Estrogens, Phytoestrogens, and Breast Cancer

  • Robert Clarke
  • Leena Hilakivi-Clarke
  • Elizabeth Cho
  • Mattie R. James
  • Fabio Leonessa
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 401)

Abstract

Estrogens have been widely implicated in the genesis and progression of breast cancer. Over 200 years ago, the Italian physician Ramazzini observed an increased incidence of breast cancer among nuns. Almost 100 years ago the Scottish physician Beatson described the beneficial effects of ovariectomy on the progress of breast cancer in premenopausal women.1 Nevertheless, the precise role(s) of estrogens and estrogenic stimuli in breast cancer remains unknown. Indeed, it is difficult to provide a universal definition of either an estrogen or an estrogenic response.

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References

  1. 1.
    G. T. Beatson, On the treatment of inoperable cases of carcinoma of the mamma: suggestions from a new method of treatment with illustrative cases, Lancet ii: 104–107 (1896).CrossRefGoogle Scholar
  2. 2.
    J. R. Daling, K. E. Malone, L. F. Voigt, E. White, and N. S. Weiss, Risk of breast cancer in young women: relationship to induced abortion, J Natl Cancer Inst 86: 1584–1592 (1994).CrossRefGoogle Scholar
  3. 3.
    B. E. Henderson, R. Ross, and L. Bernstein, Estrogens as a cause of human cancer, Cancer Res 48: 246–253 (1988).Google Scholar
  4. 4.
    R. Clarke, N. Brünner, B. S. Katzenellenbogen, E. W. Thompson, M. J. Norman, C. Koppi, S. Paik, M. E. Lippman, and R. B. Dickson, Progression from hormone dependent to hormone independent growth in MCF-7 human breast cancer cells, Proc Natl Acad Sci USA 86: 3649–3653 (1989).CrossRefGoogle Scholar
  5. 5.
    K. Seibert, S. M. Shafie, T. J. Triche, J. J. Whang-Peng, S. J. O’Brien, J. H. Toney, K. K. Huff, and M. E. Lippman, Clonal variation of MCF-7 breast cancer cells in vitro and in athymic nude mice, Cancer Res 43: 2223–2239(1983).Google Scholar
  6. 6.
    R. Clarke, R. B. Dickson, and M. E. Lippman, Hormonal aspects of breast cancer: growth factors, drugs and stromal interactions, Crit Rev Oncol Hematol 12: 1–23 (1992).CrossRefGoogle Scholar
  7. 7.
    D. J. P. Ferguson and T. J. Anderson, Morphological evaluation of cell turnover in relation to the menstrual cycle in the nesting human breast, Br J Cancer 44: 177–181 (1981).CrossRefGoogle Scholar
  8. 8.
    M. Metzler, Biochemical toxicology of diethylstilbestrol, in: “Reviews in Biochemical Toxicology”, E. Hodgson et al., Elsevier, NY, pp. 191–220 (1984).Google Scholar
  9. 9.
    T. Tsutsui, H. Maizumi, J. A. McLachlan, and J. C. Barrett, Aneuploidy induction and cell transformation by diethylstilbestrol: a possible chromosomal mechanism in carcinogenesis, Cancer Res 43: 3814–3821 (1983).Google Scholar
  10. 10.
    J. Fishman, Aromatic hydroxylation of estrogens, Ann Rev Physiol 45: 61–72 (1983).CrossRefGoogle Scholar
  11. 11.
    M. Metzler, Metabolic activation of xenobiotic stilbene estrogens, Fed Proc 46: 1855–1857 (1987).Google Scholar
  12. 12.
    P. Garcia-Morales, M. Saceda, N. Kenney, N. Kim, D. S. Salomon, M. M. Gottardis, H. B. Solomon, P. F. Sholler, C.V. Jordan, and M.B. Martin, Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells, J Biol Chem 269: 16896–16901 (1994).Google Scholar
  13. 13.
    D. Duval, S. Durant, and F. Homo-Delarche, Non-genomic effects of steroids. Interactions of steroid molecules with membrane structures and functions, Biochim Biophys Acta 737: 409–442 (1983).Google Scholar
  14. 14.
    M. Farhat, S. Abi-Younes, R. Vargas, R. M. Wolfe, R. Clarke, and P. W. Ramwell, Vascular non-genomic effects of estrogen, in: “Sex Steroids and the Cardiovascular System”, RW. Ramwell et al., Springer-Verlag, Berlin, pp. 145–159 (1992).Google Scholar
  15. 15.
    R. Clarke and M.E. Lippman, Antiestrogens resistance: mechanisms and reversal, in: “Drug Resistance in Oncology”, B. A. Teicher., ed., Marcel Dekker, Inc, New York, pp. 501–536 (1992).Google Scholar
  16. 16.
    A. E. Wakeling, M. Dukes, and J. Bowler, A potent specific pure antiestrogen with clinical potential, Cancer Res 51: 3867–3873 (1991).Google Scholar
  17. 17.
