Cytotoxic activity of soy phytoestrogen coumestrol against human breast cancer MCF-7 cells: Insights into the molecular mechanism

Food and Chemical Toxicology

Volumn 99, Issue , 2017, Pages 149-161

  Zafar, Atif ^a   Singh, Swarnendra ^b   Naseem, Imrana ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Apoptosis; Breast cancer; Copper; Coumestrol; DNA damage; ROS

Indexed keywords

2,9 DIMETHYL 1,10 PHENANTHROLINE; CASPASE 3; CASPASE 9; CATALASE; COPPER ION; COUMESTROL; GLUTATHIONE; PHYTOESTROGEN; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOUREA;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA FRAGMENTATION; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG EFFECT; ENZYME ACTIVITY; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC50; MCF 7 CELL LINE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MTT ASSAY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN EXPRESSION; SCANNING ELECTRON MICROSCOPY; SOY FOOD; UPREGULATION; WESTERN BLOTTING; CELL CYCLE; CHEMISTRY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PATHOLOGY; SOYBEAN;

APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; COUMESTROL; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PHYTOESTROGENS; REACTIVE OXYGEN SPECIES; SOYBEANS;

EID: 84999780414     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2016.11.034     Document Type: Article

References (70)

1. Azmi, A.S., Bhat, S.H., Hanif, S., Hadi, S.M., Plant polyphenols mobilize endogenous copper in human peripheral lymphocytes leading to oxidative DNA breakage: a putative mechanism for anticancer properties. FEBS Lett. 580 (2006), 533–538.
2. Barnes, S., Grubbs, C., Setchell, K.D.R., Carlson, J., Soybeans inhibit mammary tumours in models of breast cancer. Mutagens and Carcinogens in the Diet, 1990, Wiley-Liss, New York, 239–253.
3. Barnes, S., The chemopreventive properties of soy isoflavonoids in animal models of breast cancer. Breast Cancer Res. Treat. 46 (1997), 169–179.
4. Bauma, M., Demichelib, R., Hrusheskyc, W., Retskyd, M., Does surgery unfavourably perturb the ‘‘natural history’’ of early breast cancer by accelerating the appearance of distant metastases?. Eur. J. Cancer 41 (2005), 508–515.
5. Beutler, E., Duron, O., Kelly, B.M., Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61 (1963), 882–888.
6. Canal Castro, C., Pagnussat, A.S., Orlandi, L., Worm, P., Moura, N., Etgen, A.M., Alexandre Netto, C., Coumestrol has neuroprotective effects before and after global cerebral ischemia in female rats. Brain Res. 1474 (2012), 82–90.
7. Chibber, S., Farhan, M., Hassan, I., Naseem, I., White light-mediated Cu(II)-5FU interaction, augments chemotherapeutic potential of 5FU: an in vitro study. Tumour Biol. 32 (2011), 881–892.
8. Constantinou, A.I., Mehta, R.G., Vaughan, A., Inhibition of N-methyl-N-nitrosourea-induced mammary tumours in rats by the soybean isoflavones. Anticancer Res. 16 (1996), 3293–3298.
9. Daniel, K.G., Gupta, P., Harbach, R.H., Guida, W.C., Dou, Q.P., Organic copper complexes as a new class of proteasome inhibitors and apoptosis inducers in human cancer cells. Biochem. Pharmacol. 67 (2004), 1139–1151.
10. da Rocha, A.B., Lopes, R.M., Schwartsmann, G., Natural products in anticancer therapy. Curr. Opin. Pharmacol. 1 (2001), 364–369.
11. de Leeuw, R., Neefjes, J., Michalides, R., A role for estrogen receptor phosphorylation in the resistance to tamoxifen. Int. J. Breast Cancer, 2011, 2011, 232435.
