Estrogen and Xenoestrogens in breast cancer

Toxicologic Pathology

Volumn 38, Issue 1, 2010, Pages 110-122

  Fernandez, S V ^a   Russo, J ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

BBP; BPA; Breast cancer; Cell transformation; Epigenetic changes; Estrogen; Neuregulin

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BONE MORPHOGENETIC PROTEIN 6; ESTRADIOL; ESTROGEN; ESTROGEN DERIVATIVE; GENE PRODUCT; NEU DIFFERENTIATION FACTOR; PHTHALIC ACID BENZYL BUTYL ESTER; PROTEIN CSS3; PROTEIN SPRY1; PROTEIN STXBP6; SPROUTY PROTEIN; UNCLASSIFIED DRUG; XENOESTROGEN DERIVATIVE; DNA (CYTOSINE 5 ) METHYLTRANSFERASE 1; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; PHENOL DERIVATIVE; PHTHALIC ACID DERIVATIVE;

BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER GENETICS; CANCER GROWTH; CANCER SUSCEPTIBILITY; CARCINOGENICITY; CELL TRANSFORMATION; CHEMICAL CARCINOGENESIS; DISEASE COURSE; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GENETIC REGULATION; GENOMICS; HUMAN; IN VITRO STUDY; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOLID TUMOR; BREAST TUMOR; CHEMICALLY INDUCED DISORDER; FEMALE; GENETIC EPIGENESIS;

BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; ESTRADIOL; FEMALE; GENE SILENCING; HUMANS; PHENOLS; PHTHALIC ACIDS;

EID: 77952296027     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623309354108     Document Type: Review

References (69)