    H.-Y. R Lam, Tamoxifen is a calmodulin antagonist in the activation of cAMP phosphodiesterase, Biochem BiophysRes Comm 118: 27–32 (1984).CrossRefGoogle Scholar
  18. 18.
    C. A. O’Brian, R.M. Liskamp, D. H. Solomon, and I. B. Weinstein, Triphenylethylenes: a new class of protein kinase C inhibitors, J Natl Cancer Inst 76: 1243–1246 (1986).Google Scholar
  19. 19.
    B. S. Katzenellenbogen, A. M. Miller, A. Mullick, and Y. Y. Sheen, Antiestrogen action in breast cancer cells: modulation of proliferation and protein synthesis, and interaction with estrogen receptors and additional antiestrogen binding sites, Breast Cancer Res Treat 5: 231–243 (1985).CrossRefGoogle Scholar
  20. 20.
    T. Akiyama, J. Ishida, S. Nakagawa, H. Ogawa, S. Watanabe, N. Itou, M. Shibata, and Y. Fukami, Genistein, a specific inhibitor of tyrosine-specific protein kinease, J Biol Chem 262: 5592–5595 (1987).Google Scholar
  21. 21.
    A. Okura, H. Arakawa, H. Oka, T. Yoshinari, and Y. Monden, Effect of genistein on topoisomerase activity and on the growth of (val 12) Ha-ras-transformed NIH 3T3 cells, Biochem Biophys Res Commun 157: 183–189(1988).Google Scholar
  22. 22.
    H. Adlercreutz, Y. Mousavi, J. Clark, K. Hockerstedt, E. Hamalainen, K. Wahala, T. Makela, and T. Hase, Dietary phytoestrogens and cancer: in vitro and in vivo studies, J Steroid Biochem Mol Biol 41: 331–337 (1992).CrossRefGoogle Scholar
  23. 23.
    T. Hirano, K. Oka, and M. Akiba, Antiproliferative effects of synthetic and naturally occurring flavoids on tumor cells of the human breast carcinoma cell line, ZR-75–1, Res Comm Chem Path Pharm 64: 69–78 (1989).Google Scholar
  24. 24.
    W. V. Welshons, C. S. Murphy, R. Koch, G. Calaf, and V. C. Jordan, Stimulation of breast cancer cells in vitro by environmental estrogens enterolactone and the phytoestrogen equol, Breast Cancer Res Treat 10: 379–381 (1987).CrossRefGoogle Scholar
  25. 25.
    P. M. Martin, K. B. Horwitz, D. S. Ryan, and W. L. McGuire, Phytoestrogen interaction with estrogen receptors in human breast cancer cells, Endocrinology 103: 1860–1867 (1978).CrossRefGoogle Scholar
  26. 26.
    W. M. Hagler, K. Tyczkowska, and P.B. Hamilton, Simultaneous occurrence of deoxynivalenol, zearalenone, and aflatoxin in 1982 scabby wheat from the Midwestern United States, Appl Environ Microbiol 47: 151–154 (1984).Google Scholar
  27. 27.
    L. W. Burgess, P. E. Nelson, and T. A. Toussoun, Characterization, geographic distribution and ecology of Fusarium crookwellense sp. nov, Trans Br Mycol Soc 79: 497–505 (1982).CrossRefGoogle Scholar
  28. 28.
    Y. Luo, T. Yoshizawa, and T. Katayama, Comparative study on the natural occurrence of fusarium mycotoxins (trichothecenes and zearalenone) in corn and wheat from high- and low-risk areas for human esophageal cancer in China, Appl Environ Microbiol 56: 3723–3726 (1990).Google Scholar
  29. 29.
    P. Golinski, R. F. Vesonder, D. Latus-Zietkiewicz, and J. Perkowski, Formation of fusarenone X, nivalenol, zearalenone, ct-trans-zearalenol, ß-trans-zearalenol, and fusarin C by Fusarium crookwellense, Appl Environ Microbiol 54: 2147–2148 (1988).Google Scholar
  30. 30.
    R. Schoental, Trichothecenes, Zearalenone, and other carcinogenic metabolites of Fusarium and related microfungi, Adv Cancer Res 45: 217–290 (1985).CrossRefGoogle Scholar
  31. 31.
    T. Kuiper-Goodman, Uncertainties in the risk assessment of three mycotoxins: aflatoxin, ochratoxin, and zearalenone, Can J Physiol Pharm 68: 1017–1024 (1990).CrossRefGoogle Scholar
  32. 32.
    P. H. Hidy and R. S. Baldwin, Method of preventing pregnancy with lactone derivates, U. S. Pat June 22: 3,966,274 (1976).Google Scholar
  33. 33.
    W. H. Utian, Comparative trial of P-1496, a new non-steroidal oestrogen analogue, Br Med J 1: 579–581 (1973).CrossRefGoogle Scholar
  34. 34.
    Sandoz Ltd, Pharmacological trials of Frideron P-1496, Sandoz Ltd (1980).Google Scholar
  35. 35.
