Rational design of new class of BH3-mimetics as inhibitors of the Bcl-xL protein

Journal of Chemical Information and Modeling

Volumn 51, Issue 6, 2011, Pages 1249-1258

  Pinto, Marta ^a,b   Del Mar Orzaez, Maria ^c   Delgado Soler, Laura ^a   Perez, Juan J ^b   Rubio Martinez, Jaime ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^c INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELL DEATH; MOLECULAR DYNAMICS; PHARMACODYNAMICS; PROTEINS; QUERY PROCESSING;

DOCKING STUDIES; IN-VITRO TESTING; MICROMOLAR RANGE; OVER-EXPRESSION; PHARMACOPHORES; PROTECTIVE FUNCTION; RATIONAL DESIGN; THERAPEUTIC TREATMENTS;

LEAD COMPOUNDS;

BIOMIMETIC MATERIAL; PROTEIN BCL X;

ARTICLE; CHEMISTRY; COMPUTER PROGRAM; DRUG ANTAGONISM; DRUG DESIGN; DRUG SCREENING; MOLECULAR DYNAMICS; PROTEIN TERTIARY STRUCTURE;

BCL-X PROTEIN; BIOMIMETIC MATERIALS; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, TERTIARY; SOFTWARE;

EID: 79959713674     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci100501d     Document Type: Article

References (55)

