Commitment and Effector Phases of the Physiological Cell Death Pathway Elucidated with Respect to Bcl-2, Caspase, and Cyclin-Dependent Kinase Activities

REFERENCES

• Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan 1996. Human ICE/Ced-3 protease nomenclature. Cell 87: 171.
   PubMed Web of Science ®Google Scholar
• Ashwell, J. D., R. E. Cunningham, P. D. Noguchi, and D. Hernandez 1987. Cell growth cycle block of T cell hybridomas upon activation with antigen. J. Exp. Med. 165: 173–194.
   PubMed Web of Science ®Google Scholar
• Baxter, G. D., P. J. Smith, and M. F. Lavin 1989. Molecular changes associated with induction of cell death in a human T-cell leukemia line: putative nucleases identified as histones. Biochem. Biophys. Res. Commun. 162: 30–37.
   PubMed Web of Science ®Google Scholar
• Beyaert, R., V. J. Kidd, S. Cornelis, M. Van de Craen, G. Denecker, J. M. Lahti, R. Gururajan, P. Vandenabeele, and W. Fiers 1997. Cleavage of PITSLRE kinases by ICE/CASP-1 and CPP32/CASP-3 during apoptosis induced by tumor necrosis factor. J. Biol. Chem. 272: 11694–11697.
   PubMedGoogle Scholar
• Blomquist, J. F. Unpublished data.
   Google Scholar
• Boise, L. H., M. Gonzalez-Garcia, C. E. Postema, L. Ding, T. Lindsten, L. A. Turka, X. Mao, G. Nuñez, and C. B. Thompson 1993. bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597–608.
   PubMed Web of Science ®Google Scholar
• Boise, L. H., and C. B. Thompson 1997. Bcl-xL can inhibit apoptosis in cells that have undergone Fas-induced protease activation. Proc. Natl. Acad. Sci. USA 94: 3759–3764.
   PubMed Web of Science ®Google Scholar
• Borner, C. 1996. Diminished cell proliferation associated with the death-protective activity of Bcl-2. J. Biol. Chem. 271: 12695–12698.
   PubMed Web of Science ®Google Scholar
• Boulakia, C. A., C. Chen, F. W. H. Ng, J. G. Teodoro, P. E. Branton, D. W. Nicholson, G. G. Poirier, and G. C. Shore 1996. Bcl-2 and adenovirus E1B 19 kDa protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene 12: 529–535.
   PubMedGoogle Scholar
• Casciola-Rosen, L., D. W. Nicholson, T. Chong, K. R. Rowan, N. A. Thornberry, D. K. Miller, and A. Rosen 1996. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J. Exp. Med. 183: 1957–1964.
   PubMed Web of Science ®Google Scholar
• Chang, S. H., and D. S. Ucker. Unpublished data.
   Google Scholar
• Chen, Y.-Y., and N. Rosenberg 1992. Lymphoid cells transformed by Abelson virus require the v-abl protein-tyrosine kinase only during early G1. Proc. Natl. Acad. Sci. USA 89: 6683–6687.
   PubMedGoogle Scholar
• Chinnaiyan, A. M., K. Orth, K. O’Rourke, H. Duan, G. G. Poirier, and V. M. Dixit 1996. Molecular ordering of the cell death pathway: Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271: 4573–4576.
   PubMed Web of Science ®Google Scholar
• Datta, R., H. Kojima, D. Banach, N. J. Bump, R. V. Talanian, E. S. Alnemri, R. R. Weichselbaum, W. W. Wong, and D. W. Kufe 1997. Activation of a CrmA-insensitive, p35-sensitive pathway in ionizing radiation-induced apoptosis. J. Biol. Chem. 272: 1965–1969.
   PubMed Web of Science ®Google Scholar
• Deshmukh, M., J. Vasilakos, T. L. Deckwerth, P. A. Lampe, B. D. Shivers, Johnson E. M., Jr. 1996. Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE family proteases. J. Cell Biol. 135: 1341–1354.
   PubMed Web of Science ®Google Scholar
• Di Stasi, A. M. M., V. Gallo, M. Ceccarini, and T. C. Petrucci 1991. Neuronal fodrin proteolysis occurs independently of excitatory amino acid-induced neurotoxicity. Neuron 6: 445–454.
   PubMedGoogle Scholar
• Ellis, H. M., and H. R. Horvitz 1986. Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817–829.
   PubMed Web of Science ®Google Scholar
• Emoto, Y., Y. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, M. Robertson, T. Ghayur, W. W. Wong, R. Kamen, R. Weichselbaum, and D. Kufe 1995. Proteolytic activation of protein kinase C δ by an ICE-like protease in apoptotic cells. EMBO J. 14: 6148–6156.