1. Akingbemi, B. T., Sottas, C. M., Koulova, A. I., Klinefelter, G. R., and Hardy, M. P. (2004). Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 145, 592-603.
2. Andersen, H. R., Andersson, A. M., Arnold, S. F., Autrup, H., Barfoed, M., Beresford, N. A., Bjerregaard, P., Christiansen, L. B., Gissel, B., Hummel, R., Jørgensen, E. B., Korsgaard, B., Le Guevel, R., Leffers, H., McLachlan, J., Møller, A., Nielsen, J. B., Olea, N., Oles-Karasko, A., Pakdel, F., Pedersen, K. L., Perez, P., Skakkeboek, N. E., Sonnenschein, C., Soto, A. M., et al. (1999). Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. Environ Health Perspect 107 Suppl 1, 89-108.
3. Bakken, K., Alsaker, E., Eggen, A. E., and Lund, E. (2004). Hormone replacement therapy and incidence of hormone-dependent cancers in the Norwegian Women and Cancer study. Int J Cancer 112, 130-134
4. Belinsky, S. A., Nikula, K. J., Baylin, S. B., and Issa, J. P. (1996). Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer. Proc Natl Acad Sci U S A 93, 4045-4050
5. Beral, V. (2003). Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362, 419-427
6. Bernstein, L., and Ross, R. K. (1993). Endogenous hormones and breast cancer risk. Epidemiol Rev 15, 48-65.
7. Brede, C., Fjeldal, P., Skjevrak, I., and Herikstad, H. (2003). Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing. Food Addit Contam 20, 684-689
8. Brotons, J. A., Olea-Serrano, M. F., Villalobos, M., Pedraza, V., and Olea, N. (1995). Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 103, 608-612
9. Burridge, E. (2003). Eur. Chem. News (April 14-20), 17.
10. Calafat, A. M., Kuklenyik, Z., Reidy, J. A., Caudill, S. P., Ekong, J., and Needham, L. L. (2005). Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113, 391-395
11. Chlebowski, R. T., Hendrix, S. L., Langer, R. D., Stefanick, M. L., Gass, M., Lane, D., Rodabough, R. J, Gilligan, M. A., Cyr, M. G., Thomson, C. A., Khandekar, J., Petrovitch, H., McTiernan, A., and Women's Health Initiative Investigators (2003). Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: The Women's Health Initiative Randomized Trial. JAMA 289, 3243-3253 (Pubitemid 37430077)
12. Chua, Y., and Paw, E. (2006). The NEUREGULIN1 gene and breast cancer. Breast Cancer Res 8 (Suppl 2), 5.
13. Chua, Y. L., Pole, J. C. M., Chin, S.-F., Ellis, I. O., Caldas, C., O'Hare, M. J., et al. (2008). The NRG1 gene is frequently silenced by methylation in breast cancers and is a strong candidate for the 8p tumor suppressor gene. Breast Cancer Res 10 (Suppl 2), 11.
14. Clement, J. H., Sanger, J., and Hoffken, K. (1999). Expression of bone morphogenetic protein 6 in normal mammary tissue and breast cancer cell lines and its regulation by epidermal growth factor. Int J Cancer 80, 250-256
15. Colditz, G. A. (1998). Relationship between estrogen levels, use of hormone replacement therapy, and breast cancer. J Natl Cancer Inst 90, 814-823
16. Colditz, G. A. (2005). Estrogen, estrogen plus progestin therapy, and risk of breast cancer. Clin Cancer Res 11(2 Pt 2), 909s-917s.
17. Collaborative Group on Hormonal factors in Breast Cancer (1997). Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 350, 1047-1059
18. Ema, M. and Miyawaki, E. (2002). Effects on development of the reproductive system in male offspring of rats given butyl benzyl phthalate during late pregnancy. Reprod Toxicol 16, 71-76.
19. Ema, M., Miyawaki, E., Hirose, A., and Kamata, E. (2003). Decreased anogenital distance and increased incidence of undescended testes in fetuses of rats given monobenzyl phthalate, a major metabolite of butyl benzyl phthalate. Reprod Toxicol 17, 407-412
20. Fernandez, S. V., Russo, I. H., Lareef, M., Balsara, B., and Russo, J. (2005). Comparative genomic hybridization of human breast epithelial cells transformed by estrogen and its metabolites. Int J Oncol 26, 691-695
21. Fernandez, S. V., Russo, I. H., and Russo, J. (2006). Estradiol and its metabolites 4-hydroxyestradiol and 2-hydroxyestradiol induce mutations in human breast epithelial cells. Int J Cancer 118, 1862-1868
22. Fernandez, S. V., Wu, Y.-Z., Russo, I. H., Plass, C., and Russo, J. (2006). The role of DNA methylation in estrogen-induced transformation of human breast epithelial cells. Proc Am Assoc Cancer Res 47, 1590.
23. Friel, P. N., Hinchcliffe, C., and Wright, J. V. (2005). Hormone replacement with estradiol: Conventional oral doses result in excessive exposure to estrone. Altern Med Rev 10, 36-41.
