Differential induction of quinone reductase by phytoestrogens and protection against oestrogen-induced DNA damage

Biochemical Journal

Volumn 385, Issue 1, 2005, Pages 279-287

  Bianco, Nicole R ^a   Chaplin, Laura J ^a   Montano, Monica M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Breast cancer; Oestrogen; Oestrogen receptor ; Oxidative damage; Phytoestrogens; Quinone reductase

Indexed keywords

ANTIOXIDANTS; CELLS; ENZYMES; METABOLITES; REDUCTION; TUMORS;

BREAST CANCER; OESTROGENS; PHYTOESTROGENS; QUINONE REDUCTASE (QR);

DNA;

BIOCHANIN A; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR BETA; GENISTEIN; PHYTOESTROGEN; QUININE DERIVATIVE; QUININE REDUCTASE; RESVERATROL; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; BREAST CANCER; CELL FUNCTION; CELL PROTECTION; CELL SPECIFICITY; CONTROLLED STUDY; DETOXIFICATION; DNA DAMAGE; ENZYME INDUCTION; ESTROGEN ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR BINDING; STATISTICAL SIGNIFICANCE; TRANSACTIVATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; DNA DAMAGE; ENZYME INDUCTION; ESTROGEN RECEPTOR BETA; ESTROGENS; GENISTEIN; HUMANS; LIGANDS; NAD(P)H DEHYDROGENASE (QUINONE); OXIDATIVE STRESS; PHYTOESTROGENS; RESPONSE ELEMENTS; STILBENES; TRANSCRIPTION, GENETIC;

CINCHONA PUBESCENS;

EID: 12744280974     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040959     Document Type: Article

References (48)

