Direct binding of Bcl-2 family proteins by quercetin triggers its pro-apoptotic activity

ACS Chemical Biology

Volumn 9, Issue 12, 2014, Pages 2737-2741

  Primikyri, Alexandra ^a   Chatziathanasiadou, Maria V ^a   Karali, Evdoxia ^b,c   Kostaras, Eleftherios ^b,c   Mantzaris, Michalis D ^b   Hatzimichael, Eleftheria ^a,b   Shin, Jae Sun ^d   Chi, Seung Wook ^d   Briasoulis, Evangelos ^a,b   Kolettas, Evangelos ^b,c   Gerothanassis, Ioannis P ^a,b   Tzakos, Andreas G ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

^c Cancer Biobank Center University of Ioannina ^*  (Greece)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL; QUERCETIN; ANTINEOPLASTIC AGENT; BCL2 PROTEIN, HUMAN; BCL2L1 PROTEIN, HUMAN; PROTEIN BCL X; PROTEIN BINDING; RECOMBINANT PROTEIN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CALCULATION; CANCER CELL; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PHYSICAL CHEMISTRY; PROTEIN DOMAIN; PROTEIN EXPRESSION; CHEMISTRY; DRUG EFFECTS; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; JURKAT CELL LINE; METABOLISM; MOLECULAR DOCKING; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-X PROTEIN; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JURKAT CELLS; MOLECULAR DOCKING SIMULATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS C-BCL-2; QUERCETIN; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84919621417     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500259e     Document Type: Article

References (29)