    A. T. Ralston, Effect of zearalanol on weaning weight of male calves, J Anim Sci 47: 1203–1206 (1978).Google Scholar
  36. 36.
    J. P Wiggins, H. Rothenbacher, L. L. Wilson, R. J. Martin, P. J. Wangness, and J. H. Ziegler, Growth and endocrine responses of lambs to zearanol implants: effects of preimplant growth rate and breed of sire, J Anim Sci 49: 291–297 (1979).Google Scholar
  37. 37.
    R. Schoental, Role of podophyllotoxin in the bedding and dietary zearalenone on incidence of “spontaneous” tumors in laboratory animals, Cancer Res 34: 2419 (1974).Google Scholar
  38. 38.
    E. W. Thompson, D. Katz, T. B. Shima, A. E. Wakeling, M. E. Lippman, and R. B. Dickson, ICI 164,384: a pure antagonist of estrogen-stimulated MCF-7 cell proliferation and invasiveness, Cancer Res 49: 6929–6934 (1989).Google Scholar
  39. 39.
    H. H. Keasling and F. W. Schueler, The relationship between estrogenic activity and chemical constitution in a group of azomethine derivatives, J Am Pharm Assoc 39: 87–90 (1950).Google Scholar
  40. 40.
    J. P. Raynaud, T. Ojasco, M. M. Bouton, E. Bignon, M. Pons, and A. Crastes de Paulet, Structure-activity relationships of steroid estrogens, in: “Estrogens in the Environment”, J. A. McLachlan., ed., Elsevier Science Publishing Company, New York, pp. 24–41 (1985).Google Scholar
  41. 41.
    W. L. Duax and J. F. Griffin, Structure-activity relationships of estrogenic chemicals, in: “Estrogens in the Environment”, J. A. McLachlan., ed., Elsevier Science Publishing Company, New York, pp. 15–23 (1985).Google Scholar
  42. 42.
    J. A. Katzenellenbogen, B. S. Katzenellenbogen, T. Tatee, D. W. Robertson, and S. W. Landvatter, The chemistry of estrogens and antiestrogens: relationships between structure, receptor binding and biological activity, in: “Estrogens in the Environment”, J. A. McLachlan., ed., Elsevier North Holland, New York, pp. 33–52(1980).Google Scholar
  43. 43.
    W. L. Duax and C. M. Weeks, Molecular basis of estrogenicity: X-ray crystallographic studies, in: “Estrogens in the Environment”, J. A. McLachlan., ed., Elsevier North Holland, New York, pp. 11–32 (1980).Google Scholar
  44. 44.
    J. P. Raynaud, T. Ojasoo, M. M. Bouton, and D. Philibert, Receptor binding as a tool in the development of new bioactive steroids, Drug Design viii: 169–214 (1979).Google Scholar
  45. 45.
    G. M. Anstead and P. R. Kym, Benz(a)anthracene diols: predicted carcinogenicity and structure-estrogen reecptor binding affinity relationships, Steroids 60: 383–394 (1995).CrossRefGoogle Scholar
  46. 46.
    D. Thouvenot and R. F. Morfin, Interferences of zearalenone, zearalenol or estradiol-17ß with the steroid metabolizing enzymes of the human prostate gland, J Steroid Biochem 13: 1337–1345 (1980).CrossRefGoogle Scholar
  47. 47.
    J. J. Li, S. A. Li, J. K. Klicka, and J. A. Heller, Some biological and toxicological studies of various estrogen mycotoxins and phytoestrogens, in: “Estrogens in the Environment”, J. A. McLachlan., ed., Elsevier Science Publishing Company, New York, pp. 168–183 (1985).Google Scholar
  48. 48.
    B. M. Weichman and A. C. Notides, Estrogen receptor activation and the dissociation kinetics of estradiol, estriol and estrone, Endocrinology 106: 434–439 (1980).CrossRefGoogle Scholar
  49. 49.
    G. Stack, K. Korach, and J. Gorski, Relative mitogenic activities of various estrogens and antiestrogens, Steroids 54: 227–243 (1989).CrossRefGoogle Scholar
  50. 50.
    D. P. McDonnell, D. L. Clemm, T. Hermann, M. E. Goldman, and J. W. Pike, Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens, Mol Endocrinol 9: 659–669 (1995).CrossRefGoogle Scholar
  51. 51.
    R. Clarke and N. Briinner, Cross resistance and molecular mechanisms in antiestrogen resistance, Endocr Related Cancer 2: 59–72 (1995).CrossRefGoogle Scholar
  52. 52.
    R. Clarke, T. Skaar, F. Leonessa, B. Brankin, M. R. James, N. Briinner, and M. E. Lippman, The acquisition of an antiestrogen resistant phenotype in breast cancer: the role of cellular and molecular mechanisms, in: “Advances in Cancer Research”, W. Hait., ed., Kluwer, Norwell, pp. in press (1996).Google Scholar
  53. 53.
