Apoptosome: A platform for the activation of initiator caspases

Cell Death and Differentiation

Volumn 14, Issue 1, 2007, Pages 56-65

  Bao, Q ^a   Shi, Y ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CAENORHABDITIS ELEGANS PROTEIN; CASPASE 10; CASPASE 2; CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 8; CASPASE 9; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYSTEINE PROTEINASE; CYTOCHROME C; DEOXYADENOSINE TRIPHOSPHATE; DROSOPHILA PROTEIN; ENZYME PRECURSOR; FAS ANTIGEN; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN CED; PROTEIN P53; TUMOR NECROSIS FACTOR;

APOPTOSIS; CAENORHABDITIS ELEGANS; CRYOELECTRON MICROSCOPY; DIMERIZATION; DROSOPHILA; ENZYME ACTIVATION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC CODE; HUMAN; MAMMAL CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; APOPTOSOMES; CASPASES, INITIATOR; DIMERIZATION; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 33845501864     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4402028     Document Type: Review

References (80)

1. Danial NN, Korsmeyer SJ. Cell death: Critical control points. Cell 2004; 116: 205-219.
2. Peter ME, Krammer PH. The CD95(AP0-1/Fas) DISC and beyond. Cell Death Differ 2003; 10: 26-35.
3. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15: 2922-2933.
4. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004; 5: 897-907.
5. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene Ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993; 75: 641-652.
6. Xue D, Shaham S, Horvitz HR. 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 1996; 10: 1073-1083.
7. Shi Y. Mechanisms of caspase inhibition and activation during apoptosis. Mot Cell 2002; 9: 459-470.
8. Salvesen GS, Dixit VM. Caspase activation: The induced-proximity model. Proc Natl Acad Sci USA 1999; 96: 10964-10967.
9. Fuentes-Prior P, Salvesen GS. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 2004; 384: 201-232.
10. Stennicke HR, Deveraux QL, Humke EW, Reed JC, Dixit VM, Salvesen GS. Caspase-9 can be activated without proteolytic processing. J Biol Chem 1999; 274: 8350-8362.
11. Srinivasula SM, Saleh A, Hedge R, Datta P, Shiozaki E, Chai J et al. A conserved XIAP- interaction motif in caspase-9 and Smac/DIABLO mediates opposing effects on caspase activity and apoptosis. Nature 2001; 409: 112-116.
12. Shi Y. Caspase activation: Revisiting the induced proximity model. Cell 2004; 117: 855-858.
13. Tinel A, Tschopp J. The PIDDosome, a protein complex implicated in activation of caspase-2 in response to genotoxic stress. Science 2004; 304: 843-846.
14. Kischkel FC, Hellbardt S, Behrmann I, Gemer M, Pawlita M, Krammer PH et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995; 14: 5579-5588.
15. Zou H, Li Y, Liu X, Wang X. An APAF-1-cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999; 274: 11549-11556.
16. Saleh A, Srinivasula SM, Acharya S, Fishel R, Alnemri ES. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J Biol Chem 1999; 274: 17941-17945.
17. Hu Y, Benedict MA, Ding L, Nunez G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis. EMBO J 1999; 18: 3586-3595.
18. Rodriguez J, Lazebnik Y. Caspase-9 and Apaf-1 form an active holoenzyme. Genes Dev 1999; 13: 3179-3184.
19. Cain K, Brown DG, Langlais C, Cohen GM. caspase activation involves the formation of the aposome, a large (∼ 700 kDa) caspase-activating complex. J Biol Chem 1999; 274: 22686-22692.
20. Rodriguez A, Oliver H, Zou H, Chen P, Wang X, Abrams JM. Dark is a drosophila homolog of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat Cell Biol 1999; 1: 272-279.
21. Zhou L, Song Z, Tittel J, Steller H. HAC-1, a Drosophila homolog of Apaf-1 and CED-4 functions in developmental and radiation-induced apoptosis. Mol Cell 1999; 4: 745-755.
22. Kanuka H, Sawamoto K, Inohara N, Matsuno K, Okano H, Miura M. Control of the cell death pathway by Dapaf-1, a Drosophita Apaf-1/CED-4-related caspase activator. Mol Cell 1999; 4: 757-769.
23. Lettre G, Hengartner MO. Developmental apoptosis in C. elegans: A complex CEDnario. Nat Rev Mol Cell Biol 2006; 7: 97-108.
24. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 2002; 297: 1352-1354.
