HAC-1, a Drosophila homolog of APAF-1 and CED-4, functions in developmental and radiation-induced apoptosis

Molecular Cell

Volumn 4, Issue 5, 1999, Pages 745-755

  Zhou, Lei ^a   Song, Zhiwei ^a   Tittel, Jan ^a   Steller, Hermann ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; PROTEASE ACTIVATING FACTOR 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; DNA SEQUENCE; DROSOPHILA; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IRRADIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

EID: 0033231548     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80385-8     Document Type: Article

References (95)

1. Abrams, J.M., White, K., Fessier, L.I., and Steller, H. (1993). Programmed cell death during Drosophila embryogenesis. Development 777, 29-43.
2. Berge, C., and Karlin, S. (1997). Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94.
3. Bergmann, A., Agapite, J., McCall, K., and Steller, H. (1998a). The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95, 331-341.
4. Bergmann, A., Agapite, J., and Steller, H. (1998b). Mechanisms and control of programmed cell death in invertebrates. Oncogene 77, 3215-3223.
5. Cecconi, F., Alvarez-Bolado, G., Meyer, B.I., Roth, K.A., and Gruss, P. (1998). Apafl (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727-737.
6. The C. elegans sequencing consortium (1998). Genome sequence fo the nematode C. elegans: a plate form for investigating biology. Science 282, 2012-2018.
7. Chen, P., Nordstrom, W., Gish, B., and Abrams, J.M. (1996). grim, a novel cell death gene in Drosophila. Genes Dev. 70, 1773-1782.
8. Chen, P., Rodriguez, A., Erskine, R., Thach, T., and Abrams, J.M. (1998). Dredd, a novel effector of the apoptosis activators reaper, grim, and hid in Drosophila. Dev. Biol. 207, 202-216.
9. 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.
10. Claveria, C., Albar, J.P., Serrano, A., Buesa, J.M., Barbero, J.L., Martínez-A, C., and Torres, M. (1998). Drosophila grim induces apoptosis in mammalian cells. EMBO J. 77, 7199-7208.
11. Deveraux, Q.L., and Reed, J.C. (1999). IAP family proteins-suppressors of apoptosis. Genes Dev. 73, 239-252.
12. Dorstyn, L., Colussi, P.A., Quinn, L.M., Richardson, H., and Kumar, S. (1999). DRONC, an ecdysone-inducible Drosophila caspase. Proc. Natl. Acad. Sci. USA 96, 4307-4312.
13. Draizen, T., Ewer, J., and Robinow, S. (1999). Genetic and hormonal regulation of the death of peptidergic neurons in the Drosophila central nervous system. J. Neurobiol. 38, 455-465.
14. Ellis, H.M., and Horvitz, H.R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817-829.
15. Ellis, R.E., Yuan, J., and Horvitz, H.R. (1991). Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698.
16. Evans, E.K., Kuwana, T., Strum, S.L., Smith, J.J., Newmeyer, D.D., and Kornbluth, S. (1997). Reaper-induced apoptosis in a vertebrate system. EMBO J. 76, 7372-7381.
17. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 397, 806-811.
18. Franc, N.C., Heitzler, P., Ezekowitz, R.A.B., and White, K. (1999). Requirement for croquemort in phagocytosis of apoptotic Cells in Drosophila. Science 284, 1991-1994.
19. Fraser, A.G., and Evan, G.I. (1997). Identification of a Drosophila melanogaster ICE/CED-3-related protease, drICE. EMBO J. 76, 2805-2813.
20. Green, D.R., and Reed, J.C. (1998). Mitochondria and apoptosis. Science 281, 1309-1312.
21. Grether, M.E., Abrams, J.M., Agapite, J., White, K., and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708.
22. Grundy, W.N., Bailey, T.L., Elkan, C.P., and Baker, M.E. (1997). MetaMEME: motif-based hidden Markov models of protein families. Comput. Appl. Biosci. 73, 397-406.
23. Haining, W.N., Carboy-Newcomb, C., Wei, C.L., and Steller, H. (1999). The proapoptotic function of Drosophila Hid is conserved in mammalian cells. Proc. Natl. Acad. Sci. USA 96, 4936-4941.
24. Hay, B.A., Wolff, T., and Rubin, G.M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 720, 2121-2129.
25. Hay, B.A., Wassarman, D.A., and Rubin, G.M. (1995). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
26. Hengartner, M.O. (1996). Programmed cell death in invertebrates. Curr. Opin. Genet. Dev. 6, 34-38.
27. Hengartner, M.O., and Horvitz, H.R. (1994a). C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian protooncogene bcl-2. Cell 76, 665-676.
28. Hengartner, M.O., and Horvitz, H.R. (1994b). Programmed cell death in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 4, 581-586.
29. Hengartner, M.O., Ellis, R.E., and Horvitz, H.R. (1992). Caenorhabditis elegansgene ced-9 protects cells from programmed cell death. Nature 356, 494-499.