   PubMed Web of Science ®Google Scholar
• Enari, M., H. Hug, and S. Nagata 1995. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 375: 78–81.
   PubMed Web of Science ®Google Scholar
• Enari, M., R. V. Talanian, W. W. Wong, and S. Nagata 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380: 723–726.
   PubMed Web of Science ®Google Scholar
• Fernandes-Alnemri, T., G. Litwack, and E. S. Alnemri 1994. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1β-converting enzyme. J. Biol. Chem. 269: 30761–30764.
   PubMed Web of Science ®Google Scholar
• Fotedar, R., J. Flatt, S. Gupta, R. L. Margolis, P. Fitzgerald, H. Messier, and A. Fotedar 1995. Activation-induced T-cell death is cell cycle dependent and regulated by cyclin B. Mol. Cell. Biol. 15: 932–942.
   PubMedGoogle Scholar
• Freeman, R. S., S. Estus, Johnson E. M., Jr. 1994. Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12: 343–355.
   PubMed Web of Science ®Google Scholar
• Galaktionov, K., X. Chen, and D. Beach 1996. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382: 511–517.
   PubMed Web of Science ®Google Scholar
• Ghayur, T., M. Hugunin, R. V. Talanian, S. Ratnofsky, C. Quinlan, Y. Emoto, P. Pandey, R. Datta, Y. Huang, S. Kharbanda, H. Allen, R. Kamen, W. Wong, and D. Kufe 1996. Proteolytic activation of protein kinase C δ by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med. 184: 2399–2404.
   PubMed Web of Science ®Google Scholar
• Harmon, J. M., M. R. Norman, B. J. Fowlkes, and E. B. Thompson 1979. Dexamethasone induces irreversible G1 arrest and death of a human lymphoid cell line. J. Cell. Physiol. 98: 267–278.
   PubMed Web of Science ®Google Scholar
• Hengartner, M. O., R. E. Ellis, and H. R. Horvitz 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356: 494–499.
   PubMed Web of Science ®Google Scholar
• Hengartner, M. O., and H. R. Horvitz 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76: 665–675.
   PubMed Web of Science ®Google Scholar
• Hoang, A. T., K. J. Cohen, J. F. Barrett, D. A. Bergstrom, and C. V. Dang 1994. Participation of cyclin A in Myc-induced apoptosis. Proc. Natl. Acad. Sci. USA 91: 6875–6879.
   PubMedGoogle Scholar
• Hockenbery, D., G. Nuñez, C. Milliman, R. D. Schreiber, and S. J. Korsmeyer 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348: 334–336.
   PubMed Web of Science ®Google Scholar
• Hooper, L. V., and J. U. Baenziger 1993. Sulfotransferase and glycosyltransferase analyses using a 96-well filtration plate. Anal. Biochem. 212: 128–133.
   PubMedGoogle Scholar
• Huang, D. C. S., S. Cory, and A. Strasser 1997. Bcl-2, Bcl-xL and adenovirus protein E1B19kD are functionally equivalent in their ability to inhibit cell death. Oncogene 14: 405–414.
   PubMed Web of Science ®Google Scholar
• Jacobson, M. D., M. Weil, and M. C. Raff 1996. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133: 1041–1051.
   PubMedGoogle Scholar
• Kaufmann, S. H. 1989. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49: 5870–5878.
   PubMed Web of Science ®Google Scholar
• Kearse, K. P., and G. W. Hart 1991. Lymphocyte activation induces rapid changes in nuclear and cytoplasmic glycoproteins. Proc. Natl. Acad. Sci. USA 88: 1701–1705.
   PubMedGoogle Scholar
• Kranenburg, O., A. J. van der Eb, and A. Zantema 1996. Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J. 15: 46–54.
   PubMed Web of Science ®Google Scholar
• Krishan, A. 1975. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J. Cell Biol. 66: 188–193.
   PubMed Web of Science ®Google Scholar
• Kuida, K., J. A. Lippke, G. Ku, M. W. Harding, D. J. Livingston, M. S.-S. Su, and R. A. Flavell 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1β converting enzyme. Science 267: 2000–2006.
   PubMed Web of Science ®Google Scholar
• Kuida, K., T. S. Zheng, S. Na, C.-Y. Kuan, D. Yang, H. Karasuyama, P. Rakic, and R. A. Flavell 1996. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384: 368–372.
   PubMed Web of Science ®Google Scholar
• Lahti, J. M., J. Xiang, L. S. Heath, D. Campana, and V. J. Kidd 1995. PITSLRE protein kinase activity is associated with apoptosis. Mol. Cell. Biol. 15: 1–11.
   PubMed Web of Science ®Google Scholar
• Liu, X., C. N. Kim, J. Pohl, and X. Wang 1996. Purification and characterization of an interleukin-1β-converting enzyme family protease that activates cysteine protease p32 (CPP32). J. Biol. Chem. 271: 13371–13376.
