Apaf1 is required for mitochondrial pathways of apoptosis and brain development

Cell

Volumn 94, Issue 6, 1998, Pages 739-750

  Yoshida, Hiroki ^a,b   Kong, Young Yun ^a,b   Yoshida, Ritsuko ^a,b   Elia, Andrew J ^a,b   Hakem, Anne ^a,b   Hakem, Razqallah ^a,b   Penninger, Josef M ^a,b   Mak, Tak W ^a,b  

^a AMGEN INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CYSTEINE PROTEINASE; CYTOSKELETON PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN MATURATION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; EMBRYO; ENZYME ACTIVITY; GENE TARGETING; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; T LYMPHOCYTE;

EID: 0032544564     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81733-X     Document Type: Article

References (64)

1. Armstrong, R.C., Aja, T., Xiang, J., Gaur, S., Krebs, J.F., Hoang, K., Bai, X., Korsmeyer, S.J., Karanewsky, D.S., Fritz, L.C., and Tomaselli, K.J. (1996). Fas-induced activation of the cell death-related protease CPP32 Is inhibited by Bcl2 and by ICE family protease inhibitors. J. Biol. Chem. 271, 16850-16855.
2. Barde, Y.A. (1989). Trophic factors and neuronal survival. Neuron 2, 1525-1534.
3. Blaschke, A.J., Staley, K., and Chun, J. (1996). Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122, 1165-1174.
4. Boise, L.H., and Thompson, C.B. (1997). Bcl-x(L) can inhibit apoptosis in cells that have undergone Fas-induced protease activation. Proc. Natl. Acad. Sci. USA 94, 3759-3764.
5. Bossy-Wetzel, E., Newmeyer, D.D., and Green, D.R. (1998). Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17, 37-49.
6. Caviness, V.S., Jr., Takahashi, T., and Nowakowski, R.S. (1995). Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383.
7. Cecconi, F., Alvarez-Bolado, G., Meyer, B.I., Roth, K.A., and Gruss, P. (1998). Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, this issue, 727-737.
8. Chinnaiyan, A.M., O'Rourke, K., Lane, B.R., and Dixit, V.M. (1997). Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 275, 1122-1126.
9. Clarke, P.G., and Clarke, S. (1996). Nineteenth century research on naturally occurring cell death and related phenomena. Anat. Embryol. (Berl) 193, 81-99.
10. Ellis, H.M., and Horvitz, H.R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817-829.
11. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D. L., and Henson, P.M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
12. Fernandes-Alnemri, T., Litwack, G., and Alnemri, E.S. (1994). CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J. Biol. Chem. 269, 30761-30764.
13. Golstein, P. (1997). Controlling cell death. Science 275, 1081-1082.
14. Hakem, R., Hakem, A., Duncan, G.S., Henderson, J.T., Woo, M., Soengas, M. S., Elia, A., de la Pompa, J.L., Kägi, D., Khoo, W., Potter, J., Yoshida, R., Kaufman, S.A., Lowe, S.W., Penninger, J.M., and Mak, T.W. (1998). Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94, 339-352.
15. Hengartner, M.O., and Horvitz, H.R. (1994). C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian protooncogene bcl-2. Cell 76, 665-676.
16. Hockenbery, D., Núñez, G., Milliman, C., Schreiber, R.D., and Korsmeyer, S.J. (1990). Bcl2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348, 334-336.
17. Hofmann, K., Bucher, P., and Tschopp, J. (1997). The CARD domain: a new apoptotic signaling motif. Trends Biochem. Sci. 22, 155-156.
18. Horvitz, H.R., Sternberg, P.W., Greenwald, I.S., Fixsen, W., and Ellis, H.M. (1983). Mutations that affect neural cell lineages and cell fates during the development of the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 48(2), 453-463.
19. Hu, Y., Benedict, M.A., Wu, D., Inohara, N., and Núñez, G. (1998). Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl. Acad. Sci. USA 95, 4386-4391.
20. Hui, C.C., and Joyner, A.L. (1993). A mouse model of greig cephalo-polysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3, 241-246.
21. Jacobson, M.D., Weil, M., and Raff, M.C. (1996). Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell. Biol. 133, 1041-1051.
22. Jacobson, M.D., Weil, M., and Raff, M.C. (1997). Programmed cell death in animal development. Cell 88, 347-354.
23. Kluck, R.M., Bossy-Wetzel, E., Green, D.R., and Newmeyer, D.D. (1997). The release of cytochrome c from mitochondria: a primary site for Bcl2 regulation of apoptosis. Science 275, 1132-1136.
24. Korsmeyer, S.J. (1992). Bcl2: a repressor of lymphocyte death. Immunol. Today 13, 285-288.
25. Kroemer, G., Petit, P., Zamzami, N., Vayssiere, J.L., and Mignotte, B. (1995). The biochemistry of programmed cell death. FASEB J. 9, 1277-1287.
26. Kroemer, G., Zamzami, N., and Susin, S.A. (1997). Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
27. Kuida, K., Zheng, T.S., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P., and Flavell, R.A. (1996). Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384, 368-372.
28. Kuida, K., Haydar, T.F., Kuan, C.-Y., Gu, Y., Taya, C., Karasuyama, H., Su, M.S.-S., Rakic, P., and Flavell, R.A. (1998). Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325-337.
29. Kumar, S., Kinoshita, M., Noda, M., Copeland, N.G., and Jenkins, N.A. (1994). Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme. Genes Dev. 8, 1613-1626.
30. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S., and Wang, X. (1997a). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
31. Li, H., Bergeron, L., Cryns, V., Pasternack, M.S., Zhu, H., Shi, L., Greenberg, A., and Yuan, J. (1997b). Activation of caspase-2 in apoptosis. J. Biol. Chem. 272, 21010-21017.
32. Li, H., Zhu, H., Xu, C.-j., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
33. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
34. Medema, J.P., Scaffidi, C., Kischkel, F.C., Shevchenko, A., Mann, M., Krammer, P.H., and Peter, M.E. (1997). FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 16, 2794-2804.
35. Muzio, M., Chinnaiyan, A.M., Kischkel, F.C., O'Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J.D., Zhang, M., Gentz, R., et al. (1996). FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85, 817-827.
36. Nagata, S. (1997). Apoptosis by death factor. Cell 88, 355-365.
37. Nicholson, D.W., and Thornberry, N.A. (1997). Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
38. Oppenheim, R.W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
39. Oppenheim, R.W., Prevette, D., Yin, Q.W., Collins, F., and MacDonald, J. (1991). Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251, 1616-1618.
40. Pan, G., O'Rourke, K., and Dixit, V.M. (1998). Caspase-9, Bcl-XL, and Apaf-1 form a ternary complex. J. Biol. Chem. 273, 5841-5845.
41. Petit, P.X., Lecoeur, H., Zorn, E., Dauguet, C., Mignotte, B., and Gougeon, M.L. (1995). Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell. Biol. 130, 157-167.
42. Reed, J.C. (1994). Bcl2 and the regulation of programmed cell death. J. Cell. Biol. 124, 1-6.
43. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K.M., Krammer, P.H., and Peter, M.E. (1998). Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675-1687.
44. Sentman, C.L., Shutter, J.R., Hockenbery, D., Kanagawa, O., and Korsmeyer, S.J. (1991). bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67, 879-888.
45. Shaham, S., and Horvitz, H.R. (1996). Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev. 10, 578-591.
46. Shimizu, S., Eguchi, Y., Kamiike, W., Waguri, S., Uchiyama, Y., Matsuda, H., and Tsujimoto, Y. (1996). Bcl2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13, 21-29.
47. Shortman, K., Egerton, M., Spangrude, G.J., and Scollay, R. (1990). The generation and fate of thymocytes. Semin. Immunol. 2, 3-12.
48. Spector, M.S., Desnoyers, S., Hoeppner, D.J., and Hengartner, M.O. (1997). Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature 385, 653-656.
49. Srinivasula, S.M., Ahmad, M., Fernandes-Alnemri, T., Litwack, G., and Alnemri, E.S. (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.
50. Surh, C.D., and Sprent, J. (1994). T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372, 100-103.
51. Susin, S.A., Zamzami, N., Castedo, M., Daugas, E., Wang, H.G., Geley, S., Fassy, F., Reed, J.C., and Kroemer, G. (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.
52. Takahashi, T., Nowakowski, R.S., and Caviness, V.S., Jr. (1995). The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046-6057.
53. Takayama, S., Sato, T., Krajewski, S., Kochel, K., Irie, S., Millan, J. A., and Reed, J.C. (1995). Cloning and functional analysis of BAG-1: a novel Bcl2-binding protein with anti-cell death activity. Cell 80, 279-284.
54. Thornberry, N.A. (1998). Caspases: key mediators of apoptosis. Chem. Biol. 5, R97-R103.
55. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. (1982). Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951.
56. Weller, M., Schulz, J.B., Wullner, U., Loschmann, P.A., Klockgether, T., and Dichgans, J. (1997). Developmental and genetic regulation of programmed neuronal death. J. Neural. Transm. Suppl. 50, 115-123.
57. Woo, M., Hakem, R., Soengas, M.S., Duncan, G.S., Shahinian, A., Kägi, D., Hakem, A., McCurrach, M., Khoo, W., Kaufman, S.A., et al. (1998). Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev. 12, 806-819.
58. Wu, D., Wallen, H.D., Inohara, N., and Núñez, G. (1997a). Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J. Biol. Chem. 272, 21449-21454.
59. Wu, D., Wallen, H.D., and Núñez, G. (1997b). Interaction and regulation of subcellular localization of CED-4 by CED-9. Science 275, 1126-1129.
60. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng, T. I., Jones, D.P., and Wang, X. (1997). Prevention of apoptosis by Bcl2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
61. Yoshida, H., Nishina, H., Takimoto, H., Marengère, L.E., Wakeham, A.C., Bouchard, D., Kong, Y.Y., Ohteki, T., Shahinian, A., Bachmann, M., et al. (1998). The transcription factor NF-ATc1 regulates lymphocyte proliferation and Th2 cytokine production. Immunity 8, 115-124.
62. Yuan, J., Shaham, S., Ledoux, S., Ellis, H.M., and Horvitz, H.R. (1993). The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75, 641-652.
63. Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S.A., Petit, P.X., Mignotte, B., and Kroemer, G. (1995). Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182, 367-377.
64. Zou, H., Henzel, W.J., Liu, X., Lutschg, A., and Wang, X. (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405-413.