The estrogen receptor α-cistrome beyond breast cancer

Molecular Endocrinology

Volumn 30, Issue 10, 2016, Pages 1046-1058

  Droog, Marjolein ^a   Mensink, Mark ^a   Zwart, Wilbert ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; TRANSCRIPTION FACTOR; LIGAND; PROTEIN BINDING;

BREAST CANCER; CHROMOSOME STRUCTURE; CONFORMATIONAL TRANSITION; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; REVIEW; ANIMAL; BINDING SITE; BREAST TUMOR; GENE EXPRESSION REGULATION; GENETICS;

ANIMALS; BINDING SITES; BREAST NEOPLASMS; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIGANDS; PROTEIN BINDING;

EID: 84990051122     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2016-1062     Document Type: Review

References (174)

1. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology. 1997;138:4613-4621.
2. Ropero AB, Eghbali M, Minosyan TY, Tang G, Toro L, Stefani E. Heart estrogen receptor α: distinct membrane and nuclear distribution patterns and regulation by estrogen. J Mol Cell Cardiol. 2006;41:496-510.
3. Li Z, Tuteja G, Schug J, Kaestner KH. Foxa1 and Foxa2 are essential for sexual dimorphism in liver cancer. Cell. 2012;148:72-83.
4. Zwart W, Terra H, Linn SC, Schagen SB. Cognitive effects of endocrine therapy for breast cancer: keep calm and carry on? Nat Rev Clin Oncol. 2015;12:597-606.
5. Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359-E386.
6. Harvey JM, Clark GM, Osborne CK, Allred DC. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol. 1999;17:1474-1481.
7. Allred DC, Brown P, Medina D. The origins of estrogen receptor α-positive and estrogen receptor α-negative human breast cancer. Breast Cancer Res. 2004;6:240-245.
8. Fisher B, Costantino JP, Redmond CK, Fisher ER, Wickerham DL, Cronin WM. Endometrial cancer in tamoxifen-treated breast cancer patients: findings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14. J Natl Cancer Inst. 1994;86:527-537.
9. Lahti E, Blanco G, Kauppila A, Apaja-Sarkkinen M, Taskinen PJ, Laatikainen T. Endometrial changes in postmenopausal breast cancer patients receiving tamoxifen. Obstet Gynecol. 1993;81:660-664.
10. van Leeuwen FE, Benraadt J, Coebergh JW, et al. Risk of endometrial cancer after tamoxifen treatment of breast cancer. Lancet. 1994;343:448-452.
11. Galea GL, Meakin LB, Sugiyama T, et al. Estrogen receptor α mediates proliferation of osteoblastic cells stimulated by estrogen and mechanical strain, but their acute down-regulation of the Wnt antagonist Sost is mediated by estrogen receptor β. J Biol Chem. 2013;288:9035-9048.
12. Nuttall ME, Stroup GB, Fisher PW, Nadeau DP, Gowen M, Suva LJ. Distinct mechanisms of action of selective estrogen receptor modulators in breast and osteoblastic cells. Am J Physiol Cell Physiol. 2000;279:C1550-C1557.
13. Flach KD, Zwart W. The first decade of estrogen receptor cistromics in breast cancer. J Endocrinol. 2016;229:R43-R56.
14. Nunn TW. On Cancer of the Breast. London, United Kingdom: J. & A. Churchill; 1882 p71
15. Boyd S. On oophorectomy in cancer of the breast. BMJ. 1900;2:1161-1167.
16. Love RR, Philips J. Oophorectomy for breast cancer: history revisited. J Natl Cancer Inst. 2002;94:1433-1434.
17. Reid G, Hübner MR, Métivier R, et al. Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol Cell. 2003;11:695-707.
18. Mohammed H, Taylor C, Brown GD, Papachristou EK, Carroll JS, D’Santos CS. Rapid immunoprecipitation mass spectrometry of endogenous proteins (RIME) for analysis of chromatin complexes. Nat Protoc. 2016;11:316-326.
19. Simpson ER, Mahendroo MS, Means GD, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev. 1994;15:342-355.
20. Hemsell DL, Grodin JM, Brenner PF, Siiteri PK, MacDonald PC. Plasma precursors of estrogen. II. Correlation of the extent of conversion of plasma androstenedione to estrone with age. J Clin Endocrinol Metab. 1974;38:476-479.