1. Talalay, P. and Dinkova-Kostova, A. T. (2004) Role of nicotinamide quinone oxidoreductase 1 (NQ01) in protection against toxicity of electrophiles and reactive oxygen intermediates. Methods Enzymol. 382, 355-364
2. Begleiter, A. and Fourie, J. (2004) Induction of NQ01 in cancer cells. Methods Enzymol. 382, 320-351
3. Barkhem, T., Nilsson, S. and Gustafsson, J. A. (2004) Molecular mechanisms, physiological consequences and pharmacological implications of estrogen receptor action. Am. J. Pharmacogenomics 4, 19-28
4. Montano, M. M., Jaiswal, A. K. and Katzenellenbogen, B. S. (1998) Transcriptional regulation of the human quinone reductase gene by antiestrogen-liganded estrogen receptor-α and estrogen receptor-β. J. Biol. Chem. 273, 25443-25449
5. Fisher, B., Costantino, J. P., Wickerham, D. L., Redmond, C. K., Kavanah, M., Cronin, W. M., Vogel, V., Robidoux, A., Dimitrov, N., Atkins, J. et al. (1998) Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J. Natl. Cancer Inst. 90, 1371-1388
6. Veronesi, U., Maisonneuve, P., Rotmensz, N., Costa, A., Sacchini, V., Travaglini, R., D'Aiuto, G., Lovison, F., Gucciardo, G., Muraca, M. G. et al. (2003) Italian randomized trial among women with hysterectomy: tamoxifen and hormone-dependent breast cancer in high-risk women. J. Natl. Cancer Inst. 95, 160-165
7. Cauley, J. A., Norton, L., Lippman, M. E., Eckert, S., Krueger, K. A., Purdie, D. W., Farrerons, J., Karasik, A., Mellstrom, D., Ng, K. W. et al. (2001) Continued breast cancer risk reduction in postmenopausal women treated with raloxifene: 4-year results from the MORE trial. Multiple outcomes of raloxifene evaluation. Breast Cancer Res. Treat. 65, 125-134
8. Bianco, N. R., Perry, G., Smith, M. A., Templeton, D. J. and Montano, M. M. (2003) Functional implications of antiestrogen induction of quinone reductase: inhibition of estrogen-induced DNA damage. Mol. Endocrinol. 17, 1344-1355
9. Castagnetta, L. A., Granata, O. M., Traina, A., Ravazzolo, B., Amoroso, M., Miele, M., Bellavia, V., Agostara, B. and Carruba, G. (2002) Tissue content of hydroxyestrogens in relation to survival of breast cancer patients. Clin. Cancer Res. 8, 3146-3155
10. Liehr, J. G. (2000) Is estradiol a genotoxic mutagenic carcinogen? Endocrinol. Rev. 21, 40-54
11. Bhat, H. K., Calaf, G., Hei, T. K., Loya, T. and Vadgama, J. V. (2003) Critical role of oxidative stress in estrogen-induced carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 3913-3918
12. Hiraku, Y., Yamashita, N., Nishiguchi, M. and Kawanishi, S. (2001) Catechol estrogens induce oxidative DNA damage and estradiol enhances cell proliferation. Int. J. Cancer 92, 333-337
13. Roy, D. and Liehr, J. G. (1988) Temporary decrease in renal quinone reductase activity induced by chronic administration of estradiol to male Syrian hamsters. Increased superoxide formation by redox cycling of estrogen. J. Biol. Chem. 263, 3646-3651
14. Shen, L., Pisha, E., Huang, Z., Pezzuto, J. M., Krol, E., Alam, Z., van Breemen, R. B. and Bolton, J. L. (1997) Bioreductive activation of catechol estrogen-ortho-quinones: aromatization of the B ring in 4-hydroxyequilenin markedly alters quinoid formation and reactivity. Carcinogenesis 18, 1093-1101
15. Ross, J. A. and Kasum, C. M. (2002) Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 22, 19-34
16. This, P., De La Rochefordiere, A., Clough, K., Fourquet, A. and Magdelenat, H. (2001) Phytoestrogens after breast cancer. Endocr. Relat. Cancer 8, 129-134
17. Mizunuma, H., Kanazawa, K., Ogura, S., Otsuka, S. and Nagai, H. (2002) Anticarcinogenic effects of isoflavones may be mediated by genistein in mouse mammary tumor virus-induced breast cancer. Oncology 62, 78-84
18. Whitten, P. L. and Patisaul, H. B. (2001) Cross-species and interassay comparisons of phytoestrogen action. Environ. Health Perspect. 109 (Suppl. 1), 5-20
19. Peelers, P. H., Keinan-Boker, L., van der Schouw, Y. T. and Grobbee, D. E. (2003) Phytoestrogens and breast cancer risk. Review of the epidemiological evidence. Breast Cancer Res. Treat 77, 171-183
20. An, J., Tzagarakis-Foster, C., Scharschmidt, T. C., Lomri, N. and Leitman, D. C. (2001) Estrogen receptor β-selective transcriptional activity and recruitment of coregulators by Phytoestrogens. J. Biol. Chem. 276, 17808-17814
21. Kuiper, G. G., Lemmen, J. G., Carlsson, B., Corton, J. C., Safe, S. H., van der Saag, P. T., van der Burg, B. and Gustafsson, J. A. (1998) Interaction of estrogenic chemicals and Phytoestrogens with estrogen receptor β. Endocrinology 139, 4252-4263
22. Morito, K., Aomori, T., Hirose, T., Kinjo, J., Hasegawa, J., Ogawa, S., Inoue, S., Muramatsu, M. and Masamune, Y. (2002) Interaction of phytoestrogens with estrogen receptors α and β (II). Biol. Pharm. Bull. 25, 48-52
23. Morito, K., Hirose, T., Kinjo, J., Hirakawa, T., Okawa, M., Nohara, T., Ogawa, S., Inoue, S., Muramatsu, M. and Masamune, Y. (2001) Interaction of phytoestrogens with estrogen receptors α and β. Biol. Pharm. Bull. 24, 351-356
24. Wang, W., Liu, L. Q., Higuchi, C. M. and Chen, H. (1998) Induction of NADPH:quinone reductase by dietary phytoestrogens in colonic Colo205 cells. Biochem. Pharmacol. 56, 189-195
