Estrogen receptor b: The guardian of the endometrium

Human Reproduction Update

Volumn 21, Issue 2, 2015, Pages 174-193

  Hapangama, D K ^a   Kamal, A M ^a,b   Bulmer, J N ^c  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b BAGHDAD TEACHING HOSPITAL   (Iraq)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Endometrial cancer; Endometrial proliferation; Endometrium; Estrogen receptor b; Hormone receptors

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ISOPROTEIN; ESTROGEN;

ADENOMYOSIS; ARTICLE; BREAST CANCER; CELL FATE; CELL FUNCTION; ENDOMETRIAL DISEASE; ENDOMETRIOSIS; ENDOMETRIUM; ENDOMETRIUM CANCER; ENDOMETRIUM HYPERPLASIA; ENDOMETRIUM POLYP; HORMONAL REGULATION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MENSTRUAL CYCLE; MITOSIS; NONHUMAN; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SCORING SYSTEM; SYSTEMATIC REVIEW; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRIMATE; UTERUS DISEASE;

ANIMALS; ENDOMETRIUM; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; HUMANS; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PRIMATES; UTERINE DISEASES;

EID: 84929940702     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmu053     Document Type: Article

References (213)

1. Argenta P, Svendsen C, Elishaev E, Gloyeske N, Geller MA, Edwards RP, Linkov F. Hormone receptor expression patterns in the endometrium of asymptomatic morbidly obese women before and after bariatric surgery. Gynecol Oncol 2014; 133:78–82.
2. Arnal JF, Gourdy P, Lenfant F. In vivo dissection of the estrogen receptor alpha: uncoupling of its physiological effects and medical perspectives. Ann Endocrinol 2013;74:82–89.
3. Benecke A, Chambon P, Gronemeyer H. Synergy between estrogen receptor alpha activation functions AF1 and AF2 mediated by transcription intermediary factor TIF2. EMBO Rep 2001;1:151–157.
4. Berbic M, Fraser IS. Immunology of normal and abnormal menstruation. Womens Health 2013;9:387–395.
5. Bernardi LA, Pavone ME. Endometriosis: an update on management. Womens Health 2013;9:233–250.
6. Blair IA. Analysis of estrogens in serum and plasma from postmenopausal women: past present, and future. Steroids 2010;75:297 – 306.
7. Blois SM, Klapp BF, Barrientos G. Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells. J Reprod Immunol 2011;88:86–92.
8. Borzychowski AM, Chantakru S, Minhas K, Paffaro VA, Yamada AT, He H, Korach KS, Croy BA. Functional analysis of murine uterine natural killer cells genetically devoid of estrogen receptors. Placenta 2003;24:403 – 411.
9. Bottner M, Thelen P, Jarry H. Estrogen receptor beta: tissue distribution and the still largely enigmatic physiological function. J Steroid Biochem Mol Biol 2014; 139:245–251.
10. Brandenberger AW, Lebovic DI, Tee MK, Ryan IP, Tseng JF, Jaffe RB, Taylor RN. Estrogen receptor (ER)-alpha and ER-beta isoforms in normal endometrial and endometriosis-derived stromal cells. Mol Hum Reprod 1999;5:651–655.
11. Brosens JJ, Tullet J, Varshochi R, Lam EWF. Steroid receptor action. Best Pract Res Clin Obstet Gynaecol 2004;18:265–283.
12. Bukulmez O, Hardy DB, Carr BR, Word RA, Mendelson CR. Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 2007;149:1190–1204.
13. Bulmer JN, Lunny DP, Hagin SV. Immunohistochemical characterization of stromal leucocytes in nonpregnant human endometrium. Am J Reprod Immunol Microbiol 1988;17:83–90.
14. Bulmer JN, Longfellow M, Ritson A. Leukocytes and resident blood cells in endometrium. Ann N Y Acad Sci 1991a;622:57–68.
15. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991b;6:791–798.
16. Bulun SE, Monsavais D, Pavone ME, Dyson M, Xue Q, Attar E, Tokunaga H, Su EJ. Role of estrogen receptor-beta in endometriosis. Semin Reprod Med 2012;30:39 – 45.