30. Horvitz, H.R. (1999). Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res. (Suppl.) 59, 1701s-1706s.
31. Hu, Y., Ding, L., Spenser, D.M., and Nunez, G. (1998). WD-40 repeat region regulates Apaf-1 self-association and Caspase 9 activation. J. Biol. Chem. 273, 33489-33494.
32. Hu, Y., Benedict, M.A., Ding, L., and Nuñez, G. (1999). Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis. EMBO J. 18, 3586-3595.
33. Jacobson, M.D., Weil, M., and Raff, M.C. (1997). Programmed cell death in animal development. Cell 88, 347-354.
34. Jiang, C., Baehrecke, E.H., and Thummel, C.S. (1997). Steroid regulated programmed cell death during Drosophila metamorphosis. Development 724, 4673-4683.
35. Kanuka, H., Sawamoto, K., Inohara, N., Matsuno, K., Okano, H., and Miura, M. (1999). Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-related caspase activator. Mol. Cell 4, this issue, 757-769.
36. Kennerdell, J.R., and Carthew, R.W. (1998). Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95, 1017-1026.
37. L inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res. 57, 3115-3120.
38. Kimmerly, W., Stultz, S., Lewis, S., Lewis, K., Lustre, V., Romero, R., Benke, J., Sun, D., Shirley, G., Martin, C., and Palazzolo, M. (1996). A P1-based physical map of the Drosophila euchromatic genome. Genome Res. 6, 414-430.
39. 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 Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
40. Kurada, P., and White, K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95, 319-329.
41. Li, P., Nijhawan, D., Budihardjo, L., Srinivasula, S.M., Ahmad, M., Alnemri, E.S., and Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade. Cell 97, 479-489.
42. Liu, X., Kim, C.N., Yang, J., Jemmerson, R., and Wang, X. (1996). Induction of apoptotic program in cell-free extracts: requirement of dATP and cytochrome c. Cell 86, 147-157.
43. MacCorkle, R.A., Freeman, K.W., and Spencer, D.M. (1998). Synthetic activation of caspases: artificial death switches. Proc. Natl. Acad. Sci. USA 95, 3655-3660.
44. McCall, K., and Steller, H. (1997). Facing death in the fly: genetic analysis of apoptosis in Drosophila. Trends Genet. 73, 222-226.
45. McCarthy, J.V., and Dixit, V.M. (1998). Apoptosis induced by Drosophila reaper and grim in a human system. Attenuation by inhibitor of apoptosis proteins (clAPs). J. Biol. Chem. 23, 24009-24015.
46. Meier, P., and Evan, G. (1998). Dying like flies. Cell 95, 295-298.
47. Misquitta, L., and Paterson, B.M. (1999). Targeted disuption of gene function in Drosophila by RNA interference (RNA-i): a role for nautilus in embryonic somatic muscle formation. Proc. Natl. Acad. Sci. USA 96, 1451-1456.
48. Muzio, M., Stockwell, B.R., Stennicke, H.R., Salvesen, G.S., and Dixit, V.M. (1998). An induced proximity model for caspase-8 activation. J. Biol. Chem. 273, 2926-2930.
49. Nagata, S. (1997). Apoptosis by death factor. Cell 88, 355-365.
50. Nassif, C., Daniel, A., Lengyel, J., and Hartenstein, V. (1998). The role of morphogenetic cell death during Drosophila embryonic head development. Development 797, 170-186.
51. Nicholson, D.W., and Thornberry, N.A. (1997). Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
52. Nordstrom, W., Chen, P., Steller, H., and Abrams, J.M. (1996). Activation of the reaper gene during ectopic cell killing in Drosophila. Dev. Biol. 180, 213-226.
53. O'Neill, E.M., Rebay, I., Tijan, R., and Rubin, G.M. (1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137-147.
54. Pettmann, B., and Henderson, C.E. (1998). Neuronal cell death. Neuron 20, 633-647.
55. Raff, M.C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
56. Raff, M. (1998). Cell suicide for beginners. Nature 396, 119-122.
57. Raff, M.C., Barres, B.A., Burne, J.F., Coles, H.S., Ishizaki, Y., and Jacobson, M.D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695-700.
58. Reed, J.C. (1997a). Cytochromec: can't live with it-can't live without it. Cell 97, 559-562.
59. Reed, J.C. (1997b). Double identity for proteins of the Bcl-2 family. Nature 387, 773-776.
60. Rich, T., Watson, C.J., and Wyllie, A. (1999). Apoptosis: the germs of death. Nat. Cell Biol. 7, E69-E71.
61. Robinow, S., Draizen, T.A., and Truman, J.W. (1997). Genes that induce apoptosis: transcriptional regulation in identified, doomed neurons of the Drosophila CNS. Dev. Biol. 790, 206-213.
62. Rodriguez, A., Oliver, H., Zou, H., Chen, P., Wang, X., and Abrams, J.M. (1999). Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell. Biol. 7, 272-280.
