The role of estrogens and estrogen receptors in normal prostate growth and disease

Steroids

Volumn 73, Issue 3, 2008, Pages 233-244

  Prins, Gail S ^a   Korach, Kenneth S ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Estradiol; Estrogen receptor; Estrogens; Prostate; Prostate cancer

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; MITOGEN ACTIVATED PROTEIN KINASE; NATURAL PRODUCT; PHYTOESTROGEN; RALOXIFENE; TORIMIFENE; TRIOXIFENE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CARCINOGENESIS; CHEMOPROPHYLAXIS; CLINICAL TRIAL; DISEASE COURSE; DNA SEQUENCE; DRUG INHIBITION; DRUG MECHANISM; ESTROGEN RESPONSIVE ELEMENT; HOMEOSTASIS; HORMONE BLOOD LEVEL; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; LIGAND BINDING; NONHUMAN; PROSTATE CANCER; PROSTATE DISEASE; PROSTATE HYPERTROPHY; PROSTATITIS; REVIEW; TISSUE DIFFERENTIATION;

ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; HUMANS; MALE; PROSTATE; PROSTATIC DISEASES; PROSTATIC NEOPLASMS; RECEPTORS, ESTROGEN;

EID: 38649140488     PISSN: 0039128X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.steroids.2007.10.013     Document Type: Review

References (141)

1. Matzkin H., and Soloway M.S. Immunohistochemical evidence of the existence and localization of aromatase in human prostatic tissues. Prostate 21 (1992) 309-314
2. Risbridger G.P., Bianco J.J., Ellem S.J., and McPherson S.J. Estrogens and prostate cancer. Endocr Relat Cancer 10 (2003) 187-191
3. Zondek T., Mansfield M.D., Attree S.L., and Zondek L.H. Hormone levels in the fetal and neonatal prostate. Acta Endocr 112 (1986) 447-456
4. Wernet N., Kern L., Heitz P.H., Bonkhoff H., Goebbels I.R., Seitz G., et al. Morphological and immunohistochemical investigations of the utriculus prostaticus from the fetal period up to adulthood. Prostate 17 (1990) 19-30
5. Rajfer J., and Coffey D.S. Sex steroid imprinting of the immature prostate. Invest Urol 16 3 (1978) 186-190
6. Henderson B.E., Bernstein L., Ross R.K., Depue R.H., and Judd H.L. The early in utero oestrogen and testosterone environment of blacks and whites: potential effects on male offspring. Br J Cancer 57 2 (1988) 216-218
7. Platz E.A., and Giovannucci E. The epidemiology of sex steroid hormones and their signaling and metabolic pathways in the etiology of prostate cancer. J Steroid Biochem Mol Biol 92 (2004) 237-253
8. Ekbom A., Wuu J., Adami H.O., Lu C.M., Lagiou P., Trichopoulos D., et al. Duration of gestation and prostate cancer risk in offspring. Cancer Epidemiol Biomarkers Prev 9 2 (2000) 221-223
9. Ekbom A., Hsieh C.C., Lipworth L., Wolk A., Ponten J., Adami H.O., et al. Perinatal characteristics in relation to incidence of and mortality from prostate cancer. Br Med J 313 (1996) 337-341
10. Driscoll S.G., and Taylor S.H. Effects of prenatal maternal estrogen on the male urogenital system. Obstet Gynecol 56 5 (1980) 537-542
11. Yonemura C.Y., Cunha G.R., Sugimura Y., and Mee S.L. Temporal and spatial factors in diethylstilbestrol-induced squamous metaplasia in the developing human prostate. II. Persistent changes after removal of diethylstilbestrol. Acta Anatom 153 (1995) 1-11
12. Giusti R.M., Iwamoto K., and Hatch E.E. Diethylstilbestrol revisited: a review of the long-term health effects. Ann Int Med 122 10 (1995) 778-788
13. Arai Y., Mori T., Suzuki Y., and Bern H.A. Long-term effects of perinatal exposure to sex steroids and diethylstilbestrol on the reproductive system of male mammals. In: Bourne GHaD J.F. (Ed). International review of cytology vol. 84 (1983), Academic Press, Inc, New York 235-268
