An optically pure apogossypolone derivative as potent pan-active inhibitor of anti-apoptotic Bcl-2 family proteins

Frontiers in Oncology

Volumn 1, Issue SEP, 2011, Pages

  Wei, Jun ^a   Stebbins, John L ^a   Kitada, Shinichi ^a   Dash, Rupesh ^b   Zhai, Dayong ^a   Placzek, William J ^a   Wu, Bainan ^a   Rega, Michele F ^a   Zhang, Ziming ^a   Barile, Elisa ^a   Yang, Li ^a   Dahl, Russell ^a   Fisher, Paul B ^b   Reed, John C ^a   Pellecchia, Maurizio ^a  

^a BURNHAM INSTITUTE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5, 5' apogossypolone derivatives; Anti apoptotic Bcl 2; Apogossypolone; Apoptosis; Cancer

Indexed keywords

EID: 84871197721     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2011.00028     Document Type: Article

References (51)

1. Adams, J. M., and Cory, S. (1998). The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326.
2. Arnold, A. A., Aboukameel, A., Chen, J., Yang, D., Wang, S., Al-Katib, A., and Mohammad, R. M. (2008). Preclinical studies of apogossypolone: a new nonpeptidic pan small-molecule inhibitor of Bcl-2, Bcl-XL and Mcl-1 proteins in follicular small cleaved cell lymphoma model. Mol. Cancer 7, 20.
3. Becattini, B., Kitada, S., Leone, M., Monosov, E., Chandler, S., Zhai, D., Kipps, T. J., Reed, J. C., and Pellecchia, M. (2004). Rational design and real time, in-cell detection of the proapoptotic activity of a novel compound targeting Bcl-X(L). Chem. Biol. 11, 389-395.
4. Brien, G., Trescol-Biemont, M. C., and Bonnefoy-Berard, N. (2007). Downregulation of Bfl-1 protein expression sensitizes malignant B cells to apoptosis. Oncogene 26, 5828-5832.
5. Bruncko, M., Oost, T. K., Belli, B. A., Ding, H., Joseph, M. K., Kunzer, A., Martineau, D., Mcclellan, W. J., Mitten, M., Ng, S. C., Nimmer, P. M., Oltersdorf, T., Park, C. M., Petros, A. M., Shoemaker, A. R., Song, X., Wang, X., Wendt, M. D., Zhang, H., Fesik, S. W., Rosenberg, S. H., and Elmore, S. W. (2007). Studies leading to potent, dual inhibitors of Bcl-2 and Bcl-xL. J. Med. Chem. 50, 641-662.
6. Cory, S., and Adams, J. M. (2005). Killing cancer cells by flipping the Bcl-2/Bax switch. Cancer Cell 8, 5-6.
7. Coward, L., Gorman, G., Noker, P., Kerstner-Wood, C., Pellecchia, M., Reed, J. C., and Jia, L. (2006). Quantitative determination of apogossypol, a pro-apoptotic analog of gossypol, in mouse plasma using LC/MS/MS. J. Pharm. Biomed. Anal. 42, 581-586.
8. Dash, R., Azab, B., Quinn, B. A., Shen, X., Wang, X. Y., Das, S. K., Rahmani, M., Wei, J., Hedvat, M., Dent, P., Dmitriev, I. P., Curiel, D. T., Grant, S., Wu, B., Stebbins, J. L., Pellecchia, M., Reed, J. C., Sarkar, D., and Fisher, P. B. (2011). Apogossypol derivative BI-97C1 (Sabutoclax) targeting Mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc. Natl. Acad. Sci. U.S.A. 108, 8785-8790.
9. Dash, R., Richards, J. E., Su, Z. Z., Bhutia, S. K., Azab, B., Rahmani, M., Dasmahapatra, G., Yacoub, A., Dent, P., Dmitriev, I. P., Curiel, D. T., Grant, S., Pellecchia, M., Reed, J. C., Sarkar, D., and Fisher, P. B. (2010). Mechanism by which Mcl-1 regulates cancer-specific apoptosis triggered by mda-7/IL-24, an IL-10-related cytokine. Cancer Res. 70, 5034-5045.
10. Day, C. L., Chen, L., Richardson, S. J., Harrison, P. J., Huang, D. C., and Hinds, M. G. (2005). Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands. J. Biol. Chem. 280, 4738-4744.
11. Degterev, A., Lugovskoy, A., Cardone, M., Mulley, B., Wagner, G., Mitchison, T., and Yuan, J. (2001). Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nat. Cell Biol. 3, 173-182.
12. Eldridge, M. D., Murray, C. W., Auton, T. R., Paolini, G. V., and Mee, R. P. (1997). Empirical scoring functions: I. The development of a fast empirical scoring function to estimate the binding affinity of ligands in receptor complexes. J. Comput. Aided Mol. Des. 11, 425-445.
13. Ferreira, C. G., Span, S. W., Peters, G. J., Kruyt, F. A., and Giaccone, G. (2000). Chemotherapy triggers apoptosis in a caspase-8-dependent and mitochondria-controlled manner in the non-small cell lung cancer cell line NCI-H460. Cancer Res. 60, 7133-7141.
