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Science 13 November 1998:
Vol. 282. no. 5392, pp. 1318 - 1321
DOI: 10.1126/science.282.5392.1318
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Reports

Regulation of Cell Death Protease Caspase-9 by Phosphorylation

Michael H. Cardone, *dagger Natalie Roy, * Henning R. Stennicke, Guy S. Salvesen, Thomas F. Franke, Eric Stanbridge, Steven Frisch, John C. Reed ddagger

Caspases are intracellular proteases that function as initiators and effectors of apoptosis. The kinase Akt and p21-Ras, an Akt activator, induced phosphorylation of pro-caspase-9 (pro-Casp9) in cells. Cytochrome c-induced proteolytic processing of pro-Casp9 was defective in cytosolic extracts from cells expressing either active Ras or Akt. Akt phosphorylated recombinant Casp9 in vitro on serine-196 and inhibited its protease activity. Mutant pro-Casp9(Ser196Ala) was resistant to Akt-mediated phosphorylation and inhibition in vitro and in cells, resulting in Akt-resistant induction of apoptosis. Thus, caspases can be directly regulated by protein phosphorylation.

M. H. Cardone, Program on Apoptosis and Cell Death Research, The Burnham Institute, La Jolla, CA 92037, USA, and Department of Biology, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA. N. Roy, H. R. Stennicke, G. S. Salvesen, S. Frisch, J. C. Reed, Program on Apoptosis and Cell Death Research, The Burnham Institute, La Jolla, CA 92037, USA. T. F. Franke, Department of Pharmacology, Columbia University, New York, NY 10032, USA. E. Stanbridge, Department of Microbiology and Molecular Genetics, University of California at Irvine, Irvine, CA 92697-4025, USA.
*   These authors contributed equally to this work.

dagger    Present address: Department of Biology, MIT, Cambridge, MA 02139, USA.

ddagger    To whom correspondence should be addressed at The Burnham Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA. E-mail: jreed{at}burnham-inst.org.

