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© The Rockefeller University Press, 0021-9525/1999//281 $5.00
The Journal of Cell Biology, Volume 144, Number 2, , 1999 281-292

Ordering the Cytochrome c–initiated Caspase Cascade: Hierarchical Activation of Caspases-2, -3, -6, -7, -8, and -10 in a Caspase-9–dependent Manner

Elizabeth A. Slee^*, Mary T. Harte^*, Ruth M. Kluck, Beni B. Wolf, Carlos A. Casiano, Donald D. Newmeyer, Hong-Gang Wang^||, John C. Reed^||, Donald W. Nicholson^¶, Emad S. Alnemri^**, Douglas R. Green, and Seamus J. Martin^*

^* Molecular Cell Biology Laboratory, Department of Biology, National University of Ireland, Maynooth, Co. Kildare, Ireland; Division of Cellular Immunology, La Jolla Institute for Allergy and Immunology, San Diego, California 92121; Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, California 92037; ^|| The Burnham Institute, La Jolla, California 92037; ^¶ Departments of Biochemistry and Molecular Biology, Merck Frosst Centre for Therapeutic Research, Pointe Claire-Dorval, Quebec, H9R 4P8, Canada; and ^** Center for Apoptosis Research and The Kimmel Cancer Institute, Jefferson Medical College, Philadelphia, Pennsylvania 19107

Exit of cytochrome c from mitochondria into the cytosol has been implicated as an important step in apoptosis. In the cytosol, cytochrome c binds to the CED-4 homologue, Apaf-1, thereby triggering Apaf-1–mediated activation of caspase-9. Caspase-9 is thought to propagate the death signal by triggering other caspase activation events, the details of which remain obscure. Here, we report that six additional caspases (caspases-2, -3, -6, -7, -8, and -10) are processed in cell-free extracts in response to cytochrome c, and that three others (caspases-1, -4, and -5) failed to be activated under the same conditions. In vitro association assays confirmed that caspase-9 selectively bound to Apaf-1, whereas caspases-1, -2, -3, -6, -7, -8, and -10 did not. Depletion of caspase-9 from cell extracts abrogated cytochrome c–inducible activation of caspases-2, -3, -6, -7, -8, and -10, suggesting that caspase-9 is required for all of these downstream caspase activation events. Immunodepletion of caspases-3, -6, and -7 from cell extracts enabled us to order the sequence of caspase activation events downstream of caspase-9 and reveal the presence of a branched caspase cascade. Caspase-3 is required for the activation of four other caspases (-2, -6, -8, and -10) in this pathway and also participates in a feedback amplification loop involving caspase-9.

Key Words: Apaf-1 • apoptosis • caspases • cell-free • cytochrome c

Abbreviations used in this paper: CEB, cell extract buffer; ES, embryonic stem.

