Biological functions and clinical implications of oestrogen receptors alfa and beta in epithelial tissues

Journal of Internal Medicine

Volumn 264, Issue 2, 2008, Pages 128-142

  Morani, A ^a   Warner, M ^a   Gustafsson, J A ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Chronic obstructive pulmonary disease; Epithelium; Extracellular matrix; Oestrogen receptor; Prostate cancer; SERMs

Indexed keywords

21 (4 DIETHYLAMINOMETHYL 2 METHOXYPHENOXY) 7ALPHA METHYL 19 NORPREGNA 1,3,5(10) TRIEN 3 OL; ANDROGEN; CELL NUCLEUS RECEPTOR; CYTOCHROME P450; DROLOXIFENE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FOLLITROPIN RECEPTOR; FULVESTRANT; GLYCOPROTEIN; IDOXIFENE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LUTEINIZING HORMONE; PRASTERONE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SEX HORMONE; STEROID HORMONE; TAMOXIFEN; TOREMIFENE; ZK 253; ZK 703;

APOPTOSIS; AUTOIMMUNITY; BIOSYNTHESIS; BREAST CANCER; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMICAL STRUCTURE; DRUG INHIBITION; DRUG MECHANISM; ENDOMETRIUM; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GRANULOSA CELL; HORMONE METABOLISM; HORMONE SYNTHESIS; HUMAN; LIGAND BINDING; LUNG ALVEOLUS; LUNG ALVEOLUS EPITHELIUM; MENOPAUSE; NONHUMAN; OVARY FOLLICLE; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROSTATE VENTRAL LOBE; PROTEIN EXPRESSION; REVIEW; STEROID METABOLISM; SYSTEMIC LUPUS ERYTHEMATOSUS;

AUTOIMMUNE DISEASES; EPITHELIUM; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR MODULATORS; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LUNG; MALE; UTERUS;

EID: 46949089089     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2008.01976.x     Document Type: Review

References (114)