1. Hanahan, D. and Weinberg, R. A. (2011) Hallmarks of cancer: The next generation Cell 144, 646-674
2. Adams, J. M. and Cory, S. (2007) The Bcl-2 apoptotic switch in cancer development and therapy Oncogene 26, 1324-1337
3. Brunelle, J. K. and Letai, A. (2009) Control of mitochondrial apoptosis by the Bcl-2 family J. Cell Sci. 122, 437-441
4. Kitada, S., Pedersen, I. M., Schimmer, A. D., and Reed, J. C. (2002) Dysregulation of apoptosis genes in hematopoietic malignancies Oncogene 21, 3459-3474
5. Dalafave, D. S. and Prisco, G. (2010) Inhibition of antiapoptotic BCL-XL, BCL-2, and MCL-1 proteins by small molecule mimetics Cancer Inform 9, 169-177
6. Souers, A. J., Leverson, J. D., Boghaert, E. R., Ackler, S. L., Catron, N. D., Chen, J., Dayton, B. D., Ding, H., Enschede, S. H., Fairbrother, W. J., Huang, D. C., Hymowitz, S. G., Jin, S., Khaw, S. L., Kovar, P. J., Lam, L. T., Lee, J., Maecker, H. L., Marsh, K. C., Mason, K. D., Mitten, M. J., Nimmer, P. M., Oleksijew, A., Park, C. H., Park, C. M., Phillips, D. C., Roberts, A. W., Sampath, D., Seymour, J. F., Smith, M. L., Sullivan, G. M., Tahir, S. K., Tse, C., Wendt, M. D., Xiao, Y., Xue, J. C., Zhang, H., Humerickhouse, R. A., Rosenberg, S. H., and Elmore, S. W. (2013) ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets Nat. Med. 19, 202-208
7. Vaillant, F., Merino, D., Lee, L., Breslin, K., Pal, B., Ritchie, M. E., Smyth, G. K., Christie, M., Phillipson, L. J., Burns, C. J., Mann, G. B., Visvader, J. E., and Lindeman, G. J. (2013) Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer Cancer Cell 24, 120-129
8. Janga, S. C. and Tzakos, A. (2009) Structure and organization of drug-target networks: insights from genomic approaches for drug discovery Mol. BioSyst. 5, 1536-1548
9. Kontogianni, V. G., Tomic, G., Nikolic, I., Nerantzaki, A. A., Sayyad, N., Stosic-Grujicic, S., Stojanovic, I., Gerothanassis, I. P., and Tzakos, A. G. (2013) Phytochemical profile of Rosmarinus officinalis and Salvia officinalis extracts and correlation to their antioxidant and anti-proliferative activity Food Chem. 136, 120-129
10. Liu, G., Kelly, W. K., Wilding, G., Leopold, L., Brill, K., and Somer, B. (2009) An open-label, multicenter, phase I/II study of single-agent AT-101 in men with castrate-resistant prostate cancer Clin. Cancer Res. 15, 3172-3176
11. Sonpavde, G., Matveev, V., Burke, J. M., Caton, J. R., Fleming, M. T., Hutson, T. E., Galsky, M. D., Berry, W. R., Karlov, P., Holmlund, J. T., Wood, B. A., Brookes, M., and Leopold, L. (2012) Randomized phase II trial of docetaxel plus prednisone in combination with placebo or AT-101, an oral small molecule Bcl-2 family antagonist, as first-line therapy for metastatic castration-resistant prostate cancer Ann. Oncol 23, 1803-1808
12. Spagnuolo, C., Cerella, C., Russo, M., Chateauvieux, S., Diederich, M., and Russo, G. L. (2011) Quercetin downregulates Mcl-1 by acting on mRNA stability and protein degradation Br. J. Cancer 105, 221-230
13. Cheng, S., Gao, N., Zhang, Z., Chen, G., Budhraja, A., Ke, Z., Son, Y. O., Wang, X., Luo, J., and Shi, X. (2010) Quercetin induces tumor-selective apoptosis through downregulation of Mcl-1 and activation of Bax Clin. Cancer Res. 16, 5679-5691
14. Russo, M., Spagnuolo, C., Tedesco, I., Bilotto, S., and Russo, G. L. (2012) The flavonoid quercetin in disease prevention and therapy: Facts and fancies Biochem. Pharmacol. 83, 6-15
15. Batsi, C., Markopoulou, S., Kontargiris, E., Charalambous, C., Thomas, C., Christoforidis, S., Kanavaros, P., Constantinou, A. I., Marcu, K. B., and Kolettas, E. (2009) Bcl-2 blocks 2-methoxyestradiol induced leukemia cell apoptosis by a p27(Kip1)-dependent G1/S cell cycle arrest in conjunction with NF-kappaB activation Biochem. Pharmacol. 78, 33-44
16. 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
17. Hou, D. X. and Kumamoto, T. (2010) Flavonoids as protein kinase inhibitors for cancer chemoprevention: Direct binding and molecular modeling Antioxid Redox Signal 13, 691-719
18. Krishnamoorthy, J., Yu, V. C., and Mok, Y. K. (2010) Auto-FACE: An NMR based binding site mapping program for fast chemical exchange protein-ligand systems PLoS One 5, e8943
19. Tzakos, A. G. and Gerothanassis, I. P. (2005) Domain-selective ligand-binding modes and atomic level pharmacophore refinement in angiotensin I converting enzyme (ACE) inhibitors Chembiochem 6, 1089-1103
20. Ku, B., Liang, C., Jung, J. U., and Oh, B. H. (2011) Evidence that inhibition of BAX activation by BCL-2 involves its tight and preferential interaction with the BH3 domain of BAX Cell Res. 21, 627-641
21. 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
22. Leone, M., Zhai, D., Sareth, S., Kitada, S., Reed, J. C., and Pellecchia, M. (2003) Cancer prevention by tea polyphenols is linked to their direct inhibition of antiapoptotic Bcl-2-family proteins Cancer Res. 63, 8118-8121
23. 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
24. 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 tumors Nature 435, 677-681
25. Tzakos, A. G., Fokas, D., Johannes, C., Moussis, V., Hatzimichael, E., and Briasoulis, E. (2011) Targeting oncogenic protein-protein interactions by diversity oriented synthesis and combinatorial chemistry approaches Molecules 16, 4408-4427
26. Magnani, F., Pappas, C. G., Crook, T., Magafa, V., Cordopatis, P., Ishiguro, S., Ohta, N., Selent, J., Bosnyak, S., Jones, E. S., Gerothanassis, I. P., Tamura, M., Widdop, R. E., and Tzakos, A. G. (2014) Electronic sculpting of ligand-GPCR subtype selectivity: The case of angiotensin II ACS Chem. Biol. 9, 1420-1425
27. Vermes, I., Haanen, C., Steffens-Nakken, H., and Reutelingsperger, C. (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V J. Immunol Methods 184, 39-51
28. Petros, A. M., Medek, A., Nettesheim, D. G., Kim, D. H., Yoon, H. S., Swift, K., Matayoshi, E. D., Oltersdorf, T., and Fesik, S. W. (2001) Solution structure of the antiapoptotic protein Bcl-2 Proc. Natl. Acad. Sci. U.S.A. 98, 3012-3017
29. Xu, H., Ye, H., Osman, N. E., Sadler, K., Won, E. Y., Chi, S. W., and Yoon, H. S. (2009) The MDM2-binding region in the transactivation domain of p53 also acts as a Bcl-X(L)-binding motif Biochemistry 48, 12159-12168