21. MacDonald PC, Edman CD, Hemsell DL, Porter JC, Siiteri PK. Effect of obesity on conversion of plasma androstenedione to estrone in postmenopausal women with and without endometrial cancer. Am J Obstet Gynecol. 1978;130:448-455.
22. Edman CD, MacDonald PC. Effect of obesity on conversion of plasma androstenedione to estrone in ovulatory and anovulator young women. Am J Obstet Gynecol. 1978;130:456-461.
23. Harada N. A unique aromatase (P-450AROM) mRNA formed by alternative use of tissue-specific exons 1 in human skin fibroblasts. Biochem Biophys Res Commun. 1992;189:1001-1007.
24. Jordan VC, Collins MM, Rowsby L, Prestwich G. A monohydroxylated metabolite of tamoxifen with potent antioestrogenic activity. J Endocrinol. 1977;75:305-316.
25. Preissner SC, Hoffmann MF, Preissner R, Dunkel M, Gewiess A, Preissner S. Polymorphic cytochrome P450 enzymes (CYPs) and their role in personalized therapy. PLoS One. 2013;8:e82562.
26. Pan CC, Woolever CA, Bhavnani BR. Transport of equine estrogens: binding of conjugated and unconjugated equine estrogens with human serum proteins. J Clin Endocrinol Metab. 1985;61:499-507.
27. Anderson JN, Peck EJ Jr, Clark JH. Nuclear receptor-estrogen complex: in vivo and in vitro binding of estradiol and estriol as influenced by serum albumin. J Steroid Biochem. 1974;5:103-107.
28. Dunn JF, Nisula BC, Rodbard D. Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma. J Clin Endocrinol Metab. 1981;53:58-68.
29. Södergård R, Bäckström T, Shanbhag V, Carstensen H. Calculation of free and bound fractions of testosterone and estradiol-17 β to human plasma proteins at body temperature. J Steroid Biochem. 1982;16:801-810.
30. Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem. 2001;276:36869-36872.
31. Bocchinfuso WP, Korach KS. Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J Mammary Gland Biol Neoplasia. 1997;2:323-334.
32. Schomberg DW, Couse JF, Mukherjee A, et al. Targeted disruption of the estrogen receptor-α gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology. 1999;140:2733-2744.
33. Tibbetts TA, Mendoza-Meneses M, O’Malley BW, Conneely OM. Mutual and intercompartmental regulation of estrogen receptor and progesterone receptor expression in the mouse uterus. Biol Reprod. 1998;59:1143-1152.
34. Tang S, Han H, Bajic VB. ERGDB: estrogen responsive genes database. Nucleic Acids Res. 2004;32:D533-536.
35. Tang S, Zhang Z, Tan SL, et al. KBERG: knowledge base for estrogen responsive genes. Nucleic Acids Res. 2007;35:D732-736.
36. Brzozowski AM, Pike AC, Dauter Z, et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature. 1997;389:753-758.
37. 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;95:927-937.
38. Liu H, Park WC, Bentrem DJ, et al. Structure-function relationships of the raloxifene-estrogen receptor-α complex for regulating transforming growth factor-α expression in breast cancer cells. J Biol Chem. 2002;277:9189-9198.
39. Levenson AS, Jordan VC. The key to the antiestrogenic mechanism of raloxifene is amino acid 351 (aspartate) in the estrogen receptor. Cancer Res. 1998;58:1872-1875.
40. Collins B, Mackenzie J, Stewart A, Bielajew C, Verma S. Cognitive effects of hormonal therapy in early stage breast cancer patients: a prospective study. Psychooncology. 2009;18:811-821.
41. Jenkins V, Shilling V, Fallowfield L, Howell A, Hutton S. Does hormone therapy for the treatment of breast cancer have a detrimental effect on memory and cognition? A pilot study. Psychooncology. 2004;13:61-66.
42. Schilder CM, Seynaeve C, Beex LV, et al. Effects of tamoxifen and exemestane on cognitive functioning of postmenopausal patients with breast cancer: results from the neuropsychological side study of the tamoxifen and exemestane adjuvant multinational trial. J Clin Oncol. 2010;28:1294-1300.
