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Dual roles of estrogen metabolism in mammary carcinogenesis

  • Chang, Min-Sun (Department of Medical and Pharmaceutical Science, College of Science, Sookmyung Women's University)
  • Received : 2011.06.29
  • Published : 2011.07.31

Abstract

A female hormone, estrogen, is linked to breast cancer incidence. Estrogens undergo phase I and II metabolism by which they are biotransformed into genotoxic catechol estrogen metabolites and conjugate metabolites are produced for excretion or accumulation. The molecular mechanisms underlying estrogen-mediated mammary carcinogenesis remain unclear. Cell proliferation through activation of estrogen receptor (ER) by its agonist ligands and is clearly considered as one of carcinogenic mechanisms. Recent studies have proposed that reactive oxygen species generated from estrogen or estrogen metabolites are attributed to genotoxic effects and signal transduction through influencing redox sensitive transcription factors resulting in cell transformation, cell cycle, migration, and invasion of the breast cancer. Conjuguation metabolic pathway is thought to protect cells from genotoxic and cytotoxic effects by catechol estrogen metabolites. However, methoxylated catechol estrogens have been shown to induce ER-mediated signaling pathways, implying that conjugation is not a simply detoxification pathway. Dual action of catechol estrogen metabolites in mammary carcinogenesis as the ER-signaling molecules and chemical carcinogen will be discussed in this review.

Keywords

References

  1. Beatson, G. T. (1896) On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new method of treatment with illustrative cases. Lancet 2, 104-107.
  2. Simpson, E. R. (2003) Sources of estrogen and their importance. J. Steroid Biochem. Mol. Biol. 86, 225-230. https://doi.org/10.1016/S0960-0760(03)00360-1
  3. Boukari, K., Ciampi, M. L., Guiochon-Mantel, A., Young, J., Lombes, M. and Meduri, G. (2007) Human fetal testis:source of estrogen and target of estrogen action. Hum. Reprod. 22, 1885-1892. https://doi.org/10.1093/humrep/dem091
  4. Colditz, G. A. (1998) Relationship between estrogen levels, use of hormone replacement therapy, and breast cancer. J. Natl. Cancer I. 90, 814-823. https://doi.org/10.1093/jnci/90.11.814
  5. Feigelson, H. S. and Henderson, B. E. (1996) Estrogens and breast cancer. Carcinogenesis 17, 2279-2284. https://doi.org/10.1093/carcin/17.11.2279
  6. Xu, W. H., Xiang, Y. B., Ruan, Z. X., Zheng, W., Cheng, J. R., Dai, Q., Gao, Y. T. and Shu, X. O. (2004) Menstrual and reproductive factors and endometrial cancer risk: results from a population-based case-control study in urban Shanghai. Int. J. Cancer 108, 613-619. https://doi.org/10.1002/ijc.11598
  7. Kaaks, R., Berrino, F., Key, T., Rinaldi, S., Dossus, L., Biessy, C., Secreto, G., Amiano, P., Bingham, S., Boeing, H., Bueno de Mesquita, H. B., Chang-Claude, J., Clavel-Chapelon, F., Fournier, A., van Gils, C. H., Gonzalez, C. A., Gurrea, A. B., Critselis, E., Khaw, K. T., Krogh, V., Lahmann, P. H., Nagel, G., Olsen, A., Onland-Moret, N. C., Overvad, K., Palli, D., Panico, S., Peeters, P., Quiros, J. R., Roddam, A., Thiebaut, A., Tjonneland, A., Chirlaque, M. D., Trichopoulou, A., Trichopoulos, D., Tumino, R., Vineis, P., Norat, T., Ferrari, P., Slimani, N. and Riboli, E. (2005) Serum sex steroids in premenopausal women and breast cancer risk within the European Prospective Investigation into Cancer and Nutrition (EPIC). J. Natl. Cancer Inst. 97, 755-765. https://doi.org/10.1093/jnci/dji132
  8. Zucchetto, A., Serraino, D., Polesel, J., Negri, E., De Paoli, A., Dal Maso, L., Montella, M., La Vecchia, C., Franceschi, S. and Talamini, R. (2009) Hormone-related factors and gynecological conditions in relation to endometrial cancer risk. Eur. J. Cancer Prev. 18, 316-321. https://doi.org/10.1097/CEJ.0b013e328329d830
  9. Russo, J., Hu, Y. F., Yang, X. and Russo, I. H. (2000) Developmental, cellular, and molecular basis of human breast cancer. J. Natl. Cancer Inst. Monogr. 27, 17-37.
