Estrogen receptors and human disease: An update

Archives of Toxicology

Volumn 86, Issue 10, 2012, Pages 1491-1504

  Burns, Katherine A ^a   Korach, Kenneth S ^a  

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

Author keywords

Cancer; Endometriosis; Estrogen; Estrogen receptors; Fibroids; Human disease; Ovary

Indexed keywords

ANDROGEN; AROMATASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GESTAGEN; GONADORELIN AGONIST; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; MICRORNA; MICRORNA 22; MICRORNA 221; MICRORNA 222; ORAL CONTRACEPTIVE AGENT; PROGESTERONE RECEPTOR; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SOMATOMEDIN C; TAMOXIFEN; TRANSCRIPTION FACTOR PBX1;

BREAST CANCER; CANCER HORMONE THERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER RISK; CARDIOVASCULAR DISEASE; CAUSE SPECIFIC SURVIVAL; COLON CANCER; DISEASE FREE SURVIVAL; DNA METHYLATION; ENDOMETRIOSIS; ENDOMETRIUM CANCER; ESTROGEN RECEPTOR BETA GENE; ESTROGEN RESPONSIVE ELEMENT; GENE; GENETIC PREDISPOSITION; HEART PROTECTION; HUMAN; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; POSTMENOPAUSE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; RECURRENCE FREE SURVIVAL; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; UTERUS MYOMA;

ANIMALS; CARDIOVASCULAR DISEASES; DISEASE PROGRESSION; ENDOMETRIOSIS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; HUMANS; LEIOMYOMA; NEOPLASMS;

MAMMALIA;

EID: 84866536282     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-012-0868-5     Document Type: Review

References (183)

1. Al-Ghnaniem R, Peters J et al (2007) Methylation of estrogen receptor alpha and mutL homolog 1 in normal colonic mucosa: Association with folate and vitamin B-12 status in subjects with and without colorectal neoplasia. Am J Clin Nutr 86(4):1064-1072
2. Allgeier SH, Vezina CM et al (2009) Estrogen signaling is not required for prostatic bud patterning or for its disruption by 2,3,7,8- tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 239(1):80-86
3. Al-Nakhle H, Burns PA et al (2010) Estrogen receptor {beta}1 expression is regulated by miR-92 in breast cancer. Cancer Res 70(11):4778-4784
4. Anagnostis A, Papadopoulos AI (2009) Effects of a diet rich in sesame (Sesamum indicum) pericarp on the expression of oestrogen receptor alpha and oestrogen receptor beta in rat prostate and uterus. Br J Nutr 102(5):703-708
5. Asada H, Yamagata Y et al (2008) Potential link between estrogen receptor-alpha gene hypomethylation and uterine fibroid formation. Mol Hum Reprod 14(9):539-545
6. Bakas P, Liapis A et al (2008) Estrogen receptor alpha and beta in uterine fibroids: A basis for altered estrogen responsiveness. Fertil Steril 90(5):1878-1885
7. Barone I, Iacopetta D et al (2010a) Phosphorylation of the mutant K303R estrogen receptor alpha at serine 305 affects aromatase inhibitor sensitivity. Oncogene 29(16):2404-2414
8. Barone M, Scavo MP et al (2010b) ERbeta expression in normal, adenomatous and carcinomatous tissues of patients with familial adenomatous polyposis. Scand J Gastroenterol 45(11):1320-1328
9. Bernardo GM, Lozada KL et al (2010) FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development 137(12):2045-2054
10. Bhat-Nakshatri P, Wang G et al (2009) Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res 37(14):4850-4861
11. Bianco B, Christofolini DM et al (2009) 1730 G/A polymorphism of the estrogen receptor beta gene (ERbeta) may be an important genetic factor predisposing to endometriosis. Acta Obstet Gynecol Scand 88(12):1397-1401
12. Bischoff F, Simpson JL (2004) Genetic basis of endometriosis. Ann N Y Acad Sci 1034:284-299
13. Bolego C, Rossoni G et al (2010) Selective estrogen receptor-alpha agonist provides widespread heart and vascular protection with enhanced endothelial progenitor cell mobilization in the absence of uterotrophic action. FASEB J 24(7):2262-2272
14. Borgquist S, Holm C et al (2008) Oestrogen receptors alpha and beta show different associations to clinicopathological parameters and their co-expression might predict a better response to endocrine treatment in breast cancer. J Clin Pathol 61(2):197-203