1. Thompson, C. B. Apoptosis in the pathogenesis and treatment of disease Science 1995, 267, 1456-1462
2. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer Cell 2000, 100, 57-70 (Pubitemid 30046295)
3. Grütter, M. G. Caspases: key players in programmed cell death Curr. Opin. Struct. Biol. 2000, 10, 649-655 (Pubitemid 32061479)
4. Yin, X. M. Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways Cell Res. 2000, 10, 161-167
5. Zimmermann, K. C.; Bonzon, C.; Green, D. R. The machinery of programmed cell death Pharmacol. Ther. 2001, 92, 57-70 (Pubitemid 34032022)
6. Chao, D. T.; Korsmeyer, S. J. Bcl-2 family: regulators of cell death Annu. Rev. Immunol. 1998, 16, 395-419 (Pubitemid 28183370)
7. Adams, J. M.; Cory, S. The Bcl-2 protein family: arbiters of cell survival Science 1998, 281, 1322-1326 (Pubitemid 28406819)
8. Reed, J. C. Bcl-2 family proteins Oncogene 1998, 17, 3225-3236 (Pubitemid 29043975)
9. Kuwana, T.; Newmeyer, D. D. Bcl-2-family proteins and the role of mitochondria in apoptosis Curr. Opin. Cell Biol. 2003, 15, 691-696
10. Youle, R. J.; Strasser, A. The Bcl-2 protein family: opposing activities that mediate cell death Nat. Rev. Mol. Cell Biol. 2008, 9, 47-59
11. L-Bak peptide complex: recognition between regulators of apoptosis Science 1997, 275, 983-986 (Pubitemid 27087715)
12. L/Bim fragment complex: implications for Bim function Immunity 2003, 19, 341-352 (Pubitemid 37153411)
13. L/Bad peptide complex formation from structure, mutagenesis, and biophysical studies Protein Sci. 2000, 9, 2528-2534 (Pubitemid 32105735)
14. L-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein J. Biol. Chem. 2007, 282, 13123-13132 (Pubitemid 47100641)
15. Cosulich, S. C.; Worrall, V.; Hedge, P. J.; Green, S.; Clarke, P. R. Regulation of apoptosis by BH3 domains in a cell-free system Curr. Biol. 1997, 7, 913-920 (Pubitemid 28017068)
16. L function and induce apoptosis through cytochrome c-independent activation of caspases J. Biol. Chem. 1999, 274, 13298-13304
17. Wang, J. L.; Liu, D.; Zhang, Z. J.; Shan, S.; Han, X.; Srinivasula, S. M.; Croce, C. M.; Alnemri, E. S.; Huang, Z. Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 7124-7129 (Pubitemid 30431428)
18. Brewis, N. D.; Phelan, A.; Normand, N.; Choolun, E.; O'Hare, P. Particle assembly incorporating a VP22-BH3 fusion protein, facilitating intracellular delivery, regulated release, and apoptosis Mol. Ther. 2003, 7, 262-270 (Pubitemid 36395362)
19. Goldsmith, K. C.; Liu, X.; Dam, V.; Morgan, B. T.; Shabbout, M.; Cnaan, A.; Letai, A.; Korsmeyer, S. J.; Hogarty, M. D. BH3 peptidomimetics potently activate apoptosis and demonstrate single agent efficacy in neuroblastoma Oncogene 2006, 25, 4525-4533 (Pubitemid 44175112)
20. Li, R.; Boehm, A. L.; Miranda, M. B.; Shangary, S.; Grandis, J. R.; Johnson, D. E. Targeting anti-apoptotic Bcl-2 family members with cell-permeable BH3 peptides induces apoptosis signaling and death in head and neck squamous cell carcinoma cells Neoplasia 2007, 9, 801-811 (Pubitemid 47623420)
21. Wang, J. L.; Zhang, Z. J.; Choksi, S.; Shan, S.; Lu, Z.; Croce, C. M.; Alnemri, E. S.; Korngold, R.; Huang, Z. Cell permeable Bcl-2 binding peptides: a chemical approach to apoptosis induction in tumor cells Cancer Res. 2000, 60, 1498-1502 (Pubitemid 30183413)
22. Tzung, S. P.; Kim, K. M.; Basañez, G.; Giedt, C. D.; Simon, J.; Zimmerberg, J.; Zhang, K. Y.; Hockenbery, D. M. Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3 Nat. Cell Biol. 2001, 3, 183-191 (Pubitemid 32118372)
23. Enyedy, I. J.; Ling, Y.; Nacro, K.; Tomita, Y.; Wu, X.; Cao, Y.; Guo, R.; Li, B.; Zhu, X.; Huang, Y.; Long, Y. Q.; Roller, P. P.; Yang, D.; Wang, S. Discovery of small-molecule inhibitors of Bcl-2 through structure-based computer screening J. Med. Chem. 2001, 44, 4313-4324 (Pubitemid 33131658)
24. L Nat. Cell Biol. 2001, 3, 173-182 (Pubitemid 32118371)
25. L Chem. Biol. 2004, 11, 389-395 (Pubitemid 39403878)
26. Mohammad, R.; Young, D.; Chen, B.; Aboukameel, A.; Chen, J.; Nikolovska-Coleska, Z. ApoG2, a potent, non-toxic small-molecule inhibitor of Bcl-2 family: a preclinical trial in lymphoma. Proc. Amer. Assoc. Cancer Res. 2006, 47, Abstract 1335.
27. Wang, G.; Nikolovska-Coleska, Z.; Yang, C. Y.; Wang, R.; Tang, G.; Guo, J.; Shangary, S.; Qiu, S.; Gao, W.; Yang, D.; Meagher, J.; Stuckey, J.; Krajewski, K.; Jiang, S.; Roller, P. P.; Abaan, H. O.; Tomita, Y.; Wang, S. Structure-based design of potent small-molecule inhibitors of anti-apoptotic Bcl-2 proteins J. Med. Chem. 2006, 49, 6139-6142 (Pubitemid 44595187)