  10. Castagnetta, L., Granata, O. M., Cocciadiferro, L., Saetta, A., Polito, L., Bronte, G., Rizzo, S., Campisi, I., Agostara, B. and Carruba, G. (2004) Sex steroids, carcinogenesis, and cancer progression. Ann. N.Y. Acad. Sci. 1028, 233-246. https://doi.org/10.1196/annals.1321.028
  11. Bocchinfuso, W. P. and Korach, K. S. (1997) Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J. Mal. Gland Biol. Neoplasia 2, 323-334. https://doi.org/10.1023/A:1026339111278
  12. The National Toxicology Program (NTP). (2002) Federal Report on Carcinogens. 177283-177285.
  13. WHO (1999) Hormonal Contraception and Post-Menopausal Hormonal Therapy; in IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, pp. 399-530, IARCPress, Lyon, France.
  14. Yager, J. D. and Davidson, N. E. (2006) Estrogen carcinogenesis in breast cancer. N. Engl. J. Med. 354, 270-282. https://doi.org/10.1056/NEJMra050776
  15. Russo, J. and Russo, I. H. (2006) The role of estrogen in the initiation of breast cancer. J. Steroid Biochem. Mol. Biol. 102, 89-96. https://doi.org/10.1016/j.jsbmb.2006.09.004
  16. Sarabia, S. F., Zhu, B. T., Kurosawa, T., Tohma, M. and Liehr, J. G. (1997) Mechanism of cytochrome P450-catalyzed aromatic hydroxylation of estrogens. Chem. Res. Toxicol. 10, 767-771. https://doi.org/10.1021/tx970021f
  17. Raftogianis, R., Creveling, C., Weinshilboum, R. and Weisz, J. (2000) Estrogen metabolism by conjugation. J. Natl. Cancer Inst. Monogr. 27, 113-124.
  18. Hachey, D. L., Dawling, S., Roodi, N. and Parl, F. F. (2003) Sequential action of phase I and II enzymes cytochrome p450 1B1 and glutathione S-transferase P1 in mammary estrogen metabolism. Cancer Res. 63, 8492-8499.
  19. Yue, W., Santen, R. J., Wang, J. P., Li, Y., Verderame, M. F., Bocchinfuso, W. P., Korach, K. S., Devanesan, P., Todorovic, R., Rogan, E. G. and Cavalieri, E. L. (2003) Genotoxic metabolites of estradiol in breast: potential mechanism of estradiol induced carcinogenesis. J. Steroid Biochem. Mol. Biol. 86, 477-486. https://doi.org/10.1016/S0960-0760(03)00377-7
  20. Russo, J., Fernandez, S. V., Russo, P. A., Fernbaugh, R., Sheriff, F. S., Lareef, H. M., Garber, J. and Russo, I. H. (2006) 17-Beta-estradiol induces transformation and tumorigenesis in human breast epithelial cells. FASEB J. 20, 1622-1634. https://doi.org/10.1096/fj.05-5399com
  21. Russo, J., Hasan Lareef, M., Balogh, G., Guo, S. and Russo, I. H. (2003) Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 87, 1-25. https://doi.org/10.1016/S0960-0760(03)00390-X
  22. Peng, K. W., Chang, M., Wang, Y. T., Wang, Z., Qin, Z., Bolton, J. L. and Thatcher, G. R. (2010) Unexpected hormonal activity of a catechol equine estrogen metabolite reveals reversible glutathione conjugation. Chem. Res. Toxicol. 23, 1374-1383. https://doi.org/10.1021/tx100129h
  23. Schutze, N., Vollmer, G. and Knuppen, R. (1994) Catecholestrogens are agonists of estrogen receptor dependent gene expression in MCF-7 cells. J. Steroid Biochem. Mol. Biol. 48, 453-461. https://doi.org/10.1016/0960-0760(94)90193-7
  24. Zhu, B. T. and Conney, A. H. (1998) Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis 19, 1-27. https://doi.org/10.1093/carcin/19.1.1
  25. Chang, M., Peng, K. W., Kastrati, I., Overk, C. R., Qin, Z. H., Yao, P., Bolton, J. L. and Thatcher, G. R. (2007) Activation of estrogen receptor-mediated gene transcription by the equine estrogen metabolite, 4-methoxyequilenin, in human breast cancer cells. Endocrinology 148, 4793-4802. https://doi.org/10.1210/en.2006-1568
  26. Tsutsui, T., Tamura, Y., Hagiwara, M., Miyachi, T., Hikiba, H., Kubo, C. and Barrett, J. C. (2000) Induction of mammalian cell transformation and genotoxicity by 2-methoxyestradiol, an endogenous metabolite of estrogen. Carcinogenesis 21, 735-740. https://doi.org/10.1093/carcin/21.4.735
  27. Sutherland, T. E., Schuliga, M., Harris, T., Eckhardt, B. L., Anderson, R. L., Quan, L. and Stewart, A. G. (2005) 2-Methoxyestradiol is an estrogen receptor agonist that supports tumor growth in murine xenograft models of breast cancer. Clin. Cancer Res. 11, 1722-1732. https://doi.org/10.1158/1078-0432.CCR-04-1789
  28. Parl, F. F., Egan, K. M., Li, C. and Crooke, P. S. (2009) Estrogen exposure, metabolism, and enzyme variants in a model for breast cancer risk prediction. Cancer Inform. 7, 109-121.
