Resveratrol enhances the efficacy of sorafenib mediated apoptosis in human breast cancer MCF7 cells through ROS, cell cycle inhibition, caspase 3 and PARP cleavage

Biomedicine and Pharmacotherapy

Volumn 84, Issue , 2016, Pages 1906-1914

  Mondal, Arindam ^a,b   Bennett, Lunawati L ^a  

^a UNION UNIVERSITY   (United States)

^b FLORIDA A AND M UNIVERSITY   (United States)

Author keywords

Apoptosis; Cell cycle inhibition; MCF7; Resveratrol; ROS; Sorafenib

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; CYCLIN B1; CYCLIN D1; DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RESVERATROL; SORAFENIB; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE; STILBENE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL STRUCTURE; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; DRUG EFFICACY; DRUG POTENTIATION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BREAST NEOPLASMS; CELL CYCLE CHECKPOINT; CELL SURVIVAL; COMBINATION DRUG THERAPY; DOSE RESPONSE; DRUG EFFECTS; FEMALE; MCF-7 CELL LINE; METABOLISM; PHYSIOLOGY; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BREAST NEOPLASMS; CASPASE 3; CELL CYCLE CHECKPOINTS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; FEMALE; HUMANS; MCF-7 CELLS; NIACINAMIDE; PHENYLUREA COMPOUNDS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; STILBENES; TREATMENT OUTCOME;

EID: 85002248994     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2016.10.096     Document Type: Article

References (31)