15. Brandenberger AW, Tee MK et al (1998) Estrogen receptor alpha (ER-alpha) and beta (ER-beta) mRNAs in normal ovary, ovarian serous cystadenocarcinoma and ovarian cancer cell lines: Downregulation of ER-beta in neoplastic tissues. J Clin Endocrinol Metab 83(3):1025-1028
16. Brodowska A, LaszczynskaMet al (2007) The localization of estrogen receptor alpha and its function in the ovaries of postmenopausal women. Folia Histochem Cytobiol 45(4):325-330
17. Bukulmez O, Hardy DB et al (2008) Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 149(3):1190-1204
18. Bulun SE, Imir G et al (2005) Aromatase in endometriosis and uterine leiomyomata. J Steroid Biochem Mol Biol 95(1-5):57-62
19. Burges A, Bruning A et al (2010) Prognostic significance of estrogen receptor alpha and beta expression in human serous carcinomas of the ovary. Arch Gynecol Obstet 281(3):511-517
20. Burns KA, Li Y et al (2011) Selective mutations in estrogen receptor alpha D-domain alters nuclear translocation and non-estrogen response element gene regulatory mechanisms. J Biol Chem 286 (14):12640-12649
21. Capellino S, Montagna P et al (2006) Role of estrogens in inflammatory response: Expression of estrogen receptors in peritoneal fluid macrophages from endometriosis. Ann N Y Acad Sci 1069:263-267
22. Castellano L, Giamas G et al (2009) The estrogen receptor-alphainduced microRNA signature regulates itself and its transcriptional response. Proc Natl Acad Sci USA 106(37):15732-15737
23. Castiglione F, Taddei A et al (2008) Expression of estrogen receptor beta in colon cancer progression. Diagn Mol Pathol 17(4):231-236
24. Cavallini A, Resta L et al (2011) Involvement of estrogen receptorrelated receptors in human ovarian endometriosis. Fertil Steril 96(1):102-106
25. Chae YK, Huang HY et al (2009) Genetic polymorphisms of estrogen receptors alpha and beta and the risk of developing prostate cancer. PLoS ONE 4(8):e6523
26. Chakravarty D, Srinivasan R et al (2008) Estrogen receptor beta (ERbeta) in endometrial simple hyperplasia and endometrioid carcinoma. Appl Immunohistochem Mol Morphol 16(6):535-542
27. Chan KK, Wei N et al (2008) Estrogen receptor subtypes in ovarian cancer: A clinical correlation. Obstet Gynecol 111(1):144-151
28. Charn TH, Liu ET et al (2010) Genome-wide dynamics of chromatin binding of estrogen receptors alpha and beta: Mutual restriction and competitive site selection. Mol Endocrinol 24(1):47-59
29. Chen JQ, Russo PA et al (2007a) ERbeta shifts from mitochondria to nucleus during estrogen-induced neoplastic transformation of human breast epithelial cells and is involved in estrogen-induced synthesis of mitochondrial respiratory chain proteins. Biochim Biophys Acta 1773(12):1732-1746
30. Chen YC, Kraft P et al (2007b) Sequence variants of estrogen receptor beta and risk of prostate cancer in the National Cancer Institute Breast and Prostate Cancer Cohort Consortium. Cancer Epidemiol Biomarkers Prev 16(10):1973-1981
31. Chen Y, Jin X et al (2009) Estrogen-replacement therapy promotes angiogenesis after acute myocardial infarction by enhancing SDF-1 and estrogen receptor expression. Microvasc Res 77(2):71-77
32. Chlebowski RT, Kuller LH et al (2009) Breast cancer after use of estrogen plus progestin in postmenopausal women. N Engl J Med 360(6):573-587
33. Choi JH, Lee KT et al (2011) Estrogen receptor alpha pathway is involved in leptin-induced ovarian cancer cell growth. Carcinogenesis 32(4):589-596
34. Chong K, Subramanian A et al (2011) Measuring IGF-1, ER-alpha and EGFR expression can predict tamoxifen-resistance in ERpositive breast cancer. Anticancer Res 31(1):23-32
35. Cleveland AG, Oikarinen SI et al (2009) Disruption of estrogen receptor signaling enhances intestinal neoplasia in Apc(Min/?) mice. Carcinogenesis 30(9):1581-1590
36. Collins F, MacPherson S et al (2009) Expression of oestrogen receptors, ERalpha, ERbeta, and ERbeta variants, in endometrial cancers and evidence that prostaglandin F may play a role in regulating expression of ERalpha. BMC Cancer 9:330
37. Cox DG, Bretsky P et al (2008) Haplotypes of the estrogen receptor beta gene and breast cancer risk. Int J Cancer 122(2):387-392
38. Cummings M, Iremonger J et al (2009) Gene expression of ERbeta isoforms in laser microdissected human breast cancers: Implications for gene expression analyses. Cell Oncol 31(6):467-473