24. Gray, L. E., Jr., Ostby, J., Furr, J., Price, M., Veeramachaneni, D. N., and Parks, L. (2000). Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 58, 350-365
25. Gupta, C. (2000).Reproductivemalformation of the male offspring following maternal exposure to estrogenic chemicals. Proc Soc Exp Biol Med 224, 61-68.
26. Harris, C. A., Henttu, P., Parker, M. G., and Sumpter, J. P. (1997). The estrogenic activity of phthalate esters in vitro. Environ Health Perspect 105, 802-811
27. Harris, J. R., Lippman, M. E., Veronesi, U., and Willett, W. (1992). Breast cancer (1). N Engl J Med 327, 319-328
28. Henderson, B. E., Ross, R. K., and Pike, M. C. (1991). Toward the primary prevention of cancer. Science 254, 1131-1138
29. Hirai, Y., Lochter, A., Galosy, S., Koshida, S., Niwa, S., and Bissell, M. J. (1998). Epimorphin functions as a key morphoregulator for mammary epithelial cells. J Cell Biol 140, 159-169
30. Hong, E. J., Ji, Y. K., Choi, K. C., Manabe, N., and Jeung, E. B. (2005). Conflict of estrogenic activity by various phthalates between in vitro and in vivo models related to the expression of Calbindin-D9k. J Reprod Dev 51, 253-263
31. Howdeshell, K. L., Peterman, P. H., Judy, B. M., Taylor, J. A., Orazio, C. E., Ruhlen, R. L., Vom Saal, F. S., and Welshons, W. V. (2003). Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ Health Perspect 111, 1180-1187
32. Huang, Y., Fernandez, S. V., Goodwin, S., Russo, P. A., Russo, I. H., Sutter, T. R., and Russo, J. (2007). Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17beta-estradiol. Cancer Res 67, 11147-11157 (Pubitemid 350248539)
33. Huang, Z., Hankinson, S. E., Colditz, G. A., Stampfer, M. J., Hunter, D. J., Manson, J. E., Hennekens, C. H., Rosner, B., Speizer, F. E., and Willett, W. C. (1997). Dual effects of weight and weight gain on breast cancer risk. JAMA 278, 1407-1411
34. Ikezuki, Y., Tsutsumi, O., Takai, Y., Kamei, Y., and Taketani, Y. (2002). Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 17, 2839-2841
35. IPCS (1999). Concise International Chemical Assessment Document 17, Butyl benzyl phthalate. Geneva, World Health Organization, International Programme on Chemical Safety.
36. Jobling, S., Reynolds, T.,White, R., Parker, M. G., and Sumpter, J. P. (1995). A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ Health Perspect 103, 582-587
37. Key, T., Appleby, P., Barnes, I., and Reeves, G. (2002). Endogenous sex hormones and breast cancer in postmenopausal women: Reanalysis of nine prospective studies. J Natl Cancer Inst 94, 606-616
38. Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L., and Feldman, D. (1993). Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132, 2279-2286
39. Lareef, M. H., Garber, J., Russo, P. A., Russo, I. H., Heulings, R., and Russo, J. (2005). The estrogen antagonist ICI-182-780 does not inhibit the transformation phenotypes induced by 17-beta-estradiol and 4-OH estradiol in human breast epithelial cells. Int J Oncol 26, 423-429
40. Lee, P. J., Washer, L. L., Law, D. J., Boland, C. R., Horon, I. L., and Feinberg, A. P. (1996). Limited up-regulation of DNA methyltransferase in human colon cancer reflecting increased cell proliferation. Proc Natl Acad Sci U S A 93, 10366-10370
41. Levy, G., Lutz, I., Kruger, A., and Kloas, W. (2004). Bisphenol A induces feminization in Xenopus laevis tadpoles. Environ Res 94, 102-111
42. Li, C. I., Malone, K. E., Porter, P. L., Weiss, N. S., Tang, M. T., Cushing-Haugen, K. L., and Daling, J. R. (2003). Relationship between long durations and different regimens of hormone therapy and risk of breast cancer. JAMA 289, 3254-3263
43. Lo, T. L., Yusoff, P., Fong, C. W., Guo, K., McCaw, B. J., Phillips, W. A., Yang, H., Wong, E. S., Leong, H. F., Zeng, Q., Putti, T. C., and Guy, G. R. (2004). The ras/mitogen-activated protein kinase pathway inhibitor and likely tumor suppressor proteins, sprouty 1 and sprouty 2 are deregulated in breast cancer. Cancer Res 64, 6127-6136
44. Long, W., Wagner, K. U., Lloyd, K. C., Binart, N., Shillingford, J. M., Hennighausen, L., and Jones, F. E. (2003). Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5. Development 130, 5257-5268
45. Maruyama, S., Fujimoto, N., Yin, H., and Ito, A. (1999). Growth stimulation of a rat pituitary cell line MtT/E-2 by environmental estrogens in vitro and in vivo. Endocr J 46, 513-520
46. Matsumoto, A., Kunugita, N., Kitagawa, K., Isse, T., Oyama, T., Foureman, G. L., Morita, M., and Kawamoto, T. (2003). Bisphenol A levels in human urine. Environ Health Perspect 111, 101-104