1. [1] DiSipio, T., Rye, S., Newman, B., Hayes, S., Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol. 14 (2013), 500–515, 10.1016/S1470-2045(13)70076-7.
2. [2] Knobf, M.T., The influence of endocrine effects of adjuvant therapy on quality of life outcomes in younger breast cancer survivors. Breast Cancer Oncol. 11 (2006), 96–110, 10.1634/theoncologist.11-2-96.
3. [3] Coley, H.M., Mechanisms and strategies to overcome chemotherapy resistance in metastatic breast cancer. Cancer Treat. Rev. 34 (2008), 378–390, 10.1016/j.ctrv.2008.01.007.
4. [4] Block, K.I., Gyllenhaal, C., Lowe, L., Amedei, A., Amin, A.R., Amin, A., Aquilano, K., Arbiser, J., Arreola, A., Arzumanyan, A., Ashraf, S.S., Azmi, A.S., Benencia, F., Bhakta, D., Bilsland, A., Bishayee, A., Blain, S.W., Block, P.B., Boosani, C.S., Carey, T.E., Carnero, A., Carotenuto, M., Casey, S.C., Chakrabarti, M., Chaturvedi, R., Chen, G.Z., Chen, H., Chen, S., Chen, Y.C., Choi, B.K., Ciriolo, M.R., Coley, H.M., Collins, A.R., Connell, M., Crawford, S., Curran, C.S., Dabrosin, C., Damia, G., Dasgupta, S., DeBerardinis, R.J., Decker, W.K., Dhawan, P., Diehl, A.M., Dong, J.T., Dou, Q.P., Drew, J.E., Elkord, E., El-Rayes, B., Feitelson, M.A., Felsher, D.W., Ferguson, L.R., Fimognari, C., Firestone, G.L., Frezza, C., Fujii, H., Fuster, M.M., Generali, D., Georgakilas, A.G., Gieseler, F., Gilbertson, M., Green, M.F., Grue, B., Guha, G., Halicka, D., Helferich, W.G., Heneberg, P., Hentosh, P., Hirschey, M.D., Hofseth, L.J., Holcombe, R.F., Honoki, K., Hsu, H.Y., Huang, G.S., Jensen, L.D., Jiang, W.G., Jones, L.W., Karpowicz, P.A., Keith, W.N., Kerkar, S.P., Khan, G.N., Khatami, M., Ko, Y.H., Kucuk, O., Kulathinal, R.J., Kumar, N.B., Kwon, B.S., Le, A., Lea, M.A., Lee, H.Y., Lichtor, T., Lin, L.T., Locasale, J.W., Lokeshwar, B.L., Longo, V.D., Lyssiotis, C.A., MacKenzie, K.L., Malhotra, M., Marino, M., Martinez-Chantar, M.L., Matheu, A., Maxwell, C., McDonnell, E., Meeker, A.K., Mehrmohamadi, M., Mehta, K., Michelotti, G.A., Mohammad, R.M., Mohammed, S.I., Morre, D.J., Muralidhar, V., Muqbil, I., Murphy, M.P., Nagaraju, G.P., Nahta, R., Niccolai, E., Nowsheen, S., Panis, C., Pantano, F., Parslow, V.R., Pawelec, G., Pedersen, P.L., Poore, B., Poudyal, D., Prakash, S., Prince, M., Raffaghello, L., Rathmell, J.C., Rathmell, W.K., Ray, S.K., Reichrath, J., Rezazadeh, S., Ribatti, D., Ricciardiello, L., Robey, R.B., Rodier, F., Rupasinghe, H.P., Russo, G.L., Ryan, E.P., Samadi, A.K., Sanchez-Garcia, I., Sanders, A.J., Santini, D., Sarkar, M., Sasada, T., Saxena, N.K., Shackelford, R.E., Shantha Kumara, H.M., Sharma, D., Shin, D.M., Sidransky, D., Siegelin, M.D., Signori, E., Singh, N., Sivanand, S., Sliva, D., Smythe, C., Spagnuolo, C., Stafforini, D.M., Stagg, J., Subbarayan, P.R., Sundin, T., Talib, W.H., Thompson, S.K., Tran, P.T., Ungefroren, H., Vander Heiden, M.G., Venkateswaran, V., Vinay, D.S., Vlachostergios, P.J., Wang, Z., Wellen, K.E., Whelan, R.L., Yang, E.S., Yang, H., Yang, X., Yaswen, P., Yedjou, C., Yin, X., Zhu, J., Zollo, M., Designing a broad-spectrum integrative approach for cancer prevention and treatment. Semin. Cancer Biol. 35:Suppl (2015), S276–304, 10.1016/j.semcancer.2015.09.007.
5. [5] Wilhelm, S.M., Adnane, L., Newell, P., Villanueva, A., Llovet, J.M., Lynch, M., Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol. Cancer Ther. 7 (2008), 3129–3140, 10.1158/1535-7163.MCT-08-0013.
6. [6] Wilhelm, S., Carter, C., Lynch, M., Lowinger, T., Dumas, J., Smith, R.A., Schwartz, B., Simantov, R., Kelley, S., Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat. Rev. Drug Discov. 5 (2006), 835–844, 10.1038/nrd2130.
7. [7] Pal, H.C., Baxter, R.D., Hunt, K.M., Agarwal, J., Elmets, C.A., Athar, M., Afaq, F., Fisetin, a phytochemical, potentiates sorafenib-induced apoptosis and abrogates tumor growth in athymic nude mice implanted with BRAF-mutated melanoma cells. Oncotarget 6 (2015), 28296–28311, 10.18632/oncotarget.5064.
8. [8] Cohen, S.M., Mukerji, R., Timmermann, B.N., Samadi, A.K., Cohen, M.S., A novel combination of withaferin A and sorafenib shows synergistic efficacy against both papillary and anaplastic thyroid cancers. Am. J. Surg. 204 (2012), 895–901, 10.1016/j.amjsurg.2012.07.027.
9. [9] Ibrahim, N., Yu, Y., Walsh, W.R., Yang, J.L., Molecular targeted therapies for cancer: sorafenib mono-therapy and its combination with other therapies (review). Oncol. Rep. 27 (2012), 1303–1311, 10.3892/or.2012.1675.
10. [10] Savouret, J.F., Quesne, M., Resveratrol and cancer: a review. Biomed. Pharmacother. 56 (2002), 84–87, 10.1016/S0753-3322(01)00158-5.
11. [11] Shi, Y., Yang, S., Troup, S., Lu, X., Callaghan, S., Park, D.S., Xing, Y., Yang, X., Resveratrol induces apoptosis in breast cancer cells by E2F1-mediated up-regulation of ASPP1. Oncol. Rep. 25 (2011), 1713–1719, 10.3892/or.2011.1248.