    R. T. Turner, B. L. Riggs, and T. C. Spelsberg, Skeletal effects of estrogens, Endocrine Rev 15: 275–300 (1994).Google Scholar
  54. 54.
    J. A. O’Keefe, E. B. Pedersen, A. J. Castro, and R. J. Handa, Estrogen receptors in hippocampal and neocortical transplants during development, Society for Neuroscience abstracts 16: (1990).Google Scholar
  55. 55.
    C. J. Coscia, W. T. Bern, G. E. Thomas, J. Y Mamone, B. K. Levy, M. Szucs, and F. E. Johnson, Sigma and opioid receptors in human cancers, Society for Neuroscience abstracts 16: (1990).Google Scholar
  56. 56.
    R. E. Watson, Jr., M. C. Langub, Jr., and J. W. Landis, Further evidence that LHRH neurons are not directly estrogen responsive: LHRH and estrogen receptor immunoreactivity in the guinea pig brain, Society for Neuroscience abstracts 16: (1990).Google Scholar
  57. 57.
    T. L. Dellovade, J. D. Blaustein, and E. F. Rissman, Distribution of estrogen receptors in the brain of the female musk shrew: an immunocytochemical study, Society for Neuroscience abstracts 16: (1990).Google Scholar
  58. 58.
    D. W. Pfaff, Estrogens and Brain Function, Springer, New York, (1980).Google Scholar
  59. 59.
    N. G. Simon and R. E. Whalen, Hormonal regulation of aggression: evidence for a relationship among genotype, receptor binding, and behavioral sensitivity to androgens and estrogen, Aggress Behav 12: 255–266 (1986).CrossRefGoogle Scholar
  60. 60.
    L. A. Hilakivi-Clarke, P. K. Arora, M. B. Sabol, R. Clarke, R. B. Dickson, and M. E. Lippman, Alterations in behavior, steroid hormones and natural killer cell activity in male transgenic TGF-a mice, Brain Res 588: 97–103 (1992).CrossRefGoogle Scholar
  61. 61.
    G. N. Wade and J. M. Gray, Gonadal effects on food intake and adiposity: a metabolic hypothesis, Physiol Behav 22: 583–593 (1979).CrossRefGoogle Scholar
  62. 62.
    S. G. Beck, W. P. Clarke, and J. Goldfarb, Chronic estrogen effects on 5-hydroxytryptamine-mediated responses in hippocampal pyramidal cells of female rats, Neurosci Lett 106: 181–187 (1989).CrossRefGoogle Scholar
  63. 63.
    K. Sinchak, C. E. Roselli, and L. G. Clemens, Determination of aromatase activity and estrogen receptor levels in discrete brain regions from intact and castrated hybrid B6D2F1 male house mice that copulate and those that do not, Society for Neuroscience abstracts 16: (1990).Google Scholar
  64. 64.
    K.-P. Lesch and S. Gross, Estrogen receptor immunoreactivity in meningiomas, J Neurosurg 67: 237–243 (1987).CrossRefGoogle Scholar
  65. 65.
    P. Bouillot, J. F. Pellissier, B. Devictor, N. Graziani, N. Bianco, F. Grisoli, and D. Figarella-Branger, Quantitative imaging of estrogen and progesterone receptors, estrogen-regulated protein, and growth fraction: immunocytochemical assays in 52 meningiomas, correlation with clinical and morphological data, J. Neurosurg. 81: 765–773 (1994).CrossRefGoogle Scholar
  66. 66.
    K. Iwasaki, S. A. Toms, G. H. Barnett, M. L. Estes, M. K. Gupta, and B. P. Barna, Inhibitory effects of tamoxifen and tumor necrosis factor alpha on human glioblastoma cells, Cancer Immunol. Immunother. 40: 228–234 (1995).CrossRefGoogle Scholar
  67. 67.
    G. Baltuch, G. Shenouda, A. Langleben, and J. G. Villemure, High dose tamoxifen in the treatment of recurrent high grade glioma: a report of clinical stabilization and tumour regression, Can. J.Neurol. Sci. 20: 168–170 (1993).Google Scholar
  68. 68.
    J. P Geisler, M. C. Wiemann, G. A. Miller, Z. Zhou, and H. E. Geisler, Estrogen and progesterone receptors in malignant mixed mesodermal tumors of the ovary, J. Surg. Oncol. 59: 45–47 (1995).CrossRefGoogle Scholar
  69. 69.
    S. Li, Relationship between cellular DNA synthesis, PCNA expression and sex steroid hormone receptor status in the developing mouse ovary, uterus and oviduct, Histochemistry 102: 405–413 (1994).CrossRefGoogle Scholar
  70. 70.
    G. Scambia, L. Catozzi, P. B. Panici, G. Ferrandina, F. Coronetta, R. Barozzi, G. Baiocchi, L. Uccelli, A. Piffanelli, and S. Mancuso, Expression of ras oncogene p21 protein in normal and neoplastic ovarian tissues: correlation with histopathologic features and receptors for estrogen, progesterone, and epidermal growth factor, Am. J. Obstet. Gynecol. 168: 71–78 (1993).Google Scholar
  71. 71.