1. Jensen EV, Jacobson HI, Smith S, Jungblut PW, De Sombre ER. The use of estrogen antagonists in hormone receptor studies. Gynecol Invest 1972 3 : 108 23.
2. Smith EP, Boyd J, Frank GR et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 1994 331 : 1056 61.
3. Green S, Walter P, Greene G et al. Cloning of the human oestrogen receptor cDNA. J Steroid Biochem 1986 24 : 77 83.
4. Greene GL, Nolan C, Engler JP, Jensen EV. Monoclonal antibodies to human estrogen receptor. Proc Natl Acad Sci U S A 1980 77 : 5115 9.
5. Walter P, Green S, Greene G et al. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci U S A 1985 82 : 7889 93.
6. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 1996 93 : 5925 30.
7. Kuiper GG, Carlsson B, Grandien K et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997 138 : 863 70.
8. Weihua Z, Makela S, Andersson LC et al. A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc Natl Acad Sci U S A 2001 98 : 6330 5.
9. Cheng G, Weihua Z, Makinen S et al. A role for the androgen receptor in follicular atresia of estrogen receptor beta knockout mouse ovary. Biol Reprod 2002 66 : 77 84.
10. Patrone C, Cassel TN, Pettersson K et al. Regulation of postnatal lung development and homeostasis by estrogen receptor beta. Mol Cell Biol 2003 23 : 8542 52.
11. Giguere V, Hollenberg SM, Rosenfeld MG, Evans RM. Functional domains of the human glucocorticoid receptor. Cell 1986 46 : 645 52.
12. Hollenberg SM, Evans RM. Multiple and cooperative trans-activation domains of the human glucocorticoid receptor. Cell 1988 55 : 899 906.
13. Kumar V, Green S, Stack G, Berry M, Jin JR, Chambon P. Functional domains of the human estrogen receptor. Cell 1987 51 : 941 51.
14. Luisi BF, Xu WX, Otwinowski Z, Freedman LP, Yamamoto KR, Sigler PB. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 1991 352 : 497 505.
15. Picard D, Yamamoto KR. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J 1987 6 : 3333 40.
16. Graupner G, Wills KN, Tzukerman M, Zhang XK, Pfahl M. Dual regulatory role for thyroid-hormone receptors allows control of retinoic-acid receptor activity. Nature 1989 340 : 653 6.
17. Pratt WB, Jolly DJ, Pratt DV et al. A region in the steroid binding domain determines formation of the non-DNA-binding, 9 S glucocorticoid receptor complex. J Biol Chem 1988 263 : 267 73.
18. Webster NJ, Green S, Jin JR, Chambon P. The hormone-binding domains of the estrogen and glucocorticoid receptors contain an inducible transcription activation function. Cell 1988 54 : 199 207.
19. Vegeto E, Allan GF, Schrader WT, Tsai MJ, McDonnell DP, O'Malley BW. The mechanism of RU486 antagonism is dependent on the conformation of the carboxy-terminal tail of the human progesterone receptor. Cell 1992 69 : 703 13.
20. Nilsson S, Makela S, Treuter E et al. Mechanisms of estrogen action. Physiol Rev 2001 81 : 1535 65.
21. Kushner PJ, Agard DA, Greene GL et al. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 2000 74 : 311 7.
22. Saville B, Wormke M, Wang F et al. Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J Biol Chem 2000 275 : 5379 87.
23. Galien R, Garcia T. Estrogen receptor impairs interleukin-6 expression by preventing protein binding on the NF-kappaB site. Nucleic Acids Res 1997 25 : 2424 9.
24. Ray A, Prefontaine KE, Ray P. Down-modulation of interleukin-6 gene expression by 17 beta-estradiol in the absence of high affinity DNA binding by the estrogen receptor. J Biol Chem 1994 269 : 12940 6.
25. Heldring N, Pike A, Andersson S et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007 87 : 905 31.
26. Kato S, Endoh H, Masuhiro Y et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995 270 : 1491 4.
27. Coutts AS, Murphy LC. Elevated mitogen-activated protein kinase activity in estrogen-nonresponsive human breast cancer cells. Cancer Res 1998 58 : 4071 4.
28. Shim WS, Conaway M, Masamura S et al. Estradiol hypersensitivity and mitogen-activated protein kinase expression in long-term estrogen deprived human breast cancer cells in vivo. Endocrinology 2000 141 : 396 405.
29. Smith CL, Nawaz Z, O'Malley BW. Coactivator and corepressor regulation of the agonist/antagonist activity of the mixed antiestrogen, 4-hydroxytamoxifen. Mol Endocrinol 1997 11 : 657 66.
30. Webb P, Nguyen P, Kushner PJ. Differential SERM effects on corepressor binding dictate ERalpha activity in vivo. J Biol Chem 2003 278 : 6912 20.