47. Matthews, J. B., Twomey, K., and Zacharewski, T. R. (2001). In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol 14, 149-157
48. Melki, J. R., Warnecke, P., Vincent, P. C., and Clark, S. J. (1998). Increased DNA methyltransferase expression in leukaemia. Leukemia 12, 311-316
49. Olea, N., Pulgar, R., Perez, P., Olea-Serrano, F., Rivas, A., Novillo-Fertrell, A., Pedraza, V., Soto, A. M., and Sonnenschein, C. (1996). Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104, 298-305.
50. Ouchi, K., and Watanabe, S. (2002). Measurement of bisphenol A in human urine using liquid chromatography with multi-channel coulometric electrochemical detection. J Chromatogr B Analyt Technol Biomed Life Sci 780, 365-370
51. Pike, M. C., Krailo, M. D., Henderson, B. E., Casagrande, J. T., and Hoel, D. G. (1983). "Hormonal" risk factors, "breast tissue age" and the ageincidence of breast cancer. Nature 303, 767-770
52. Ramos, J. G., Varayoud, J., Sonnenschein, C., Soto, A. M., Munoz De Toro, M., and Luque, E. H. (2001). Prenatal exposure to low doses of bisphenol A alters the periductal stroma and glandular cell function in the rat ventral prostate. Biol Reprod 65, 1271-1277
53. Rossouw, J. E., Anderson, G. L., Prentice, R. L., LaCroix, A. Z., Kooperberg, C., Stefanick, M. L., Jackson, R., D., Beresford, S. A., Howard, B. V., Johnson, K. C., Kotchen, J. M., Ockene, J., and the Writing Group for the Women's Health Initiative Investigators. (2002). Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results From the Women's Health Initiative randomized controlled trial. JAMA 288, 321-333
54. Routledge, E. J., White, R., Parker, M. G., and Sumpter, J. P. (2000). Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 275, 35986-35993
55. 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
56. 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.
57. Russo, J., Lareef, M. H., Tahin, Q., Hu, Y. F., Slater, C., Ao, X., and Russo, I. H. (2002). 17Beta-estradiol is carcinogenic in human breast epithelial cells. J Steroid Biochem Mol Biol 80, 149-162
58. Sartor, C. I., Zhou, H., Kozlowska, E., Guttridge, K., Kawata, E., Caskey, L., Harrelson, J., Hynes, N., Ethier, S., Calvo, B., and Earp, H. S. 3rd. (2001). Her4 mediates ligand-dependent antiproliferative and differentiation responses in human breast cancer cells. Mol Cell Biol 21, 4265-4275
59. Schonfelder, G., Wittfoht, W., Hopp, H., Talsness, C. E., Paul, M., and Chahoud, I. (2002). Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 110, A703-7.
60. Schwartz, N. B., and Domowicz, M. (2002). Chondrodysplasias due to proteoglycan defects. Glycobiology 12, 57R-68R.
61. Smiraglia, D. J., and Plass, C. (2002). The study of aberrant methylation in cancer via restriction landmark genomic scanning. Oncogene 21, 5414-5426
62. Sonnenschein, C., and Soto, A. M. (1998). An updated review of environmental estrogen and androgen mimics and antagonists. J Steroid Biochem Mol Biol 65, 143-150
63. Soule, H. D., Maloney, T. M., Wolman, S. R., Peterson, W. D., Jr., Brenz, R., McGrath, C. M., Russo, J., Pauley, R. J., Jones, R. F., and Brooks, S. C. (1990). Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50, 6075-6086 (Pubitemid 20331424)
64. Suzuki, A., Sugihara, A., Uchida, K., Sato, T., Ohta, Y., Katsu, Y., Watanabe, H., and Iguchi, T. (2002). Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod Toxicol 16, 107-116
65. Takao, T., Nanamiya, W., Nagano, I., Asaba, K., Kawabata, K., and Hashimoto, K. (1999). Exposure with the environmental estrogen bisphenol A disrupts the male reproductive tract in young mice. Life Sci 65, 2351-2357
66. Tidcombe, H., Jackson-Fisher, A., Mathers, K., Stern, D. F., Gassmann, M., and Golding, J. P. (2003). Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc Natl Acad Sci U S A 100, 8281-8286
67. Yang, M., Kim, S. Y., Lee, S. M., Chang, S. S., Kawamoto, T., Jang, J. Y., et al. (2003). Biological monitoring of bisphenol a in a Korean population. Arch Environ Contam Toxicol 44, 546-551
68. Yang, Y., Spitzer, E., Meyer, D., Sachs, M., Niemann, C., Hartmann, G., Weidner, K., M., Birchmeier, C., and Birchmeier, W. (1995). Sequential requirement of hepatocyte growth factor and neuregulin in the morphogenesis and differentiation of the mammary gland. J Cell Biol 131, 215-226
69. Zacharewski, T. R., Meek, M. D., Clemons, J. H., Wu, Z. F., Fielden, M. R., and Matthews, J. B. (1998). Examination of the in vitro and in vivo estrogenic activities of eight commercial phthalate esters. Toxicol Sci 46, 282-293