  29. Crooke, P. S., Justenhoven, C., Brauch, H. B., Dawling, S., Roodi, N., Higginbotham, K. S., Plummer, W. D., Jr., Schuyler, P. A., Sanders, M. E., Page, D. L., Smith, J. R., Dupont, W. D. and Parl, F. F. (2011) Estrogen metabolism and exposure in a genotypic-phenotypic model for breast cancer risk prediction. Cancer Epidemiol. Biomarkers Prev. 20, 1502-1515. https://doi.org/10.1158/1055-9965.EPI-11-0060
  30. Williamson, D. G. (1979) The biochemistry of the 17-hydroxysteroid dehydrogenases; in Steroid Biochemistry. (Hobkirk, R., ed.), pp. 83-110, CRC Press, Boca Raton, FL.
  31. Suchar, L. A., Chang, R. L., Rosen, R. T., Lech, J. and Conney, A. H. (1995) High-performance liquid chromatography separation of hydroxylated estradiol metabolites: formation of estradiol metabolites by liver microsomes from male and female rats. J. Pharmacol. Exp. Ther. 272, 197-206.
  32. Liehr, J. G., Fang, W. F., Sirbasku, D. A. and Ari- Ulubelen, A. (1986) Carcinogenicity of catechol estrogens in Syrian hamsters. J. Steroid Biochem. Mol. Biol. 24, 353-356. https://doi.org/10.1016/0022-4731(86)90080-4
  33. Li, J. J. and Li, S. A. (1987) Estrogen carcinogenesis in Syrian hamster tissues: role of metabolism. Fed. Proc. 46, 1858-1863.
  34. Newbold, R. R. and Liehr, J. G. (2000) Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res. 60, 235-237.
  35. Li, K. M., Todorovic, R., Devanesan, P., Higginbotham, S., Kofeler, H., Ramanathan, R., Gross, M. L., Rogan, E. G. and Cavalieri, E. L. (2004) Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25, 289-297.
  36. El-Bayoumy, K., Ji, B. Y., Upadhyaya, P., Chae, Y. H., Kurtzke, C., Rivenson, A., Reddy, B. S., Amin, S. and Hecht, S. S. (1996) Lack of tumorigenicity of cholesterol epoxides and estrone-3,4-quinone in the rat mammary gland. Cancer Res. 56, 1970-1973.