25. Schweizer A, Briand C, Grutter MG. Crystal structure of caspase-2, apical initiator of the intrinsic apoptotic pathway. J Biol Chem 2003; 278: 42441-42447.
26. Baliga BC, Read SH, Kumar S. The biochemical mechanism of caspase-2 activation. Cell Death Differ 2004; 11: 1234-1241.
27. Read SH, Baliga BC, Ekert PG, Vaux DL, Kumar S. A novel Apaf-1-independent putative caspase-2 activation complex. J Cell Biol 2002; 159: 739-745.
28. Chou JJ, Matsuo H, Duan H, Wagner G. Solution structure of the RAIDD CARD and Model for CARD/CARD interaction in Caspase-2 and Caspase-9 recruitment. Cell 1998; 94: 171-180.
29. Park HH, Wu H. Crystal structure of RAIDD death domain implicates potential mechanism of PIDDosome assembly. J Mol Biol 2006; 357: 358-364.
30. Chinnaiyan AM, Tepper CG, Seldin MF, O'Rourke K, Kischkel FC, Hellbardt S et al. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J Biol Chem 1996; 271: 4961-4965.
31. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death - inducing signaling complex. Cell 1996; 85: 817-827.
32. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1 and TNF receptor-induced cell death, Cell 1996; 85: 803-815.
33. Yan N, Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 2005; 21: 35-56.
34. Huang B, Eberstadt M, Olejniczak ET, Meadows RP, Fesik SW. NMR structure and mutagenesis of the Fas (APO-1/CD95) death domain. Nature 1996; 384: 638-641.
35. Berglund H, Olerenshaw D, Sankar A, Federwisch M, McDonald NO, Driscoll PC. The three-dimensional solution structure and dynamic properties of the human FADD death domain. J Mol Biol 2000; 302: 171-188.
36. Jeong EJ, Bang S, Lee TH, Park YI, Sim WS, Kim KS. The solution structure of FADD death domain. Structural basis of death domain interactions of Fas and FADD. J Biol Chem 1999; 274: 16337-16342.
37. Eberstadt M, Huang B, Chen Z, Meadows RP, Ng S-C, Zheng L et al. NMR structure and mutagenesis of the FADD (Mort1) death-effector domain. Nature 1998; 392: 941-945.
38. Sandu C, Gavathiotis E, Huang T, Wegorzewska I, Wemer MH. A mechanism for death receptor discrimination by death adaptors. J Biol Chem 2005; 280: 31974-31980.
39. Hill JM, Morisawa G, Kim T, Huang T, Wei Y, Wei Y et al. Identification of an expanded binding surface on the FADD death domain responsible for interaction with CD95/Fas. J Biol Chem 2004; 279: 1474-1481.
40. Carrington PE, Sandu C, Wei Y, Hill JM, Morisawa G, Huang T et al. The structure of FADD and its mode of interaction with procaspase-8. Mol Cell 2006; 22: 599-610.
41. Li FY, Jeffrey PD, Yu JW, Shi Y. Crystal structure of a viral FLIP: insights into FLIP-mediated inhibition of death receptor signaling. J Biol Chem 2005; 281: 2960-2968.
42. Yang JK, Wang L, Zheng L, Wan F, Ahmed M, Lenardo MJ et al. Crystal structure of MC159 reveals molecular mechanism of DISC assembly and FLIP inhibition. Mol Cell 2005; 20: 939-949.
43. Sandu C, Morisawa G, Wegorzewska I, Huang T, Arechiga AF, Hill JM et al. FADD self-association is required for stable interaction with an activated death receptor. Cell Death Differ 2006 2006 May 19 (Epub ahead of print).
44. Donepudi M, Mac Sweeney A, Briand C, Grutter MG. Insights into the regulatory mechanism for caspase-8 activation. Mol Cell 2003; 11: 543-549.
45. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM et al. A unified model for apical caspase activation. Mol Cell 2003; 11: 529-541.
46. Chang DW, Xing Z, Pan Y, Algeciras-Schimnich A, Bamhart BC, Yaish-Ohad S et al. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J 2002; 21: 3704-3714.
47. Micheau O, Thome M, Schneider P, Holler N, Tschopp J, Nicholson DW et al. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 2002; 277: 45162-45171.
48. Boatright KM, Deis C, Denault JB, Sutherlin DP, Salvesen GS. Activation of caspases-8 and -10 by FLIP(L). Biochem, J 2004; 382: 651-657.
49. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptosis program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 1996; 86: 147-157.
50. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90: 405-413.
51. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmed M, Alnemri ES et al. Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9 Complex Initiates an Apoptotic Protease Cascade. Cell 1997; 91: 479-019.