12. [12] Trung, L.Q., Espinoza, J.L., Takami, A., Nakao, S., Resveratrol induces cell cycle arrest and apoptosis in malignant NK cells via JAK2/STAT3 pathway inhibition. PLoS One, 8, 2013, e55183, 10.1371/journal.pone.0055183.
13. [13] Khan, M.A., Chen, H.C., Wan, X.X., Tania, M., Xu, A.H., Chen, F.Z., Zhang, D.Z., Regulatory effects of resveratrol on antioxidant enzymes: a mechanism of growth inhibition and apoptosis induction in cancer cells. Mol. Cells 35 (2013), 219–225, 10.1007/s10059-013-2259-z.
14. [14] Sareen, D., Darjatmoko, S.R., Albert, D.M., Polans, A.S., Mitochondria, calcium, and calpain are key mediators of resveratrol-induced apoptosis in breast cancer. Mol. Pharmacol. 72 (2007), 1466–1475, 10.1124/mol.107.039040.
15. [15] Follo-Martinez, A.D., Banerjee, N., Li, X., Safe, S., Mertens-Talcott, S., Resveratrol and quercetin in combination have anticancer activity in colon cancer cells and repress oncogenic microRNA-27a. Nutr. Cancer 65 (2013), 494–504, 10.1080/01635581.2012.725194.
16. [16] Alayev, A., Berger, S.M., Kramer, M.Y., Schwartz, N.S., Holz, M.K., The combination of rapamycin and resveratrol blocks autophagy and induces apoptosis in breast cancer cells. J. Cell Biochem. 116 (2015), 450–457, 10.1002/jcb.24997.
17. [17] Kim, T.H., Shin, Y.J., Won, A.J., Lee, B.M., Choi, W.S., Jung, J.H., Chung, H.Y., Kim, H.S., Resveratrol enhances chemosensitivity of doxorubicin in multidrug-resistant human breast cancer cells via increased cellular influx of doxorubicin. Biochim. Biophys. Acta Gen. Subj. 1840 (2014), 615–625, 10.1016/j.bbagen.2013.10.023.
18. [18] Du, Q., Hu, B., An, H.M., Shen, K.E.P., Xu, L., Deng, S., Wei, M.M., Synergistic anticancer effects of curcumin and resveratrol in Hepa1-6 hepatocellular carcinoma cells. Oncol. Rep. 29 (2013), 1851–1858, 10.3892/or.2013.2310.
19. [19] Chou, T.C., Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 70:2 (2010), 440–446, 10.1158/0008-5472.CAN-09-1947.
20. [20] Kumar, D., Basu, S., Parija, L., Rout, D., Manna, S., Dandapat, J., Debata, P.R., Curcumin and ellagic acid synergistically induce ROS generation, DNA damage, p53 accumulation and apoptosis in HeLa cervical carcinoma cells. Biomed. Pharmacother. 81 (2016), 31–37, 10.1016/j.biopha.2016.03.037.
21. [21] Dai, W., Wang, F., Lu, J., Xia, Y., He, L., Chen, K., Li, J., Li, S., Liu, T., Zheng, Y., Wang, J., Lu, W., Zhou, Y., Yin, Q., Abudumijiti, H., Chen, R., Zhang, R., Zhou, L., Zhou, Z., Zhu, R., Yang, J., Wang, C., Zhang, H., Zhou, Y., Xu, L., Guo, C., By reducing hexokinase 2, resveratrol induces apoptosis in HCC cells addicted to aerobic glycolysis and inhibits tumor growth in mice. Oncotarget 6 (2015), 13703–13717, 10.18632/oncotarget.3800.
22. [22] Hengartner, M.O., The biochemistry of apoptosis. Nature 407 (2000), 770–776, 10.1038/35037710.
23. [23] Nagata, S., Apoptotic DNA fragmentation. Exp. Cell Res. 256 (2000), 12–18, 10.1006/excr.2000.4834.
24. [24] Simon, H.U., Haj-Yehia, A., Levi-Schaffer, F., Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5 (2000), 415–418, 10.1023/A:1009616228304.
25. [25] Mates, J.M., Sanchez-Jimenez, F.M., Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int. J. Biochem. Cell Biol. 32 (2000), 157–170, 10.1016/S1357-2725(99)00088-6.
26. [26] Zhang, T., Brazhnik, P., Tyson, J.J., Exploring mechanisms of the DNA-damage response: p53 pulses and their possible relevance to apoptosis. Cell Cycle 6 (2007), 85–94, 10.4161/cc.6.1.3705.
27. [27] Penninger, J.M., Kroemer, G., Mitochondria, AIF and caspases-rivaling for cell death. Nat. Cell Biol. 5 (2003), 97–99, 10.1038/ncb0203-97.
28. [28] Aarts, M., Linardopoulos, S., Turner, N.C., Tumour selective targeting of cell cycle kinases for cancer treatment. Curr. Opin. Pharmacol. 13 (2013), 529–535, 10.1016/j.coph.2013.03.012.
29. [29] Roy, P.G., Thompson, A.M., Cyclin D1 and breast cancer. Breast 15 (2006), 718–727, 10.1016/j.breast.2006.02.005.
30. [30] Suzuki, T., Urano, T., Miki, Y., Moriya, T., Akahira, J.I., Ishida, T., Horie, K., Inoue, S., Sasano, H., Nuclear cyclin B1 in human breast carcinoma as a potent prognostic factor. Cancer Sci. 98 (2007), 644–651, 10.1111/j.1349-7006.2007.00444.x.
31. [31] Jiang, W.G., Sanders, A.J., Katoh, M., Ungefroren, H., Gieseler, F., Prince, M., Thompson, S.K., Zollo, M., Spano, D., Dhawan, P., Sliva, D., Subbarayan, P.R., Sarkar, M., Honoki, K., Fujii, H., Georgakilas, A.G., Amedei, A., Niccolai, E., Amin, A., Ashraf, S.S., Ye, L., Helferich, W.G., Yang, X., Boosani, C.S., Guha, G., Ciriolo, M.R., Aquilano, K., Chen, S., Azmi, A.S., Keith, W.N., Bilsland, A., Bhakta, D., Halicka, D., Nowsheen, S., Pantano, F., Santini, D., Tissue invasion and metastasis: molecular, biological and clinical perspectives. Semin. Cancer Biol. 35:Suppl (2015), S244–S275, 10.1016/j.semcancer.2015.03.008.