12. de Lemos, M.L., Effects of soy phytoestrogens genistein and daidzein on breast cancer growth. Ann. Pharmacother. 35 (2001), 1118–1121.
13. Dikalov, S., Landmesser, U., Harrison, D.G., Geldanamycin leads to superoxide formation by enzymatic and non-enzymatic redox cycling. Implications for studies of Hsp90 and endothelial cell nitric-oxide synthase. J. Biol. Chem. 277 (2002), 25480–25485.
14. Dixon-Shanies, D., Shaikh, N., Growth inhibition of human breast cancer cells by herbs and phytoestrogens. Oncol. Rep. 6 (1999), 1383–1387.
15. Dong, J.Y., Qin, L.Q., Dietary glycemic index, glycemic load, and risk of breast cancer: meta-analysis of prospective cohort studies. Breast Cancer Res. Treat. 126 (2011), 287–294.
16. Ebadi, M., Swanson, S., The status of zinc, copper, and metallothionein in cancer patients. Prog. Clin. Biol. Res. 259 (1988), 161–175.
17. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L., Henson, P.M., Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148 (1992), 2207–2216.
18. Fritz, W.A., Coward, L., Wang, J., Lamartiniere, C.A., Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat. Carcinogenesis 19 (1998), 2151–2158.
19. Fulda, S., Debatin, K.M., Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25 (2006), 4798–4811.
20. Ganz, P.A., Kwan, L., Stanton, A.L., Bower, J.E., Belin, T.R., Physical and psychosocial recovery in the year after primary treatment of breast cancer. J. Clin. Oncol. 29 (2011), 1101–1109.
21. Gorrini, C., Harris, I.S., Mak, T.W., Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12 (2013), 931–947.
22. Green, D.R., Apoptotic pathways: ten minutes to dead. Cell 121 (2005), 671–674.
23. Gross, A., McDonnell, J.M., Korsmeyer, S.J., BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13 (1999), 1899–1911.
24. Hadi, S.M., Asad, S.F., Singh, S., Ahmad, A., Putative mechanism for anticancer and apoptosis-inducing properties of plant-derived polyphenolic compounds. IUBMB Life 50 (2000), 167–171.
25. Hadi, S.M., Bhat, S.H., Azmi, A.S., Hanif, S., Shamim, U., Ullah, M.F., Oxidative breakage of cellular DNA by plant polyphenols: a putative mechanism for anticancer properties. Semin. Cancer Biol. 17 (2007), 370–376.
26. Hsu, J.T., Hung, H.C., Chen, C.J., Hsu, W.L., Ying, C., Effects of the dietary phytoestrogen biochanin A on cell growth in the mammary carcinoma cell line MCF-7. J. Nutr. Biochem. 10 (1999), 510–517.
27. Huang, Y.L., Sheu, J.Y., Lin, T.H., Association between oxidative stress and changes of trace elements in patients with breast cancer. Clin. Biochem. 32 (1999), 131–136.
28. Huang, X., Powell, J., Mooney, L.A., Li, C., Frenkel, K., Importance of complete DNA digestion in minimizing variability of 8-oxo-dG analyses. Free Radic. Biol. Med. 31 (2001), 1341–1351.
29. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., Thun, M.J., Cancer statistics, 2008. CA Cancer J. Clin. 58 (2008), 71–96.
30. Kagan, V.E., Gleiss, B., Tyurina, Y.Y., Tyurin, V.A., Elenström-Magnusson, C., Liu, S.X., Serinkan, F.B., Arroyo, A., Chandra, J., Orrenius, S., Fadeel, B., A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J. Immunol. 169 (2002), 487–499.
31. Kagawa, T.F., Geierstanger, B.H., Wang, A.H., Ho, P.S., Covalent modification of guanine bases in double-stranded DNA. The 1.2-A Z-DNA structure of d(CGCGCG) in the presence of CuCl2. J. Biol. Chem. 266 (1991), 20175–20184.