14. Gross, A., Mcdonnell, J. M., and Korsmeyer, S. J. (1999). BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899-1911.
15. Hu, Z. Y., Zhu, X. F., Zhong, Z. D., Sun, J., Wang, J., Yang, D., and Zeng, Y. X. (2008). ApoG2, a novel inhibitor of antiapoptotic Bcl-2 family proteins, induces apoptosis and suppresses tumor growth in nasopharyngeal carcinoma xenografts. Int. J. Cancer 123, 2418-2429.
16. Johnstone, R. W., Ruefli, A. A., and Lowe, S. W. (2002). Apoptosis: a link between cancer genetics and chemotherapy. Cell 108, 153-164.
17. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997). Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748.
18. Katsumata, M., Siegel, R. M., Louie, D. C., Miyashita, T., Tsujimoto, Y., Nowell, P. C., Greene, M. I., and Reed, J. C. (1992). Differential effects of Bcl-2 on T and B cells in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 89, 11376-11380.
19. Kitada, S., Kress, C. L., Krajewska, M., Jia, L., Pellecchia, M., and Reed, J. C. (2008). Bcl-2 antagonist apogossypol (NSC736630) displays single-agent activity in Bcl-2-transgenic mice and has superior efficacy with less toxicity compared with gossypol (NSC19048). Blood 111, 3211-3219.
20. Kitada, S., Leone, M., Sareth, S., Zhai, D., Reed, J. C., and Pellecchia, M. (2003). Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins. J. Med. Chem. 46, 4259-4264.
21. Lee, E. F., Czabotar, P. E., Smith, B. J., Deshayes, K., Zobel, K., Colman, P. M., and Fairlie, W. D. (2007). Crystal structure of ABT-737 complexed with Bcl-xL: implications for selectivity of antagonists of the Bcl-2 family. Cell Death Differ. 14, 1711-1713.
22. Li, J., Viallet, J., and Haura, E. B. (2008). A small molecule pan-Bcl-2 family inhibitor, GX15-070, induces apoptosis and enhances cisplatin-induced apoptosis in non-small cell lung cancer cells. Cancer Chemother. Pharmacol. 61, 525-534.
23. Lin, J., Wu, Y.-J., Yang, D.-J., and Zhao, Y.-Q. (2009). Effect of apogossypolone on induction apoptosis in multiple myeloma cells and its mechanisms. Zhongguo Shi Yan Xue Ye Xue Za Zhi 17, 92-98.
24. Meng, Y., Tang, W., Dai, Y., Wu, X., Liu, M., Ji, Q., Ji, M., Pienta, K., Lawrence, T., and Xu, L. (2008). Natural BH3 mimetic (-)-gossypol chemosensitizes human prostate cancer via Bcl-xL inhibition accompanied by increase of Puma and Noxa. Mol. Cancer Ther. 7, 2192-2202.
25. Mi, J. X., Wang, G. F., Wang, H. B., Sun, X. Q., Ni, X. Y., Zhang, X. W., Tang, J. M., and Yang, D. J. (2008). Synergistic antitumoral activity and induction of apoptosis by novel pan Bcl-2 proteins inhibitor apogossypolone with adriamycin in human hepatocellular carcinoma. Acta Pharmacol. Sin. 29, 1467-1477.
26. Mohammad, R. M., Wang, S., Aboukameel, A., Chen, B., Wu, X., Chen, J., and Al-Katib, A. (2005). Preclinical studies of a nonpeptidic small-molecule inhibitor of Bcl-2 and Bcl-X(L) [(-)-gossypol] against diffuse large cell lymphoma. Mol. Cancer Ther. 4, 13-21.
27. Muchmore, S. W., Sattler, M., Liang, H., Meadows, R. P., Harlan, J. E., Yoon, H. S., Nettesheim, D., Chang, B. S., Thompson, C. B., Wong, S. L., Ng, S. L., and Fesik, S. W. (1996). X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341.
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., and Rosenberg, S. H. (2005). An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681.
29. Placzek, W. J., Wei, J., Kitada, S., Zhai, D., Reed, J. C., and Pellecchia, M. (2010). A survey of the anti-apoptotic Bcl-2 subfamily expression in cancer types provides a platform to predict the efficacy of Bcl-2 antagonists in cancer therapy. Cell Death Dis. 1, 1-9.
30. Ramjaun, A. R., Tomlinson, S., Eddaoudi, A., and Downward, J. (2007). Upregulation of two BH3-only proteins, Bmf and Bim, during TGF beta-induced apoptosis. Oncogene 26, 970-981.
31. Reed, J. C. (1997). Bcl-2 family proteins: strategies for overcoming chemoresistance in cancer. Adv. Pharmacol. (San Diego, Calif.) 41, 501-532.
32. Reed, J. C. (1998). Bcl-2 family proteins. Oncogene 17, 3225-3236.
33. Reed, J. C. (1999). Dysregulation of apoptosis in cancer. J. Clin. Oncol. 17, 2941-2953.