28. Oltersdorf, T.; Elmore, S. W.; Shoemaker, A. R.; Armstrong, R. C.; Augeri, D. J.; Belli, B. A.; Bruncko, M.; Deckwerth, T. L.; Dinges, J.; Hajduk, P. J.; Joseph, M. K.; Kitada, S.; Korsmeyer, S. J.; Kunzer, A. R.; Letai, A.; Li, C.; Mitten, M. J.; Nettesheim, D. G.; Ng, S.; Nimmer, P. M.; O'Connor, J. M.; Oleksijew, A.; Petros, A. M.; Reed, J. C.; Shen, W.; Tahir, S. K.; Thompson, C. B.; Tomaselli, K. J.; Wang, B.; Wendt, M. D.; Zhang, H.; Fesik, S. W.; Rosenberg, S. H. An inhibitor of Bcl-2 family proteins induces regression of solid tumours Nature 2005, 435, 677-681 (Pubitemid 40825512)
29. Wendt, M. D.; Shen, W.; Kunzer, A.; McClellan, W. J.; Bruncko, M.; Oost, T. K.; Ding, H.; Joseph, M. K.; Zhang, H.; Nimmer, P. M.; Ng, S. C.; Shoemaker, A. R.; Petros, A. M.; Oleksijew, A.; Marsh, K.; Bauch, J.; Oltersdorf, T.; Belli, B. A.; Martineau, D.; Fesik, S. W.; Rosenberg, S. H.; Elmore, S. W. Discovery and structure-activity relationship of antagonists of B-cell lymphoma 2 family proteins with chemopotentiation activity in vitro and in vivo J. Med. Chem. 2006, 49, 1165-1181 (Pubitemid 43221663)
30. L potentiates the activity of cytotoxic drugs in vitro and in vivo Cancer Res. 2006, 66, 8731-8739 (Pubitemid 44449190)
31. Kitada, S.; Leone, M.; Sareth, S.; Zhai, D.; Reed, J. C.; Pellecchia, M. Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins J. Med. Chem. 2003, 46, 4259-4264 (Pubitemid 37153007)
32. Tse, C.; Shoemaker, A. R.; Adickes, J.; Anderson, M. G.; Chen, J.; Jin, S.; Johnson, E. F.; Marsh, K. C.; Mitten, M. J.; Nimmer, P.; Roberts, L.; Tahir, S. K.; Xiao, Y.; Yang, X.; Zhang, H.; Fesik, S.; Rosenberg, S. H.; Elmore, S. W. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor Cancer Res. 2008, 68, 3421-3428
33. L: implications for selectivity of antagonists of the Bcl-2 family Cell Death Differ. 2007, 14, 1711-1713 (Pubitemid 47278856)
34. Lugovskoy, A. A.; Degterev, A. I.; Fahmy, A. F.; Zhou, P.; Gross, J. D.; Yuan, J.; Wagner, G. A novel approach for characterizing protein ligand complexes: molecular basis for specificity of small-molecule Bcl-2 inhibitors J. Am. Chem. Soc. 2002, 124, 1234-1240 (Pubitemid 34169130)
35. Lama, D.; Sankararamakrishnan, R. Anti-apoptotic Bcl-XL protein in complex with BH3 peptides of pro-apoptotic Bak, Bad, and Bim proteins: comparative molecular dynamics simulations Proteins 2008, 73, 492-514
36. L and Bcl-2 proteins J. Comput.-Aided Mol. Des. 2004, 18, 13-22 (Pubitemid 39127587)
37. Friesner, R. A.; Banks, J. L.; Murphy, R. B.; Halgren, T. A.; Klicic, J. J.; Mainz, D. T.; Repasky, M. P.; Knoll, E. H.; Shelley, M.; Perry, J. K.; Shaw, D. E.; Francis, P.; Shenkin, P. S. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy J. Med. Chem. 2004, 47, 1739-1749 (Pubitemid 38380917)
38. Maestro, version 8.5; Schrödinger: New York, 2009.
39. Sherman, W.; Day, T.; Jacobson, M. P.; Friesner, R. A.; Farid, R. Novel procedure for modeling ligand/receptor induced fit effects J. Med. Chem. 2006, 49, 534-553 (Pubitemid 43157487)
40. Prime, version 1.6; Schrödinger: New York, 2009.
41. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Merz, K. M.; Pearlman, D. A.; Crowley, M.; Walker, R. C.; Zhang, W.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Wong, K. F.; Paesani, F.; Wu, X.; Brozell, S.; Tsui, V.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Beroza, P.; Mathews, D. H.; Schafmeister, C.; Ross, W. S.; Kollman, P. A. AMBER 9; University of California, San Francisco: San Francisco, CA, 2006.
42. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 2003, 24, 1999-2012
43. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157-1174
44. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
45. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An Nlog(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089-10092
46. Berendsen, H. J. C.; Postman, J. P. M.; Van Gunsteren, W. F.; Di Nola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
47. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Chem. 1977, 23, 327-341
48. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Srivasan, J.; Case, D. A.; Cheatam, T. E., III. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33, 889-897 (Pubitemid 32056774)
49. Onufriev, A.; Bashford, D.; Case, D. A. Modification of the Generalized Born Model Suitable for Macromolecules J. Phys. Chem. B 2000, 104, 3712-3720
50. Weiser, J.; Shemkin, P. S.; Still, W. C. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO) J. Comput. Chem. 1999, 20, 217-230 (Pubitemid 129653030)
51. Gohlke, H.; Kiel, C.; Case, D. A. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes J. Mol. Biol. 2003, 330, 891-913
52. L Anal. Biochem. 2002, 307, 70-75
53. L Bioorg. Med. Chem. Lett. 2009, 19, 1592-1595
54. L through Virtual Screening J. Chem. Inf. Model. 2010, 50, 906-923
55. Seidler, J.; McGover, S. L.; Doma, T. N.; Schoichet, B. K. Identification and prediction of promiscuous aggregating inhibitors among known drugs J. Med. Chem. 2003, 46, 4477-4486 (Pubitemid 37238749)