    Y. Ohno, K. Hosokawa, T. Tamura, Y. Fujimoto, M. Kawashima, K. Koishi, and H. Okada, Endometrial oestrogen and progesterone receptors and their relationship to sonographic endometrial appearance, Hum. Reprod. 10: 708–711(1995).Google Scholar
  72. 72.
    P. C. Morris, J. R. Anderson, B. Anderson, and R. E. Buller, Steroid hormone receptor content and lymph node status in endometrial cancer, Gynecol. Oncol. 56: 406–411 (1995).CrossRefGoogle Scholar
  73. 73.
    I. Cohen, A. Shulman, M. Altaras, R. Tepper, M. Cordoba, and Y. Beyth, Estrogen and progesterone receptor expression of decidual endometrium in a postmenopausal woman treated with tamoxifen and megestrol acetate, Gynecol. Obstet. Invest. 38: 127–129 (1994).CrossRefGoogle Scholar
  74. 74.
    T. Paavonen, L. C. Andersson, and H. Adlercreutz, Sex hormone regulation of in vitro immune response. Estradiol enhances human B cell maturation via inhibition of suppressor T cells in pokeweed mitogen stimulated cultures, J Exp Med 154: 1935–1945 (1981).CrossRefGoogle Scholar
  75. 75.
    A. S. Ahmed, M. J. Dauphinee, and N. Talal, Effects of short term administration of sex hormones on normal and autoimmune mice, J Immunol 134: 204–210 (1985).Google Scholar
  76. 76.
    Z. M. Sthoeger, N. Chiorazzi, and R.G. Lahita, Regulation of the immune response by sex steroids. I. In vitro effects of estradiol and testosterone on pokeweed mitogen-induced human B cell differentiation, J Immunol 141:91–98 (1988).Google Scholar
  77. 77.
    I. Screpanti, A. Santoni, A. Gulino, R. B. Herberman, and L. Frati, Estrogen and antiestrogen modulation of mouse natural killer activity and large granular lymphocytes, Cell Immunol 106: 191–202 (1987).CrossRefGoogle Scholar
  78. 78.
    W. E. Seaman, M. A. Blackman, T. D. Gindhart, J.R. Roubinian, J. M. Loeb, and N. Talal, ß-Estradiol reduces natural killer cells in mice, J Immunol 121: 2193–2198 (1978).Google Scholar
  79. 79.
    N. Hanna and M. Schneider, Enhancement of tumor metastases and suppression of natural killer cell activity by ß-estradiol treatment, J Immunol 130: 974–980 (1983).Google Scholar
  80. 80.
    W. E. Seaman and N. Talal, The effect of 17ß-estradiol on natural killing in the mouse, in: “Natural Cell-Mediated Immunity Against Tumors”, R. B. Herberman., ed., Academic Press, New York, pp. 765–777(1980).Google Scholar
  81. 81.
    M. M. Gottardis, R. J. Wagner, E. C. Borden, and C. V. Jordan, Differential ability of antiestrogens to stimulate breast cancer cell (MCF-7) growth in vivo and in vitro, Cancer Res 49: 4765–4769 (1989).Google Scholar
  82. 82.
    L. Boix, J. Bruix, A. Castells, J. Fuster, C. Bru, J. Visa, F. Rivera, and J. Rodes, Sex hormone receptors in hepatocellular carcinoma. Is there a rationale for hormonal treatment?, J. Hepatol. 17: 187–191 (1993).CrossRefGoogle Scholar
  83. 83.
    S. Masood, A. B. West, and K. W. Barwick, Expression of steroid hormone receptors in benign hepatic tumors. An immunocytochemical study, Arch. Pathol. Lab. Med. 116: 1355–1359 (1992).Google Scholar
  84. 84.
    D. R. Ciocca, A. D. Jorge, O. Jorge, C. Milutin, R. Hosokawa, M. Diaz Lestren, E. Muzzio, S. Schulkin, and R. Schirbu, Estrogen receptors, progesterone receptors and heat-shock 27-kd protein in liver biopsy specimens from patients with hepatitis b virus infection, Hepatology 13: 838–844 (1991).CrossRefGoogle Scholar
  85. 85.
    C. W. Hendrickse, C. E. Jones, I. A. Donovan, J. P. Neoptolemos, and P. R. Baker, Oestrogen and progester one receptors in colorectal cancer and human colonic cancer cell lines, Br. J. Surg. 80: 636–640 (1993).CrossRefGoogle Scholar
  86. 86.
    S. Galandiuk, S. Miseljic, A. R. Yang, M. Early, M. D. McCoy, and J. L. Wittliff, Expression of hormone receptors, cathepsin d, and her-2/neu oncoprotein in normal colon and colonic disease, Arch. Surg. 128: 637–642 (1993).Google Scholar
  87. 87.