43. Eastell R, Adams JE, Coleman RE, et al. Effect of anastrozole on bone mineral density: 5-year results from the anastrozole, tamoxifen, alone or in combination trial 18233230. J Clin Oncol. 2008;26:1051-1057.
44. Ihionkhan CE, Chambliss KL, Gibson LL, Hahner LD, Mendelsohn ME, Shaul PW. Estrogen causes dynamic alterations in endothelial estrogen receptor expression. Circ Res. 2002;91:814-820.
45. Pinzone JJ, Stevenson H, Strobl JS, Berg PE. Molecular and cellular determinants of estrogen receptor α expression. Mol Cell Biol. 2004;24:4605-4612.
46. Kaneko KJ, Furlow JD, Gorski J. Involvement of the coding sequence for the estrogen receptor gene in autologous ligand-dependent down-regulation. Mol Endocrinol. 1993;7:879-888.
47. Yang X, Phillips DL, Ferguson AT, Nelson WG, Herman JG, Davidson NE. Synergistic activation of functional estrogen receptor (ER)-α by DNA methyltransferase and histone deacetylase inhibition in human ER-α-negative breast cancer cells. Cancer Res. 2001;61:7025-7029.
48. Flouriot G, Brand H, Denger S, et al. Identification of a new isoform of the human estrogen receptor-α (hER-α) that is encoded by distinct transcripts and that is able to repress hER-α activation function 1. EMBO J. 2000;19:4688-4700.
49. Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, Deuel TF. Identification, cloning, and expression of human estrogen receptor-α36, a novel variant of human estrogen receptor-α66. Biochem Biophys Res Commun. 2005;336:1023-1027.
50. Irsik DL, Carmines PK, Lane PH. Classical estrogen receptors and ERα splice variants in the mouse. PLoS One. 2013;8:e70926.
51. Thomas RS, Sarwar N, Phoenix F, Coombes RC, Ali S. Phosphorylation at serines 104 and 106 by Erk1/2 MAPK is important for estrogen receptor-α activity. J Mol Endocrinol. 2008;40:173-184.
52. Chen D, Washbrook E, Sarwar N, et al. Phosphorylation of human estrogen receptor α at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene. 2002;21:4921-4931.
53. de Leeuw R, Flach K, Bentin Toaldo C, et al. PKA phosphorylation redirects ERα to promoters of a unique gene set to induce tamoxifen resistance. Oncogene. 2013;32:3543-3551.
54. Zwart W, Griekspoor A, Berno V, et al. PKA-induced resistance to tamoxifen is associated with an altered orientation of ERα towards co-activator SRC-1. EMBO J. 2007;26:3534-3544.
55. Michalides R, Griekspoor A, Balkenende A, et al. Tamoxifen resistance by a conformational arrest of the estrogen receptor α after PKA activation in breast cancer. Cancer Cell. 2004;5:597-605.
56. Kim MY, Woo EM, Chong YT, Homenko DR, Kraus WL. Acetylation of estrogen receptor α by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol Endocrinol. 2006;20:1479-1493.
57. Wilson BJ, Tremblay AM, Deblois G, Sylvain-Drolet G, Giguère V. An acetylation switch modulates the transcriptional activity of estrogen-related receptor α. Mol Endocrinol. 2010;24:1349-1358.
58. Garbán HJ, Márquez-Garbán DC, Pietras RJ, Ignarro LJ. Rapid nitric oxide-mediated S-nitrosylation of estrogen receptor: regulation of estrogen-dependent gene transcription. Proc Natl Acad Sci USA. 2005;102:2632-2636.
59. Merenbakh-Lamin K, Ben-Baruch N, Yeheskel A, et al. D538G mutation in estrogen receptor-α: a novel mechanism for acquired endocrine resistance in breast cancer. Cancer Res. 2013;73:6856-6864.
60. Robinson DR, Wu YM, Vats P, et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat Genet. 2013;45:1446-1451.
61. Toy W, Shen Y, Won H, et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet. 2013;45:1439-1445.
62. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet. 2011;43:27-33.
