Structure of an apoptosome-procaspase-9 CARD complex

Structure

Volumn 18, Issue 5, 2010, Pages 571-583

  Yuan, Shujun ^a   Yu, Xinchao ^a   Topf, Maya ^b   Ludtke, Steven J ^c   Wang, Xiaodong ^d   Akey, Christopher W ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

CELLBIO; PROTEINS; SIGNALLING

Indexed keywords

APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE; CASPASE RECRUITMENT DOMAIN PROTEIN; CYTOCHROME C; HETERODIMER; PROCASPASE 9; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MAPPING; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY SEQUENCE; SEQUENCE ANALYSIS;

APOPTOSOMES; CASPASE 9; CYTOCHROME C GROUP; CYTOCHROMES C; HUMANS; PROTEINS;

EID: 77952652352     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.04.001     Document Type: Article

References (60)

1. Acehan D., Jiang X., Morgan D.G., Heuser J.E., Wang X., Akey C.W. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding and activation. Mol. Cell 2002, 9:423-432.
2. Bao Q., Lu W., Rabinowitz J.D., Shi Y. Calcium blocks formation of apoptosome by preventing nucleotide exchange in Apaf-1. Mol. Cell 2007, 25:181-192.
3. Boatright K.M., Renatus M., Scott F.L., Sperandio S., Shin H., Pedersen I.M., Ricci J.E., Edris W.A., Sutherlin D.P., Green D.R., Salvesen G.S. A unified model for apical caspase activation. Mol. Cell 2003, 11:529-541.
4. Chao Y., Shiozaki E.N., Srinivasula S.M., Rigotti D.J., Fairman R., Shi Y. Engineering a dimeric caspase-9: a re-evaluation of the induced proximity model for caspase activation. PLoS Biol. 2005, 3:1079-1087.
5. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
6. Danot O., Marquenet E., Vidal-Ingigliardi D., Richet E. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 2009, 17:172-182.
7. DeLaBarre B., Brunger A.T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat. Struct. Biol. 2003, 10:856-863.
8. Diemand A.V., Lupas A.N. Modeling AAA+ ring complexes from monomeric structures. J. Struct. Biol. 2006, 156:230-243.
9. Ferraro E., Corvaro M., Cecconi F. Physiological and pathological roles of Apaf1 and the apoptosome. J. Cell. Mol. Med. 2003, 7:21-34.
10. Green D.R., Evan G.I. A matter of life and death. Cancer Cell 2002, 1:19-30.
11. Goddard T.D., Huang C.C., Ferrin T.E. Software extensions to UCSF chimera for interactive visualization of large molecular assemblies. Structure 2005, 13:473-482.
12. Hanson P.I., Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 2005, 6:519-529.
13. Hao Z., Duncan G.S., Chang C.C., Elia A., Fang M., Wakeham A., Okada H., Calzascia T., Jang Y., You-Ten A., et al. Specific ablation of the apoptotic functions of cytochrome c reveals a differential requirement for cytochrome c and Apaf-1 in apoptosis. Cell 2005, 121:579-591.
14. Harlan J., Chen Y., Gubbins E., Mueller R., Roch J.-M., Walter K., Lake M., Olsen T., Metzger P., Dorwin S., et al. Variants in Apaf-1 segregating with major depression promote apoptosome function. Mol. Psychiatry 2006, 11:76-85.
15. Hill M.M., Adrain C., Duriez P.J., Creagh E.M., Martin S.J. Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes. EMBO J. 2004, 23:2134-2145.
16. Hu Y., Benedict M.A., Ding L., Núñez G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis. EMBO J. 1999, 18:3586-3595.
17. Hugot J.P., Chamaillard M., Zouali H., Lesage S., Cezard J.P., Belaiche J., Almer S., Tysk C., O'Morain C.A., Gassull M., et al. Association of Nod2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
18. Inohara N., Nunez G. NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 2003, 3:371-382.
19. Jiang X., Wang X. Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to apaf-1. J. Biol. Chem. 2000, 275:31199-31203.
20. Kanazawa N., Okafuji I., Kambe N., Nishikomori R., Nakata-Hizume M., Nagai S., Fuji A., Yuasa T., Manki A., Sakurai Y., et al. Early-onset sarcoidosis and CARD15 mutations with constitutive nuclear factor-kappaB activation: common genetic etiology with Blau syndrome. Blood 2005, 105:1195-1197.
21. Kim H.-E., Du F., Fang M., Wang X. 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, 102:17545-17550.
22. Kleywegt G.J., Harris M.R., Zou J.Y., Taylor T.C., Wählby A., Jones T.A. The Uppsala Electron-Density Server. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2240-2249.
23. Leipe D.D., Koonin E.V., Aravind L. 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. 2004, 343:1-28.
24. Li J., Yuan J. Caspases in apoptosis and beyond. Oncogene 2008, 27:6194-6206.
25. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
26. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86:147-157.
27. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 1999, 128:82-97.
28. Miceli-Richard C., Lesage S., Rybojad M., Prieur A.M., Manouvrier-Hanu S., Hafner R., Chamaillard M., Zouali H., Thomas G., Hugot J.-P. CARD15 mutations in Blau syndrome. Nat. Genet. 2001, 29:19-20.