  37. Franks, S., MacLusky, N. J. and Naftolin, F. (1982) Comparative pharmacology of oestrogens and catechol oestrogens: actions on the immature rat uterus in vivo and in vitro. J. Endocrinol. 94, 91-98. https://doi.org/10.1677/joe.0.0940091
  38. Van Aswegen, C. H., Purdy, R. H. and Wittliff, J. L. (1989) Binding of 2-hydroxyestradiol and 4-hydroxyestradiol to estrogen receptors from human breast cancers. J. Steroid Biochem. 32, 485-492. https://doi.org/10.1016/0022-4731(89)90380-4
  39. Spink, D. C., Zhang, F., Hussain, M. M., Katz, B. H., Liu, X., Hilker, D. R. and Bolton, J. L. (2001) Metabolism of equilenin in MCF-7 and MDA-MB-231 human breast cancer cells. Chem. Res. Toxicol. 14, 572-581. https://doi.org/10.1021/tx000219r
  40. Yamazaki, H., Shaw, P. M., Guengerich, F. P. and Shimada, T. (1998) Roles of cytochromes P450 1A2 and 3A4 in the oxidation of estradiol and estrone in human liver microsomes. Chem. Res. Toxicol. 11, 659-665. https://doi.org/10.1021/tx970217f
  41. Zhang, F. and Bolton, J. L. (1999) Synthesis of the equine estrogen metabolites 2-hydroxyequilin and 2-hydroxyequilenin. Chem. Res. Toxicol. 12, 200-203. https://doi.org/10.1021/tx980189g
  42. Roy, D., Bernhardt, A., Strobel, H. W. and Liehr, J. G. (1992) Catalysis of the oxidation of steroid and stilbene estrogens to estrogen quinone metabolites by the beta-naphthoflavone-inducible cytochrome P450 IA family. Arch. Biochem. Biophys. 296, 450-456. https://doi.org/10.1016/0003-9861(92)90596-O
  43. Markides, C. S., Roy, D. and Liehr, J. G. (1998) Concentration dependence of prooxidant and antioxidant properties of catecholestrogens. Arch. Biochem. Biophys. 360, 105-112. https://doi.org/10.1006/abbi.1998.0934
  44. Roy, D. and Liehr, J. G. (1999) Estrogen, DNA damage and mutations. Mutat. Res. 424, 107-115. https://doi.org/10.1016/S0027-5107(99)00012-3
  45. Rajapakse, N., Butterworth, M. and Kortenkamp, A. (2005) Detection of DNA strand breaks and oxidized DNA bases at the single-cell level resulting from exposure to estradiol and hydroxylated metabolites. Environ. Mol. Mutagen. 45, 397-404. https://doi.org/10.1002/em.20104
  46. Hobkirk, R. (1985) Steroid sulfotransferases and steroid sulfate sulfatases: characteristics and biological roles. Can. J. Biochem. Cell Biol. 63, 1127-1144. https://doi.org/10.1139/o85-141
  47. Roy, A. K. (1992) Regulation of steroid hormone action in target cells by specific hormone-inactivating enzymes. Proc. Soc. Exp. Biol. Med. 199, 265-272. https://doi.org/10.3181/00379727-199-43356A
  48. Ball, P. and Knuppen, R. (1990) Formation, metabolism, and physiologic importance of catecholestrogens. Am. J. Obstet. Gynecol. 163, 2163-2170. https://doi.org/10.1016/0002-9378(90)90558-O
  49. Merriam, G. R., MacLusky, N. J., Picard, M. K. and Naftolin, F. (1980) Comparative properties of the catechol estrogens, I: methylation by catechol-O-methyltransferase and binding to cytosol estrogen receptors. Steroids 36, 1-11. https://doi.org/10.1016/0039-128X(80)90062-8
  50. Yue, T. L., Wang, X., Louden, C. S., Gupta, S., Pillarisetti, K., Gu, J. L., Hart, T. K., Lysko, P. G. and Feuerstein, G. Z. (1997) 2-Methoxyestradiol, an endogenous estrogen metabolite, induces apoptosis in endothelial cells and inhibits angiogenesis: possible role for stress-activated protein kinase signaling pathway and Fas expression. Mol. Pharmacol. 51, 951-962. https://doi.org/10.1124/mol.51.6.951
  51. Schumacher, G. and Neuhaus, P. (2001) The physiological estrogen metabolite 2-methoxyestradiol reduces tumor growth and induces apoptosis in human solid tumors. J. Cancer Res. Clin. Oncol. 127, 405-410. https://doi.org/10.1007/s004320000233
  52. Schumacher, G., Kataoka, M., Roth, J. A. and Mukhopadhyay, T. (1999) Potent antitumor activity of 2-methoxyestradiol in human pancreatic cancer cell lines. Clin. Cancer Res. 5, 493-499.