63. Knowlden JM, Hutcheson IR, Jones HE, et al. Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology. 2003;144:1032-1044.
64. Jansen MP, Knijnenburg T, Reijm EA, et al. Hallmarks of aromatase inhibitor drug resistance revealed by epigenetic profiling in breast cancer. Cancer Res. 2013;73:6632-6641.
65. Ross-Innes CS, Stark R, Holmes KA, et al. Cooperative interaction between retinoic acid receptor-α and estrogen receptor in breast cancer. Genes Dev. 2010;24:171-182.
66. Zwart W, Flach KD, Rudraraju B, et al. SRC3 phosphorylation at Serine 543 is a positive independent prognostic factor in ER positive breast cancer. Clin Cancer Res. 2016;22:479-491.
67. Ross-Innes CS, Stark R, Teschendorff AE, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481:389-393.
68. Zwart W, Koornstra R, Wesseling J, Rutgers E, Linn S, Carroll JS. A carrier-assisted ChIP-seq method for estrogen receptor-chromatin interactions from breast cancer core needle biopsy samples. BMC Genomics. 2013;14:232.
69. Carroll JS, Liu XS, Brodsky AS, et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell. 2005;122:33-43.
70. Nautiyal J, Steel JH, Mane MR, et al. The transcriptional co-factor RIP140 regulates mammary gland development by promoting the generation of key mitogenic signals. Development. 2013;140:1079-1089.
71. Tan SK, Lin ZH, Chang CW, et al. AP-2γ regulates oestrogen receptor-mediated long-range chromatin interaction and gene transcription. EMBO J. 2011;30:2569-2581.
72. Petz LN, Ziegler YS, Loven MA, Nardulli AM. Estrogen receptor α and activating protein-1 mediate estrogen responsiveness of the progesterone receptor gene in MCF-7 breast cancer cells. Endocrinology. 2002;143:4583-4591.
73. Carroll JS, Meyer CA, Song J, et al. Genome-wide analysis of estrogen receptor binding sites. Nat Genet. 2006;38:1289-1297.
74. Franco HL, Nagari A, Kraus WL. TNFα signaling exposes latent estrogen receptor binding sites to alter the breast cancer cell transcriptome. Mol Cell. 2015;58:21-34.
75. Gertz J, Savic D, Varley KE, et al. Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol Cell. 2013;52:25-36.
76. Korch C, Spillman MA, Jackson TA, et al. DNA profiling analysis of endometrial and ovarian cell lines reveals misidentification, redundancy and contamination. Gynecol Oncol. 2012;127:241-248.
77. Gertz J, Reddy TE, Varley KE, Garabedian MJ, Myers RM. Genistein and bisphenol A exposure cause estrogen receptor 1 to bind thousands of sites in a cell type-specific manner. Genome Res. 2012;22:2153-2162.
78. Kalet BT, Anglin SR, Handschy A, et al. Transcription factor Ets1 cooperates with estrogen receptor α to stimulate estradiol-dependent growth in breast cancer cells and tumors. PLoS One. 2013;8:e68815.
79. Droog M, Nevedomskaya E, Kim Y, et al. Comparative cistromics reveals genomic crosstalk between FOXA1 and ER-α in tamoxifen-associated endometrial carcinomas. Cancer Res. 2016;76:3773-3784.
80. Hewitt SC, Li L, Grimm SA, et al. Research resource: whole-genome estrogen receptor α binding in mouse uterine tissue revealed by ChIP-seq. Mol Endocrinol. 2012;26:887-898.
81. Magnani L, Ballantyne EB, Zhang X, Lupien M. PBX1 genomic pioneer function drives ERα signaling underlying progression in breast cancer. PLoS Genet. 2011;7:e1002368.
82. Gao H, Fält S, Sandelin A, Gustafsson JA, Dahlman-Wright K. Genome-wide identification of estrogen receptor α-binding sites in mouse liver. Mol Endocrinol. 2008;22:10-22.
83. Welboren WJ, van Driel MA, Janssen-Megens EM, et al. ChIP-Seq of ERα and RNA polymerase II defines genes differentially responding to ligands. EMBO J. 2009;28:1418-1428.