14. Prins G.S. Developmental estrogenization of the prostate gland. In: Naz R.K. (Ed). Prostate: basic and clinical aspects (1997), C.R.C. Press, Boca Raton 247-265 [Chapter 10]
15. Prins G.S., Huang L., Birch L., and Pu Y. The role of estrogens in normal and abnormal development of the prostate gland. Ann N Y Acad Sci 1089 (2006) 1-13
16. McLachlan J.A. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 22 3 (2001) 319-341
17. Ho S.M., Tang W.Y., Belmonte J., and Prins G.S. Developmental exposure estradiol and bisphenol A (BPA) increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodisesterase type 4 variant (PDE4D4) in the rat prostate. Cancer Res 66 11 (2006) 5624-5632
18. Kaufman J.M., and Vermeulen A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocrin Rev 26 (2005) 833-875
19. Vermeulen A., Kaufman J.M., Goemaere S., and van Pottelberg I. Estradiol in elderly men. Aging Male 5 2 (2002) 98-102
20. Ho S.M. Estrogens and antiestrogens: key mediators of prostate carcinogenesis and new therapeutic candidates. J Cell Biochem 91 (2004) 491-503
21. King K.J., Nicholson H.D., and Assinder S.J. Effect of increasing ratio of estrogen:androgen on proliferation of normal and human prostate stromal and epithelial cells and the malignant cell line LNCaP. Prostate 66 (2006) 105-114
22. Thomas J.A., and Keenan E.J. Effects of estrogen on the prostate. J Androl 15 2 (1994) 97-99
23. Castagnetta L.A.M., and Carruba G. Human prostate cancer: a direct role for oestrogens. Non-reproductive actions of sex steroids (1995), Wiley, Chichester 269-289
24. Price D. Normal development of the prostate and seminal vesicles of the rat with a study of experimental postnatal modifications. Am J Anat 60 (1936) 79-127
25. Leav I., Ho S., Ofner P., Merk F., Kwan P., and Damassa D. Biochemical alterations in sex hormone-induced hyperplasia and dysplasia of the dorsolateral prostates of Noble rats. J Natl Cancer Inst 80 13 (1988) 1045-1053
26. Coffey D., and Walsh P. Clinical and experimental studies of benign prostatic hyperplasia. Urol Clin North Am 17 3 (1990) 461-475
27. DeKlerk D., Coffey D., Weing L., McDermott I., Reiener W., Robinson C., et al. Comparison of spontaneous and experimentally induced canine prostatic hyperplasia. J Clin Invest 64 (1979) 842-849
28. Krieg M., Klotzl G., Kaufmann J., and Voigt K. Stroma of human benign prostatic hyperplasia: preferential tissue for androgen metabolism and oestrogen binding. Acta Endocr 96 (1981) 422-432
29. Lee C., Prins G.S., Henneberry M.O., and Grayhack J.T. Effect of estradiol on the rat prostate in the presence and absence of testosterone and pituitary. J Androl 2 6 (1981) 293-299
30. Gilleran J.P., Putz O., De Jong M., De Jong S., Birch L., Pu Y., et al. The role of prolactin in the prostatic inflammatory response to neonatal estrogen. Endocrinology 144 5 (2003) 2046-2054
31. Lane K., Leav I., Ziar J., Bridges R., Rand W., and Ho S.M. Suppression of testosterone and estradiol-17beta-induced dysplasia in the dorsolateral prostate of Noble rats by bromocriptine. Carcinogenesis 18 8 (1997) 1505-1520
32. Huggins C., and Hodges C.F. Studies on prostatic cancer. I. The effect of castration, of estrogen, and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. Cancer Res 1 (1941) 293-297