17. Burns KA, Korach KS. Estrogen receptors and human disease: an update. Arch Toxicol 2012;86:1491–1504.
18. Cervello I, Gil-Sanchis C, Mas A, Delgado-Rosas F, Martinez-Conejero JA, Galan A, Martinez-Romero A, Martinez S, Navarro I, Ferro J et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One 2010;5:e10964.
19. Chakravarty D, Srinivasan R, Ghosh S, Gopalan S, Rajwanshi A, Majumdar S. Estrogen receptor b1 and the b2/bcx isoforms in nonneoplastic endometrium and in endometrioid carcinoma. Int J Gynecol Cancer 2007;17:905–913.
20. Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells (Dayton, Ohio) 2006;24:1529–1538.
21. Chen JQ, Russo PA, Cooke C, Russo IH, Russo J. 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 2007;1773:1732–1746.
22. Cheng G, Wilczek B, Warner M, Gustafsson JA, Landgren BM. Isoflavone treatment for acute menopausal symptoms. Menopause 2007;14:468 – 473.
23. Chhieng D, Hui P. Normal histology of female genital organs. In: Chhieng D, Hui P (eds). Current Clinical Pathology. NJ, USA: Humana Press, 2011, 1 – 13.
24. Collins F, Macpherson S, Brown P, Bombail V, Williams A, Anderson R, Jabbour H, Saunders P. Expression of estrogen 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 2009;9:330.
25. Cooke PS, Spencer TE, Bartol FF, Hayashi K. Uterine glands: development, function and experimental model systems. Mol Hum Reprod 2013;19:547 – 558.
26. Costa-Paiva L, Godoy CE Jr, Antunes A Jr, Caseiro JD, Arthuso M, Pinto-Neto AM. Risk of malignancy in endometrial polyps in premenopausal and postmenopausal women according to clinicopathologic characteristics. Menopause 2011;18: 1278–1282.
27. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 1999;20:358 – 417.
28. Crandall CJ, Barrett-Connor E. Endogenous sex steroid levels and cardiovascular disease in relation to the menopause: a systematic review. Endocrinol Metab Clin North Am 2013;42:227–253.
29. Critchley HOD, Saunders PTK. Hormone receptor dynamics in a receptive human endometrium. Reprod Sci 2009;16:191–199.
30. Critchley HOD, Brenner RM, Henderson TA, Williams K, Nayak NR, Slayden OD, Millar MR, Saunders PTK. Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab 2001;86:1370–1378.
31. Critchley HOD, Henderson TA, Kelly RW, Scobie GS, Evans LR, Groome NP, Saunders PTK, Critchley HOD, Henderson TA, Kelly RW et al. Wild-type estrogen receptor (ERbeta1) and the splice variant (ERbetacx/beta2) are both expressed within the human endometrium throughout the normal menstrual cycle. J Clin Endocrinol Metab 2002;87:5265–5273.
32. Critchley HO, Kelly RW, Baird DT, Brenner RM. Regulation of human endometrial function: mechanisms relevant to uterine bleeding. Reprod Biol Endocrinol 2006; 4(Suppl. 1):S5.
33. Donnez O, Van Langendonckt A, Defrere S, Colette S, Van Kerk O, Dehoux JP, Squifflet J, Donnez J. Induction of endometriotic nodules in an experimental baboon model mimicking human deep nodular lesions. Fertil Steril 2012; 99:783–789.e783.
34. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000;127:4277 – 4291.
35. Engemise SL, Willets JM, Taylor AH, Emembolu JO, Konje JC. Changes in glandular and stromal estrogen and progesterone receptor isoform expression in eutopic and ectopic endometrium following treatment with the levonorgestrel-releasing intrauterine system. Eur J Obstet Gynecol Reprod Biol 2011;157:101 – 106.
36. Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjold M, Gustafsson JA. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 1997; 82:4258–4265.
37. Erdemoglu E, Guney M, Karahan N, Mungan T. Expression of cyclooxygenase-2, matrix metalloproteinase-2 and matrix metalloproteinase-9 in premenopausal and postmenopausal endometrial polyps. Maturitas 2008;59:268 – 274.