84. Gröschel S, Sanders MA, Hoogenboezem R, et al. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell. 2014;157:369-381.
85. Lupiáñez DG, Kraft K, Heinrich V, et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell. 2015;161:1012-1025.
86. Dixon JR, Selvaraj S, Yue F, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376-380.
87. Mercer EM, Lin YC, Benner C, et al. Multilineage priming of enhancer repertoires precedes commitment to the B and myeloid cell lineages in hematopoietic progenitors. Immunity. 2011;35:413-425.
88. Andersson R, Gebhard C, Miguel-Escalada I, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507:455-461.
89. Ostuni R, Piccolo V, Barozzi I, et al. Latent enhancers activated by stimulation in differentiated cells. Cell. 2013;152:157-171.
90. Korkmaz G, Lopes R, Ugalde AP, et al. Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9. Nat Biotechnol. 2016;34:192-198.
91. Miranda-Carboni GA, Guemes M, Bailey S, et al. GATA4 regulates estrogen receptor-α-mediated osteoblast transcription. Mol Endocrinol. 2011;25:1126-1136.
92. Zwart W, Theodorou V, Kok M, Canisius S, Linn S, Carroll JS. Oestrogen receptor-co-factor-chromatin specificity in the transcriptional regulation of breast cancer. EMBO J. 2011;30:4764-4776.
93. Barnett DH, Sheng S, Charn TH, et al. Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res. 2008;68:3505-3515.
94. Deschênes J, Bourdeau V, White JH, Mader S. Regulation of GREB1 transcription by estrogen receptor α through a multipartite enhancer spread over 20 kb of upstream flanking sequences. J Biol Chem. 2007;282:17335-17339.
95. Fullwood MJ, Liu MH, Pan YF, et al. An oestrogen-receptor-α-bound human chromatin interactome. Nature. 2009;462:58-64.
96. Hsu PY, Hsu HK, Singer GA, et al. Estrogen-mediated epigenetic repression of large chromosomal regions through DNA looping. Genome Res. 2010;20:733-744.
97. Pan YF, Wansa KD, Liu MH, et al. Regulation of estrogen receptor-mediated long range transcription via evolutionarily conserved distal response elements. J Biol Chem. 2008;283:32977-32988.
98. Kim TH, Abdullaev ZK, Smith AD, et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell. 2007;128:1231-1245.
99. Xie X, Mikkelsen TS, Gnirke A, Lindblad-Toh K, Kellis M, Lander ES. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc Natl Acad Sci USA. 2007;104:7145-7150.
100. Chan CS, Song JS. CCCTC-binding factor confines the distal action of estrogen receptor. Cancer Res. 2008;68:9041-9049.
101. Ross-Innes CS, Brown GD, Carroll JS. A co-ordinated interaction between CTCF and ER in breast cancer cells. BMC Genomics. 2011;12:593.
102. Oñate SA, Tsai SY, Tsai MJ, O’Malley BW. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science. 1995;270:1354-1357.
103. Hong H, Kohli K, Garabedian MJ, Stallcup MR. GRIP1, a transcriptional coactivator for the AF-2 transactivation domain of steroid, thyroid, retinoid, and vitamin D receptors. Mol Cell Biol. 1997;17:2735-2744.
104. Anzick SL, Kononen J, Walker RL, et al. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science. 1997;277:965-968.
105. Chen H, Lin RJ, Schiltz RL, et al. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell. 1997;90:569-580.
106. Suen CS, Berrodin TJ, Mastroeni R, Cheskis BJ, Lyttle CR, Frail DE. A transcriptional coactivator, steroid receptor coactivator-3, selectively augments steroid receptor transcriptional activity. J Biol Chem. 1998;273:27645-27653.
107. Torchia J, Rose DW, Inostroza J, et al. The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature. 1997;387:677-684.
108. Shang Y, Brown M. Molecular determinants for the tissue specificity of SERMs. Science. 2002;295:2465-2468.
109. Hisamatsu Y, Tokunaga E, Yamashita N, et al. Impact of GATA-3 and FOXA1 expression in patients with hormone receptor-positive/HER2-negative breast cancer. Breast Cancer. 2015;22:520-528.
110. Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747-752.