   PubMed Web of Science ®Google Scholar
• MacFarlane, M., K. Cain, X.-M. Sun, E. S. Alnemri, and G. M. Cohen 1997. Processing/activation of at least four interleukin-1β converting enzyme-like proteases occurs during the execution phase of apoptosis in human monocytic tumor cells. J. Cell Biol. 137: 469–479.
   PubMed Web of Science ®Google Scholar
• Margolin, N., S. A. Raybuck, K. P. Wilson, W. Chen, T. Fox, Y. Gu, and D. J. Livingston 1997. Substrate and inhibitor specificity of interleukin-1β-converting enzyme and related caspases. J. Biol. Chem. 272: 7223–7228.
   PubMed Web of Science ®Google Scholar
• Mazel, S., D. Burtrum, and H. T. Petrie 1996. Regulation of cell division cycle progression by bcl-2 expression: a potential mechanism for inhibition of programmed cell death. J. Exp. Med. 183: 2219–2226.
   PubMed Web of Science ®Google Scholar
• McCarthy, N. J., M. K. B. Whyte, C. S. Gilbert, and G. I. Evan 1997. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136: 215–227.
   PubMed Web of Science ®Google Scholar
• Meikrantz, W., S. Gisselbrecht, S. W. Tam, and R. Schlegel 1994. Activation of cyclin A-dependent protein kinases during apoptosis. Proc. Natl. Acad. Sci. USA 91: 3754–3758.
   PubMed Web of Science ®Google Scholar
• Meikrantz, W., and R. Schlegel 1996. Suppression of apoptosis by dominant negative mutants of cyclin-dependent protein kinases. J. Biol. Chem. 271: 10205–10209.
   PubMed Web of Science ®Google Scholar
• Meyerson, M., G. H. Enders, C.-L. Wu, L.-K. Su, C. Gorka, C. Nelson, E. Harlow, and L.-H. Tsai 1992. A family of human cdc2-related protein kinases. EMBO J. 11: 2909–2917.
   PubMed Web of Science ®Google Scholar
• Milligan, C. E., D. Prevette, H. Yaginuma, S. Homma, C. Cardwell, L. C. Fritz, K. J. Tomaselli, R. W. Oppenheim, and L. M. Schwartz 1995. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 15: 385–393.
   PubMed Web of Science ®Google Scholar
• Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, N. A. Munday, S. M. Raju, M. E. Smulson, T.-T. Yamin, V. L. Yu, and D. K. Miller 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37–43.
   PubMed Web of Science ®Google Scholar
• Odaka, C., and D. S. Ucker 1996. Apoptotic morphology reflects mitotic-like aspects of physiological cell death and is independent of genome digestion. Microsc. Res. Tech. 34: 267–271.
   PubMedGoogle Scholar
• Oltvai, Z. N., C. L. Milliman, and S. J. Korsmeyer 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell 74: 609–619.
   PubMed Web of Science ®Google Scholar
• Pines, J., and T. Hunter 1991. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115: 1–17.
   PubMed Web of Science ®Google Scholar
• Rao, L., D. Perez, and E. White 1996. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135: 1441–1455.
   PubMed Web of Science ®Google Scholar
• Redinbaugh, M. G., and R. B. Turley 1986. Adaptation of the bicinchoninic acid protein assay for use with micotiter plates and sucrose gradient fractions. Anal. Biochem. 153: 267–271.
   PubMed Web of Science ®Google Scholar
• Robertson, N. M., J. Zangrilli, T. Fernandes-Alnemri, P. D. Friesen, G. Litwack, and E. S. Alnemri 1997. Baculovirus P35 inhibits the glucocorticoid-mediated pathway of cell death. Cancer Res. 57: 43–47.
   PubMedGoogle Scholar
• Schlegel, J., I. Peters, S. Orrenius, D. K. Miller, N. A. Thornberry, T.-T. Yamin, and D. W. Nicholson 1996. CPP32/Apopain is a key interleukin 1β converting enzyme-like protease involved in Fas-mediated apoptosis. J. Biol. Chem. 271: 1841–1844.
   PubMed Web of Science ®Google Scholar
• Shi, L., G. Chen, D. He, D. G. Bosc, D. W. Litchfield, and A. H. Greenberg 1996. Granzyme B induces apoptosis and cyclin A-associated cyclin-dependent kinase activity in all stages of the cell cycle. J. Immunol. 157: 2381–2385.
   PubMedGoogle Scholar
• Shi, L., W. K. Nishioka, J. Th’ng, E. M. Bradbury, D. W. Litchfield, and A. H. Greenberg 1994. Premature p34cdc2 activation required for apoptosis. Science 263: 1143–1145.
