Regulation of apoptosis: Uncovering the binding determinants

Current Opinion in Structural Biology

Volumn 15, Issue 6, 2005, Pages 690-699

  Hinds, Mark G ^a   Day, Catherine L ^b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ANTINEOPLASTIC AGENT; APOPTOSIS INHIBITOR; INHIBITOR OF APOPTOSIS PROTEIN; PROTEIN BCL 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; UNCLASSIFIED DRUG;

APOPTOSIS; BINDING AFFINITY; CELL ASSAY; CELL DAMAGE; CELL DIFFERENTIATION; CONFORMATIONAL TRANSITION; HUMAN; MEDICAL RESEARCH; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ANIMALS; APOPTOSIS; CASPASES; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 27944497377     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2005.10.003     Document Type: Review

References (44)

1. N.N. Danial, and S.J. Korsmeyer Cell death: critical control points Cell 116 2004 205 219
2. S. Cory, D.C. Huang, and J.M. Adams The Bcl-2 family: roles in cell survival and oncogenesis Oncogene 22 2003 8590 8607
3. H.R. Horvitz Genetic control of programmed cell death in the nematode Caenorhabditis elegans Cancer Res 59 1999 1701s 1706s
4. L, an inhibitor of programmed cell death Nature 381 1996 335 341
5. A.M. Petros, A. Medek, D.G. Nettesheim, D.H. Kim, H.S. Yoon, K. Swift, E.D. Matayoshi, T. Oltersdorf, and S.W. Fesik Solution structure of the anti-apoptotic protein bcl-2 Proc Natl Acad Sci USA 98 2001 3012 3017
6. M.G. Hinds, M. Lackmann, G.L. Skea, P.J. Harrison, D.C. Huang, and C.L. Day The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity EMBO J 22 2003 1497 1507 This paper reports the most complete structure of a pro-survival Bcl-2 protein. Of particular note was the observation that the C-terminal residues, truncated from other molecules used in structural studies, occupy the hydrophobic ligand-binding groove and restrict binding of BH3-only proteins.
7. J.S. Woo, J.S. Jung, N.C. Ha, J. Shin, K.H. Kim, W. Lee, and B.H. Oh Unique structural features of a BCL-2 family protein CED-9 and biophysical characterization of CED-9/EGL-1 interactions Cell Death Differ 10 2003 1310 1319
8. C.L. Day, L. Chen, S.J. Richardson, P.J. Harrison, D.C. Huang, and M.G. Hinds Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands J Biol Chem 280 2005 4738 4744
9. A.Y. Denisov, M.S. Madiraju, G. Chen, A. Khadir, P. Beauparlant, G. Attardo, G.C. Shore, and K. Gehring Solution structure of human BCL-w: modulation of ligand binding by the C-terminal helix J Biol Chem 278 2003 21124 21128
10. L. Implications for the function of the Bcl-2 protein family J Biol Chem 272 1997 27886 27892
11. H. Puthalakath, and A. Strasser Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins Cell Death Differ 9 2002 505 512
12. L-Bak peptide complex: recognition between regulators of apoptosis Science 275 1997 983 986
13. L/Bad peptide complex formation from structure, mutagenesis, and biophysical studies Protein Sci 9 2000 2528 2534
14. L bound to a fragment of Bim containing a BH3 domain is reported. This complex includes the largest fragment of a BH3-only protein bound to a pro-survival protein. It reveals an extended interaction interface, including contacts with residues C terminal to the conserved BH3 domain.
15. L and its ligands. This report established that the mode of ligand recognition is conserved between worms and mammals.
16. •,18 ] reveal the selective binding properties of both pro-survival and pro-apoptotic proteins. Remarkably, some molecules were found to have promiscuous binding properties, whereas others show very restricted binding.
17. •].
18. A. Letai, M.C. Bassik, L.D. Walensky, M.D. Sorcinelli, S. Weiler, and S.J. Korsmeyer Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics Cancer Cell 2 2002 183 192
19. J. Wilson-Annan, L.A. O'Reilly, S.A. Crawford, G. Hausmann, J.G. Beaumont, L.P. Parma, L. Chen, M. Lackmann, T. Lithgow, and M.G. Hinds Proapoptotic BH3-only proteins trigger membrane integration of prosurvival Bcl-w and neutralize its activity J Cell Biol 162 2003 877 887
20. L sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers EMBO J 23 2004 2146 2155
21. M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 2001 727 730
22. A. Cuconati, C. Mukherjee, D. Perez, and E. White DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells Genes Dev 17 2003 2922 2932