39. Dannenmann C, Shabani N et al (2008) The metastasis-associated gene MTA1 is upregulated in advanced ovarian cancer, represses ERbeta, and enhances expression of oncogenic cytokine GRO. Cancer Biol Ther 7(9):1460-1467
40. De Stefano I, Zannoni GF et al (2011) Cytoplasmic expression of estrogen receptor beta (ERbeta) predicts poor clinical outcome in advanced serous ovarian cancer. Gynecol Oncol 122(3):573-579
41. Deroo BJ, Korach KS (2006) Estrogen receptors and human disease. J Clin Invest 116(3):561-570
42. Di Leo A, Barone M et al (2008) ER-beta expression in large bowel adenomas: Implications in colon carcinogenesis. Dig Liver Dis 40(4):260-266
43. Di Leva G, Gasparini P et al (2010) MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 102(10):706-721
44. Doherty JA, Rossing MA et al (2010) ESR1/SYNE1 polymorphism and invasive epithelial ovarian cancer risk: An Ovarian Cancer Association Consortium study. Cancer Epidemiol Biomarkers Prev 19(1):245-250
45. Dunning AM, Healey CS et al (2009) Association of ESR1 gene tagging SNPs with breast cancer risk. Hum Mol Genet 18(6): 1131-1139
46. Einarsdottir K, Darabi H et al (2009) Common genetic variability in ESR1 and EGF in relation to endometrial cancer risk and survival. Br J Cancer 100(8):1358-1364
47. Ellem SJ, Risbridger GP (2007) Treating prostate cancer: A rationale for targeting local oestrogens. Nat Rev Cancer 7(8):621-627
48. Endo Y, Toyama T et al (2011) High estrogen receptor expression and low Ki67 expression are associated with improved time to progression during first-line endocrine therapy with aromatase inhibitors in breast cancer. Int J Clin Oncol 16(5):512-518
49. Fang YJ, Lu ZH et al (2010) Prognostic impact of ERbeta and MMP7 expression on overall survival in colon cancer. Tumour Biol 31(6):651-658
50. Farquhar CM, Marjoribanks J et al (2005) Long term hormone therapy for perimenopausal and postmenopausal women Cochrane Database Syst Rev (3):CD004143
51. Favre J, Gao J et al (2010) Endothelial estrogen receptor {alpha} plays an essential role in the coronary and myocardial protective effects of estradiol in ischemia/reperfusion. Arterioscler Thromb Vasc Biol 30(12):2562-2567
52. Fullwood MJ, Liu MH et al (2009) An oestrogen-receptor-alphabound human chromatin interactome. Nature 462(7269):58-64
53. Galle PC (1989) Clinical presentation and diagnosis of endometriosis. Obstet Gynecol Clin North Am 16(1):29-42
54. Generali D, Buffa FM et al (2009) Phosphorylated ERalpha, HIF-1alpha, and MAPK signaling as predictors of primary endocrine treatment response and resistance in patients with breast cancer. J Clin Oncol 27(2):227-234
55. Giroux V, Bernatchez G et al (2011) Chemopreventive effect of ERbeta-Selective agonist on intestinal tumorigenesis in Apc (Min/?) mice. Mol Carcinog 50(5):359-369
56. Giudice LC, Kao LC (2004) Endometriosis. Lancet 364(9447):1789-1799
57. Govindan S, Shaik NA et al (2009) Estrogen receptor-alpha gene (T/C) Pvu II polymorphism in endometriosis and uterine fibroids. Dis Markers 26(4):149-154
58. Grivas PD, Tzelepi V et al (2009) Expression of ERalpha, ERbeta and co-regulator PELP1/MNAR in colorectal cancer: Prognostic significance and clinicopathologic correlations. Cell Oncol 31(3): 235-247
59. Grober OM, Mutarelli M et al (2011) Global analysis of estrogen receptor beta binding to breast cancer cell genome reveals an extensive interplay with estrogen receptor alpha for target gene regulation. BMC Genomics 12:36
60. Gruvberger-Saal SK, Bendahl PO et al (2007) Estrogen receptor beta expression is associated with tamoxifen response in ERalphanegative breast carcinoma. Clin Cancer Res 13(7):1987-1994
61. Halon A, Nowak-Markwitz E et al (2011) Loss of estrogen receptor beta expression correlates with shorter overall survival and lack of clinical response to chemotherapy in ovarian cancer patients. Anticancer Res 31(2):711-718
62. Hamada H, Kim MK et al (2006) Estrogen receptors alpha and beta mediate contribution of bone marrow-derived endothelial progenitor cells to functional recovery after myocardial infarction. Circulation 114(21):2261-2270
63. Hamilton-Burke W, Coleman L et al (2010) Phosphorylation of estrogen receptor beta at serine 105 is associated with good prognosis in breast cancer. Am J Pathol 177(3):1079-1086