63. Rupp, R.A.W., Snider, L., and Weintraub, H. (1994). Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8, 1311-1323.
64. Salvesen, G.S., and Dixit, V.M. (1997). Caspases: intracellular signaling by proteolysis. Cell 97, 443-446.
65. Seshagiri, S., and Miller, L.K. (1997). Caenorhabditis elegans CED-4 stimulates CED-3 processing and CED-3-induced apoptosis. Curr. Biol. 7, 455-460.
66. Shaham, S., and Horvitz, H.R. (1996). An alternatively spliced C. elegans ced-4 RNA encodes a novel cell death inhibitor. Cell 86, 201-208.
67. Song, Z., McCall, K., and Steller, H. (1997). DCP-1, a Drosophila cell death protease essential for development. Science 275, 536-540.
68. Spradling, A.C., Stern, D., Kiss, I., Roote, J., Laverty, T., and Rubin, G.M. (1995). Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92, 10824-10830.
69. Steller, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445-1449.
70. Steller, H., and Grether, M.E. (1994). Programmed cell death in Drosophila. Neuron 73, 1269-1274.
71. Takahashi, A., and Earnshaw, W.C. (1996). ICE-related proteases in apoptosis. Curr. Opin. Genet. Dev. 6, 50-55.
72. Thompson, C.B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
73. Thornberry, N.A., Rano, T.A., Peterson, E.P., Rasper, D.M., Timkey, T., Garcia-Calvo, M., Houtzager, V.M., Nordstrom, P.A., Roy, S., Vaillancourt, J.P. et al. (1997). A combinatorial approach defines specificities of members of the caspase family and granzyme B. J. Biol. Chem. 272, 17907-17911.
74. Thummel, C.S., Boulet, A.M., and Lipshitz, H.D. (1988). Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74, 445-456.
75. Uren, A., Coulson, E., and Vaux, D. (1998). Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRs) in virus, nematodes, vertebrates and yeasts. Trends Biochem. Sci. 23, 159-162.
76. Van der Biezen, E.A., and Jones, J.D.G. (1998). The NB-ARC domain: a novel signaling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226-R227.
77. Varkey, J., Chen, P., Jemmerson, R., and Abrams, J.M. (1999). Altered cytochrome c display precedes apoptotic cell death in Drosophila. J. Cell Biol. 744, 701-710.
78. Vaux, D.L., and Korsmeyer, S.J. (1999). Cell death in development. Cell 96, 245-254.
79. Vucic, D., Kaiser, W.J., Harvey, A.J., and Miller, L.K. (1997a). Inhibition of Reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc. Natl. Acad. Sci. USA 94, 10183-10188.
80. Vucic, D., Seshagiri, S., and Miller, L.K. (1997b). Characterization of Reaper-and FADD-induced apoptosis in a lepidopteran cell line. Mol. Cell. Biol. 77, 667-676.
81. Vucic, D., Kaiser, W.J., and Miller, L.K. (1998). Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol. Cell. Biol. 18, 3300-3309.
82. Wang, S.L., Hawkins, C.J., Yoo, S.J., Müller, H.-A.J., and Hay, B.A. (1999). The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell. 98, 453-463.
83. Weil, M., Jacobson, M.D., Coles, H.S., Davies, T.J., Gardner, R.L., Raff, K.D., and Raff, M.C. (1996). Constitutive expression of the machinery for programmed cell death. J. Cell Biol. 733, 1053-1059.
84. White, E. (1996). Life, death, and the pursuit of apoptosis. Genes Dev. 70, 1-15.
85. White, K., Grether, M.E., Abrams, J.M., Young, L., Farrell, K., and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
86. White, K., Tahaoglu, E., and Steller, H. (1996). Cell killing by the Drosophila gene reaper. Science 277, 805-807.
87. Wu, D., Wallen, H.D., Inohara, N., and Nuñez, G. (1997). Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J. Biol. Chem. 272, 21449-21454.
88. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng, T.-I., Jones, O.P., and Wang, X. (1997). Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
89. Yang, X., Chang, H.Y., and Baltimore, D. (1998). Autoproteolytic activation of pro-caspases by oligomerization. Mol. Cell 1, 319-325.
90. Yoshida, H., Kong, Y.-Y., Yoshida, R., Elia, A.J., Hakem, A., Hakem, R., Penninger, J.M., and Mak, T.W. (1998). Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739-750.
91. Yuan, J., and Horvitz, H.R. (1992). The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 776, 309-320.
92. 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-1β-converting enzyme. Cell 75, 641-652.
93. Zhou, L., Hashimi, H., Schwanz, L.M., and Nambu, J.R. (1995). Programmed cell death in the Drosophila central nervous system midline. Curr. Biol. 5, 784-790.
94. Zhou, L., Schnitzler, A., Agapite, J., Schwanz, L.M., Steller, H., and Nambu, J.R. (1997). Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system cells. Proc. Natl. Acad. Sci. USA 94, 5131-5136.
95. 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.