  53. Pribluda, V. S., Gubish, E. R., Jr., Lavallee, T. M., Treston, A., Swartz, G. M. and Green, S. J. (2000) 2-Methoxyestradiol: an endogenous antiangiogenic and antiproliferative drug candidate. Cancer Metastasis Rev. 19, 173-179. https://doi.org/10.1023/A:1026543018478
  54. Yao, J., Li, Y., Chang, M., Wu, H., Yang, X., Goodman, J. E., Liu, X., Liu, H., Mesecar, A. D., Van Breemen, R. B., Yager, J. D. and Bolton, J. L. (2003) Catechol estrogen 4-hydroxyequilenin is a substrate and an inhibitor of catechol- O-methyltransferase. Chem. Res. Toxicol. 16, 668-675. https://doi.org/10.1021/tx0340549
  55. Yao, J., Chang, M., Li, Y., Pisha, E., Liu, X., Yao, D., Elguindi, E. C., Blond, S. Y. and Bolton, J. L. (2002) Inhibition of cellular enzymes by equine catechol estrogens in human breast cancer cells: specificity for glutathione S-transferase P1-1. Chem. Res. Toxicol. 15, 935-942. https://doi.org/10.1021/tx020018i
  56. Chang, M., Shin, Y. G., van Breemen, R. B., Blond, S. Y. and Bolton, J. L. (2001) Structural and functional consequences of inactivation of human glutathione S-transferase P1-1 mediated by the catechol metabolite of equine estrogens, 4-hydroxyequilenin. Biochemistry 40, 4811-4820. https://doi.org/10.1021/bi002513o
  57. Li, Y., Yao, J., Chang, M., Nikolic, D., Yu, L., Yager, J. D., Mesecar, A. D., van Breemen, R. B. and Bolton, J. L. (2004) Equine catechol estrogen 4-hydroxyequilenin is a more potent inhibitor of the variant form of catechol-Omethyltransferase. Chem. Res. Toxicol. 17, 512-520. https://doi.org/10.1021/tx0342464
  58. Loriaux, D. L., Ruder, H. J., Knab, D. R. and Lipsett, M. B. (1972) Estrone sulfate, estrone, estradiol and estriol plasma levels in human pregnancy. J. Clin. Endocrinol. Metab. 35, 887-891. https://doi.org/10.1210/jcem-35-6-887
  59. Ruder, H. J., Loriaux, L. and Lipsett, M. B. (1972) Estrone sulfate: production rate and metabolism in man. J. Clin. Invest. 51, 1020-1033. https://doi.org/10.1172/JCI106862
  60. Carlstrom, K., Bergqvist, A. and Ljungberg, O. (1988) Metabolism of estrone sulfate in endometriotic tissue and in uterine endometrium in proliferative and secretory cycle phase. Feril. Steril. 49, 229-233. https://doi.org/10.1016/S0015-0282(16)59707-6
  61. Santen, R. J., Leszczynski, D., Tilson-Mallet, N., Feil, P. D., Wright, C., Manni, A. and Santner, S. J. (1986) Enzymatic control of estrogen production in human breast cancer: relative significance of aromatase versus sulfatase pathways. Ann. N. Y. Acad. Sci. 464, 126-137. https://doi.org/10.1111/j.1749-6632.1986.tb16000.x
  62. Zhu, B. T., Evaristus, E. N., Antoniak, S. K., Sarabia, S. F., Ricci, M. J. and Liehr, J. G. (1996) Metabolic deglucuronidation and demethylation of estrogen conjugates as a source of parent estrogens and catecholestrogen metabolites in Syrian hamster kidney, a target organ of estrogen- induced tumorigenesis. Toxicol. Appl. Pharmacol. 136, 186-193. https://doi.org/10.1006/taap.1996.0023
  63. Walaszek, Z. (1990) Potential use of D-glucaric acid derivatives in cancer prevention. Cancer Lett. 54, 1-8. https://doi.org/10.1016/0304-3835(90)90083-A
  64. Watanabe, K., Takanashi, K., Imaoka, S., Funae, Y., Kawano, S., Inoue, K., Kamataki, T., Takagi, H. and Yoshizawa, I. (1991) Comparison of cytochrome P-450 species which catalyze the hydroxylations of the aromatic ring of estradiol and estradiol 17-sulfate. J. Steroid Biochem. Mol. Biol. 38, 737-743. https://doi.org/10.1016/0960-0760(91)90087-L
  65. Purohit, A., Reed, M. J., Morris, N. C., Williams, G. J. and Potter, B. V. (1996) Regulation and inhibition of steroid sulfatase activity in breast cancer. Ann. N. Y. Acad. Sci. 784, 40-49. https://doi.org/10.1111/j.1749-6632.1996.tb16226.x
  66. Duncan, L., Purohit, A., Howarth, N. M., Potter, B. V. and Reed, M. J. (1993) Inhibition of estrone sulfatase activity by estrone-3-methylthiophosphonate: a potential therapeutic agent in breast cancer. Cancer Res. 53, 298-303.