52. Qin H, Srinivasula SM, Wu G, Fernandes-Alnemri T, Alnemri ES, Shi Y. Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature 1999; 399: 547-555.
53. Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y. Structure of the apoptotic protease activating factor 1 bound to ADP. Nature 2005; 434: 926-933.
54. Acehan D, Jiang X, Morgan DG, Hauser JE, Wang X, Akey CW. Three-dimensional structure of the apoptosome: Implications for assembly, procaspase-9 binding and activation. Mol Cell 2002; 9: 423-432.
55. Yu X, Acehan D, Menetret JF, Booth CR, Ludtke SJ, Riedi SJ et al. A structure of the human apoptosome at 12.8 A resolution provides insights into this cell death platform. Structure 2005; 13: 1725-1735.
56. Kim HE, Du F, Fang M, Wang X. Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1. Proc Natl Acad Sci USA 2005; 102: 17545-17550.
57. Jiang X, Kim HE, Shu H, Zhao Y, Zhang H, Kotron J et al. Distinctive roles of PHAP proteins and prothymosin-alpha in a death regulatory pathway. Science 2003; 299: 223-226.
58. Muro I, Monser K, Clem RJ. Mechanism of Dronc activation in Drosophila cells. J Cell Sci 2004; 117: 5035-5041.
59. Yu X, Wang L, Acehan D, Wang X, Akey C. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J Mol Biol 2006; 355: 577-589.
60. Diemand AV, Lupas AN. Modeling AAA+ ring complexes from monomeric structures. J Struct Biol 2006 2006 May 7 (Epub ahead of print).
61. Yan N, Huh JR, Schirf V, Demeler B, Hay BA, Shi Y. Structure and activation mechanism of the Drosophila initiator caspase Dronc. J Biol Chem 2006; 281: 8667-8674.
62. Horvitz HR. Worms, life, and death (Nobel Lecture). Chembiochem 2003; 4: 697-711.
63. Yang X, Chang HY, Baltimore D. Essential Role of CED-4 oligomerization in CED-3 activation and apoptosis. Science 1998; 281: 1355-1357.
64. Fairlie W, Perugini M, Kvansakul M, Chen L, Huang D, Colman P. CED-4 forms a 2:2 heterotetrameric complex with CED-9 until specifically displaced by EGL-1 or CED-13. Cell Death Differ 2005; 13: 426-434.
65. Yan N, Chai J, Lee ES, Gu L, Liu O, He J et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature 2005; 437: 831-837.
66. Yan N, Xu Y, Shi Y. 2:1 Stoichiometry of the CED-4-CED-9 complex and the tetrameric CED-4: Insights into the regulation of CED-3 activation. Cell Cycle 2006; 5: 31-34.
67. Chai J, Wu Q, Shiozaki E, Srinivasula SM, Alnemri ES, Shi Y. Crystal structure of a procaspase-7 zymogen: Mechanisms of activation and substrate binding. Cell 2001; 107: 399-407.
68. Riedl SJ, Fuentes-Prior P, Renatus M, Kairies N, Krapp S, Huber R et al. Structural basis for the activation of human procaspase-7. Proc Natl Acad Sci USA 2001; 98: 14790-14795.
69. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM. An induced proximity model for caspase-8 activation. J Biol Chem 1998; 273: 2926-2930.
70. Yang X, Chang HY, Baltimore D. Autoproteolylic activation of pro-caspases by oligomerization. Mol Cell 1998; 1: 319-325.
71. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1998; 1: 949-957.
72. MacCorlde RA, Freeman KW, Spencer DM. Synthetic activation of caspases: artificial death switches. Proc Natl Acad Sci USA 1998; 95: 3655-3660.
73. Boatright KM, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol 2003; 15: 725-731.
74. Renatus M, Stennicke HR, Scott FL, Liddington RC, Salvesen GS. Dimer formation drives the activation of the cell death protease caspase 9. Proc Natl Acad Sci USA 2001; 98: 14250-14255.
75. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM et al. Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 2003; 11: 519-527.
76. Pop C, Timmer J, Sperandio S, Salvesen GS. The apoptosome activates caspase-9 by dimerization. Mol Cell 2006; 22: 269-275.
77. Yin Q, Park HH, Chung JY, Lin SC, Lo YC, da Graca LS et al. Caspase-9 holoenzyme is a specific and optimal procaspase-3 processing machine. Mol Cell 2006; 22: 259-268.
78. Chao Y, Shiozaki EN, Srinivasula SM, Rigotti DJ, Fainman R, Shi Y. Engineering a dimeric caspase-9: A re-evaluation of the induced proximity model for caspase activation. PLoS Biol 2005; 3: E183.
79. Shiozaki E, Chai J, Shi Y. Oligomerization and activation of caspase-9 induced by Apaf-1 CARD. Proc Natl Acad Sci USA 2002; 99: 4197-4202.
80. Shi Y. Apoptosome: The cellular engine for the activation of caspase-9. Structure 2002; 10: 285-288.