29. Mirkin N., Jaconcic J., Stojanoff V., Moreno A. High resolution X-ray crystallographic structure of bovine heart cytochrome c and its application to the design of an electron transfer biosensor. Proteins 2008, 70:83-92.
30. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003, 112:481-490.
31. Ogawa T., Shiga K., Hashimoto S., Kobayashi T., Horii A., Furukawa T. APAF-1-ALT, a novel alternative splicing form of APAF-1, potentially causes impeded ability of undergoing DNA damage-induced apoptosis in the LNCaP human prostate cancer cell line. Biochem. Biophys. Res. Commun. 2003, 306:537-543.
32. Proell M., Riedl S.J., Fritz J.H., Rojas A.M., Schwarzenbacher R. The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS ONE 2008, 3:e2119.
33. Pop C., Timmer J., Sperandio S., Salvesen G.S. The apoptosome activates caspase-9 by dimerization. Mol. Cell 2006, 22:269-275.
34. Purring-Koch C., McLendon G. Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength. Proc. Natl. Acad. Sci. USA 2000, 97:11928-11931.
35. Qin H., Srinivasula S.M., Wu G., Fernandes-Alnemri T., Alnemri E.S., Shi Y. Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature 1999, 399:549-557.
36. Renatus M., Stennicke H.R., Scott F.L., Liddington R.C., Salvesen G.S. Dimer formation drives the activation of the cell death protease caspase-9. Proc. Natl. Acad. Sci. USA 2001, 98:14250-14255.
37. Reubold T.F., Wohlgemuth S., Eschenburg S. A new model for the transition of APAF-1 from inactive monomer to caspase-activating apoptosome. J. Biol. Chem. 2009, 284:32717-32724.
38. Riedl S.J., Fuentes-Prior P., Renatus M., Kairies N., Krapp S., Huber R., Salvesen G.S., Bode W. Structural basis for the activation of human procaspase-7. Proc. Natl. Acad. Sci. USA. 2001, 98:14790-14795.
39. Riedl S.J., Li W., Chao Y., Schwarzenbacher R., Shi Y. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 2005, 434:926-933.
40. Rodriguez J., Lazebnik Y. Caspase-9 and Apaf-1 form an active holoenzyme. Genes Dev. 1999, 13:3179-3184.
41. Saleh A., Srinivasula S.M., Acharya S., Fishel R., Alnemri E.S. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J. Biol. Chem. 1999, 274:17941-17945.
42. Salvesen G.S., Dixit V.M. Caspases: intracellular signaling by proteolysis. Cell 1997, 91:443-446.
43. Shiozaki E.N., Chai J., Shi Y. Oligomerization and activation of caspase-9, induced by Apaf-1 CARD. Proc. Natl. Acad. Sci. USA 2002, 99:4197-4202.
44. Song Z., Steller H. Death by design: mechanism and control of apoptosis. Trends Cell Biol. 1999, 9:M49-M52.
45. Sousa D., Grigorieff N. Ab initio resolution measurement for single particle structures. J. Struct. Biol. 2007, 157:201-210.
46. Srinivasula S.M., Ahmad M., Fernandes-Alnemri T., Alnemri E.S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell 1998, 1:949-957.
47. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267:1456-1462.
48. Topf M., Lasker K., Webb B., Wolfson H., Chiu W., Sali A. Protein structure fitting and refinement guided by CryoEM density. Structure 2008, 16:295-307.
49. van Duist M.M., Albrecht M., Podswiadek M., Giachino D., Lengauer T., Punzi L., De Marchi M. A new CARD15 mutation in Blau syndrome. Eur. J. Hum. Genet. 2005, 13:742-747.
50. Voegtli W.C., Madrona A.Y., Wilson D.K. The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J. Biol. Chem. 2003, 278:34373-34379.
51. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001, 15:2922-2933.
52. Wilmanski J.M., Petnicki-Ocwiejia T., Kobayashi K.S. NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J. Leukoc. Biol. 2008, 83:13-30.
53. Yan N., Chai J., Lee E.S., Gu L., Liu Q., He J., Wu J.W., Kokel D., Li H., Hao Q., et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature 2005, 437:831-837.
54. Yin Q., Park H.H., Chung J.Y., Lin S.C., Lo Y.C., da Graca L.S., Jiang X., Wu H. Caspase-9 holoenzyme is a specific and optimal procaspase-3 processing machine. Mol. Cell 2006, 22:259-268.
55. Yu T., Wang X., Purring-Koch C., Wei Y., McLendon G.L. A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 2001, 276:13034-13038.
56. Yu X., Acehan D., Menetret J.F., Booth C.R., Ludtke S.J., Riedl S.J., Shi Y., Wang X., Akey C.W. A structure of the human apoptosome at 12.8 Å resolution provides insights into this cell death platform. Structure 2005, 13:1725-1735.
57. Yu X., Wang L., Acehan D., Wang X., Akey C.W. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J. Mol. Biol. 2006, 355:577-589.
58. Zhang X., Shaw A., Bates P.A., Newman R.H., Gowen B., Orlova E., Gorman M.A., Kondo H., Dokurno P., Lally J., et al. Structure of the AAA+ ATPase p97. Mol. Cell 2000, 6:1473-1484.
59. Zou H., Henzel W.J., 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.
60. 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.