33. Prins G.S. Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology 130 6 (1992) 3703-3714
34. Nevalainen M.T., Harkonen P.L., Valve E.M., Ping W., Nurmi M., and Martikainen P.M. Hormone regulation of human prostate in organ culture. Cancer Res 53 (1993) 5199-5207
35. Jarred R., Cancilla B., Prins G.S., Thayer K., Cunha G.R., and Risbridger G. Evidence that estrogens directly alter androgen-regulated prostate development. Endocrinology 141 9 (2000) 3471-3477
36. Nebert D.W., Adesnik M., Coon M.J., Estabrook R.W., Gonzalez F.J., Guengerich F.P., et al. The P450 gene superfamily: recommended nomenclature. DNA 6 (1987) 1-11
37. Committee NRN. A unified nomenclature system for the nuclear receptor superfamily. Cell 97 (1999) 161-163
38. Walter P., Green S., Greene G., Krust A., Bornert J.-M., Jeltsch J.-M., et al. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci USA 82 (1985) 7889-7893
39. Laudet V., and Gronemeyer H. The nuclear receptor factsbook (2002), Academic Press, San Diego
40. White R., Lees J.A., Needham M., Ham J., and Parker M. Structural organization and expression of the mouse estrogen receptor. Mol Endocrinol 1 (1987) 735-744
41. Miksicek R.J. Steroid receptor variants and their potential role in cancer. Sem Cancer Biol 5 (1994) 369-379
42. Sluyser M. Mutations in the estrogen receptor gene. Hum Mutat 6 (1995) 97-103
43. Kuiper G.G.J.M., Enmak E., Pelto-Huikko M., Nilsson S., and Gustaffson J.A. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acac Sci USA 93 (1996) 5925-5930
44. Mosselman S., Polman J., and Dijkema R. ER B: identification and characterization of a novel human estrogen receptor. FEBS 392 (1996) 49-53
45. Leung Y.K., Mak P., Hassan S., and Ho S.M. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc Natl Acad Sci USA 103 35 (2006) 13162-13167
46. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schutz G., Umesono K., et al. The nuclear receptor superfamily: the second decade. Cell 83 (1995) 835-839
47. Aranda A., and Pascual A. Nuclear hormone receptors and gene expression. Physiol Rev 81 (2001) 1269-1304
48. Ueda T., Bruchovsky N., and Sadar M.D. Activation of the androgen receptor N-terminal domain by interleukin-6 via MAPK and STAT3 signal transduction pathways. J Biol Chem 277 (2002) 7076-7085
49. Katzenellenbogen B.S., Montano M.M., Ediger T.R., Sun J., Ekena K., Lazennec G., Martini P.G., McInerney E.M., Delage-Mourroux R., Weis K., and Katzenellenbogen J.A. Estrogen receptors: selective ligands, partners, and distinctive pharmacology. Recent Prog Horm Res 55 (2000) 163-193 [discussion, 194-165]
50. Delaunay F., Pettersson K., Tujague M., and Gustafsson J.A. Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol Pharmacol 58 (2000) 584-590
51. Watanabe T., Inoue S., Ogawa S.I., shii Y., Hiroi H., Ikeda K., et al. Agonist effect of tamoxifen is dependent on cell type, ERE-promoter context, and estrogen receptor subtype: functional difference between estrogen receptors α and β. Biochem Biophys Res Commun 236 (1997) 140-145
52. Cowley S.M., and Parker M.G. A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol 69 (1999) 165-175
53. Kuiper G.G.J.M., and Gustafsson J.-A. The novel estrogen receptor-b subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410 (1997) 87-90
54. Kim K., Thu N., Saville B., and Safe S. Domains of estrogen receptor alpha (ERalpha) required for ERalpha/Sp1-mediated activation of GC-rich promoters by estrogens and antiestrogens in breast cancer cells. Mol Endocrinol 17 (2003) 804-817