32. Kapoor, R., Kakkar, P., Protective role of morin, a flavonoid, against high glucose induced oxidative stress mediated apoptosis in primary rat hepatocytes. PLoS One, 7, 2012, e41663.
33. Khan, H.Y., Zubair, H., Faisal, M., Ullah, M.F., Farhan, M., Sarkar, F.H., Ahmad, A., Hadi, S.M., Plant polyphenol induced cell death in human cancer cells involves mobilization of intracellular copper ions and reactive oxygen species generation: a mechanism for cancer chemopreventive action. Mol. Nutr. Food Res. 58 (2014), 437–446.
34. Koopman, G., Reutelingsperger, C.P., Kuijten, G.A., Keehnen, R.M., Pals, S.T., van Oers, M.H., Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994), 1415–1420.
35. Lee, J.H., Lee, B.W., Kim, J.H., Jeong, T.S., Kim, M.J., Lee, W.S., Park, K.H., LDL-antioxidant pterocarpans from roots of Glycine max (L.) Merr. J. Agric. Food Chem. 54 (2006), 2057–2063.
36. Lee, Y.H., Yuk, H.J., Park, K.H., Bae, Y.S., Coumestrol induces senescence through protein kinase CKII inhibition-mediated reactive oxygen species production in human breast cancer and colon cancer cells. Food Chem. 141 (2013), 381–388.
37. Lewandowska, U., Szewczyk, K., Owczarek, K., Hrabec, Z., Podsedek, A., Koziołkiewicz, M., Hrabec, E., Flavanols from evening primrose (Oenothera paradoxa) defatted seeds inhibit prostate cells invasiveness and cause changes in Bcl-2/Bax mRNA ratio. J. Agric. Food Chem. 61 (2013), 2987–2998.
38. Leu, J.I., Dumont, P., Hafey, M., Murphy, M.E., George, D.L., Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat. Cell Biol. 6 (2004), 443–450.
39. Lowndes, S.A., Harris, A.L., The role of copper in tumour angiogenesis. J. Mammary Gland. Biol. Neoplasia 10 (2005), 299–310.
40. Magee, P.J., McGlynn, H., Rowland, I.R., Differential effects of isoflavones and lignans on invasiveness of MDA-MB-231 breast cancer cells in vitro. Cancer Lett. 208 (2004), 35–41.
41. Martin, S.J., Reutelingsperger, C.P., McGahon, A.J., Rader, J.A., van Schie, R.C., LaFace, D.M., Green, D.R., Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182 (1995), 1545–1556.
42. Mohindru, A., Fisher, J.M., Rabinovitz, M., 2,9-Dimethyl-1,10-phenanthroline (neocuproine): a potent, copper-dependent cytotoxin with anti-tumor activity. Biochem. Pharmacol. 32 (1983), 3627–3632.
43. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983), 55–63.
44. Musgrove, E.A., Sutherland, R.L., Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer 9 (2009), 631–643.
45. Nasulewicz, A., Mazur, A., Opolski, A., Role of copper in tumour angiogenesis–clinical implications. J. Trace Elem. Med. Biol. 18 (2004), 1–8.
46. NCCN_Guidelines, NCCN Clinical Guidelines in Oncology—breast Cancer. 2014.
47. Newman, D.J., Cragg, G.M., Natural products as sources of new drugs over the 30 Years from 1981 to 2010. J. Nat. Prod. 75 (2012), 311–335.
48. Nogueira, V., Hay, N., Molecular pathways: reactive oxygen species homeostasis in cancer cells and implications for cancer therapy. Clin. Cancer Res. 19 (2013), 4309–4314.
49. Norbury, C.J., Zhivotovsky, B., DNA damage-induced apoptosis. Oncogene 23 (2004), 2797–2808.
50. Peng, F., Lu, X., Janisse, J., Muzik, O., Shields, A.F., PET of human prostate cancer xenografts in mice with increased uptake of CuCl2. J. Nucl. Med. 47 (2006), 1649–1652.