31. Ghayee HK, Auchus RJ. Basic concepts and recent developments in human steroid hormone biosynthesis. Rev Endocr Metab Disord 2007 8 : 289 300.
32. Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 2004 25 : 947 70.
33. Hess RA. Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol 2003 1 : 52.
34. Sasano H, Okamoto M, Mason JI et al. Immunolocalization of aromatase, 17 alpha-hydroxylase and side-chain-cleavage cytochromes P-450 in the human ovary. J Reprod Fertil 1989 85 : 163 9.
35. Havelock JC, Rainey WE, Carr BR. Ovarian granulosa cell lines. Mol Cell Endocrinol 2004 228 : 67 78.
36. Schlessinger J, Lax I, Lemmon M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell 1995 83 : 357 60.
37. Sasisekharan R, Moses MA, Nugent MA, Cooney CL, Langer R. Heparinase inhibits neovascularization. Proc Natl Acad Sci U S A 1994 91 : 1524 8.
38. Goetzl MA, Van Veldhuizen PJ, Thrasher JB. Effects of soy phytoestrogens on the prostate. Prostate Cancer Prostatic Dis 2007 10 : 216 23.
39. Krege JH, Hodgin JB, Couse JF et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 1998 95 : 15677 82.
40. Imamov O, Morani A, Shim GJ et al. Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc Natl Acad Sci U S A 2004 101 : 9375 80.
41. Omoto Y, Imamov O, Warner M, Gustafsson JA. Estrogen receptor alpha and imprinting of the neonatal mouse ventral prostate by estrogen. Proc Natl Acad Sci U S A 2005 102 : 1484 9.
42. Signoretti S, Loda M. Estrogen receptor beta in prostate cancer: brake pedal or accelerator? Am J Pathol 2001 159 : 13 6.
43. Chang WY, Prins GS. Estrogen receptor-beta: implications for the prostate gland. Prostate 1999 40 : 115 24.
44. Bardin A, Boulle N, Lazennec G, Vignon F, Pujol P. Loss of ERbeta expression as a common step in estrogen-dependent tumor progression. Endocr Relat Cancer 2004 11 : 537 51.
45. Horvath LG, Henshall SM, Lee CS et al. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res 2001 61 : 5331 5.
46. Nojima D, Li LC, Dharia A et al. CpG hypermethylation of the promoter region inactivates the estrogen receptor-beta gene in patients with prostate carcinoma. Cancer 2001 92 : 2076 83.
47. Zhu X, Leav I, Leung YK et al. Dynamic regulation of estrogen receptor-beta expression by DNA methylation during prostate cancer development and metastasis. Am J Pathol 2004 164 : 2003 12.
48. Leav I, Lau KM, Adams JY et al. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol 2001 159 : 79 92.
49. Bruchovsky N, Wilson JD. The conversion of testosterone to 5-alpha-androstan-17-beta-ol-3-one by rat prostate in vivo and in vitro. J Biol Chem 1968 243 : 2012 21.
50. Mahendroo MS, Cala KM, Hess DL, Russell DW. Unexpected virilization in male mice lacking steroid 5 alpha-reductase enzymes. Endocrinology 2001 142 : 4652 62.
51. Warner M, Stromstedt M, Moller L, Gustafsson JA. Distribution and regulation of 5 alpha-androstane-3 beta,17 beta-diol hydroxylase in the rat central nervous system. Endocrinology 1989 124 : 2699 706.
52. Weihua Z, Lathe R, Warner M, Gustafsson JA. An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta,17beta-diol, and CYP7B1, regulates prostate growth. Proc Natl Acad Sci U S A 2002 99 : 13589 94.
53. Voigt KD, Bartsch W. Intratissular androgens in benign prostatic hyperplasia and prostatic cancer. J Steroid Biochem 1986 25 : 749 57.
54. Guerini V, Sau D, Scaccianoce E et al. The androgen derivative 5alpha-androstane-3beta,17beta-diol inhibits prostate cancer cell migration through activation of the estrogen receptor beta subtype. Cancer Res 2005 65 : 5445 53.
55. Oliveira AG, Coelho PH, Guedes FD, Mahecha GA, Hess RA, Oliveira CA. 5alpha-Androstane-3beta, 17beta-diol (3beta-diol), an estrogenic metabolite of 5alpha-dihydrotestosterone, is a potent modulator of estrogen receptor ERbeta expression in the ventral prostrate of adult rats. Steroids 2007 72 : 914 22.
56. Ahmed N, Thompson EW, Quinn MA. Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm. J Cell Physiol 2007 213 : 581 8.
57. Sar M, Welsch F. Differential expression of estrogen receptor-beta and estrogen receptor-alpha in the rat ovary. Endocrinology 1999 140 : 963 71.
58. Findlay JK, Britt K, Kerr JB et al. The road to ovulation: the role of oestrogens. Reprod Fertil Dev 2001 13 : 543 7.
59. Weihua Z, Saji S, Makinen S et al. Estrogen receptor (ER) beta, a modulator of ERalpha in the uterus. Proc Natl Acad Sci U S A 2000 97 : 5936 41.