38. Evans T, Sany O, Pearmain P, Ganesan R, Blann A, Sundar S. Differential trends in the rising incidence of endometrial cancer by type: data from a UK population-based registry from 1994 to 2006. Br J Cancer 2011;104: 1505–1510.
39. Fazleabas AT, Brudney A, Chai D, Langoi D, Bulun SE. Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 2003; 80(Suppl. 2):820–827.
40. Fearnley EJ, Marquart L, Spurdle AB, Weinstein P, Webb PM. Polycystic ovary syndrome increases the risk of endometrial cancer in women aged less than 50 years: an Australian case-control study. Cancer Causes Control 2010;21:2303 – 2308.
41. Ferenczy A. Studies on the cytodynamics of human endometrial regeneration. II. Transmission electron microscopy and histochemistry. Am J Obstet Gynecol 1976; 124:582–595.
42. Ferenczy A. Regeneration of the human endometrium. In: Wolff CMFaM (ed). Progress in Surgical Pathology. New York, USA: Masson, 1980, 157 – 173.
43. Ferenczy A, Guralnicik M. Endometrial microstructure: structure–function relationships throughout the menstrual cycle. Semin Reprod Endocrinol 1983; 1:205–219.
44. Ferenczy A, Bergeron C. Histology of the human endometrium: from birth to senescence. Ann N Y Acad Sci 1991;622:6–27.
45. Fernandez JW, Grizzell JA, Wecker L. The role of estrogen receptor beta and nicotinic cholinergic receptors in postpartum depression. Prog Neuropsychopharmacol Biol Psychiatry 2012;40:199 – 206.
46. Filant J, Spencer TE. Endometrial glands are essential for blastocyst implantation and decidualization in the mouse uterus. Biol Reprod 2013;88:93.
47. Frasor J, Barnett DH, Danes JM, Hess R, Parlow AF, Katzenellenbogen BS. Response-specific and ligand dose-dependent modulation of estrogen receptor (ER) alpha activity by ERbeta in the uterus. Endocrinology 2003;144:3159–3166.
48. Fujimoto J, Hirose R, Sakaguchi H, Tamaya T. Expression of estrogen receptor-alpha and -beta in ovarian endometriomata. Mol Hum Reprod 1999;5:742–747.
49. Fujimoto J, Sakaguchi H, Aoki I, Khatun S, Toyoki H, Tamaya T. Review: steroid receptors and metastatic potential in endometrial cancers. J Steroid Biochem Mol Biol 2000;75:209–212.
50. Fujimura T, Takahashi S, Urano T, Ogawa S, Ouchi Y, Kitamura T, Muramatsu M, Inoue S. 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 2001;289:692–699.
51. Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod 2010; 16:818–834.
52. Gargett CE, Chan RW, Schwab KE. Hormone and growth factor signaling in endometrial renewal: role of stem/progenitor cells. Mol Cell Endocrinol 2008; 288:22–29.
53. Gargett CE, Nguyen HP, Ye L. Endometrial regeneration and endometrial stem/ progenitor cells. Rev Endocr Metab Disord 2012;13:235–251.
54. Grady D, Sawaya GF, Johnson KC, Koltun W, Hess R, Vittinghoff E, Kristof M, Tagliaferri M, Cohen I, Ensrud KE. MF101, a selective estrogen receptor beta modulator for the treatment of menopausal hot flushes: a phase II clinical trial. Menopause (New York, NY) 2009;16:458–465.
55. Greaves E, Collins F, Critchley HO, Saunders PT. ERbeta-dependent effects on uterine endothelial cells are cell specific and mediated via Sp1. Hum Reprod (Oxford, England) 2013;28:2490 – 2501.
56. Gustafsson JA. What pharmacologists can learn from recent advances in estrogen signalling. Trends Pharmacol Sci 2003;24:479–485.
57. Hachisuga T, Miyakawa T, Tsujioka H, Horiuchi S, Emoto M, Kawarabayashi T. K-ras mutation in tamoxifen-related endometrial polyps. Cancer 2003;98:1890–1897.
58. Hall JM, Mcdonnell DP. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 1999; 140:5566–5578.
59. Hall JM, Mcdonnell DP. Coregulators in nuclear estrogen receptor action—from concept to therapeutic targeting. Mol Interv 2005;5:343–357.
60. Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, Lydon JP, Demayo FJ, O’malley BW. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med 2012;18:1102–1111.