    F. Meggouh, P. Lointier, and S. Saez, Sex steroid and 1,25-dihydroxyvitamin d3 receptors in human colorectal adenocarcinoma and normal mucosa, Cancer Res 51: 1227–1233 (1991).Google Scholar
  88. 88.
    G. Viale, C. Doglioni, M. Gambacorta, G. Zamboni, G. Coggi, and C. Bordi, Progesterone receptor immunoreactivity in pancreatic endocrine tumors. An immunocytochemical study of 156 neuroendocrine tumors of the pancreas, gastrointestinal and respiratory tracts, and skin, Cancer 70: 2268–2277 (1992).CrossRefGoogle Scholar
  89. 89.
    A. Andren-Sandberg and J. Johansson, Influence of sex hormones on pancreatic cancer, Int. J. Pancreatol 7: 167–176(1990).Google Scholar
  90. 90.
    T. O. Siu and W. B. Kwan, Hormones in chemotherapy for pancreatic cancer, chemoagents or carriers?, In Vivo. 3: 255–258(1989).Google Scholar
  91. 91.
    L. A. Hilakivi-Clarke, J. Rowland, R. Clarke, and M. E. Lippman, Psychosocial factors in the development and progression of breast cancer, Breast Cancer Res Treat 29: 141–160 (1993).CrossRefGoogle Scholar
  92. 92.
    R. Clarke, N. Brünner, D. Katz, P. Glanz, R. B. Dickson, M.E. Lippman, and F. Kern, The effects of a constitutive production of TGF-α on the growth of MCF-7 human breast cancer cells in vitro and in vivo, Mol Endocrinol 3: 372–380 (1989).CrossRefGoogle Scholar
  93. 93.
    W. Imagawa, G. K. Bandyopadhyay, and S. Nandi, Regulation of mammary epithelial cell growth in mice and rats, Endocrine Rev 11: 494–523 (1990).CrossRefGoogle Scholar
  94. 94.
    S. Coleman, G. B. Silberstein, and C. W. Daniel, Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor, Dev Biology 127: 304–315 (1988).CrossRefGoogle Scholar
  95. 95.
    J. Russo and I. H. Russo, Biological and molecular bases of mammary carcinogenesis, Lab Invest 57: 112–137(1987).Google Scholar
  96. 96.
    B. Heuberger, I. Fitzka, G. Wasner, and K. Kratochwil, Induction of androgen receptor formation by epithelium-mesenchyme interaction in embryonic mouse mammary gland, Proc Natl Acad Sci USA 79: 2957–2961 (1982).CrossRefGoogle Scholar
  97. 97.
    K. Kratochwil, Organ specifity in mesenchymal induction demonstrated in the embryonic development of the mammary gland of the mouse, Dev Biology 20: 46–71 (1969).CrossRefGoogle Scholar
  98. 98.
    K. Kratochwil, Development and loss of androgen responsiveness in the embryonic rudiment of the mouse mammary gland, Dev Biology 61: 358–365 (1977).CrossRefGoogle Scholar
  99. 99.
    H. Wasner and C. W. Turner, Ontogeny of mesenchymal androgen receptors in the embryonic mouse mammary gland, Endocrinology 113: 1771–1780 (1983).CrossRefGoogle Scholar
  100. 100.
    A. Raynaud, Observations sur les modifications provoquees pas les hormones oestrogenes, du mode de developpement des mamelons des foetus de souris, CR Acad Sci 240: 674–676 (1955).Google Scholar
  101. 101.
    I. H. Russo, J. Medado, and J. Russo, Endocrine influences on the mammary gland, in: “Integument and Mammary Glands”, T. C. Jones et al., Springer-Verlag, Berlin, pp. 252–266 (1994).Google Scholar
  102. 102.
    M. R. Warner, Effect of various doses of estrogen to BALB/cCrgl neonatal female mice on mammary growth and branching at 5 weeks of age, Cell Tissue Kinet 9: 429–438 (1976).Google Scholar
  103. 103.
    T. Tamooka and H. A. Bern, Growth of mouse mammary glands after neonatal sex hormone treatment, J Natl Cancer Inst 69: 1347–1352 (1982).Google Scholar
  104. 104.
    L. Hilakivi-Clarke, E. Cho, M. Raygada, and N. Kenney, Alterations in mammary gland development following neonatal exposure to estradiol, transforming growth factor alpha, and estrogen receptor antagonist ICI 182,780, Endocrinology Submitted: (1995).Google Scholar
  105. 105.
    L. A. Jones and H.A. Bern, Cervicovaginal and mammary gland abnormalities in BALB/cCrgl mice treated neonatally with progesterone and estrogen, alone or in combination, Cancer Res 39: 2560–2567 (1979).Google Scholar
  106. 106.
    R. E. Frisch, Adipose Tissue and Reproduction, Karger, Basel, (1990).Google Scholar
  107. 107.