55. Shiau A.K., Barstad D., Radek J.T., Meyers M.J., Nettles K.W., Katzenellenbogen B.S., et al. Structural characterization of a subtype-selective ligand reveals a novel mode of estrogen receptor antagonism. Nat Struct Biol 9 5 (2002)
56. Stoica A., Saceda Ma A., Solomon H.B., Fenster B.D., and Martin M.B. Regulation of estrogen receptor-alpha gene expression by 1,25-dihydroxyvitamin D in MCF-7 cells. J Cell Biochem 75 (1999) 640-651
57. Kuiper G.G.J.M., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and B. Endocrinology 138 3 (1997) 863-870
58. Kuiper G.G.J.M., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139 10 (1998) 4252-4263
59. Harris H.A., Bapat A.R., Gonder D.S., and Frail D.E. The ligand binding profiles of estrogen receptors alpha and beta are species dependent. Steroids 67 (2002) 379-384
60. Harris H.A., Katzenellenbogen J.A., and Katzenellenbogen B.S. Characterization of the biological roles of the estrogen receptors, ERalpha and ERbeta, in estrogen target tissues in vivo through the use of an ERalpha-selective ligand. Endocrinology 143 (2002) 4172-4177
61. Montano M.M., Muller V., Trobaugh A., and Katzenellenbogen B.S. The carboxy-terminal F domain of the human estrogen receptor: role in the transcriptional activity of the receptor and the effectiveness of antiestrogens as estrogen antagonists. Mol Endocrinol 9 (1995) 814-825
62. Koide A., Zhao C., Naganuma M., Abrams J., Deighton-Collins S., Skafar D.F., et al. Identification of Regions within the F domain of the human estrogen receptor {alpha} that are important for modulating transactivation and protein-protein interactions. Mol Endocrinol 21 (2007) 829-842
63. Gougeleta A., Mueller S.O., Korach K.S., and Renoir J.M. Oestrogen receptors pathways to oestrogen responsive elements: The transactivation function-1 acts as the keystone of oestrogen receptor (ER)alpha-mediated transcriptional repression of ERalpha. J Steroid Biochem Mol Biol 104 3-5 (2007) 110-122
64. Ignar-Trowbridge D.M., Nelson K.G., Bidwell M.C., Curtis S.W., Washburn T.F., McLachlan J.A., et al. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci USA 89 (1992) 4658-4662
65. Coleman K.M., and Smith C.L. Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. Front Biosci 6 (2001) D1379-D1391
66. Klotz D.M., Hewitt S.C., Ciana P., Raviscioni M., Lindzey J.K., Foley J., et al. Requirement of estrogen receptor-alpha in insulin-like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor cross-talk. J Biol Chem 277 (2002) 8531-8537
67. Klotz D.M., Hewitt S.C., Korach K.S., and Diaugustine R.P. Activation of a uterine insulin-like growth factor I signaling pathway by clinical and environmental estrogens: requirement of estrogen receptor-alpha. Endocrinology 141 (2000) 3430-3439
68. Safe S., and Kim K. Nuclear receptor-mediated transactivation through interaction with Sp proteins. Prog Nucleic Acid Res Mol Biol 77 (2004) 1-36
69. Kushner P.J., Agard D.A., Greene G.L., Scanlan T.S., Shiau A.K., Uht R.M., et al. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 74 (2000) 311-317
70. Schulze H., and Claus S. Histological localization of estrogen receptors in normal and diseased human prostates by immunocytochemistry. Prostate 16 (1990) 331-343
71. Schulze H., and Barrack E. Immunocytochemical localization of estrogen receptors in the normal male and female canine urinary tract and prostate. Endocrinology 121 5 (1987) 1773-1783