111. Lupien M, Eeckhoute J, Meyer CA, et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell. 2008;132:958-970.
112. Mehta RJ, Jain RK, Leung S, et al. FOXA1 is an independent prognostic marker for ER-positive breast cancer. Breast Cancer Res Treat. 2012;131:881-890.
113. Cowper-Sal lari R, Zhang X, Wright JB, et al. Breast cancer risk-associated SNPs modulate the affinity of chromatin for FOXA1 and alter gene expression. Nat Genet. 2012;44:1191-1198.
114. Wolf I, Bose S, Williamson EA, Miller CW, Karlan BY, Koeffler HP. FOXA1: growth inhibitor and a favorable prognostic factor in human breast cancer. Int J Cancer. 2007;120:1013-1022.
115. Tangen IL, Krakstad C, Halle MK, et al. Switch in FOXA1 status associates with endometrial cancer progression. PLoS One. 2014;9:e98069.
116. Nakatani T, Roy G, Fujimoto N, Asahara T, Ito A. Sex hormone dependency of diethylnitrosamine-induced liver tumors in mice and chemoprevention by leuprorelin. Jpn J Cancer Res. 2001;92:249-256.
117. Naugler WE, Sakurai T, Kim S, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 2007;317:121-124.
118. Shen N, Gong J, Wang Y, et al. Integrative genomic analysis identifies that SERPINA6-rs1998056 regulated by FOXA/ERα is associated with female hepatocellular carcinoma. PLoS One. 2014;9:e107246.
119. Krum SA, Miranda-Carboni GA, Lupien M, Eeckhoute J, Carroll JS, Brown M. Unique ERα cistromes control cell type-specific gene regulation. Mol Endocrinol. 2008;22:2393-2406.
120. Wang J, Bao W, Qiu M, et al. Forkhead-box A1 suppresses the progression of endometrial cancer via crosstalk with estrogen receptor α. Oncol Rep. 2014;31:1225-1234.
121. Theodorou V, Stark R, Menon S, Carroll JS. GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibility. Genome Res. 2013;23:12-22.
122. Park JT, Shih IEM, Wang TL. Identification of Pbx1, a potential oncogene, as a Notch3 target gene in ovarian cancer. Cancer Res. 2008;68:8852-8860.
123. Kikugawa T, Kinugasa Y, Shiraishi K, et al. PLZF regulates Pbx1 transcription and Pbx1-HoxC8 complex leads to androgen-independent prostate cancer proliferation. Prostate. 2006;66:1092-1099.
124. Dintilhac A, Bihan R, Guerrier D, et al. PBX1 intracellular localization is independent of MEIS1 in epithelial cells of the developing female genital tract. Int J Dev Biol. 2005;49:851-858.
125. Ellis MJ, Ding L, Shen D, et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature. 2012;486:353-360.
126. Kong SL, Li G, Loh SL, Sung WK, Liu ET. Cellular reprogramming by the conjoint action of ERα, FOXA1, and GATA3 to a ligand-inducible growth state. Mol Syst Biol. 2011;7:526.
127. Mohammed H, Russell IA, Stark R, et al. Progesterone receptor modulates ERα action in breast cancer. Nature. 2015;523:313-317.
128. Love RR, Mazess RB, Barden HS, et al. Effects of tamoxifen on bone mineral density in postmenopausal women with breast cancer. N Engl J Med. 1992;326:852-856.
129. Nakshatri H, Badve S. FOXA1 as a therapeutic target for breast cancer. Expert Opin Ther Targets. 2007;11:507-514.
130. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology. 2003;144:4562-4574.
131. Fisher B, Costantino J, Redmond C, et al. A randomized clinical trial evaluating tamoxifen in the treatment of patients with node-negative breast cancer who have estrogen-receptor-positive tumors. N Engl J Med. 1989;320:479-484.
132. Powles TJ, Hardy JR, Ashley SE, et al. A pilot trial to evaluate the acute toxicity and feasibility of tamoxifen for prevention of breast cancer. Br J Cancer. 1989;60:126-131.
133. Wolmark N, Redmond C, Fisher B. A comparison of two and three years of adjuvant tamoxifen. Horm Res. 1989;32(suppl 1):166-168.