    H. Adlercreutz, Diet and sex hormone metabolism, in: “Nutrition, Toxicity, and Cancer”, I. R. Rowland., ed., CRC Press, Boca Raton, pp. 137–195 (1991).Google Scholar
  108. 108.
    D. Trichopoulos, Hypothesis: does breast cancer originate in utero?, Lancet 335: 939–940 (1990).CrossRefGoogle Scholar
  109. 109.
    A. Ekbom, D. Trichopoulos, H. O. Adami, C. C. Hsieh, and S. J. Lan, Evidence of prenatal influences on breast cancer risk, Lancet 340: 1015–1018 (1992).CrossRefGoogle Scholar
  110. 110.
    R. Anbazhagan, B. Nathan, and B. A. Gusterson, Prenatal influences and breast cancer, Lancet 340: 1477–1478 (1992).CrossRefGoogle Scholar
  111. 111.
    J. Lopez, L. Ogren, R. Verjan, and F. Talamantes, Effects of perinatal exposure to a synthetic estrogen and progestin on mammary tumorigenesis in mice, Teratology 38: 129–134 (1988).CrossRefGoogle Scholar
  112. 112.
    B. E. Walker, Tumors of female offspring of mice exposed prenatally to diethylstilbestrol, J Natl Cancer Inst 73: 133–140 (1984).Google Scholar
  113. 113.
    L. Hilakivi-Clarke, R. Clarke, I. Onojafe, M. Raygada, E. Cho, and M. E. Lippman, Maternal dietary fat increases breast cancer risk among female offspring, submitted (1995).Google Scholar
  114. 114.
    T. Colton, R. Greenberg, K. Noller, L. Resseguie, C… Bennekom, T. Heeren, and Y. Zhang, Breast cancer in mothers prescribed diethylstilbestrol in pregnancy, J Am Med Assoc 269: 2096–2100 (1993).CrossRefGoogle Scholar
  115. 115.
    R. A. Rhoades and G. A. Tanner, Medical Physiology, Little, Brown and Company, Boston, (1995).Google Scholar
  116. 116.
    M. L. Casey, P. C. MacDonald, and E. R. Simpson, Textbook of Endocrinology, W. B. Saunders Company, New York, (1992).Google Scholar
  117. 117.
    B. A. Williams, K. T. Mills, C. D. Burroughs, and H. A. Bern, Reproductive alterations in female C57BL/Crgl mice exposed neonatally to zearalenone, an estrogenic mycotoxin, Cancer Lett 46: 225–230 (1989).CrossRefGoogle Scholar
  118. 118.
    C. A. Lamartiniere, J. B. Moore, J. B. Holland, and S. Barnes, Chemoprevention of mammary cancer from neonatal genistein treatment, Proc. Am. Assoc. Cancer Res. 35: Abstract 3689 (1994).Google Scholar
  119. 119.
    J. Russo, G. Wilgus, and LH. Russo, Susceptibility of the mammary gland to carcinogenesis: Differentiation of the mammary gland as determinant of tumor incidence and type of lesion, Am J Pathol 96: 721–736(1979).Google Scholar
  120. 120.
    R. W. Engelman, N. K. Day, and R. A. Good, Calorie intake during mammary development influences cancer risk: lasting inhibition of C3H/HeOu mammary tumorigenesis by prepubertal calorie restriction, Cancer Res 54: 5724–5730 (1994).Google Scholar
  121. 121.
    S. Z. Haslam, Progesterone effects on deoxyribonucleic acid synthesis in normal mouse mammary glands, Endocrinology 122: 464–470 (1988).CrossRefGoogle Scholar
  122. 122.
    Y. Folman and G. S. Pope, The interaction in the immature mouse of potent oestrogens with coumestrol, genistein and other utero-vaginotrophic compounds of low potency, J Endocrinol 34: 215–225 (1966).CrossRefGoogle Scholar
  123. 123.
    D. T. Kiang, B. J. Kennedy, S. V. Pathre, and C. J. Mirocha, Binding characteristics of zearalenone analogs to estrogen receptors, Cancer Res 38: 3611–3615 (1978).Google Scholar
  124. 124.
    U. E. Mayr, Estrogen-controlled gene expression in tissue culture cells by zearalenone, FEBS Lett 239: 223–226 (1988).CrossRefGoogle Scholar
  125. 125.
    J. J. Michnovicz and H. L. Bradlow, Induction of estradiol metabolism by dietary indole-3-carbinol in humans, J Natl Cancer Inst 82: 947–949 (1990).CrossRefGoogle Scholar
  126. 126.
    H. L. Bradlow, R. E. Hershcopf, and J. Fishman, Oestradiol 16α-hydroxylase: a risk marker for breast cancer, Cancer Surv 5: 573–583 (1986).Google Scholar
  127. 127.
    A.L. Harris, The epidermal growth factor receptor as a target for therapy. Cancer Cells 2: 321–323 (1990).Google Scholar
  128. 128.