72. Brenner R.M., West N., and McClellena M. Estrogen and progestin receptors in the reproductive tract of male and female primates. Biol Reprod 42 (1990) 11-19
73. Prins G.S., and Birch L. Neonatal estrogen exposure up-regulates estrogen receptor expression in the developing and adult rat prostate lobes. Endocrinology 138 5 (1997) 1801-1809
74. Tsurusaki T., Aoki D., Kanetake H., Inoue S., Muramatsu M., Hishikawa Y., et al. Zone-dependent expression of estrogen receptors alpha and beta in human benign prostatic hyperplasia. J Clin Endocr Metab 88 (2003) 1333-1340
75. Tilley W.D., Horsfall D.J., Skinner J.M., Henderson D.W., and Marshall V.R. Effect of pubertal development on estrogen receptor levels and stromal morphology in the guinea pig prostate. Prostate 15 (1989) 195-210
76. Adams J.Y., Leav I., Lau K.M., Ho S.M., and Pflueger S.M. Expression of estrogen receptor beta in the fetal, neonatal, and prepubertal human prostate. Prostate 52 1 (2002) 69-81
77. Kruithof-Dekker I.G., Tetu B., Janssen P.J., and Van der Kwast T.H. Elevated estrogen receptor expression in human prostatic stromal cells by androgen ablation therapy. J Urol 156 (1996) 1194-1197
78. Tilley W., HJorsfall D., McGee M., Alderman J., and Marshall V. Effects of ageing and hormonal manipulations on the level of oestrogen receptors in the guinea-pig prostate. J Endocr 112 (1987) 139-144
79. Shapiro E., Huang H., Masch R.J., McFadden D.E., Wilson E.L., and Wu X.R. Immunolocalization of estrogen receptor alpha and beta in human fetal prostate. J Urol 174 5 (2005) 2051-2053
80. Kozak I., Bartsch W., Krieg M., and Voight K. Nuclei of stroma: site of highest estrogen concentration in human benign prostatic hyperplasia. Prostate 3 (1982) 433-438
81. Risbridger G.P., Wang H., Young P., Takeshi K., Wong Y.Z., Lubahn D., et al. Evidence that epithelial and mesenchymal estrogen receptor-α mediates effects of estrogen on prostatic epithelium. Develop Biol 229 (2001) 432-444
82. Prins G.S., Birch L., Couse J.F., Choi I., Katzenellenbogen B., and Korach K.S. Estrogen imprinting of the developing prostate gland in mediated through stromal estrogen receptor α: studies with αERKO and βERKO mice. Cancer Res 61 (2001) 6089-6097
83. Eddy E.M., Washburn T.F., Bunch D.O., Goulding E.H., Gladen B.C., Lubahn D.B., et al. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137 11 (1996) 4796-4805
84. Donaldson K.M., Tong S.Y., Washburn T., Lubahn D.B., Eddy E.M., Hutson J.M., et al. Morphometric study of the gubernaculum in male estrogen receptor mutant mice. J Androl 17 2 (1996) 91-95
85. Li L., Chui R., Nakajima K., Oh B.R., Au H.C., and Dahiya R. Frequent methylation of estrogen receptor in prostate cancer: correlation with tumor progression. Cancer Res 60 (2000) 702-706
86. Lau K.M., LaSpina M., Long J., and Ho S.M. Expression of estrogen receptor (ER)-α and ER-β in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Res 60 (2000) 3175-3182
87. Bonkhoff H., Fixemer T., Hunsicker I., and Remberger K. Estrogen receptor in prostate cancer and premalignant lesions. Am J Pathol 155 2 (1999) 641-647
88. Leav I., Lau K.M., Adams J., NcNeal J., Taplin M., Wang J., et al. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate gland, dysplasia, and in primary and metastatic carcinoma. Am J Pathol 1 (2001) 79-92