  67. Bjornstrom, L. and Sjoberg, M. (2005) Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 19, 833-842. https://doi.org/10.1210/me.2004-0486
  68. Marino, M., Galluzzo, P. and Ascenzi, P. (2006) Estrogen signaling multiple pathways to impact gene transcription. Curr. Genomics 7, 497-508. https://doi.org/10.2174/138920206779315737
  69. Safe, S. and Kim, K. (2008) Non-classical genomic estrogen receptor (ER)/specificity protein and ER/activating protein-1 signaling pathways. J. Mol. Endocrinol. 41, 263-275. https://doi.org/10.1677/JME-08-0103
  70. Levin, E. R. (2002) Cellular functions of plasma membrane estrogen receptors. Steroids 67, 471-475. https://doi.org/10.1016/S0039-128X(01)00179-9
  71. Stoica, G. E., Franke, T. F., Moroni, M., Mueller, S., Morgan, E., Iann, M. C., Winder, A. D., Reiter, R., Wellstein, A., Martin, M. B. and Stoica, A. (2003) Effect of estradiol on estrogen receptor-alpha gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway. Oncogene 22, 7998-8011. https://doi.org/10.1038/sj.onc.1206769
  72. Levin, E. R. (2003) Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol. Endocrinol. 17, 309-317. https://doi.org/10.1210/me.2002-0368
  73. Liao, J. K. (2003) Cross-coupling between the oestrogen receptor and phosphoinositide 3-kinase. Biochem. Soc. Trans. 31, 66-70. https://doi.org/10.1042/bst0310066
  74. Chen, J. Q. and Yager, J. D. (2004) Estrogen's effects on mitochondrial gene expression: mechanisms and potential contributions to estrogen carcinogenesis. Ann. N. Y. Acad. Sci. 1028, 258-272. https://doi.org/10.1196/annals.1322.030
  75. Chen, J. Q., Delannoy, M., Cooke, C. and Yager, J. D. (2004) Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am. J. Physiol. Endocrinol. Metab. 286, E1011-1022. https://doi.org/10.1152/ajpendo.00508.2003
  76. Demonacos, C. V., Karayanni, N., Hatzoglou, E., Tsiriyiotis, C., Spandidos, D. A. and Sekeris, C. E. (1996) Mitochondrial genes as sites of primary action of steroid hormones. Steroids 61, 226-232. https://doi.org/10.1016/0039-128X(96)00019-0
  77. Zhu, B. T., Han, G. Z., Shim, J. Y., Wen, Y. and Jiang, X. R. (2006) Quantitative structure-activity relationship of various endogenous estrogen metabolites for human estrogen receptor alpha and beta subtypes: Insights into the structural determinants favoring a differential subtype binding. Endocrinology 147, 4132-4150. https://doi.org/10.1210/en.2006-0113
  78. Vincent, T. L. and Gatenby, R. A. (2008) An evolutionary model for initiation, promotion, and progression in carcinogenesis. Int. J. Oncol. 32, 729-737.
  79. Lavigne, J. A., Goodman, J. E., Fonong, T., Odwin, S., He, P., Roberts, D. W. and Yager, J. D. (2001) The effects of catechol-O-methyltransferase inhibition on estrogen metabolite and oxidative DNA damage levels in estradiol-treated MCF-7 cells. Cancer Res. 61, 7488-7494.
  80. Banerjee, S. K., Banerjee, S., Li, S. A. and Li, J. J. (1994) Induction of chromosome aberrations in Syrian hamster renal cortical cells by various estrogens. Mutat. Res. 311, 191-197. https://doi.org/10.1016/0027-5107(94)90176-7
  81. Valko, M., Izakovic, M., Mazur, M., Rhodes, C. J. and Telser, J. (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem. 266, 37-56. https://doi.org/10.1023/B:MCBI.0000049134.69131.89
  82. Chen, Z. H., Na, H. K., Hurh, Y. J. and Surh, Y. J. (2005) 4-Hydroxyestradiol induces oxidative stress and apoptosis in human mammary epithelial cells: possible protection by NF-kappaB and ERK/MAPK. Toxicol. Appl. Pharmacol. 208, 46-56. https://doi.org/10.1016/j.taap.2005.01.010
  83. Cavalieri, E., Chakravarti, D., Guttenplan, J., Hart, E., Ingle, J., Jankowiak, R., Muti, P., Rogan, E., Russo, J., Santen, R. and Sutter, T. (2006) Catechol estrogen quinones as initiators of breast and other human cancers: implications for biomarkers of susceptibility and cancer prevention. Biochim. Biophys. Acta 1766, 63-78.