60. Pettersson K, Gustafsson JA. Role of estrogen receptor beta in estrogen action. Annu Rev Physiol 2001 63 : 165 92.
61. -/-) mice. Proc Natl Acad Sci U S A 2007 104 : 600 5.
62. Yang Y, Balla A, Danilovich N, Sairam MR. Developmental and molecular aberrations associated with deterioration of oogenesis during complete or partial follicle-stimulating hormone receptor deficiency in mice. Biol Reprod 2003 69 : 1294 302.
63. Danilovich N, Roy I, Sairam MR. Ovarian pathology and high incidence of sex cord tumors in follitropin receptor knockout (FORKO) mice. Endocrinology 2001 142 : 3673 84.
64. Couse JF, Yates MM, Deroo BJ, Korach KS. Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 2005 146 : 3247 62.
65. Farquhar CM. The role of ovarian surgery in polycystic ovary syndrome. Best Pract Res Clin Obstet Gynaecol 2004 18 : 789 802.
66. Massaro D, Massaro GD. Estrogen receptor regulation of pulmonary alveolar dimensions: alveolar sexual dimorphism in mice. Am J Physiol Lung Cell Mol Physiol 2006 290 : L866 70.
67. Massaro GD, Mortola JP, Massaro D. Estrogen modulates the dimensions of the lung's gas-exchange surface area and alveoli in female rats. Am J Physiol 1996 270 : L110 4.
68. Massaro D, Massaro GD. Estrogen regulates pulmonary alveolar formation, loss, and regeneration in mice. Am J Physiol Lung Cell Mol Physiol 2004 287 : L1154 9.
69. Massaro D, Clerch LB, Massaro GD. Estrogen receptor-alpha regulates pulmonary alveolar loss and regeneration in female mice: morphometric and gene expression studies. Am J Physiol Lung Cell Mol Physiol 2007 293 : L222 8.
70. -/-) mice. Proc Natl Acad Sci U S A 2006 103 : 7165 9.
71. -/- mouse heart. Proc Natl Acad Sci U S A 2004 101 : 14234 9.
72. Powell FL, Hopkins SR. Comparative physiology of lung complexity: implications for gas exchange. News Physiol Sci 2004 19 : 55 60.
73. Neas LM, Schwartz J. The determinants of pulmonary diffusing capacity in a national sample of U.S. adults. Am J Respir Crit Care Med 1996 153 : 656 64.
74. Real FG, Svanes C, Omenaas ER et al. Lung function, respiratory symptoms, and the menopausal transition. J Allergy Clin Immunol 2007 121 : 72 80.
75. Real FG, Svanes C, Omenaas ER et al. Menstrual irregularity and asthma and lung function. J Allergy Clin Immunol 2007 120 : 557 64.
76. Pata O, Atis S, Utku Oz A et al. The effects of hormone replacement therapy type on pulmonary functions in postmenopausal women. Maturitas 2003 46 : 213 8.
77. 1 in elderly women. Am J Respir Crit Care Med 2001 163 : 423 8.
78. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 1993 90 : 11162 6.
79. Shyamala G, Singh RK, Ruh MF, Ruh TS. Relationships between mammary estrogen receptor and estrogenic sensitivity. II. Binding of cytoplasmic receptor to chromatin. Endocrinology 1986 119 : 819 26.
80. Saji S, Jensen EV, Nilsson S, Rylander T, Warner M, Gustafsson JA. Estrogen receptors alpha and beta in the rodent mammary gland. Proc Natl Acad Sci U S A 2000 97 : 337 42.
81. Zhang HZ, Bennett JM, Smith KT, Sunil N, Haslam SZ. Estrogen mediates mammary epithelial cell proliferation in serum-free culture indirectly via mammary stroma-derived hepatocyte growth factor. Endocrinology 2002 143 : 3427 34.
82. Forster C, Makela S, Warri A et al. Involvement of estrogen receptor beta in terminal differentiation of mammary gland epithelium. Proc Natl Acad Sci U S A 2002 99 : 15578 83.
83. Cheng G, Weihua Z, Warner M, Gustafsson JA. Estrogen receptors ER alpha and ER beta in proliferation in the rodent mammary gland. Proc Natl Acad Sci U S A 2004 101 : 3739 46.
84. Hartman J, Muller P, Foster JS, Wimalasena J, Gustafsson JA, Strom A. HES-1 inhibits 17beta-estradiol and heregulin-beta1-mediated upregulation of E2F-1. Oncogene 2004 23 : 8826 33.
85. Strom A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci U S A 2004 101 : 1566 71.
86. Eckstein B. Blood concentrations and biological effects of androstanediols at the onset of puberty in the female rat. J Steroid Biochem 1983 19 : 883 6.
87. Wu JJ, Geimonen E, Andersen J. Increased expression of estrogen receptor beta in human uterine smooth muscle at term. Eur J Endocrinol 2000 142 : 92 9.
88. Tessier C, Deb S, Prigent-Tessier A et al. Estrogen receptors alpha and beta in rat decidua cells: cell-specific expression and differential regulation by steroid hormones and prolactin. Endocrinology 2000 141 : 3842 51.