   PubMed Web of Science ®Google Scholar
• Srinivasula, S. M., M. Ahmad, T. Fernandes-Alnemri, G. Litwack, and E. S. Alnemri 1996. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA 93: 14486–14491.
   PubMed Web of Science ®Google Scholar
• Strasser, A., A. W. Harris, D. C. S. Huang, P. H. Krammer, and S. Cory 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14: 6136–6147.
   PubMed Web of Science ®Google Scholar
• Susin, S. A., N. Zamzami, M. Castedo, E. Daugas, H.-G. Wang, S. Geley, F. Fassy, J. C. Reed, and G. Kroemer 1997. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 186: 25–37.
   PubMed Web of Science ®Google Scholar
• Talanian, R. V., C. Quinian, S. Trautz, M. C. Hackett, J. A. Mankovich, D. Banach, T. Ghayur, K. D. Brady, and W. W. Wong 1997. Substrate specificities of caspase family proteases. J. Biol. Chem. 272: 9677–9682.
   PubMed Web of Science ®Google Scholar
• Tewari, M., and V. M. Dixit 1995. Fas- and TNF-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 270: 3255–3360.
   PubMed Web of Science ®Google Scholar
• Tewari, M., L. T. Quan, K. O’Rourke, S. Desnoyers, Z. Zeng, D. R. Beidler, G. G. Poirier, G. S. Salvesen, and V. M. Dixit 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801–809.
   PubMed Web of Science ®Google Scholar
• Thornberry, N. A., H. G. Bull, J. R. Calaycay, K. T. Chapman, A. D. Howard, M. J. Kostura, D. K. Miller, S. M. Molineaux, J. R. Weidner, J. Aunins, K. O. Elliston, J. M. Ayala, F. J. Casano, J. Chin, G. J.-F. Ding, L. A. Egger, E. P. Gaffney, G. Limjuco, O. C. Palyha, S. M. Raju, A. M. Rolando, J. P. Salley, T.-T. Yamin, T. D. Lee, J. E. Shively, M. MacCross, R. A. Mumford, J. A. Schmidt, and M. J. Tocci 1992. A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356: 768–774.
   PubMed Web of Science ®Google Scholar
• Ucker, D. S. 1991. Death by suicide: one way to go in mammalian cellular development? New Biol. 3: 103–109.
   PubMedGoogle Scholar
• Ucker, D. S. 1997. Death and dying in the immune system. Adv. Pharmacol. 41: 179–218.
   PubMedGoogle Scholar
• Ucker, D. S., J. D. Ashwell, and G. Nickas 1989. Activation-driven T cell death I. Requirements for de novo transcription and translation and association with genome fragmentation. J. Immunol. 143: 3461–3469.
   PubMed Web of Science ®Google Scholar
• Ucker, D. S., L. D. Hebshi, J. F. Blomquist, and B. E. Torbett 1994. Physiological T cell death: susceptibility is modulated by activation, aging, and transformation, but the mechanism is constant. Immunol. Rev. 142: 273–299.
   PubMedGoogle Scholar
• Ucker, D. S., P. S. Obermiller, W. Eckhart, J. R. Apgar, N. A. Berger, and J. Meyers 1992. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol. Cell. Biol. 12: 3060–3069.
   PubMed Web of Science ®Google Scholar
• Vaux, D. L., H. L. Aguila, and I. L. Weissman 1992. Bcl-2 prevents death of factor-deprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int. Immunol. 4: 821–824.
   PubMed Web of Science ®Google Scholar
• Vaux, D. L., I. L. Weissman, and S. K. Kim 1992. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258: 1955–1957.
   PubMed Web of Science ®Google Scholar
• Wang, Z.-Q., B. Auer, L. Stingl, H. Berghammer, D. Haidacher, M. Schweiger, and E. F. Wagner 1995. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9: 509–520.
   PubMed Web of Science ®Google Scholar
• Xiang, J., D. T. Chao, and S. J. Korsmeyer 1996. Bax-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93: 14559–14563.
   PubMed Web of Science ®Google Scholar
• Xue, D., and H. R. Horvitz 1995. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377: 248–251.
   PubMed Web of Science ®Google Scholar
• Xue, D., S. Shaham, and H. R. Horvitz 1996. The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev. 10: 1073–1083.
   PubMed Web of Science ®Google Scholar
• Yang, E., J. Zha, J. Jockel, L. H. Boise, C. B. Thompson, and S. J. Korsmeyer 1995. Bad, a heterodimeric partner for Bcl-xL and Bcl-2, displaces Bax and promotes cell death. Cell 80: 285–291.
   PubMed Web of Science ®Google Scholar
• Yuan, J., S. Shaham, S. Ledoux, H. M. Ellis, and H. R. Horvitz 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75: 641–652.
   PubMed Web of Science ®Google Scholar