  84. Saeed, M., Zahid, M., Gunselman, S. J., Rogan, E. and Cavalieri, E. (2005) Slow loss of deoxyribose from the N7deoxyguanosine adducts of estradiol-3,4-quinone and hexestrol-3',4'-quinone. Implications for mutagenic activity. Steroids 70, 29-35. https://doi.org/10.1016/j.steroids.2004.09.011
  85. Zhao, Z., Kosinska, W., Khmelnitsky, M., Cavalieri, E. L., Rogan, E. G., Chakravarti, D., Sacks, P. G. and Guttenplan, J. B. (2006) Mutagenic activity of 4-hydroxyestradiol, but not 2-hydroxyestradiol, in BB rat2 embryonic cells, and the mutational spectrum of 4-hydroxyestradiol. Chem. Res. Toxicol. 19, 475-479. https://doi.org/10.1021/tx0502645
  86. Saeed, M., Rogan, E., Fernandez, S. V., Sheriff, F., Russo, J. and Cavalieri, E. (2007) Formation of depurinating N3Adenine and N7Guanine adducts by MCF-10F cells cultured in the presence of 4-hydroxyestradiol. Int. J. Cancer 120, 1821-1824. https://doi.org/10.1002/ijc.22399
  87. Zahid, M., Kohli, E., Saeed, M., Rogan, E. and Cavalieri, E. (2006) The greater reactivity of estradiol-3,4-quinone vs estradiol-2,3-quinone with DNA in the formation of depurinating adducts: implications for tumor-initiating activity. Chem. Res. Toxicol. 19, 164-172. https://doi.org/10.1021/tx050229y
  88. Embrechts, J., Lemiere, F., Van Dongen, W., Esmans, E. L., Buytaert, P., Van Marck, E., Kockx, M. and Makar, A. (2003) Detection of estrogen DNA-adducts in human breast tumor tissue and healthy tissue by combined nano LC-nano ES tandem mass spectrometry. J. Am. Sco. Mass Spectr. 14, 482-491. https://doi.org/10.1016/S1044-0305(03)00130-2
  89. Liu, X., Yao, J., Pisha, E., Yang, Y., Hua, Y., van Breemen, R. B. and Bolton, J. L. (2002) Oxidative DNA damage induced by equine estrogen metabolites: role of estrogen receptor alpha. Chem. Res. Toxicol. 15, 512-519. https://doi.org/10.1021/tx0101649
  90. Chen, Y., Liu, X., Pisha, E., Constantinou, A. I., Hua, Y., Shen, L., van Breemen, R. B., Elguindi, E. C., Blond, S. Y., Zhang, F. and Bolton, J. L. (2000) A metabolite of equine estrogens, 4-hydroxyequilenin, induces DNA damage and apoptosis in breast cancer cell lines. Chem. Res. Toxicol. 13, 342-350. https://doi.org/10.1021/tx990186j
  91. Zhang, F., Swanson, S. M., van Breemen, R. B., Liu, X., Yang, Y., Gu, C. and Bolton, J. L. (2001) Equine estrogen metabolite 4-hydroxyequilenin induces DNA damage in the rat mammary tissues: formation of single-strand breaks, apurinic sites, stable adducts, and oxidized bases. Chem. Res. Toxicol. 14, 1654-1659. https://doi.org/10.1021/tx010158c
  92. Okahashi, Y., Iwamoto, T., Suzuki, N., Shibutani, S., Sugiura, S., Itoh, S., Nishiwaki, T., Ueno, S. and Mori, T. (2010) Quantitative detection of 4-hydroxyequilenin- DNA adducts in mammalian cells using an immunoassay with a novel monoclonal antibody. Nucleic Acids Res. 38, e133. https://doi.org/10.1093/nar/gkq233
  93. Ozcagli, E., Sardas, S. and Biri, A. (2005) Assessment of DNA damage in postmenopausal women under hormone replacement therapy. Maturitas 51, 280-285. https://doi.org/10.1016/j.maturitas.2004.08.010
  94. Kamata, H. and Hirata, H. (1999) Redox regulation of cellular signalling. Cell Signal. 11, 1-14. https://doi.org/10.1016/S0898-6568(98)00037-0
  95. Sauer, H., Wartenberg, M. and Hescheler, J. (2001) Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol. Biochem. 11, 173-186. https://doi.org/10.1159/000047804
  96. Circu, M. L. and Aw, T. Y. (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 48, 749-762. https://doi.org/10.1016/j.freeradbiomed.2009.12.022
  97. Surh, Y.-J., Kundu, J. K., Na, H.-K. and Lee, J.-S. (2005) Redox-Sensitive Transcription Factors as Prime Targets for Chemoprevention with Anti-Inflammatory and Antioxidative Phytochemicals. J. Nutr. 135, 2993S-3001S. https://doi.org/10.1093/jn/135.12.2993S
