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Science 13 February 2004:
Vol. 303. no. 5660, pp. 1010 - 1014
DOI: 10.1126/science.1092734
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Reports

Direct Activation of Bax by p53 Mediates Mitochondrial Membrane Permeabilization and Apoptosis

Jerry E. Chipuk,1 Tomomi Kuwana,1 Lisa Bouchier-Hayes,1 Nathalie M. Droin,1 Donald D. Newmeyer,1 Martin Schuler,2 Douglas R. Green1*

The tumor suppressor p53 exerts its anti-neoplastic activity primarily through the induction of apoptosis. We found that cytosolic localization of endogenous wild-type or trans-activation–deficient p53 was necessary and sufficient for apoptosis. p53 directly activated the proapoptotic Bcl-2protein Bax in the absence of other proteins to permeabilize mitochondria and engage the apoptotic program. p53 also released both proapoptotic multidomain proteins and BH3-only proteins [Proapoptotic Bcl-2family proteins that share only the third Bcl-2homology domain (BH3)] that were sequestered by Bcl-xL. The transcription-independent activation of Bax by p53 occurred with similar kinetics and concentrations to those produced by activated Bid. We propose that when p53 accumulates in the cytosol, it can function analogously to the BH3-only subset of proapoptotic Bcl-2proteins to activate Bax and trigger apoptosis.

1 Division of Cellular Immunology, La Jolla Institute for Allergy and Immunology, 10355 Science Center Drive, San Diego, CA 92121, USA.
2 Department of Medicine III, Johannes Gutenberg University, D-55101 Mainz, Germany.

* To whom correspondence should be addressed. E-mail: doug{at}liai.org

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   Abstract »    Full Text »    PDF »
Mechanisms for human cytomegalovirus-induced cytoplasmic p53 sequestration in endothelial cells.
B. Utama, Y. H. Shen, B. M. Mitchell, I. T. Makagiansar, Y. Gan, R. Muthuswamy, S. Duraisamy, D. Martin, X. Wang, M.-X. Zhang, et al. (2006)
J. Cell Sci. 119, 2457-2467
   Abstract »    Full Text »    PDF »
Regulation of transactivation-independent proapoptotic activity of p53 by FOXO3a.
H. You, K. Yamamoto, and T. W. Mak (2006)
PNAS 103, 9051-9056
   Abstract »    Full Text »    PDF »
p53 Is Cleaved by Caspases Generating Fragments Localizing to Mitochondria.
B. S. Sayan, A. E. Sayan, R. A. Knight, G. Melino, and G. M. Cohen (2006)
J. Biol. Chem. 281, 13566-13573
   Abstract »    Full Text »    PDF »
Genome-Wide Analysis of p53 under Hypoxic Conditions..
E. M. Hammond, D. J. Mandell, A. Salim, A. J. Krieg, T. M. Johnson, H. A. Shirazi, L. D. Attardi, and A. J. Giaccia (2006)
Mol. Cell. Biol. 26, 3492-3504
   Abstract »    Full Text »    PDF »
Roles of Apoptosis in Airway Epithelia.
Y. Tesfaigzi (2006)
Am. J. Respir. Cell Mol. Biol. 34, 537-547
   Abstract »    Full Text »    PDF »
The p53 Pathway Promotes Efficient Mitochondrial DNA Base Excision Repair in Colorectal Cancer Cells..
D. Chen, Z. Yu, Z. Zhu, and C. D. Lopez (2006)
Cancer Res. 66, 3485-3494
   Abstract »    Full Text »    PDF »
WT p53, but Not Tumor-derived Mutants, Bind to Bcl2 via the DNA Binding Domain and Induce Mitochondrial Permeabilization.
Y. Tomita, N. Marchenko, S. Erster, A. Nemajerova, A. Dehner, C. Klein, H. Pan, H. Kessler, P. Pancoska, and U. M. Moll (2006)
J. Biol. Chem. 281, 8600-8606
   Abstract »    Full Text »    PDF »
Elk-1 associates with the mitochondrial permeability transition pore complex in neurons.
L. E. Barrett, E. J. Van Bockstaele, J. Y. Sul, H. Takano, P. G. Haydon, and J. H. Eberwine (2006)
PNAS 103, 5155-5160
   Abstract »    Full Text »    PDF »
Tumor Susceptibility and Apoptosis Defect in a Mouse Strain Expressing a Human p53 Transgene..
C. Dudgeon, C. Kek, O. N. Demidov, S.-i. Saito, K. Fernandes, A. Diot, J.-C. Bourdon, D. P. Lane, E. Appella, A. J. Fornace Jr., et al. (2006)
Cancer Res. 66, 2928-2936
   Abstract »    Full Text »    PDF »
A novel transcriptional inhibitor induces apoptosis in tumor cells and exhibits antiangiogenic activity..
S. K. Radhakrishnan and A. L. Gartel (2006)
Cancer Res. 66, 3264-3270
   Abstract »    Full Text »    PDF »
Inhibition of ADP/ATP Exchange in Receptor-Interacting Protein-Mediated Necrosis..
V. Temkin, Q. Huang, H. Liu, H. Osada, and R. M. Pope (2006)
Mol. Cell. Biol. 26, 2215-2225
   Abstract »    Full Text »    PDF »
Hindlimb unloading increases muscle content of cytosolic but not nuclear Id2 and p53 proteins in young adult and aged rats.
P. M. Siu, E. E. Pistilli, Z. Murlasits, and S. E. Alway (2006)
J Appl Physiol 100, 907-916
   Abstract »    Full Text »    PDF »
Expression of the Bcl-3 proto-oncogene suppresses p53 activation.
D. Kashatus, P. Cogswell, and A. S. Baldwin (2006)
Genes & Dev. 20, 225-235
   Abstract »    Full Text »    PDF »
Parkinson's Disease {alpha}-Synuclein Transgenic Mice Develop Neuronal Mitochondrial Degeneration and Cell Death.
L. J. Martin, Y. Pan, A. C. Price, W. Sterling, N. G. Copeland, N. A. Jenkins, D. L. Price, and M. K. Lee (2006)
J. Neurosci. 26, 41-50
   Abstract »    Full Text »    PDF »
The multidomain proapoptotic molecules Bax and Bak are directly activated by heat.
L. J. Pagliari, T. Kuwana, C. Bonzon, D. D. Newmeyer, S. Tu, H. M. Beere, and D. R. Green (2005)
PNAS 102, 17975-17980
   Abstract »    Full Text »    PDF »


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