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• Raina, D., Pandey, P., Ahmad, R., Bharti, A., Ren, J., Kharbanda, S., Weichselbaum, R., Kufe, D. (2005). c-Abl Tyrosine Kinase Regulates Caspase-9 Autocleavage in the Apoptotic Response to DNA Damage. J. Biol. Chem. 280: 11147-11151 [Abstract] [Full Text]  
• Yang, J.-H., Le, W.-D., Basinger, S. F., Wu, S. M., Yang, C.-y. (2005). Mechanisms of Apoptosis in Human Retinal Pigment Epithelium Induced by TNF-{alpha} in Conditions of Heavy Metal Ion Deficiency. IOVS 46: 1039-1046 [Abstract] [Full Text]  
• Park, K.-T., Mitchell, K. A., Huang, G., Elferink, C. J. (2005). The Aryl Hydrocarbon Receptor Predisposes Hepatocytes to Fas-Mediated Apoptosis. Mol. Pharmacol. 67: 612-622 [Abstract] [Full Text]  
• Adrain, C., Murphy, B. M., Martin, S. J. (2005). Molecular Ordering of the Caspase Activation Cascade Initiated by the Cytotoxic T Lymphocyte/Natural Killer (CTL/NK) Protease Granzyme B. J. Biol. Chem. 280: 4663-4673 [Abstract] [Full Text]  
• Holubec, H., Payne, C. M., Bernstein, H., Dvorakova, K., Bernstein, C., Waltmire, C. N., Warneke, J. A., Garewal, H. (2005). Assessment of Apoptosis by Immunohistochemical Markers Compared to Cellular Morphology in Ex Vivo-stressed Colonic Mucosa. J. Histochem. Cytochem. 53: 229-235 [Abstract] [Full Text]  
• Fang, Y., Choi, D., Searles, R. P., Mathers, W. D. (2005). A Time Course Microarray Study of Gene Expression in the Mouse Lacrimal Gland after Acute Corneal Trauma. IOVS 46: 461-469 [Abstract] [Full Text]  
• Kim, J.-E., Tannenbaum, S. R. (2004). Insulin Regulates Cleavage of Procaspase-9 via Binding of X Chromosome-Linked Inhibitor of Apoptosis Protein in HT-29 Cells. Cancer Res. 64: 9070-9075 [Abstract] [Full Text]  
• Sinicrope, F. A., Penington, R. C., Tang, X. M. (2004). Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand-Induced Apoptosis Is Inhibited by Bcl-2 but Restored by the Small Molecule Bcl-2 Inhibitor, HA 14-1, in Human Colon Cancer Cells. Clin. Cancer Res. 10: 8284-8292 [Abstract] [Full Text]  
• Peng, J.-M., Liang, S.-M., Liang, C.-M. (2004). VP1 of Foot-and-Mouth Disease Virus Induces Apoptosis via the Akt Signaling Pathway. J. Biol. Chem. 279: 52168-52174 [Abstract] [Full Text]  
• Park, S.-J., Wu, C.-H., Gordon, J. D., Zhong, X., Emami, A., Safa, A. R. (2004). Taxol Induces Caspase-10-dependent Apoptosis. J. Biol. Chem. 279: 51057-51067 [Abstract] [Full Text]  
• Yang, J.-Y., Michod, D., Walicki, J., Murphy, B. M., Kasibhatla, S., Martin, S. J., Widmann, C. (2004). Partial Cleavage of RasGAP by Caspases Is Required for Cell Survival in Mild Stress Conditions. Mol. Cell. Biol. 24: 10425-10436 [Abstract] [Full Text]  
• Paasch, U., Sharma, R. K., Gupta, A. K., Grunewald, S., Mascha, E. J., Thomas, A. J. Jr, Glander, H.-J., Agarwal, A. (2004). Cryopreservation and Thawing Is Associated with Varying Extent of Activation of Apoptotic Machinery in Subsets of Ejaculated Human Spermatozoa. Biol. Reprod. 71: 1828-1837 [Abstract] [Full Text]  
• Damiano, J. S., Newman, R. M., Reed, J. C. (2004). Multiple Roles of CLAN (Caspase-Associated Recruitment Domain, Leucine-Rich Repeat, and NAIP CIIA HET-E, and TP1-Containing Protein) in the Mammalian Innate Immune Response. J. Immunol. 173: 6338-6345 [Abstract] [Full Text]  
• Crow, M. T., Mani, K., Nam, Y.-J., Kitsis, R. N. (2004). The Mitochondrial Death Pathway and Cardiac Myocyte Apoptosis. Circ. Res. 95: 957-970 [Abstract] [Full Text]  
• Tezel, G., Yang, X. (2004). Caspase-Independent Component of Retinal Ganglion Cell Death, In Vitro. IOVS 45: 4049-4059 [Abstract] [Full Text]  
• Liang, H., Salinas, R. A., Leal, B. Z., Kosakowska-Cholody, T., Michejda, C. J., Waters, S. J., Herman, T. S., Woynarowski, J. M., Woynarowska, B. A. (2004). Caspase-mediated apoptosis and caspase-independent cell death induced by irofulven in prostate cancer cells. Molecular Cancer Therapeutics 3: 1385-1396 [Abstract] [Full Text]  
• Huang, M.-B., Jin, L. L., James, C. O., Khan, M., Powell, M. D., Bond, V. C. (2004). Characterization of Nef-CXCR4 Interactions Important for Apoptosis Induction. J. Virol. 78: 11084-11096 [Abstract] [Full Text]  
• Svingen, P. A., Loegering, D., Rodriquez, J., Meng, X. W., Mesner, P. W. Jr., Holbeck, S., Monks, A., Krajewski, S., Scudiero, D. A., Sausville, E. A., Reed, J. C., Lazebnik, Y. A., Kaufmann, S. H. (2004). Components of the Cell Death Machine and Drug Sensitivity of the National Cancer Institute Cell Line Panel. Clin. Cancer Res. 10: 6807-6820 [Abstract] [Full Text]  
• Starenki, D. V., Namba, H., Saenko, V. A., Ohtsuru, A., Maeda, S., Umezawa, K., Yamashita, S. (2004). Induction of Thyroid Cancer Cell Apoptosis by a Novel Nuclear Factor {kappa}B Inhibitor, Dehydroxymethylepoxyquinomicin. Clin. Cancer Res. 10: 6821-6829 [Abstract] [Full Text]  

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