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Science 300 (5616): 135-139

Copyright © 2003 by the American Association for the Advancement of Science

BAX and BAK Regulation of Endoplasmic Reticulum Ca2+: A Control Point for Apoptosis

Luca Scorrano,12* Scott A. Oakes,1* Joseph T. Opferman,1 Emily H. Cheng,1 Mia D. Sorcinelli,1 Tullio Pozzan,23 Stanley J. Korsmeyer1dagger

BAX and BAK are "multidomain" proapoptotic proteins that initiate mitochondrial dysfunction but also localize to the endoplasmic reticulum (ER). Mouse embryonic fibroblasts deficient for BAX and BAK (DKO cells) were found to have a reduced resting concentration of calcium in the ER ([Ca2+]er) that results in decreased uptake of Ca2+ by mitochondria after Ca2+ release from the ER. Expression of SERCA (sarcoplasmic-endoplasmic reticulum Ca2+ adenosine triphosphatase) corrected [Ca2+]er and mitochondrial Ca2+ uptake in DKO cells, restoring apoptotic death in response to agents that release Ca2+ from intracellular stores (such as arachidonic acid, C2-ceramide, and oxidative stress). In contrast, targeting of BAX to mitochondria selectively restored apoptosis to "BH3-only" signals. A third set of stimuli, including many intrinsic signals, required both ER-released Ca2+ and the presence of mitochondrial BAX or BAK to fully restore apoptosis. Thus, BAX and BAK operate in both the ER and mitochondria as an essential gateway for selected apoptotic signals.

1 Howard Hughes Medical Institute, Dana-Farber Cancer Institute, Brigham and Women's Hospital, Department of Pathology and Medicine, Harvard Medical School, Boston, MA 02115, USA.
2 Venetian Institute for Molecular Medicine, 35121 Padova, Italy.
3 Department of Biomedical Sciences, University of Padova, 35121 Padova, Italy.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: stanley_korsmeyer{at}

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C. M. Martin, A. Ferdous, T. Gallardo, C. Humphries, H. Sadek, A. Caprioli, J. A. Garcia, L. I. Szweda, M. G. Garry, and D. J. Garry (2008)
Circ. Res. 102, 1075-1081
   Abstract »    Full Text »    PDF »
BI-1 Regulates Endoplasmic Reticulum Ca2+ Homeostasis Downstream of Bcl-2 Family Proteins.
C. Xu, W. Xu, A. E. Palmer, and J. C. Reed (2008)
J. Biol. Chem. 283, 11477-11484
   Abstract »    Full Text »    PDF »
Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin-interacting protein-mediated pathway.
C.-L. Chen, C.-F. Lin, W.-T. Chang, W.-C. Huang, C.-F. Teng, and Y.-S. Lin (2008)
Blood 111, 4365-4374
   Abstract »    Full Text »    PDF »
Survival Signaling by C-RAF: Mitochondrial Reactive Oxygen Species and Ca2+ Are Critical Targets.
A. V. Kuznetsov, J. Smigelskaite, C. Doblander, M. Janakiraman, M. Hermann, M. Wurm, S. F. Scheidl, R. Sucher, A. Deutschmann, and J. Troppmair (2008)
Mol. Cell. Biol. 28, 2304-2313
   Abstract »    Full Text »    PDF »
BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis.
N. Watanabe and E. Lam (2008)
J. Biol. Chem. 283, 3200-3210
   Abstract »    Full Text »    PDF »
Critical Role of the Stress Chaperone GRP78/BiP in Tumor Proliferation, Survival, and Tumor Angiogenesis in Transgene-Induced Mammary Tumor Development.
D. Dong, M. Ni, J. Li, S. Xiong, W. Ye, J. J. Virrey, C. Mao, R. Ye, M. Wang, L. Pen, et al. (2008)
Cancer Res. 68, 498-505
   Abstract »    Full Text »    PDF »
BCL-2 Family Proteins: Critical Checkpoints of Apoptotic Cell Death.
N. N. Danial (2007)
Clin. Cancer Res. 13, 7254-7263
   Abstract »    Full Text »    PDF »
Endoplasmic Reticulum Stress in the Proapoptotic Action of Edelfosine in Solid Tumor Cells.
T. Nieto-Miguel, R. I. Fonteriz, L. Vay, C. Gajate, S. Lopez-Hernandez, and F. Mollinedo (2007)
Cancer Res. 67, 10368-10378
   Abstract »    Full Text »    PDF »
Inhibition of MEK Sensitizes Human Melanoma Cells to Endoplasmic Reticulum Stress-Induced Apoptosis.
C. C. Jiang, L. H. Chen, S. Gillespie, Y. F. Wang, K. A. Kiejda, X. D. Zhang, and P. Hersey (2007)
Cancer Res. 67, 9750-9761
   Abstract »    Full Text »    PDF »
Selective progesterone receptor modulator asoprisnil induces endoplasmic reticulum stress in cultured human uterine leiomyoma cells.
Q. Xu, N. Ohara, J. Liu, K. Nakabayashi, D. DeManno, K. Chwalisz, S. Yoshida, and T. Maruo (2007)
Am J Physiol Endocrinol Metab 293, E1002-E1011
   Abstract »    Full Text »    PDF »

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