64. Hecht JL, Kotsopoulos J et al (2009) Relationship between epidemiologic risk factors and hormone receptor expression in ovarian cancer: Results from the nurses' health study. Cancer Epidemiol Biomarkers Prev 18(5):1624-1630
65. Hermon TL, Moore AB et al (2008) Estrogen receptor alpha (ERalpha) phospho-serine-118 is highly expressed in human uterine leiomyomas compared to matched myometrium. Virchows Arch 453(6):557-569
66. Hewitt SC, O'Brien JE et al (2009) Selective disruption of ER{alpha} DNA-binding activity alters uterine responsiveness to estradiol. Mol Endocrinol 23(12):2111-2116
67. Hewitt SC, Li L, et al (2012) Research resource: Whole-genome estrogen receptor alpha binding in mouse uterine tissue revealed by ChIP-Seq. Mol Endocrinol 26(5):887-898
68. Hiraoka S, Kato J et al (2010) Methylation status of normal background mucosa is correlated with occurrence and development of neoplasia in the distal colon. Hum Pathol 41(1):38-47
69. Hodges-Gallagher L, Valentine CD et al (2008) Estrogen receptor beta increases the efficacy of antiestrogens by effects on apoptosis and cell cycling in breast cancer cells. Breast Cancer Res Treat 109(2):241-250
70. Holm C, Kok M et al (2009) Phosphorylation of the oestrogen receptor alpha at serine 305 and prediction of tamoxifen resistance in breast cancer. J Pathol 217(3):372-379
71. Honma N, Horii R et al (2008) Clinical importance of estrogen receptor-beta evaluation in breast cancer patients treated with adjuvant tamoxifen therapy. J Clin Oncol 26(22):3727-3734
72. Hsieh YY, Wang YK et al (2007) Estrogen receptor alpha-351 XbaI*G and-397 PvuII*C-related genotypes and alleles are associated with higher susceptibilities of endometriosis and leiomyoma. Mol Hum Reprod 13(2):117-122
73. Huang GS, Arend RC et al (2009) Tissue microarray analysis of hormonal signaling pathways in uterine carcinosarcoma. Am J Obstet Gynecol 200(4):457.e451-457.e455
74. Huang GS, Gunter MJ et al (2010) Co-expression of GPR30 and ERbeta and their association with disease progression in uterine carcinosarcoma. Am J Obstet Gynecol 203(3):242.e241-242.e245
75. Hurtado A, Holmes KA et al (2011) FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43(1):27-33
76. Ishikawa H, Ishi K et al (2010) Progesterone is essential for maintenance and growth of uterine leiomyoma. Endocrinology 151(6):2433-2442
77. Issa RM, Lebeau A et al (2009) Estrogen receptor gene amplification occurs rarely in ovarian cancer. Mod Pathol 22(2):191-196
78. Jackson KS, Brudney A et al (2007) The altered distribution of the steroid hormone receptors and the chaperone immunophilin FKBP52 in a baboon model of endometriosis is associated with progesterone resistance during the window of uterine receptivity. Reprod Sci 14(2):137-150
79. Jazbutyte V, Arias-Loza PA et al (2008) Ligand-dependent activation of ER{beta} lowers blood pressure and attenuates cardiac hypertrophy in ovariectomized spontaneously hypertensive rats. Cardiovasc Res 77(4):774-781
80. Jesmin S, Mowa CN et al (2010) VEGF signaling is disrupted in the hearts of mice lacking estrogen receptor alpha. Eur J Pharmacol 641(2-3):168-178
81. Jiang H, Teng R et al (2008) Transcriptional analysis of estrogen receptor alpha variant mRNAs in colorectal cancers and their matched normal colorectal tissues. J Steroid Biochem Mol Biol 112(1-3):20-24
82. Jongen V, Briet J et al (2009) Expression of estrogen receptor-alpha and-beta and progesterone receptor-A and-B in a large cohort of patients with endometrioid endometrial cancer. Gynecol Oncol 112(3):537-542
83. Juhasz-Boss I, Fischer C et al (2011) Endometrial expression of estrogen receptor beta and its splice variants in patients with and without endometriosis. Arch Gynecol Obstet 284(4):885-891
84. Karita M, Yamashita Y et al (2011) Does advanced-stage endometriosis affect the gene expression of estrogen and progesterone receptors in granulosa cells? Fertil Steril 95(3):889-894
85. Kim C, Tang G et al (2011) Estrogen receptor (ESR1) mRNA expression and benefit from tamoxifen in the treatment and prevention of estrogen receptor-positive breast cancer. J Clin Oncol 29(31):4160-4167