61. Hanamura T, Niwa T, Gohno T, Kurosumi M, Takei H, Yamaguchi Y, Ito K-I, Hayashi S-I. Possible role of the aromatase-independent steroid metabolism pathways in hormone responsive primary breast cancers. Breast Cancer Res Treat 2014;143:69 – 80.
62. Hapangama D. Mifepristone: the multi-faceted nti-hormone. J Drug Eval 2003; 1:149–175.
63. Hapangama D, Bulmer J. Contemporary approaches to heavy menstrual bleeding. In: Justin Clark T, Natalie AM (eds). Pathophysiology of HMB. London, UK: Future Medicine Ltd, 2014.
64. Hapangama DK, Turner MA, Drury JA, Martin-Ruiz C, Von Zglinicki T, Farquharson RG, Quenby S. Endometrial telomerase shows specific expression patterns in different types of reproductive failure. Reprod Biomed Online 2008a; 17:416–424.
65. Hapangama DK, Turner MA, Drury JA, Quenby S, Saretzki G, Martin-Ruiz C, Von Zglinicki T. Endometriosis is associated with aberrant endometrial expression of telomerase and increased telomere length. Hum Reprod 2008b; 23:1511–1519.
66. Hapangama DK, Turner MA, Drury JA, Quenby S, Hart A, Maddick M, Martin-Ruiz C, Von Zglinicki T. Sustained replication in endometrium of women with endometriosis occurs without evoking a DNA damage response. Hum Reprod 2009;24:687 – 696.
67. Hapangama DK, Raju RS, Valentijn AJ, Barraclough D, Hart A, Turner MA, Platt-Higgins A, Barraclough R, Rudland PS. Aberrant expression of metastasis-inducing proteins in ectopic and matched eutopic endometrium of women with endometriosis: implications for the pathogenesis of endometriosis. Hum Reprod 2012;27:394–407.
68. Häring J, Schüler S, Lattrich C, Ortmann O, Treeck O. Role of estrogen receptor b in gynecological cancer. Gynecol Oncol 2012a;127:673–676.
69. Häring J, Skrzypczak M, Stegerer A, Lattrich C, Weber F, Gorse R, Ortmann O, Treeck O. Estrogen receptor beta transcript variants associate with oncogene expression in endometrial cancer. Int J Mol Med 2012b;29:1127–1136.
70. Harnish DC. Estrogen receptor ligands in the control of pathogenic inflammation. Curr Opin Investig Drugs (London, England: 2000) 2006;7:997 – 1001.
71. Harris HA. Estrogen receptor-beta: recent lessons from in vivo studies. Mol Endocrinol 2006;21:1 – 13.
72. Hawse JR, Subramaniam M, Monroe DG, Hemmingsen AH, Ingle JN, Khosla S, Oursler MJ, Spelsberg TC. Estrogen receptor beta isoform-specific induction of transforming growth factor beta-inducible early gene-1 in human osteoblast cells: an essential role for the activation function 1 domain. Mol Endocrinol 2008; 22:1579–1595.
73. Henderson TA, Saunders PT, Moffett-King A, Groome NP, Critchley HO. Steroid receptor expression in uterine natural killer cells. J Clin Endocrinol Metab 2003; 88:440–449.
74. Hertrampf T, Seibel J, Laudenbach U, Fritzemeier KH, Diel P. Analysis of the effects of estrogen receptor alpha (ERalpha)- and ERbeta-selective ligands given in combination to ovariectomized rats. Br J Pharmacol 2008;153:1432–1437.
75. Hogan AM, Collins D, Baird AW, Winter DC. Estrogen and gastrointestinal malignancy. Mol Cell Endocrinol 2009;307:19 – 24.
76. Holm A, Nilsson BO. Identification and characterization of new mechanisms in vascular estrogen signalling. Basic Clin Pharmacol Toxicol 2013;113:287 – 293.
77. Hombach-Klonisch S, Kehlen A, Fowler PA, Huppertz B, Jugert JF, Bischoff G, Schluter E, Buchmann J, Klonisch T. Regulation of functional steroid receptors and ligand-induced responses in telomerase-immortalized human endometrial epithelial cells. J Mol Endocrinol 2005;34:517–534.
78. Hong-Bing C, Yun-Feng Z, Bi-Cheng W, Ling-Ling G. Expression of estrogen receptors a and b protein in endometrial carcinoma. Cancer Ther 2008;6:907 – 911.
79. Hu K, Zhong G, He F. Expression of estrogen receptors ER[alpha] and ER[beta] in endometrial hyperplasia and adenocarcinoma. Int J Gynecol Cancer 2005; 15:537–541.