23. L and Mcl-1, which can both restrain Bak in a healthy cell, are required to induce cell death. An intact Bak BH3 domain is required for activity and the authors suggest that activation involves disruption of the Bak-pro-survival protein complex by the BH3-only protein BH3 domain.
24. T.W. Sedlak, Z.N. Oltvai, E. Yang, K. Wang, L.H. Boise, C.B. Thompson, and S.J. Korsmeyer Multiple Bcl-2 family members demonstrate selective dimerizations with Bax Proc Natl Acad Sci USA 92 1995 7834 7838
25. M. Suzuki, R.J. Youle, and N. Tjandra Structure of Bax: coregulation of dimer formation and intracellular localization Cell 103 2000 645 654
26. 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
27. 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 This paper describes the structure of Apaf-1 missing only the WD40 repeats. The structure provides a molecular basis for understanding the mechanism by which procaspase-9 binding to Apaf-1 is restricted in the latent state. An alternative model of the apoptosome structure, based on the high-resolution structure of Apaf-1, is also proposed.
28. P.I. Hanson, and S.W. Whiteheart AAA+ proteins: have engine will work Nat Rev Mol Cell Biol 6 2005 519 529
29. 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
30. C.H. Weber, and C. Vincenz The death domain superfamily: a tale of two interfaces? Trends Biochem Sci 26 2001 475 481
31. 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
32. C.L. Day, C. Dupont, M. Lackmann, D.L. Vaux, and M.G. Hinds Solution structure and mutagenesis of the caspase recruitment domain (CARD) from Apaf-1 Cell Death Differ 6 1999 1125 1132
33. P. Fuentes-Prior, and G.S. Salvesen The protein structures that shape caspase activity, specificity, activation and inhibition Biochem J 384 2004 201 232
34. 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
35. 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
36. J. Chai, Q. Wu, E. Shiozaki, S.M. Srinivasula, E.S. Alnemri, and Y. Shi Crystal structure of a procaspase-7 zymogen: mechanisms of activation and substrate binding Cell 107 2001 399 407
37. D.L. Vaux, and J. Silke Mammalian mitochondrial IAP binding proteins Biochem Biophys Res Commun 304 2003 499 504
38. J.C. Reed Apoptosis-based therapies Nat Rev Drug Discov 1 2002 111 121
39. T.K. Oost, C. Sun, R.C. Armstrong, A.S. Al-Assaad, S.F. Betz, T.L. Deckwerth, H. Ding, S.W. Elmore, R.P. Meadows, and E.T. Olejniczak Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer J Med Chem 47 2004 4417 4426
40. L.D. Walensky, A.L. Kung, I. Escher, T.J. Malia, S. Barbuto, R.D. Wright, G. Wagner, G.L. Verdine, and S.J. Korsmeyer Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix Science 305 2004 1466 1470 The authors describe the use of a hydrocarbon 'staple' to stabilize a Bid mimetic peptide. The stabilized peptide had an increased affinity for pro-survival proteins. It was found to kill leukemia cells and inhibit human leukemia xenographs, providing direct proof of the value of targeting the groove of pro-survival proteins for therapeutic intervention.
41. S.B. Shuker, P.J. Hajduk, R.P. Meadows, and S.W. Fesik Discovering high-affinity ligands for proteins: SAR by NMR Science 274 1996 1531 1534
42. L, are presented. To be successful in such a screening regime, the molecular surface of the target must be complex and hydrophobic interactions were shown to dominate small molecule-protein interactions.
43. T. Oltersdorf, S.W. Elmore, A.R. Shoemaker, R.C. Armstrong, D.J. Augeri, B.A. Belli, M. Bruncko, T.L. Deckwerth, J. Dinges, and P.J. Hajduk An inhibitor of Bcl-2 family proteins induces regression of solid tumours Nature 435 2005 677 681 The authors report the development of compounds that specifically bind pro-survival Bcl-2 proteins and have potent anti-tumor activities in cancer cell lines. A molecule (ABT-737) with nanomolar affinities for its targets was developed using a combination of SAR by NMR, fragment fusion and structure-based optimization. The report highlights the successful use of small molecules to inhibit protein-protein interactions and promises much for the development of effective anti-cancer agents that directly target the apoptotic pathway.
44. ••]. The structural and biochemical data presented in this article contribute significantly to our understanding of the steps associated with initiation of apoptosis in C. elegans.