86. Kjaergaard AD, Ellervik C et al (2007) Estrogen receptor alpha polymorphism and risk of cardiovascular disease, cancer, and hip fracture: Cross-sectional, cohort, and case-control studies and a meta-analysis. Circulation 115(7):861-871
87. Kok M, Zwart W et al (2011) PKA-induced phosphorylation of ERalpha at serine 305 and high PAK1 levels is associated with sensitivity to tamoxifen in ER-positive breast cancer. Breast Cancer Res Treat 125(1):1-12
88. Kulak J Jr, Fischer C et al (2011) Treatment with bazedoxifene, a selective estrogen receptor modulator, causes regression of endometriosis in a mouse model. Endocrinology 152(8):3226-3232
89. Lagiou P, Georgila C et al (2009) Estrogen alpha and progesterone receptor expression in the normal mammary epithelium in relation to breast cancer risk. Int J Cancer 124(2):440-442
90. Lamp M, Peters M et al (2011) Polymorphisms in ESR1, ESR2 and HSD17B1 genes are associated with fertility status in endometriosis. Gynecol Endocrinol 27(6):425-433
91. Leav I, Lau KM et al (2001) 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 159(1):79-92
92. Lebeau A, Grob T et al (2008) Oestrogen receptor gene (ESR1) amplification is frequent in endometrial carcinoma and its precursor lesions. J Pathol 216(2):151-157
93. Lee GH, Kim SH et al (2007) Estrogen receptor beta gene ?1730 G/A polymorphism in women with endometriosis. Fertil Steril 88(4): 785-788
94. Leibetseder V, Humpeler S et al (2010) Time dependence of estrogen receptor expression in human hearts. Biomed Pharmacother 64(3):154-159
95. Leigh Pearce C, Near AM et al (2008) Comprehensive evaluation of ESR2 variation and ovarian cancer risk. Cancer Epidemiol Biomarkers Prev 17(2):393-396
96. Li N, Dong J et al (2010a) Potentially functional polymorphisms in ESR1 and breast cancer risk: A meta-analysis. Breast Cancer Res Treat 121(1):177-184
97. Li S, Han B et al (2010b) Immunocytochemical localization of sex steroid hormone receptors in normal human mammary gland. J Histochem Cytochem 58(6):509-515
98. Lin Fde M, Pincerato KM et al (2012) Coordinated expression of oestrogen and androgen receptors in HER2-positive breast carcinomas: Impact on proliferative activity. J Clin Pathol 65(1): 64-68
99. Lin CY, Strom A et al (2007) Inhibitory effects of estrogen receptor beta on specific hormone-responsive gene expression and association with disease outcome in primary breast cancer. Breast Cancer Res 9(2):R25
100. Lin SL, Yan LY et al (2010) ER-alpha36, a variant of ER-alpha, promotes tamoxifen agonist action in endometrial cancer cells via the MAPK/ERK and PI3K/Akt pathways. PLoS ONE 5(2): E9013
101. Lurie G, Wilkens LR et al (2009) Genetic polymorphisms in the estrogen receptor beta (ESR2) gene and the risk of epithelial ovarian carcinoma. Cancer Causes Control 20(1):47-55
102. Lurie G, Wilkens LR et al (2011) Estrogen receptor beta rs1271572 polymorphism and invasive ovarian carcinoma risk: Pooled analysis within the Ovarian Cancer Association Consortium. PLoS ONE 6(6):e20703
103. Madak-Erdogan Z, Lupien M et al (2011) Genomic collaboration of estrogen receptor alpha and extracellular signal-regulated kinase 2 in regulating gene and proliferation programs. Mol Cell Biol 31(1):226-236
104. Maehle BO, Collett K et al (2009) Estrogen receptor beta-an independent prognostic marker in estrogen receptor alpha and progesterone receptor-positive breast cancer? APMIS 117(9): 644-650
105. Magnani L, Ballantyne EB et al (2011) PBX1 genomic pioneer function drives ERalpha signaling underlying progression in breast cancer. PLoS Genet 7(11):e1002368
106. Mandusic V, Nikolic-Vukosavljevic D et al (2007) Expression of estrogen receptor beta wt isoform (ERbeta1) and ERbetaDelta5 splice variant mRNAs in sporadic breast cancer. J Cancer Res Clin Oncol 133(8):571-579
107. Mangelsdorf DJ, Thummel C et al (1995) The nuclear receptor superfamily: The second decade. Cell 83(6):835-839
108. Manson JE, Allison MA et al (2007) Estrogen therapy and coronaryartery calcification. N Engl J Med 356(25):2591-2602
109. Marotti JD, Collins LC et al (2010) Estrogen receptor-beta expression in invasive breast cancer in relation to molecular phenotype: Results from the nurses' health study. Mod Pathol 23(2):197-204
