A structure of the human apoptosome at 12.8 Å resolution provides insights into this cell death platform

Structure

Volumn 13, Issue 11, 2005, Pages 1725-1735

  Yu, Xinchao ^a   Acehan, Devrim ^a   Ménétret, Jean François ^a   Booth, Christopher R ^c   Ludtke, Steven J ^c   Riedl, Stefan J ^d   Shi, Yigong ^d   Wang, Xiaodong ^b   Akey, Christopher W ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYTOCHROME C;

APOPTOSIS; ARTICLE; CELL DEATH; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME BINDING; NUCLEOTIDE BINDING SITE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CASPASE 9; CELL DEATH; CRYSTALLOGRAPHY, X-RAY; CYTOCHROMES C; DEOXYADENINE NUCLEOTIDES; HUMANS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, PROTEIN;

EID: 27644483812     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.09.006     Document Type: Article

References (47)

1. D. Acehan, X. Jiang, D.G. Morgan, J.E. Heuser, X. Wang, and C.W. Akey Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding and activation Mol. Cell 9 2002 423 432
2. K.M. Boatright, M. Renatus, F.L. Scott, S. Sperandio, H. Shin, I.M. Pedersen, J.E. Ricci, W.A. Edris, D.P. Sutherlin, D.R. Green, and G.S. Salvesen A unified model for apical caspase activation Mol. Cell 11 2003 529 541
3. I. Budihardjo, H. Oliver, M. Lutter, X. Luo, and X. Wang Biochemical pathways of Caspase activation during apoptosis Annu. Rev. Cell Dev. Biol. 15 1999 269 290
4. Y. Chao, E.N. Shiozaki, S.M. Srinivasula, D.J. Rigotti, R. Fairman, and Y. Shi Engineering a dimeric caspase-9: a re-evaluation of the induced proximity model for caspase activation PLoS Biol. 3 2005 e183
5. N.N. Danial, and S.J. Korsmeyer Cell death: critical control points Cell 116 2004 205 219
6. S. Desagher, and J.-C. Martinou Mitochondria as the central control point of apoptosis Trends Cell Biol. 10 2000 369 377
7. F. Fabiola, and M.S. Chapman Fitting of high-resolution structures into electron microscopy reconstruction images Structure 13 2005 389 400
8. E. Ferraro, M. Corvaro, and F. Cecconi Physiological and pathological roles of Apaf1 and the apoptosome J. Cell. Mol. Med. 7 2003 21 34
9. A. Fotin, Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz Molecular model for a complete clathrin lattice from electron cryomicroscopy Nature 432 2004 573 579
10. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
11. A. Fukami, and K. Adachi A new method of preparation of a self-perforated micro plastic grid and its application J. Electron Microsc. 14 1965 112 118
12. J.C. Goldstein, N.J. Waterhouse, P. Juin, G.I. Evan, and D.R. Green The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant Nat. Cell Biol. 2 2000 156 162
13. T.D. Goddard, C.C. Huang, and T.E. Ferrin Software extensions to UCSF chimera for interactive visualization of large molecular assemblies Structure 13 2005 473 482
14. D.R. Green, and G.I. Evan A matter of life and death Cancer Cell 1 2002 19 30
15. Z. Hao, G.S. Duncan, C.C. Chang, A. Elia, M. Fang, A. Wakeham, H. Okada, T. Calzascia, Y. Jang, and A. You-Ten Specific ablation of the apoptotic functions of cytochrome c reveals a differential requirement for cytochrome C and Apaf-1 in apoptosis Cell 121 2005 579 591
16. M.M. Hill, C. Adrain, P.J. Duriez, E.M. Creagh, and S.J. Martin Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes EMBO J. 23 2004 2134 2145
17. Y. Hu, L. Ding, D.M. Spencer, and G. Nunez WD-40 repeat region regulates Apaf-1 self-association and procaspase-9 activation J. Biol. Chem. 273 1998 33489 33494
18. Y. Hu, M.A. Benedict, L. Ding, and G. Nunez Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1 mediated caspase-9 activation and apoptosis EMBO J. 13 1999 3591 3595
19. N. Inohara, and G. Nunez NODs: intracellular proteins involved in inflammation and apoptosis Nat. Rev. Immunol. 3 2003 371 382