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Am J Physiol Cell Physiol 291, C1247-C1257
   Abstract »    Full Text »    PDF »
Chronic Protein Kinase B (PKB/c-akt) Activation Leads to Apoptosis Induced by Oxidative Stress-Mediated Foxo3a Transcriptional Up-regulation..
A. G.M. van Gorp, K. M. Pomeranz, K. U. Birkenkamp, R. C-Y. Hui, E. W-F. Lam, and P. J. Coffer (2006)
Cancer Res. 66, 10760-10769
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Fas-Mediated Apoptosis in Cholangiocarcinoma Cells Is Enhanced by 3,3'-Diindolylmethane through Inhibition of AKT Signaling and FLICE-Like Inhibitory Protein.
Y. Chen, J. Xu, N. Jhala, P. Pawar, Z. B. Zhu, L. Ma, C.-H. Byon, and J. M. McDonald (2006)
Am. J. Pathol. 169, 1833-1842
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PYK2 mediates anti-apoptotic AKT signaling in response to benzo[a]pyrene diol epoxide in mammary epithelial cells.
A. D. Burdick, I. D. Ivnitski-Steele, F. T. Lauer, and S. W. Burchiel (2006)
Carcinogenesis 27, 2331-2340
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Quercetin Induces Apoptosis via Caspase Activation, Regulation of Bcl-2, and Inhibition of PI-3-Kinase/Akt and ERK Pathways in a Human Hepatoma Cell Line (HepG2).
A. B. Granado-Serrano, M. A. Martin, L. Bravo, L. Goya, and S. Ramos (2006)
J. Nutr. 136, 2715-2721
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Rapid nongenomic actions of thyroid hormone.
Y. Hiroi, H.-H. Kim, H. Ying, F. Furuya, Z. Huang, T. Simoncini, K. Noma, K. Ueki, N.-H. Nguyen, T. S. Scanlan, et al. (2006)
PNAS 103, 14104-14109
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Overexpression of HAX-1 Protects Cardiac Myocytes From Apoptosis Through Caspase-9 Inhibition.
Y. Han, Y.-S. Chen, Z. Liu, N. Bodyak, D. Rigor, E. Bisping, W. T. Pu, and P. M. Kang (2006)
Circ. Res. 99, 415-423
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TRAIL-Mediated Apoptosis in HIV-1-Infected Macrophages Is Dependent on the Inhibition of Akt-1 Phosphorylation.
Y. Huang, N. Erdmann, H. Peng, S. Herek, J. S. Davis, X. Luo, T. Ikezu, and J. Zheng (2006)
J. Immunol. 177, 2304-2313
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A Novel Function of Plasminogen Activator Inhibitor-1 in Modulation of the AKT Pathway in Wild-type and Plasminogen Activator Inhibitor-1-deficient Endothelial Cells.
R. D. Balsara, F. J. Castellino, and V. A. Ploplis (2006)
J. Biol. Chem. 281, 22527-22536
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Determinants of Sensitivity and Resistance to Rapamycin-Chemotherapy Drug Combinations In vivo..
H.-G. Wendel, A. Malina, Z. Zhao, L. Zender, S. C. Kogan, C. Cordon-Cardo, J. Pelletier, and S. W. Lowe (2006)
Cancer Res. 66, 7639-7646
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Gene 33/RALT Is Induced by Hypoxia in Cardiomyocytes, Where It Promotes Cell Death by Suppressing Phosphatidylinositol 3-Kinase and Extracellular Signal-Regulated Kinase Survival Signaling..
D. Xu, R. D. Patten, T. Force, and J. M. Kyriakis (2006)
Mol. Cell. Biol. 26, 5043-5054
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Leptin promotes the proliferative response and invasiveness in human endometrial cancer cells by activating multiple signal-transduction pathways..
D Sharma, N K Saxena, P M Vertino, and F A Anania (2006)
Endocr. Relat. Cancer 13, 629-640
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Inhibition of Akt by the alkylphospholipid perifosine does not enhance the radiosensitivity of human glioma cells..
L. de la Pena, W. E. Burgan, D. J. Carter, M. G. Hollingshead, M. Satyamitra, K. Camphausen, and P. J. Tofilon (2006)
Mol. Cancer Ther. 5, 1504-1510
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CD86 Stimulation on a B Cell Activates the Phosphatidylinositol 3-Kinase/Akt and Phospholipase C{gamma}2/Protein Kinase C{alpha}beta Signaling Pathways..
N. W. Kin and V. M. Sanders (2006)
J. Immunol. 176, 6727-6735
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Loss of {beta}4 Integrin Subunit Reduces the Tumorigenicity of MCF7 Mammary Cells and Causes Apoptosis upon Hormone Deprivation..
G. Bon, V. Folgiero, G. Bossi, L. Felicioni, A. Marchetti, A. Sacchi, and R. Falcioni (2006)
Clin. Cancer Res. 12, 3280-3287
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Toxoplasma gondii triggers Gi-dependent PI 3-kinase signaling required for inhibition of host cell apoptosis.
L. Kim and E. Y. Denkers (2006)
J. Cell Sci. 119, 2119-2126
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Therapeutic Time Window and Dose Dependence of Neuroprotective Effects of Sodium Orthovanadate following Transient Middle Cerebral Artery Occlusion in Rats.
Y. Hasegawa, M. Morioka, S. Hasegawa, J. Matsumoto, T. Kawano, Y. Kai, S. Yano, K. Fukunaga, and J.-i. Kuratsu (2006)
J. Pharmacol. Exp. Ther. 317, 875-881
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Norepinephrine-induced oxidative stress causes PC-12 cell apoptosis by both endoplasmic reticulum stress and mitochondrial intrinsic pathway: inhibition of phosphatidylinositol 3-kinase survival pathway.
W. Mao, C. Iwai, P. C. Keng, R. Vulapalli, and C.-s. Liang (2006)
Am J Physiol Cell Physiol 290, C1373-C1384
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Induced focal adhesion kinase expression suppresses apoptosis by activating NF-{kappa}B signaling in intestinal epithelial cells.
H. M. Zhang, K. M. Keledjian, J. N. Rao, T. Zou, L. Liu, B. S. Marasa, S. R. Wang, L. Ru, E. D. Strauch, and J.-Y. Wang (2006)
Am J Physiol Cell Physiol 290, C1310-C1320
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Protein Kinase B/Akt Is Present in Activated Form throughout the Entire Replicative Cycle of {Delta}US3 Mutant Virus but Only at Early Times after Infection with Wild-Type Herpes Simplex Virus 1..
L. Benetti and B. Roizman (2006)
J. Virol. 80, 3341-3348
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Inactivation of the Akt Survival Pathway during Photoreceptor Apoptosis in the Retinal Degeneration Mouse..
C. Jomary, J. Cullen, and S. E. Jones (2006)
Invest. Ophthalmol. Vis. Sci. 47, 1620-1629
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