  98. Roy, D., Cai, Q., Felty, Q. and Narayan, S. (2007) Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J. Toxicol. Environ. Health B. Crit. Rev. 10, 235-257. https://doi.org/10.1080/15287390600974924
  99. Foster, J. S., Henley, D. C., Bukovsky, A., Seth, P. and Wimalasena, J. (2001) Multifaceted regulation of cell cycle progression by estrogen: regulation of Cdk inhibitors and Cdc25A independent of cyclin D1-Cdk4 function. Mol. Cell. Biol. 21, 794-810. https://doi.org/10.1128/MCB.21.3.794-810.2001
  100. Cui, Y., Parra, I., Zhang, M., Hilsenbeck, S. G., Tsimelzon, A., Furukawa, T., Horii, A., Zhang, Z. Y., Nicholson, R. I. and Fuqua, S. A. (2006) Elevated expression of mitogen-activated protein kinase phosphatase 3 in breast tumors: a mechanism of tamoxifen resistance. Cancer Res. 66, 5950-5959. https://doi.org/10.1158/0008-5472.CAN-05-3243
  101. Weinstein-Oppenheimer, C. R., Burrows, C., Steelman, L. S. and McCubrey, J. A. (2002) The effects of beta-estradiol on Raf activity, cell cycle progression and growth factor synthesis in the MCF-7 breast cancer cell line. Cancer Biol. Ther. 1, 256-262. https://doi.org/10.4161/cbt.77
  102. Adler, V., Yin, Z., Fuchs, S. Y., Benezra, M., Rosario, L., Tew, K. D., Pincus, M. R., Sardana, M., Henderson, C. J., Wolf, C. R., Davis, R. J. and Ronai, Z. (1999) Regulation of JNK signaling by GSTp. EMBO J. 18, 1321-1334. https://doi.org/10.1093/emboj/18.5.1321
  103. Kar, S., Wang, M., Yao, W., Michejda, C. J. and Carr, B. I. (2006) PM-20, a novel inhibitor of Cdc25A, induces extracellular signal-regulated kinase 1/2 phosphorylation and inhibits hepatocellular carcinoma growth in vitro and in vivo. Mol. Cancer Ther. 5, 1511-1519.
  104. Banerjee, S., Saxena, N., Sengupta, K. and Banerjee, S. K. (2003) 17alpha-estradiol-induced VEGF-A expression in rat pituitary tumor cells is mediated through ER independent but PI3K-Akt dependent signaling pathway. Biochem. Biophys. Res. Commun. 300, 209-215. https://doi.org/10.1016/S0006-291X(02)02830-9
  105. Lee, Y. R., Park, J., Yu, H. N., Kim, J. S., Youn, H. J. and Jung, S. H. (2005) Up-regulation of PI3K/Akt signaling by 17beta-estradiol through activation of estrogen receptor- alpha, but not estrogen receptor-beta, and stimulates cell growth in breast cancer cells. Biochem. Biophys. Res. Commun. 336, 1221-1226. https://doi.org/10.1016/j.bbrc.2005.08.256
  106. Rockhill, B., Spiegelman, D., Byrne, C., Hunter, D. J. and Colditz, G. A. (2001) Validation of the Gail et al. model of breast cancer risk prediction and implications for chemoprevention. J. Natl. Cancer Inst. 93, 358-366. https://doi.org/10.1093/jnci/93.5.358
  107. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L. and Rogan, E. G. (1997) Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U. S. A. 94, 10937-10942. https://doi.org/10.1073/pnas.94.20.10937
  108. Yager, J. D. and Liehr, J. G. (1996) Molecular mechanisms of estrogen carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 36, 203-232. https://doi.org/10.1146/annurev.pa.36.040196.001223
  109. Parl, F. F., Dawling, S., Roodi, N. and Crooke, P. S. (2009) Estrogen metabolism and breast cancer: a risk model. Ann. N. Y. Acad. Sci. 1155, 68-75. https://doi.org/10.1111/j.1749-6632.2008.03676.x
  110. Bocchinfuso, W. P., Hively, W. P., Couse, J. F., Varmus, H. E. and Korach, K. S. (1999) A mouse mammary tumor virus-Wnt-1 transgene induces mammary gland hyperplasia and tumorigenesis in mice lacking estrogen receptor-alpha. Cancer Res. 59, 1869-1876.

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