89. Alarcon-Segovia D, Alarcon-Riquelme ME, Cardiel MH et al. Familial aggregation of systemic lupus erythematosus, rheumatoid arthritis, and other autoimmune diseases in 1,177 lupus patients from the GLADEL cohort. Arthritis Rheum 2005 52 : 1138 47.
90. Peter SA, Johnson R, Taylor C et al. The incidence and prevalence of type-1 diabetes mellitus. J Natl Med Assoc 2005 97 : 250 2.
91. Bynoe MS, Grimaldi CM, Diamond B. Estrogen up-regulates Bcl-2 and blocks tolerance induction of naive B cells. Proc Natl Acad Sci U S A 2000 97 : 2703 8.
92. Wu WM, Lin BF, Su YC, Suen JL, Chiang BL. Tamoxifen decreases renal inflammation and alleviates disease severity in autoimmune NZB/W F1 mice. Scand J Immunol 2000 52 : 393 400.
93. Ishimaru N, Saegusa K, Yanagi K, Haneji N, Saito I, Hayashi Y. Estrogen deficiency accelerates autoimmune exocrinopathy in murine Sjogren's syndrome through fas-mediated apoptosis. Am J Pathol 1999 155 : 173 81.
94. Shim GJ, Kis LL, Warner M, Gustafsson JA. Autoimmune glomerulonephritis with spontaneous formation of splenic germinal centers in mice lacking the estrogen receptor alpha gene. Proc Natl Acad Sci U S A 2004 101 : 1720 4.
95. Shim GJ, Wang L, Andersson S et al. Disruption of the estrogen receptor beta gene in mice causes myeloproliferative disease resembling chronic myeloid leukemia with lymphoid blast crisis. Proc Natl Acad Sci U S A 2003 100 : 6694 9.
96. Shim GJ, Warner M, Kim HJ et al. Aromatase-deficient mice spontaneously develop a lymphoproliferative autoimmune disease resembling Sjogren's syndrome. Proc Natl Acad Sci U S A 2004 101 : 12628 33.
97. Lippman ME, Bolan G. Oestrogen-responsive human breast cancer in long term tissue culture. Nature 1975 256 : 592 3.
98. Cole MP, Jones CT, Todd ID. A new anti-oestrogenic agent in late breast cancer. An early clinical appraisal of ICI46474. Br J Cancer 1971 25 : 270 5.
99. Jordan VC. Antiestrogenic and antitumor properties of tamoxifen in laboratory animals. Cancer Treat Rep 1976 60 : 1409 19.
100. Jordan VC. Effect of tamoxifen (ICI 46,474) on initiation and growth of DMBA-induced rat mammary carcinomata. Eur J Cancer 1976 12 : 419 24.
101. Jordan VC, Dowse LJ. Tamoxifen as an anti-tumour agent: effect on oestrogen binding. J Endocrinol 1976 68 : 297 303.
102. Jordan VC, Jaspan T. Tamoxifen as an anti-tumour agent: oestrogen binding as a predictive test for tumour response. J Endocrinol 1976 68 : 453 60.
103. Jordan VC, Phelps E, Lindgren JU. Effects of anti-estrogens on bone in castrated and intact female rats. Breast Cancer Res Treat 1987 10 : 31 5.
104. Turner RT, Wakley GK, Hannon KS, Bell NH. Tamoxifen inhibits osteoclast-mediated resorption of trabecular bone in ovarian hormone-deficient rats. Endocrinology 1988 122 : 1146 50.
105. Turner RT, Wakley GK, Hannon KS, Bell NH. Tamoxifen prevents the skeletal effects of ovarian hormone deficiency in rats. J Bone Miner Res 1987 2 : 449 56.
106. Jordan VC, Robinson SP. Species-specific pharmacology of antiestrogens: role of metabolism. Fed Proc 1987 46 : 1870 4.
107. Gottardis MM, Robinson SP, Satyaswaroop PG, Jordan VC. Contrasting actions of tamoxifen on endometrial and breast tumor growth in the athymic mouse. Cancer Res 1988 48 : 812 5.
108. Baumann CK, Castiglione-Gertsch M. Estrogen receptor modulators and down regulators: optimal use in postmenopausal women with breast cancer. Drugs 2007 67 : 2335 53.
109. Brzozowski AM, Pike AC, Dauter Z et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997 389 : 753 8.
110. Paige LA, Christensen DJ, Gron H et al. Estrogen receptor (ER) modulators each induce distinct conformational changes in ER alpha and ER beta. Proc Natl Acad Sci U S A 1999 96 : 3999 4004.
111. Shiau AK, Barstad D, Loria PM et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998 95 : 927 37.
112. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS. Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 2003 206 : 13 22.
113. Harris HA, Albert LM, Leathurby Y et al. Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 2003 144 : 4241 9.
114. Robertson JF, Nicholson RI, Bundred NJ et al. Comparison of the short-term biological effects of 7alpha-[9-(4,4,5,5,5-pentafluoropentylsulfinyl) -nonyl]estra-1,3,5, (10)-triene-3,17beta-diol (Faslodex) versus tamoxifen in postmenopausal women with primary breast cancer. Cancer Res 2001 61 : 6739 46.