34. Reed, J. C. (2002). Apoptosis-based therapies. Nat. Rev. Drug Discov. 1, 111-121.
35. Sattler, M., Liang, H., Nettesheim, D., Meadows, R. P., Harlan, J. E., Eberstadt, M., Yoon, H. S., Shuker, S. B., Chang, B. S., Minn, A. J., Thompson, C. B., and Fesik, S. W. (1997). Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275, 983-986.
36. Sun, J., Li, Z.-M., Hu, Z.-Y., Zeng, Z.-L., Yang, D.-J., and Jiang, W.-Q. (2009). Apogossypolone inhibits cell growth by inducing cell cycle arrest in U937 cells. Oncol. Rep. 22, 193-198.
37. Teschner, M., Henn, C., Vollhardt, H., Reiling, S., and Brickmann, J. (1994). Texture mapping: a new tool for molecular graphics. J. Mol. Graph. 12, 98-105.
38. van de Donk, N. W., Kamphuis, M. M., Van Dijk, M., Borst, H. P., Bloem, A. C., and Lokhorst, H. M. (2003). Chemosensitization of myeloma plasma cells by an antisense-mediated downregulation of Bcl-2 protein. Leukemia 17, 211-219.
39. Vaux, D. L., and Korsmeyer, S. J. (1999). Cell death in development. Cell 96, 245-254.
40. Voortman, J., Checinska, A., Giaccone, G., Rodriguez, J. A., and Kruyt, F. A. (2007). Bortezomib, but not cisplatin, induces mitochondria-dependent apoptosis accompanied by up-regulation of noxa in the non-small cell lung cancer cell line NCI-H460. Mol. Cancer Ther. 6, 1046-1053.
41. 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., and Wang, S. (2006a). Structure-based design of potent small-molecule inhibitors of anti-apoptotic Bcl-2 proteins. J. Med. Chem. 49, 6139-6142.
42. Wang, S., Nikolovska-Coleska, Z., Yang, C.-Y., and Chen, J. (2006b). Apogossypolone and the Uses Thereof. PCT Int. Appl, WO 2006050447 A2 20060511.
43. Wang, J. L., Liu, D., Zhang, Z. J., Shan, S., Han, X., Srinivasula, S. M., Croce, C. M., Alnemri, E. S., and Huang, Z. (2000). 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. 97, 7124-7129.
44. Wang, S., and Yang, D. (2004). Small Molecular Antagonists of Bcl-2 Family Proteins. US patent applications series no. 2004/0214902 A1. 10/729,156.
45. Wei, J., Kitada, S., Rega, M. F., Emdadi, A., Yuan, H., Cellitti, J., Stebbins, J. L., Zhai, D., Sun, J., Yang, L., Dahl, R., Zhang, Z., Wu, B., Wang, S., Reed, T. A., Lawrence, N., Sebti, S., Reed, J. C., and Pellecchia, M. (2009a). Apogossypol derivatives as antagonists of antiapoptotic Bcl-2 family proteins. Mol. Cancer Ther. 8, 904-913.
46. Wei, J., Kitada, S., Rega, M. F., Stebbins, J. L., Zhai, D., Cellitti, J., Yuan, H., Emdadi, A., Dahl, R., Zhang, Z., Yang, L., Reed, J. C., and Pellecchia, M. (2009b). Apogossypol derivatives as pan-active inhibitors of antiapoptotic B-cell lymphoma/leukemia-2 (Bcl-2) family proteins. J. Med. Chem. 52, 4511-4523.
47. Wei, J., Rega, M. F., Kitada, S., Yuan, H., Zhai, D., Risbood, P., Seltzman, H. H., Twine, C. E., Reed, J. C., and Pellecchia, M. (2009c). Synthesis and evaluation of apogossypol atropisomers as potential Bcl-xL antagonists. Cancer Lett. 273, 107-113.
48. Wei, J., Kitada, S., Stebbins, J. L., Placzek, W., Zhai, D., Wu, B., Rega, M. F., Zhang, Z., Cellitti, J., Yang, L., Dahl, R., Reed, J. C., and Pellecchia, M. (2010a). Synthesis and biological evaluation of apogossypolone derivatives as pan-active inhibitors of antiapoptotic B-cell lymphoma/leukemia-2 (Bcl-2) family proteins. J. Med. Chem. 53, 8000-8011.
49. Wei, J., Stebbins, J. L., Kitada, S., Dash, R., Placzek, W., Rega, M. F., Wu, B., Cellitti, J., Zhai, D., Yang, L., Dahl, R., Fisher, P. B., Reed, J. C., and Pellecchia, M. (2010b). BI-97C1, an optically pure apogossypol derivative as pan-active inhibitor of antiapoptotic B-cell lymphoma/leukemia-2 (Bcl-2) family proteins. J. Med. Chem. 53, 4166-4176.
50. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., Macgregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001). Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730.
51. Wesarg, E., Hoffarth, S., Wiewrodt, R., Kroll, M., Biesterfeld, S., Huber, C., and Schuler, M. (2007). Targeting BCL-2 family proteins to overcome drug resistance in non-small cell lung cancer. Int. J. Cancer 121, 2387-2394.