110. Matthews J, Wihlen B et al (2006) Estrogen receptor (ER) beta modulates ERalpha-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Mol Endocrinol 20(3):534-543
111. McPherson SJ, Hussain S et al (2010) Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen independent and TNFalpha mediated. Proc Natl Acad Sci USA 107(7):3123-3128
112. Mendelsohn ME (2000) Mechanisms of estrogen action in the cardiovascular system. J Steroid Biochem Mol Biol 74(5):337-343
113. Millour J, Constantinidou D et al (2010) FOXM1 is a transcriptional target of ERalpha and has a critical role in breast cancer endocrine sensitivity and resistance. Oncogene 29(20):2983-2995
114. Mintz PJ, Habib NA et al (2008) The phosphorylated membrane estrogen receptor and cytoplasmic signaling and apoptosis proteins in human breast cancer. Cancer 113(6):1489-1495
115. Montagna P, Capellino S et al (2008) Peritoneal fluid macrophages in endometriosis: Correlation between the expression of estrogen receptors and inflammation. Fertil Steril 90(1):156-164
116. Motomura K, Ishitobi M et al (2010) Expression of estrogen receptor beta and phosphorylation of estrogen receptor alpha serine 167 correlate with progression-free survival in patients with metastatic breast cancer treated with aromatase inhibitors. Oncology 79(1-2):55-61
117. Murphy LC, Seekallu SV et al (2011) Clinical significance of estrogen receptor phosphorylation. Endocr Relat Cancer 18(1): R1-R14
118. Nassa G, Tarallo R et al (2011) A large set of estrogen receptor betainteracting proteins identified by tandem affinity purification in hormone-responsive human breast cancer cell nuclei. Proteomics 11(1):159-165
119. Novelli F, Milella M et al (2008) A divergent role for estrogen receptor-beta in node-positive and node-negative breast cancer classified according to molecular subtypes: An observational prospective study. Breast Cancer Res 10(5):R74
120. Nussler NC, Reinbacher K et al (2008) Sex-specific differences in the expression levels of estrogen receptor subtypes in colorectal cancer. Gend Med 5(3):209-217
121. O'Day E, Lal A (2010) MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res 12(2):201
122. Pan X, Zhou T et al (2011) Elevated expression of CUEDC2 protein confers endocrine resistance in breast cancer. Nat Med 17(6): 708-714
123. Pandey DP, Picard D (2009) miR-22 inhibits estrogen signaling by directly targeting the estrogen receptor alpha mRNA. Mol Cell Biol 29(13):3783-3790
124. Papaxoinis K, Patsouris E et al (2007) Insulinlike growth factor I receptor and estrogen receptor beta expressions are inversely correlated in colorectal neoplasms and affected by the insulin resistance syndrome. Hum Pathol 38(7):1037-1046
125. Papaxoinis K, Triantafyllou K et al (2010) Subsite-specific differences of estrogen receptor beta expression in the normal colonic epithelium: Implications for carcinogenesis and colorectal cancer epidemiology. Eur J Gastroenterol Hepatol 22(5):614-619
126. Park SH, Cheung LW et al (2008) Estrogen regulates snail and slug in the down-regulation of E-cadherin and induces metastatic potential of ovarian cancer cells through estrogen receptor alpha. Mol Endocrinol 22(9):2085-2098
127. Peddada SD, Laughlin SK et al (2008) Growth of uterine leiomyomata among premenopausal black and white women. Proc Natl Acad Sci USA 105(50):19887-19892
128. Qui WS, Yue L et al (2009) Co-expression of ER-beta and HER2 associated with poorer prognosis in primary breast cancer. Clin Invest Med 32(3):E250-E260
129. Rao X, Di Leva G et al (2011) MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene 30(9):1082-1097
130. Rawson JM (1991) Prevalence of endometriosis in asymptomatic women. J Reprod Med 36(7):513-515
131. Risbridger GP, Davis ID et al (2010) Breast and prostate cancer: More similar than different. Nat Rev Cancer 10(3):205-212
132. Rosa FE, Caldeira JR et al (2008) Evaluation of estrogen receptor alpha and beta and progesterone receptor expression and correlation with clinicopathologic factors and proliferative marker Ki-67 in breast cancers. Hum Pathol 39(5):720-730
133. Ross-Innes CS, Stark R et al (2012) Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 481(7381):389-393
134. Rossouw JE, Anderson GL et al (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(3):321-333