89. Hernandez J., Balic I., Johnson-Pais T.L., Higgins B.A., Torkko K.C., Thompson I., et al. Association between estrogen receptor alpha gene polymorphism and risk of prostate cancer in black men. J Urol 175 (2006) 523-527
90. Tanaka Y., Sasaki M., Kaneuchi M., Shiina H., Igawa M., and Dahiya R. Polymorphisms of estrogen receptor alpha in prostate cancer. Mol Carcinogen 37 (2003) 202-208
91. Enmark E., Pelto-Huikko M., Grandien K., Lagercrantz S., Lagercrantz J., Fried G., et al. Human estrogen receptor β-gene structure, chromosomal localization, and expression pattern. JCEM 82 12 (1997) 42584265
92. Prins G.S., Marmer M., Woodham C., Chang W.Y., Kuiper G., Gustafsson J.A., et al. Estrogen receptor-β messenger ribonucleic acid ontogeny in the prostate of normal and neonatally estrogenized rats. Endocrinology 139 3 (1998) 874-883
93. Makela S., Strauss L., Kuiper G., Valve E.M., Salmi S., Santti R., et al. Differential expression of estrogen receptors alpha and beta in adult rat accessory sex glands and lower urinary tract. Mol Cell Endocrinol 164 (2000) 109-116
94. Chang W., and Prins G. Estrogen receptor-β: implications for the prostate gland. Prostate 40 (1999) 115-124
95. Asano K., Maruyama S., Usui T., and Fujimoto N. Regulation of estrogen receptor alpha and beta expression by testosterone in the rat prostate gland. Endocr J 50 3 (2003) 281-287
96. Fixemer T., Remberger K., and Bonkoff H. Differential expression of estrogen receptor beta in human prostate tissue, premalignant changes and in primary, metastatic and recurrent prostatic adenocarcinoma. Prostate 54 (2003) 79-87
97. Fujimura T., Takahashi S., Urano T., Ogawa S., Ouchi Y., Kitamura T., et al. Differential expression of estrogen receptor beta (ERbeta) and its C-terminal truncated splice variant ERbetacx as prognostic predictors in human prostatic cancer. Biochem Biophys Res Commun 289 3 (2001) 692-699
98. Hanstein B., Liu H., Yancisin M., and Brown M. Functional analysis of a novel estrogen receptor beta isoform. Mol Endocrinol 13 (1999) 129-137
99. Maruyama K., Endoh H., Sasaki-Iwaoka H., Kanou H., Shimaya E., Hashimoto S., et al. A novel isoform of rat estrogen receptor beta with 18 amino acid insertion in the ligand binding domain as a putative dominant negative regular of estrogen action. Biochem Biophys Res Commun 246 (1998) 142-147
100. Petersen D., Tkalcevic G., Koza-Taylor P., Turi T., and Brown T. Identification of estrogen receptor beta 2: a functional variant of estrogen receptor beta expressed in normal rat tissues. Endocrinology 139 (1998) 1082-1092
101. Imamov O., Morani A., Shim G.J., Omoto Y., Thulin-Andersson C., Warner M., et al. Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc Natl Acad Sci USA 101 (2004) 9375-9380
102. Weihua Z., Makela S., Andersson L.C., Salmi S., Saji S., Webster J.I., et al. A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA 98 11 (2001) 6330-6335
103. Weihua Z., Warner M., and Gustaffson J. Estrogen receptor beta in the prostate. Mol Cell Biol 193 (2002) 1-5
104. Couse J.F., Curtis-Hewitt S., and Korach K.S. Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J Steroid Biochem Mol Biol 74 5 (2000) 287-296
105. Dupont S., Krust A., Gansmuller A., Dierich A., Chambon P., and Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127 19 (2000) 4277-4291
106. McPherson S.J., Ellem S.J., Simpson E.R., Patchev V., Fritzemeier K.H., and Risbridger G.P. Essential role for estrogen receptor beta in stromal-epithelial regulation of prostatic hyperplasia. Endocrinology 148 2 (2007) 566-574