    Y Matsukawa, N. Marui, T. Sakai, Y Satomi, M. Yoshida, K. Matsumoto, H. Nishino, and A. Aoike, Genistein arrests cell cycle progression. Cancer Res 53: 1328–1331 (1993).Google Scholar
  129. 129.
    F. Leonessa, W.-Y Lim, V. Boulay, M. E. Lippman, and R. Clarke, Effect of the phytoestrogen zearalenone on human breast cancer cells, in: “Exercise, Calories, Fat and Cancer”, M. M. Jacobs., ed., Plenum Press, New York, pp. 286 (1992).Google Scholar
  130. 130.
    T. Fotsis, M. Pepper, H. Adlercreutz, G. Fleischmann, T. Hase, R. Montesano, and L. Schweigerer, Genistein, a dietary-derived inhibitor of in vitro angiogenesis, Proc Natl Acad Sci USA 90: 2690–2694 (1993).CrossRefGoogle Scholar
  131. 131.
    J. T. J. Kellis and L. E. Vickery, Inhibition of human estrogen synthetase (aromatase) by flavones, Science 225: 1032–1034(1984).CrossRefGoogle Scholar
  132. 132.
    H. Adlercreutz, K. Hockerstedt, C. Bannwart, S. Bloigu, E. Hamalainen, T. Fotsis, and A. Ollus, Effect of dietary components, including lignans and phytoestrogens, on enterohepatic circulation and liver metablism of estrogens and on sex hormone binding globulin (SHBG), J Steroid Biochem 27: 1135–1144 (1987).CrossRefGoogle Scholar
  133. 133.
    J. R. C Sainsbury, A. J. Malcolm, D. R. Appleton, J. R. Farndon, and A. L. Harris, Presence of epidermal growth factor receptor as an indicator of poor prognosis in patients with breast cancer, J Clin Pathol 38: 1225–1228 (1985).CrossRefGoogle Scholar
  134. 134.
    S. Nicholson, J. R. C. Sainsbury, P. Halcrow, P. Chambers, J. R. Farndon, and A. L. Harris, Expression of epidermal growth factor receptors associated with lack of response to endocrine therapy in recurrent breast cancer, Lancet i: 182–184 (1989).CrossRefGoogle Scholar
  135. 135.
    S. Nicholson, J. Richard, C Sainsbury, P. Halcrow, P. Kelly, B. Angus, C. Wright, J. Henry, J. R. Farndon, and A. L. Harris, Epidermal growth factor receptors: results of a 6 year follow-up study in operable breast cancer with emphasis on the node negative subgroup, Br J Cancer 63: 146–150 (1991).CrossRefGoogle Scholar
  136. 136.
    P. Bolufer, F. Miralles, A. Rodriguez, C. Vasquez, A. Lluch, J. Garcia-Conde, and T. Olmos, Epidermal growth factor receptor in human breast cancer: correlation with cytosolic and nuclear estrogen receptors and with biological and histological tumor characteristics, Eur J Cancer 26: 283–290 (1990).CrossRefGoogle Scholar
  137. 137.
    S. Nicholson, P. Halcrow, J. R. C Sainsbury, B. Angus, P. Chambers, J. R. Farndon, and A. L. Harris, Epidermal growth factor receptor (EGFr) status associated with failure of primary endocrine therapy in elderly postmenopausal patients with breast cancer, Br J Cancer 58: 810–814 (1988).CrossRefGoogle Scholar
  138. 138.
    K. D. R. Setchell, Naturally occurring non-steroidal estrogens of dietary origin, in: “Estrogens in the environment”, J. A. McLachlan., ed., Elsevier, pp. 69–85 (1985).Google Scholar
  139. 139.
    W. S. Pierpoint, Flavonoids in the human diet, in: “Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological and Structure-Activity Relationships”, Alan R. Liss, Inc, New York, pp. 125–140 (1986).Google Scholar
  140. 140.
    K. Verdeal, R. R. Brown, T. Richardson, and D. S. Ryan, Affinity of phytoestrogens for estradiol-binding proteins and effect of coumesterol on growth of 7, 12-dimethylbenz(a)anthracene-induced rat mammary tumors, J Natl Cancer Inst 64: 285–290 (1980).Google Scholar
  141. 141.
    U. Mayr, A. Butsch, and S. Schneider, Validation of two in vitro test systems for estrogenic activities with zearalenone, phytoestrogens, and cereal extracts, Toxicology 74: 135–149 (1992).CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1996

Authors and Affiliations

  • Robert Clarke
    • 1
    • 2
  • Leena Hilakivi-Clarke
    • 1
    • 3
  • Elizabeth Cho
    • 1
  • Mattie R. James
    • 1
  • Fabio Leonessa
    • 1
    • 2
  1. 1.Vincent T Lombardi Cancer CenterGeorgetown University Medical SchoolUSA
  2. 2.Department of Physiology and BiophysicsGeorgetown University Medical SchoolUSA
  3. 3.Department of PsychiatryGeorgetown University Medical SchoolUSA

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