135. Rossouw JE, Prentice RL et al (2007) Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 297(13):1465-1477
136. Saleiro D, Murillo G et al (2010) Enhanced induction of mucindepleted foci in estrogen receptor {beta} knockout mice. Cancer Prev Res (Phila) 3(9):1198-1204
137. Salonen J, Butzow R et al (2009) Oestrogen receptors and small nuclear ring finger protein 4 (RNF4) in malignant ovarian germ cell tumours. Mol Cell Endocrinol 307(1-2):205-210
138. Sato H, Nogueira-de-Souza NC et al (2008) Intron 1 and exon 1 alpha estrogen receptor gene polymorphisms in women with endometriosis. Fertil Steril 90(6):2086-2090
139. Shaaban AM, Green AR et al (2008) Nuclear and cytoplasmic expression of ERbeta1, ERbeta2, and ERbeta5 identifies distinct prognostic outcome for breast cancer patients. Clin Cancer Res 14(16):5228-5235
140. Shabani N, Kuhn C et al (2007) Prognostic significance of oestrogen receptor alpha (ERalpha) and beta (ERbeta), progesterone receptor A (PR-A) and B (PR-B) in endometrial carcinomas. Eur J Cancer 43(16):2434-2444
141. Sharpe-Timms KL (2001) Endometrial anomalies in women with endometriosis. Ann N Y Acad Sci 943:131-147
142. Shi L, Dong B et al (2009) Expression of ER-{alpha}36, a novel variant of estrogen receptor {alpha}, and resistance to tamoxifen treatment in breast cancer. J Clin Oncol 27(21):3423-3429
143. Siddig A, Mohamed AO et al (2008) Estrogen receptor alpha gene polymorphism and breast cancer. Ann N Y Acad Sci 1138: 95-107
144. Silva RC, Costa IR et al (2011) RsaI polymorphism of the ERbeta gene in women with endometriosis. Genet Mol Res 10(1):465-470
145. Singh M, Zaino RJ et al (2007) Relationship of estrogen and progesterone receptors to clinical outcome in metastatic endometrial carcinoma: A gynecologic oncology group study. Gynecol Oncol 106(2):325-333
146. Skliris GP, Nugent ZJ et al (2010) A phosphorylation code for oestrogen receptor-alpha predicts clinical outcome to endocrine therapy in breast cancer. Endocr Relat Cancer 17(3):589-597
147. Smith L, Coleman LJ et al (2010) Expression of oestrogen receptor beta isoforms is regulated by transcriptional and post-transcriptional mechanisms. Biochem J 429(2):283-290
148. Smuc T, Hevir N et al (2009) Disturbed estrogen and progesterone action in ovarian endometriosis. Mol Cell Endocrinol 301(1-2): 59-64
149. Strissel PL, Swiatek J et al (2007) Transcriptional analysis of steroid hormone receptors in smooth muscle uterine leiomyoma tumors of postmenopausal patients. J Steroid Biochem Mol Biol 107(1-2):42-47
150. Sugiura H, Toyama T et al (2007) Expression of estrogen receptor beta wild-type and its variant ERbetacx/beta2 is correlated with better prognosis in breast cancer. Jpn J Clin Oncol 37(11): 820-828
151. Suzuki F, Akahira J et al (2008) Loss of estrogen receptor beta isoform expression and its correlation with aberrant DNA methylation of the 50-untranslated region in human epithelial ovarian carcinoma. Cancer Sci 99(12):2365-2372
152. Taylor HS, Bagot C et al (1999) HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 14(5):1328-1331
153. Treeck O, Elemenler E et al (2009) Polymorphisms in the promoter region of ESR2 gene and breast cancer susceptibility. J Steroid Biochem Mol Biol 114(3-5):207-211
154. Treeck O, Lattrich C et al (2010) Estrogen receptor beta exerts growth-inhibitory effects on human mammary epithelial cells. Breast Cancer Res Treat 120(3):557-565
155. Trukhacheva E, Lin Z et al (2009) Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J Clin Endocrinol Metab 94(2):615-622
156. Tsezou A, Tzetis M et al (2008) Association of repeat polymorphisms in the estrogen receptors alpha, beta (ESR1, ESR2) and androgen receptor (AR) genes with the occurrence of breast cancer. Breast 17(2):159-166
157. Valladares F, Frias I et al (2006) Characterization of estrogen receptors alpha and beta in uterine leiomyoma cells. Fertil Steril 86(6):1736-1743
158. van de Water W, Markopoulos C et al (2012) Association between age at diagnosis and disease-specific mortality among postmenopausal women with hormone receptor-positive breast cancer. JAMA 307(6):590-597