107. McMurray R.W. Estrogen, prolactin, and autoimmunity: actions and interactions. Int Immunopharm 1 (2001) 995-1008
108. Yellayi S., Teuscher C., Woods J.A., Welsh Jr. T.H., Tung K.S., Nakai M., et al. Normal development of thymus in male and female mice requires estrogen/estrogen receptor-alpha signaling pathway. Endocrine 12 3 (2000) 207-213
109. Harris H.A., Albert L.M., Leathurby Y., Malamas M.S., Mewshaw R.E., Miller C.P., et al. Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 144 10 (2003) 4241-4249
110. DeMarzo A.M., Marchi V.L., Epstein J.I., and Nelson W.G. Proliferative inflammatory atrophy of the prostate implications for prostatic carcinogenesis. Am J Pathol 155 6 (1999) 1985-1992
111. Montano M., Jaiswal A., and Katzenellenbogen B. Transcriptional regulation of the human quinone reductase gene by antiestrogen-liganded estrogen receptor-α and estrogen receptor-β. Fertil Steril 273 (1998) 25443-25449
112. Nelson W.G., DeWeese T.L., and DeMarzo A.M. The diet, prostate inflammation, and the development of prostate cancer. Cancer Metast Rev 21 1 (2002) 3-16
113. Pasquali D., Rossi V., Esposito D., Abbondanza C., Puca G.A., Bellastella A., et al. Loss of estrogen receptor beta expression in malignant human prostate cells in primary cultures and in prostate cancer tissues. J Clin Endocr Metab 86 (2001) 2051-2055
114. Horvath L.G., Henshall S.M., Lee C.S., Head D.R., Quinn D.I., Makela S., et al. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res 61 (2001) 5331-5335
115. Zhu X., Leav I., Leung Y., Wu M., Liu Q., Gao Y., et al. Dynamic regulation of estrogen receptor-beta expression by DNA methylation during prostate cancer development and metastasis. Am J Pathol 164 6 (2004) 1883-1886
116. Zhang X., Leung Y.K., and Ho S.M. AP-2 regulates the transcription of estrogen receptor (ER)-beta by acting through a methylation hotspot of the 0N promoter in prostate cancer cells. Oncogene 26 (2007) 7246-7254
117. Cheng J., Lee E.J., Madison L.D., and Lazennec G. Expression of estrogen receptor beta in prostate carcinoma cells inhibits invasion and proliferation and triggers apoptosis. FEBS Lett 566 (2004) 169-172
118. Lai J.S., Brown L.G., True L.D., Hawley S.J., Etzioni R.B., Higano C.S., et al. Metastases of prostate cancer express estrogen receptor-beta. Urology 64 (2004) 814-820
119. Wilson J. The pathogenesis of benign prostatic hyperplasia. Am J Med 68 (1980) 745-756
120. Guerini V., Sau D., Scaccianoce E., Rusmini P., Ciana P., Maggi A., 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 65 12 (2005) 5445-5453
121. Garcia G.E., Wisniewski H.G., Lucia M.S., Arevalo N., Slaga T.J., Kraft S.L., et al. 2-Methoxyestradiol inhibits prostate tumor development in transgenic adenocarcinoma of mouse prostate: role of tumor necrosis factor-alpha-stimulated gene 6. Clin Cancer Res 12 (2006) 980-988
122. Schulz P., Bauer H.W., Brade W.P., Keller A., and Fittler F. Evaluation of the cytotoxic activity of diethylstilbestrol and its mono- and diphosphate towards prostatic carcinoma cells. Cancer Res 48 (1988) 2867-2870
123. Kim I.Y., Kim B.C., Seong, Lee D.K., Seo J.M., Hong Y.J., et al. Raloxifene, a mixed estrogen agonist/antagonist, induces apoptosis in androgen-independent human prostate cancer cell lines. Cancer Res 62 (2002) 5365-5369