134. Sutherland RL, Hall RE, Taylor IW. Cell proliferation kinetics of MCF-7 human mammary carcinoma cells in culture and effects of tamoxifen on exponentially growing and plateau-phase cells. Cancer Res. 1983;43:3998-4006.
135. Pollard JW, Pacey J, Cheng SV, Jordan EG. Estrogens and cell death in murine uterine luminal epithelium. Cell Tissue Res. 1987;249:533-540.
136. Hess RA, Bunick D, Lee KH, et al. A role for oestrogens in the male reproductive system. Nature. 1997;390:509-512.
137. Kotoulas IG, Cardamakis E, Michopoulos J, Mitropoulos D, Dounis A. Tamoxifen treatment in male infertility. I. Effect on spermatozoa. Fertil Steril. 1994;61:911-914.
138. Torgerson DJ, Bell-Syer SE. Hormone replacement therapy and prevention of nonvertebral fractures: a meta-analysis of randomized trials. JAMA. 2001;285:2891-2897.
139. Krum SA, Miranda-Carboni GA, Hauschka PV, et al. Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival. EMBO J. 2008;27:535-545.
140. Imai Y, Youn MY, Kondoh S, et al. Estrogens maintain bone mass by regulating expression of genes controlling function and life span in mature osteoclasts. Ann NY Acad Sci. 2009;1173(suppl 1):E31-E39.
141. Grey AB, Stapleton JP, Evans MC, Tatnell MA, Ames RW, Reid IR. The effect of the antiestrogen tamoxifen on bone mineral density in normal late postmenopausal women. Am J Med. 1995;99:636-641.
142. Marttunen MB, Hietanen P, Tiitinen A, Ylikorkala O. Comparison of effects of tamoxifen and toremifene on bone biochemistry and bone mineral density in postmenopausal breast cancer patients. J Clin Endocrinol Metab. 1998;83:1158-1162.
143. Louet JF, LeMay C, Mauvais-Jarvis F. Antidiabetic actions of estrogen: insight from human and genetic mouse models. Curr Atheroscler Rep. 2004;6:180-185.
144. Bryzgalova G, Gao H, Ahren B, et al. Evidence that oestrogen receptor-α plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia. 2006;49:588-597.
145. Ogawa Y, Murata Y, Nishioka A, Inomata T, Yoshida S. Tamoxifen-induced fatty liver in patients with breast cancer. Lancet. 1998;351:725.
146. Nishino M, Hayakawa K, Nakamura Y, Morimoto T, Mukaihara S. Effects of tamoxifen on hepatic fat content and the development of hepatic steatosis in patients with breast cancer: high frequency of involvement and rapid reversal after completion of tamoxifen therapy. AJR Am J Roentgenol. 2003;180:129-134.
147. Rivera CM, Grossardt BR, Rhodes DJ, Rocca WA. Increased mortality for neurological and mental diseases following early bilateral oophorectomy. Neuroepidemiology. 2009;33:32-40.
148. Luine VN, Khylchevskaya RI, McEwen BS. Effect of gonadal steroids on activities of monoamine oxidase and choline acetylase in rat brain. Brain Res. 1975;86:293-306.
149. Sandstrom NJ, Williams CL. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci. 2001;115:384-393.
150. Wang F, He Q, Sun Y, Dai X, Yang XP. Female adult mouse cardiomyocytes are protected against oxidative stress. Hypertension. 2010;55:1172-1178.
151. Lerner DJ, Kannel WB. Patterns of coronary heart disease morbidity and mortality in the sexes: a 26-year follow-up of the Framingham population. Am Heart J. 1986;111:383-390.
152. Pérez-López FR, Chedraui P, Gilbert JJ, Pérez-Roncero G. Cardiovascular risk in menopausal women and prevalent related co-morbid conditions: facing the post-Women’s Health Initiative era. Fertil Steril. 2009;92:1171-1186.
153. Hodgin JB, Krege JH, Reddick RL, Korach KS, Smithies O, Maeda N. Estrogen receptor α is a major mediator of 17β-estradiol’s atheroprotective effects on lesion size in Apoe−/− mice. J Clin Invest. 2001;107:333-340.