159. Villanova FE, Andrade PM et al (2006) Estrogen receptor alpha polymorphism and susceptibility to uterine leiomyoma. Steroids 71(11-12):960-965
160. Voloshenyuk TG, Gardner JD (2010) Estrogen improves TIMP-MMP balance and collagen distribution in volume-overloaded hearts of ovariectomized females. Am J Physiol Regul Integr Comp Physiol 299(2):R683-R693
161. Vornehm ND, Wang M et al (2009) Acute postischemic treatment with estrogen receptor-alpha agonist or estrogen receptor-beta agonist improves myocardial recovery. Surgery 146(2):145-154
162. Vouk K, Smuc T et al (2011) Novel estrogen-related genes and potential biomarkers of ovarian endometriosis identified by differential expression analysis. J Steroid Biochem Mol Biol 125(3-5):231-242
163. Vranic S, Gatalica Z et al (2011) ER-alpha36, a novel isoform of ERalpha66, is commonly over-expressed in apocrine and adenoid cystic carcinomas of the breast. J Clin Pathol 64(1):54-57
164. Wang C, Mavrogianis PA et al (2009) Endometriosis is associated with progesterone resistance in the baboon (Papio anubis) oviduct: Evidence based on the localization of oviductal glycoprotein 1 (OVGP1). Biol Reprod 80(2):272-278
165. Wedren S, Lovmar L et al (2008) Estrogen receptor alpha gene polymorphism and endometrial cancer risk-a case-control study. BMC Cancer 8:322
166. Weige CC, Allred KF et al (2009) Estradiol alters cell growth in nonmalignant colonocytes and reduces the formation of preneoplastic lesions in the colon. Cancer Res 69(23):9118-9124
167. Weiss G, Goldsmith LT et al (2009) Inflammation in reproductive disorders. Reprod Sci 16(2):216-229
168. Welboren WJ, Sweep FC et al (2009a) Genomic actions of estrogen receptor alpha: What are the targets and how are they regulated? Endocr Relat Cancer 16(4):1073-1089
169. Welboren WJ, van Driel MA et al (2009b) ChIP-Seq of ERalpha and RNA polymerase II defines genes differentially responding to ligands. EMBO J 28(10):1418-1428
170. Williams C, Edvardsson K et al (2008) A genome-wide study of the repressive effects of estrogen receptor beta on estrogen receptor alpha signaling in breast cancer cells. Oncogene 27(7):1019-1032
171. Xue Q, Lin Z et al (2007) Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod 77(4):681-687
172. Yamashita H, Nishio M et al (2008) Low phosphorylation of estrogen receptor alpha (ERalpha) serine 118 and high phosphorylation of ERalpha serine 167 improve survival in ER-positive breast cancer. Endocr Relat Cancer 15(3):755-763
173. Yan M, Rayoo M et al (2011) Nuclear and cytoplasmic expressions of ERbeta1 and ERbeta2 are predictive of response to therapy and alters prognosis in familial breast cancers. Breast Cancer Res Treat 126(2):395-405
174. Yang J, Wang Y et al (2009) Reciprocal regulation of 17betaestradiol, interleukin-6 and interleukin-8 during growth and progression of epithelial ovarian cancer. Cytokine 46(3):382-391
175. Yang S, Thiel KW et al (2011a) Endometrial cancer: Reviving progesterone therapy in the molecular age. Discov Med 12(64): 205-212
176. Yang S, Thiel KW et al (2011b) Progesterone: The ultimate endometrial tumor suppressor. Trends Endocrinol Metab 22(4): 145-152
177. Yap OW, Bhat G et al (2009) Epigenetic modifications of the Estrogen receptor beta gene in epithelial ovarian cancer cells. Anticancer Res 29(1):139-144
178. Zahedi P, Yoganathan R et al (2012) Recent advances in drug delivery strategies for treatment of ovarian cancer. Expert Opin Drug Deliv 9(5):567-583
179. Zhao JJ, Lin J et al (2008) MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem 283(45):31079-31086
180. Zheng W, Long J et al (2009) Genome-wide association study identifies a new breast cancer susceptibility locus at 6q25.1. Nat Genet 41(3):324-328
181. Zhu J, Hua K et al (2011a) Re-expression of estrogen receptor beta inhibits the proliferation and migration of ovarian clear cell adenocarcinoma cells. Oncol Rep 26(6):1497-1503
182. Zhu ZY, Mu YQ et al (2011b) Association of CYP1B1 gene polymorphisms and the positive expression of estrogen alpha and estrogen beta with endometrial cancer risk. Eur J Gynaecol Oncol 32(2):188-191
183. Zulli K, Bianco B et al (2010) Polymorphism of the estrogen receptor beta gene is related to infertility and infertility-associated endometriosis. Arq Bras Endocrinol Metabol 54(6):567-571