124. Neubauer B.L., McNulty A.M., Chedid M., Chen K., Goode R.L., Johnson M.A., et al. The selective estrogen receptor modulator trioxifene (LY133314) inhibits metastasis and extends survival in the PAIII rat prostatic carcinoma model. Cancer Res 63 (2003) 6056-6062
125. Corey E., Quinn J.E., Emond M.J., Buhler K.R., Brown L.G., and Vessella R.L. Inhibition of androgen-independent growth of prostate cancer xenografts by 17beta-estradiol. Clin Cancer Res 8 4 (2002) 1003-1007
126. Raghow S., Hooshdraran M.Z., Katiyar S., and Steiner M.S. Toremifene prevents prostate cancer in the transgenic adenocarcinoma of mouse prostate model. Cancer Res 62 (2002) 1370-1376
127. Bergan R.C., Reed E., Myers C.E., Headlee D., Brawley O., Cho H.K., et al. A Phase II study of high-dose tamoxifen in patients with hormone-refractory prostate cancer. Clin Cancer Res 5 9 (1999) 2366-2373
128. Stein S., Zoltick B., Peacock T., Holroyde C., Haller D., Armstead B., et al. Phase II trial of toremifene in androgen-independent prostate cancer: a Penn cancer clinical trials group trial. Am J Clin Oncol 24 3 (2001) 283-285
129. Steiner M.S., and Pound C.R. Phase IIA clinical trials to test the efficacy and safety of Toremifene in men with high-grade prostatic intraepithelial neoplasia. Clin Prostate Cancer 2 1 (2003) 32-33
130. Ellem S.J., and Risbridger G.P. Aromatase and prostate cancer. Minerva Endocrinol 31 (2006) 1-12
131. Narashimamurthy J., Rao A.R., and Sastry G.N. Aromatase inhibitors: a new paradigm in breast cancer treatment. Curr Med Chem Anticancer Agents 4 6 (2004) 523-534
132. Ellem S.J., Schmitt J.F., Pedersen J.S., Frydenberg M., and Risbridger G.P. Local aromatase expression in human prostate is altered in malignancy. J Clin Endocrinol Metab 89 5 (2004) 2431-2441
133. Smith M.R., Kaufman D., George D., Oh W.K., Kazanis M., Manola J., et al. Selective aromatase inhibition for patients with androgen-independent prostate carcinoma. Cancer 95 9 (2002) 1864-1868
134. Santen R.J., Petroni G.R., Fisch M.J., Myers C.E., Theodorescu D., and Cohen R.B. Use of the aromatase inhibitor anastrozole in the treatment of patients with advanced prostate carcinoma. Cancer 92 8 (2001) 2095-2101
135. Wang J., Eltoum I.E., and Lamartiniere C.A. Dietary genistein suppresses chemically induced prostate cancer in Lobund-Wistar rats. Cancer Lett 186 11-18 (2002)
136. Mentor-Marcel R., Lamartiniere C.A., Eltoum A., Greenberg N.M., and Elgavish A. Dietary genistein improves survival and reduces expression of osteopontin in the prostate of transgenic mice with prostatic adenocarcinoma (TRAMP). J Nutr 135 5 (2005) 989-995
137. Jones S.B., DePrimo S.E., Whitfield M.L., and Brooks J.D. Resveratrol-induced gene expression profiles in human prostate cancer cells. Cancer Epidemiol Biomarkers Prev 14 (2005) 596-604
138. Lee M.M., Gomez S.L., Chang J.S., Wey M., Wang R.T., and Hsing A.W. Soy and isoflavone consumption in relation to prostate cancer risk in China. Cancer Epidemiol Biomarkers Prev 12 (2003) 665-668
139. Ozasa K., Nakao M., Watanabe Y., Hayashi K., Miki T., Mikami K., et al. Serum phytoestrogens and prostate cancer risk in a nested case-control study among Japanese men. Cancer Sci 95 1 (2004) 65-71
140. Manson M.M., Farmer P.B., Gescher A., and Steward W.P. Innovative agents in cancer prevention. Rec Results Cancer Res 166 (2005) 257-275
141. Mak P., Leung Y.K., Tang W.Y., Harwood C., and Ho S.M. Apigenin suppresses cancer cell growth through ERbeta. Neoplasia 8 11 (2006) 896-904