51. Sakamoto, T., Horiguchi, H., Oguma, E., Kayama, F., Effects of diverse dietary phytoestrogens on cell growth, cell cycle and apoptosis in estrogen-receptor-positive breast cancer cells. J. Nutr. Biochem. 21 (2010), 856–864.
52. Saraste, A., Pulkki, K., Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res. 45 (2000), 528–537.
53. Schumacker, P.T., Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10 (2006), 175–176.
54. Setchell, K.D., Cassidy, A., Dietary isoflavones: biological effects and relevance to human health. J. Nutr. 129 (1999), 758S–767S.
55. Shamim, U., Hanif, S., Ullah, M.F., Azmi, A.S., Bhat, S.H., Hadi, S.M., Plant polyphenols mobilize nuclear copper in human peripheral lymphocytes leading to oxidatively generated DNA breakage: implications for an anticancer mechanism. Free Radic. Res. 42 (2008), 764–772.
56. Trachootham, D., Alexandre, J., Huang, P., Targeting 627 cancer cells by ROS mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug. Discov. 8 (2009), 579–591.
57. Traverso, N., Ricciarelli, R., Nitti, M., Marengo, B., Furfaro, A.L., Pronzato, M.A., Marinari, U.M., Domenicotti, C., Role of glutathione in cancer progression and chemoresistance. Oxid. Med. Cell Longev., 2013, 2013, 972913.
58. Ullah, M.F., Shamim, U., Hanif, S., Azmi, A.S., Hadi, S.M., Cellular DNA breakage by soy isoflavone genistein and its methylated structural analogue biochanin A. Mol. Nutr. Food Res. 53 (2009), 1376–1385.
59. Ullah, M.F., Khan, H.Y., Zubair, H., Shamim, U., Hadi, S.M., The antioxidant ascorbic acid mobilizes nuclear copper leading to a prooxidant breakage of cellular DNA: implications for chemotherapeutic action against cancer. Cancer Chemother. Pharmacol 67 (2011), 103–110.
60. Verhoven, B., Schlegel, R.A., Williamson, P., Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med. 182 (1995), 1597–1601.
61. Vousden, K.H., Lu, X., Live or let die: the cell's response to p53. Nat. Rev. Cancer 2 (2002), 594–604.
62. Wang, C., Kurzer, M.S., Phytoestrogen concentration determines effects on DNA synthesis in human breast cancer cells. Nutr. Cancer 28 (1997), 236–247.
63. Wang, H., Joseph, J.A., Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27 (1999), 612–616.
64. Wu, X.T., Wang, B., Wei, J.N., Coumestrol promotes proliferation and osteoblastic differentiation in rat bone marrow stromal cells. J. Biomed. Mater Res. B Appl. Biomater. 90 (2009), 621–628.
65. Wyllie, A.H., Kerr, J.F., Currie, A.R., Cell death: the significance of apoptosis. Int. Rev. Cytol. 68 (1980), 251–306.
66. Yoshida, D., Ikeda, Y., Nakazawa, S., Quantitative analysis of copper, zinc and copper/zinc ratio in selected human brain tumors. J. Neurooncol 16 (1993), 109–115.
67. Zafar, A., Singh, S., Naseem, I., Cu(II)-coumestrol interaction leads to ROS-mediated DNA damage and cell death: a putative mechanism for anticancer activity. J. Nutr. Biochem. 33 (2016), 15–27.
68. Zava, D.T., Duwe, G., Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr. Cancer 27 (1997), 31–40.
69. Zowczak, M., Iskra, M., Torliński, L., Cofta, S., Analysis of serum copper and zinc concentrations in cancer patients. Biol. Trace Elem. Res. 82 (2001), 1–8.
70. Zubair, H., Khan, H.Y., Ullah, M.F., Ahmad, A., Wu, D., Hadi, S.M., Apogossypolone, derivative of gossypol, mobilizes endogenous copper in human peripheral lymphocytes leading to oxidative DNA breakage. Eur. J. Pharm. Sci. 47 (2012), 280–286.