20. X. Jiang, and X. Wang Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to apaf-1 J. Biol. Chem. 275 2000 31199 31203
21. T.A. Jones, J.-Y. Zou, and S.W. Cowan Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
22. H.-E. Kim, F. Du, M. Fang, and X. Wang Formation of an apoptosome is initiated by cytochrome c induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1 Proc. Natl. Acad. Sci. USA 2005 in press
23. G.J. Kleywegt, M.R. Harris, J.Y. Zou, T.C. Taylor, A. Wahlby, and T.A. Jones The Uppsala electron-density server Acta Crystallogr. D Biol. Crystallogr. 60 2004 2240 2249
24. T. Kuwana, and D.D. Newmeyer Bcl-2-family proteins and the role of mitochondria in apoptosis Curr. Opin. Cell Biol. 15 2003 691 699
25. D.D. Leipe, E.V. Koonin, and L. Aravind STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer J. Mol. Biol. 343 2004 1 28
26. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade Cell 91 1997 479 489
27. X. Liu, C.N. Kim, J. Yang, R. Jemmerson, and X. Wang Induction of apoptotic program in cell free extracts: requirement for dATP and cytochrome c Cell 86 1996 147 157
28. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97
29. S.J. Ludtke, D.H. Chen, J.L. Song, D.T. Chuang, and W. Chiu Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy Structure 12 2004 1129 1136
30. D.D. Newmeyer, and S. Ferguson-Miller Mitochondria: releasing power for life and unleashing the machineries of death Cell 112 2003 481 490
31. C. Purring, H. Zou, X. Wang, and G. McLendon Stoichiometry, free energy and kinetic aspects of cytochrome c:Apaf-1 binding in apoptosis J. Am. Chem. Soc. 121 1999 7435 7436
32. H. Qin, S.M. Srinivasula, G. Wu, T. Fernandes-Alnemri, E.S. Alnemri, and Y. Shi Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1 Nature 399 1999 549 557
33. M. Renatus, H.R. Stennicke, F.L. Scott, R.C. Liddington, and G.S. Salvesen Dimer formation drives the activation of the cell death protease caspase-9 Proc. Natl. Acad. Sci. USA 98 2001 14250 14255
34. S.J. Riedl, W. Li, Y. Chao, R. Schwarzenbacher, and Y. Shi Structure of the apoptotic protease-activating factor 1 bound to ADP Nature 434 2005 926 933
35. J. Rodriguez, and Y. Lazebnik Caspase-9 and Apaf-1 form an active holoenzyme Genes Dev. 13 1999 3179 3184
36. G.S. Salvesen, and V.M. Dixit Caspases: intracellular signaling by proteolysis Cell 91 1997 443 446
37. Y. Shi Apoptosome: the cellular engine for the activation of caspase-9 Structure 10 2002 285 288
38. E.N. Shiozaki, J. Chai, and Y. Shi Oligomerization and activation of caspase-9, induced by Apaf-1 CARD Proc. Natl. Acad. Sci. USA 99 2002 4197 4202
39. Z. Song, and H. Steller Death by design: mechanism and control of apoptosis Trend. Cell Biol. 12 1999 49 52
40. S.M. Srinivasula, M. Ahmad, T. Fernandes-Alnemri, and E.S. Alnemri Autoactivation of procaspase-9 by Apaf-1 mediated oligomerization Mol. Cell 1 1998 949 957
41. H.R. Stennicke, Q.L. Deveraux, E.W. Humke, J.C. Reed, V.M. Dixit, and G.S. Salvesen Caspase-9 can be activated without proteolytic processing J. Biol. Chem. 274 1999 8359 8362
42. C.B. Thompson Apoptosis in the pathogenesis and treatment of disease Science 267 1995 1456 1462
43. X. Wang The expanding role of mitochondria in apoptosis Genes Dev. 15 2001 2922 2933
44. R.C. Yu, P.I. Hanson, R. Jahn, and A.T. Brunger Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP Nat. Struct. Biol. 5 1998 803 811
45. X. Zhang, A. Shaw, P.A. Bates, R.H. Newman, B. Gowen, E. Orlova, M.A. Gorman, H. Kondo, P. Dokurno, and J. Lally Structure of the AAA+ ATPase p97 Mol. Cell 6 2000 1473 1484
46. H. Zou, W.J. Henzel, X. Liu, A. Lutschg, and X. Wang Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c dependent activation of caspase-3 Cell 90 1997 405 413
47. H. Zou, Y. Li, X. Liu, and X. Wang An Apaf-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9 J. Biol. Chem. 274 1999 11549 11556