyveromyces lactis.
D. Poliakova, B. Sokolikova, J. Kolarov, and L'u. Sabova (2002)
Microbiology 148, 2789-2795
   Abstract »    Full Text »    PDF »
Heat stress prevents mitochondrial injury in ATP-depleted renal epithelial cells.
F. Li, H. P. Mao, K. L. Ruchalski, Y. H. Wang, W. Choy, J. H. Schwartz, and S. C. Borkan (2002)
Am J Physiol Cell Physiol 283, C917-C926
   Abstract »    Full Text »    PDF »
Raloxifene, a Mixed Estrogen Agonist/Antagonist, Induces Apoptosis through Cleavage of BAD in TSU-PR1 Human Cancer Cells.
H. T. Kim, B. C. Kim, I. Y. Kim, M. Mamura, D. H. Seong, J.-J. Jang, and S.-J. Kim (2002)
J. Biol. Chem. 277, 32510-32515
   Abstract »    Full Text »    PDF »
A Novel Adenine Nucleotide Translocase Inhibitor, MT-21, Induces Cytochrome c Release by a Mitochondrial Permeability Transition-independent Mechanism.
K. Machida, Y. Hayashi, and H. Osada (2002)
J. Biol. Chem. 277, 31243-31248
   Abstract »    Full Text »    PDF »
Inhibiting mitochondrial permeability transition pore opening: a new paradigm for myocardial preconditioning?.
D. J Hausenloy, H. L Maddock, G. F Baxter, and D. M Yellon (2002)
Cardiovasc Res 55, 534-543
   Abstract »    Full Text »    PDF »
Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death.
S. P. Cregan, A. Fortin, J. G. MacLaurin, S. M. Callaghan, F. Cecconi, S.-W. Yu, T. M. Dawson, V. L. Dawson, D. S. Park, G. Kroemer, et al. (2002)
J. Cell Biol. 158, 507-517
   Abstract »    Full Text »    PDF »
Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia.
X. J. Chen (2002)
Hum. Mol. Genet. 11, 1835-1843
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Phosphorylation status modulates Bcl-2 function during glucocorticoid-induced apoptosis in T lymphocytes.
S.-T. J. HUANG and J. A. CIDLOWSKI (2002)
FASEB J 16, 825-832
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Bax-mediated Ca2+ Mobilization Promotes Cytochrome c Release during Apoptosis.
L. K. Nutt, J. Chandra, A. Pataer, B. Fang, J. A. Roth, S. G. Swisher, R. G. O'Neil, and D. J. McConkey (2002)
J. Biol. Chem. 277, 20301-20308
   Abstract »    Full Text »    PDF »
BH3-only proteins -- evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death.
P. Bouillet and A. Strasser (2002)
J. Cell Sci. 115, 1567-1574
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Type I Interferon Gene Transfer Sensitizes Melanoma Cells to Apoptosis via a Target Activity on Mitochondrial Function.
P. Matarrese, L. Di Biase, L. Santodonato, E. Straface, M. Mecchia, B. Ascione, G. Parmiani, F. Belardelli, M. Ferrantini, and W. Malorni (2002)
Am. J. Pathol. 160, 1507-1520
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Exogenous Phospholipids Specifically Affect Transmembrane Potential of Brain Mitochondria and Cytochrome c Release.
L. Piccotti, C. Marchetti, G. Migliorati, R. Roberti, and L. Corazzi (2002)
J. Biol. Chem. 277, 12075-12081
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Bax and Bak Promote Apoptosis by Modulating Endoplasmic Reticular and Mitochondrial Ca2+ Stores.
L. K. Nutt, A. Pataer, J. Pahler, B. Fang, J. Roth, D. J. McConkey, and S. G. Swisher (2002)
J. Biol. Chem. 277, 9219-9225
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Transforming Growth Factor {beta}1 Induces Apoptosis through Cleavage of BAD in a Smad3-Dependent Mechanism in FaO Hepatoma Cells.
B.-C. Kim, M. Mamura, K. S. Choi, B. Calabretta, and S.-J. Kim (2002)
Mol. Cell. Biol. 22, 1369-1378
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Mitochondrial Binding of Hexokinase II Inhibits Bax-induced Cytochrome c Release and Apoptosis.
J. G. Pastorino, N. Shulga, and J. B. Hoek (2002)
J. Biol. Chem. 277, 7610-7618
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Cytochrome c Oxidase Subunit III. A MOLECULAR MARKER FOR N-(4-HYDROXYPHENYL)RETINAMIDE-INDUCED OXIDATIVE STRESS IN HEPATOMA CELLS.
K.-R. You, J. Wen, S.-T. Lee, and D.-G. Kim (2002)
J. Biol. Chem. 277, 3870-3877
   Abstract »    Full Text »    PDF »


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