154. Adams MR, Kaplan JR, Manuck SB, et al. Inhibition of coronary artery atherosclerosis by 17-β estradiol in ovariectomized monkeys. Lack of an effect of added progesterone. Arteriosclerosis. 1990;10:1051-1057.
155. Bourassa PA, Milos PM, Gaynor BJ, Breslow JL, Aiello RJ. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA. 1996;93:10022-10027.
156. Elhage R, Arnal JF, Pieraggi MT, et al. 17 β-estradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 1997;17:2679-2684.
157. Haarbo J, Leth-Espensen P, Stender S, Christiansen C. Estrogen monotherapy and combined estrogen-progestogen replacement therapy attenuate aortic accumulation of cholesterol in ovariectomized cholesterol-fed rabbits. J Clin Invest. 1991;87:1274-1279.
158. Holm P, Stender S, Andersen HO, Hansen BF, Nordestgaard BG. Antiatherogenic effect of estrogen abolished by balloon catheter injury in cholesterol-clamped rabbits. Arterioscler Thromb Vasc Biol. 1997;17:1504-1511.
159. Caulin-Glaser T, García-Cardeña G, Sarrel P, Sessa WC, Bender JR. 17 β-estradiol regulation of human endothelial cell basal nitric oxide release, independent of cytosolic Ca2+ mobilization. Circ Res. 1997;81:885-892.
160. Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N Engl J Med. 1999;340:1801-1811.
161. Lantin-Hermoso RL, Rosenfeld CR, Yuhanna IS, German Z, Chen Z, Shaul PW. Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol. 1997;273:L119-L126.
162. Grey AB, Stapleton JP, Evans MC, Reid IR. The effect of the anti-estrogen tamoxifen on cardiovascular risk factors in normal postmenopausal women. J Clin Endocrinol Metab. 1995;80:3191-3195.
163. Massaro D, Massaro GD. Estrogen regulates pulmonary alveolar formation, loss, and regeneration in mice. Am J Physiol Lung Cell Mol Physiol. 2004;287:L1154-L1159.
164. Mollerup S, Jørgensen K, Berge G, Haugen A. Expression of estrogen receptors α and β in human lung tissue and cell lines. Lung Cancer. 2002;37:153-159.
165. Pietras RJ, Márquez DC, Chen HW, Tsai E, Weinberg O, Fishbein M. Estrogen and growth factor receptor interactions in human breast and non-small cell lung cancer cells. Steroids. 2005;70:372-381.
166. Stabile LP, Davis AL, Gubish CT, et al. Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor α and β and show biological responses to estrogen. Cancer Res. 2002;62:2141-2150.
167. Bouchardy C, Benhamou S, Schaffar R, et al. Lung cancer mortality risk among breast cancer patients treated with anti-estrogens. Cancer. 2011;117:1288-1295.
168. Priyanka HP, Krishnan HC, Singh RV, Hima L, Thyagarajan S. Estrogen modulates in vitro T cell responses in a concentration- and receptor-dependent manner: effects on intracellular molecular targets and antioxidant enzymes. Mol Immunol. 2013;56:328-339.
169. Babina M, Kirn F, Hoser D, et al. Tamoxifen counteracts the allergic immune response and improves allergen-induced dermatitis in mice. Clin Exp Allergy. 2010;40:1256-1265.
170. Joffroy CM, Buck MB, Stope MB, Popp SL, Pfizenmaier K, Knabbe C. Antiestrogens induce transforming growth factor β-mediated immunosuppression in breast cancer. Cancer Res. 2010;70:1314-1322.
171. Nalbandian G, Paharkova-Vatchkova V, Mao A, Nale S, Kovats S. The selective estrogen receptor modulators, tamoxifen and raloxifene, impair dendritic cell differentiation and activation. J Immunol. 2005;175:2666-2675.
172. Sthoeger ZM, Bentwich Z, Zinger H, Mozes E. The beneficial effect of the estrogen antagonist, tamoxifen, on experimental systemic lupus erythematosus. J Rheumatol. 1994;21:2231-2238.
173. Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M. Positive cross-regulatory loop ties GATA-3 to estrogen receptor α expression in breast cancer. Cancer Res. 2007;67:6477-6483.
174. ENCODE Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science. 2004;306:636-640