25. Yang, S. H., Kim, J. S., Oh, T. J., Kim, M. S., Lee, S. W., Woo, S. K., Cho, H. S., Choi, Y. H., Kim, Y. H., Rha, S. Y. et al. (2003) Genome-scale analysis of resveratrol-induced gene expression profile in human ovarian cancer cells using a cDNA microarray. Int. J. Oncol. 22, 741-750
26. Heo, Y. H., Kim, S., Park, J. E., Jeong, L. S. and Lee, S. K. (2001) Induction of quinone reductase activity by stilbene analogs in mouse Hepa 1c1c7 cells. Arch. Pharm. Res. 24, 597-600
27. Montano, M. M. and Katzenellenbogen, B. S. (1997) The quinone reductase gene: a unique estrogen receptor-regulated gene that is activated by antiestrogens. Proc. Natl. Acad. Sci. U.S.A. 94, 2581-2586
28. Montano, M. M., Ekena, K., Krueger, K. D., Keller, A. L. and Katzenellenbogen, B. S. (1996) Human estrogen receptor ligand activity inversion mutants: receptors that interpret antiestrogens as estrogens and estrogens as antiestrogens and discriminate among different antiestrogens. Mol. Endocrinol. 10, 230-242
29. Paulus, W., Baur, I., Boyce, F. M., Breakfield, X. O. and Reeves, S. A. (1996) Self-contained, tetracycline regulated retroviral vector system for gene delivery to mammalian cells. J. Virol. 70, 62-67
30. Girdler, F., Browell, D. A., Cunliffe, W. J., Shenton, B. K., Hemming, J. D., Scorer, P., Young, J. R. and Brotherick, I. (2001) Use of the monoclonal antibody DAKO-ERβ (8D5-8D1) to measure oestrogen receptor beta in breast cancer cells. Cytometry 45, 65-72
31. Bowers, J. L., Tyulmenkov, V. V., Jernigan, S. C. and Klinge, C. M. (2000) Resveratrol acts as a mixed agonist/antagonist for estrogen receptors α and β. Endocrinology 141, 3657-3667
32. Montano, M. M., Wittmann, B. M. and Bianco, N. R. (2000) Identification and characterization of a novel factor that regulates quinone reductase gene transcriptional activity. J. Biol. Chem. 275, 34306-34313
33. Fuqua, S. A., Schiff, R., Parra, I., Friedrichs, W. E., Su, J. L., McKee, D. D., Slentz-Kesler, K., Moore, L. B., Willson, T. M. and Moore, J. T. (1999) Expression of wild-type estrogen receptor beta and variant isoforms in human breast cancer. Cancer Res. 59, 5425-5428
34. Shang, Y., Hu, X., DiRenzo, J., Lazar, M. A. and Brown, M. (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell (Cambridge, Mass.) 103, 843-852
35. Dhakshinamoorthy, S., Long, D. J. and Jaiswal, A. K. (2000) Antioxidant regulation of genes encoding enzymes that detoxify xenobiotics and carcinogens. Curr. Top. Cell Regul. 36, 201-216
36. Nioi, P., McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 374, 337-348
37. Murata, M., Midorikawa, K., Koh, M., Umezawa, K. and Kawanishi, S. (2004) Genistein and daidzein induce cell proliferation and their metabolites cause oxidative DNA damage in relation to isoflavone-induced cancer of estrogen-sensitive organs. Biochem. J. 43, 2569-2577
38. Nguyen, T., Yang, C. S. and Pickett, C. B. (2004) The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radical Biol. Med. 37, 433-441
39. Hayashi, S., Hajiro-Nakanishi, K., Makino, Y., Eguchi, H., Yodoi, J. and Tanaka, H. (1997) Functional modulation of estrogen receptor by redox state with reference to thioredoxin as a mediator. Nucleic Acid Res. 25, 4035-4040
40. Maubach, J., Bracke, M. E., Heyerick, A., Depypere, H. T., Serreyn, R. F., Mareel, M. M. and De Keukeleire, D. (2003) Quantitation of soy-derived phytoestrogens in human breast tissue and biological fluids by high-performance liquid chromatography. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 784, 137-144
41. Pike, A. C., Brzozowski, A. M., Hubbard, R. E., Bonn, T., Thorsell, A. G., Engstrom, O., Ljunggren, J., Gustafsson, J. A. and Carlquist, M. (1999) Structure of the ligand-binding domain of oestrogen receptor β in the presence of a partial agonist and a full antagonist. EMBO J. 18, 4608-4618
42. Wei, H., Cai, Q. and Rahn, R. O. (1996) Inhibition of UV light- and Fenton reaction-induced oxidative DNA damage by the soybean isoflavone genistein. Carcinogenesis 17, 73-77
43. Wei, H., Zhang, X., Wang, Y. and Lebwohl, M. (2002) Inhibition of ultraviolet light-induced oxidative events in the skin and internal organs of hairless mice by isoflavone genistein. Cancer Lett. 185, 21-29
44. Seike, N., Wanibuchi, H., Morimura, K., Wei, M., Nishikawa, T., Hirata, K., Yoshikawa, J. and Fukushima, S. (2003) Enhancement of lung carcinogenesis by nonylphenol and genistein in a F344 rat multiorgan carcinogenesis model. Cancer Lett. 192, 25-36
45. Peterson, T. G., Coward, L., Kirk, M., Falany, C. N. and Barnes, S. (1996) The role of metabolism in mammary epithelial cell growth inhibition by the isoflavones genistein and biochanin A. Carcinogenesis 17, 1861-1869
46. Kulling, S. E., Lehmann, L. and Metzler, M. (2002) Oxidative metabolism and genotoxic potential of major isoflavone phytoestrogens. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 777, 211-218
47. Kulling, S. E., Honig, D. M. and Metzler, M. (2001) Oxidative metabolism of the soy isoflavones daidzein and genistein in humans in vitro and in vivo. J. Agric. Food Chem. 49, 3024-3033
48. Magee, P. J. and Rowland, R. I. (2004) Phyto-oestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br. J. Nutr. 91, 513-531