80. Hu J, Wang J, Xiang H, Li Z, Wang B, Cao Y, Ma X. Association of polymorphisms in the estrogen receptor beta (ESR2) with unexplained recurrent spontaneous abortion (URSA) in Chinese population. J Matern Fetal Neonatal Med 2012; 25:1727–1729.
81. Hudelist G, Keckstein J, Czerwenka K, Lass H, Walter I, Auer M, Wieser F, Wenzl R, Kubista E, Singer CF. Estrogen receptor beta and matrix metalloproteinase 1 are coexpressed in uterine endometrium and endometriotic lesions of patients with endometriosis. Fertil Steril 2005;84(Suppl. 2):1249–1256.
82. Imamov O, Shim GJ, Warner M, Gustafsson JA. Estrogen receptor beta in health and disease. Biol Reprod 2005;73:866–871.
83. Indraccolo U, Di Iorio R, Matteo M, Coron G, Greco P, Indraccolo SR. The pathogenesis of endometrial polyps: a systematic semi-quantitative review. Eur J Gynaecol Oncol 2013;34:5–22.
84. Jabbour HN, Kelly RW, Fraser HM, Critchley HOD. Endocrine regulation of menstruation. Endocr Rev 2006;27:17–46.
85. Janzen DM, Cheng D, Schafenacker AM, Paik DY, Goldstein AS, Witte ON, Jaroszewicz A, Pellegrini M, Memarzadeh S. Estrogen and progesterone together expand murine endometrial epithelial progenitor cells. Stem Cells 2013; 31:808–822.
86. Jarzabek K, Koda M, Walentowicz-Sadlecka M, Grabiec M, Laudanski P, Wolczynski S. Altered expression of ERs, aromatase, and COX2 connected to estrogen action in type 1 endometrial cancer biology. Tumour Biol 2013;34:4007 – 4016.
87. Jazaeri AA, Nunes KJ, Dalton MS, Xu M, Shupnik MA, Rice LW. Well-differentiated endometrial adenocarcinomas and poorly differentiated mixed mullerian tumors have altered ER and PR isoform expression. Oncogene 2001;20:6965–6969.
88. Jongen V, Briet J, De Jong R, Ten Hoor K, Boezen M, Van Der Zee A, Nijman H, Hollema H. 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 2009;112:537–542.
89. 2 and its splice variants in patients with and without endometriosis. Arch Gynecol Obstet 2011;284:885–891.
90. Katzenellenbogen BS. Biology and receptor interactions of estriol and estriol derivatives in vitro and in vivo. J Steroid Biochem 1984;20:1033 – 1037.
91. Katzenellenbogen B, Sun J, Harrington WR, Kraichely DM, Ganessunker D, Katzenellenbogen JA. Structure–function relationships in estrogen receptors and the characterization of novel selective estrogen receptor modulators with unique pharmacological profiles. Ann NY Acad Sci 2001;949:6–15.
92. Kayisli UA, Luk J, Guzeloglu-Kayisli O, Seval Y, Demir R, Arici A. Regulation of angiogenic activity of human endometrial endothelial cells in culture by ovarian steroids. J Clin EndocrinolMetab 2004;89:5794–5802.
93. Keay J, Bridgham JT, Thornton JW. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 2006;147:3861–3869.
94. Kim JJ, Choi YM, Choung SH, Yoon SH, Lee GH, Moon SY. Estrogen receptor betagene +1730 G/A polymorphism in women with polycystic ovary syndrome. Fertil Steril 2010;93:1942–1947.
95. Knapp P, Chabowski A, Blachnio-Zabielska A, Walentowicz-Sadlecka M, Grabiec M, Knapp PA. Expression of estrogen receptors (alpha, beta), cyclooxygenase-2 and aromatase in normal endometrium and endometrioid cancer of uterus. Adv Med Sci 2013;58:96–103.
96. Koos RD. Minireview: putting physiology back into estrogens’ mechanism of action. Endocrinology 2011;152:4481–4488.
97. Kramer PR, Wray S. 17-Beta-estradiol regulates expression of genes that function in macrophage activation and cholesterol homeostasis. J Steroid Biochem Mol Biol 2002;81:203–216.
98. Krikun G, Schatz F, Taylor R, Critchley HO, Rogers PA, Huang J, Lockwood CJ. Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. J Clin Endocrinol Metab 2005;90:1812–1818.
99. Kuiper GG, Gustafsson JA. The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 1997;410:87 – 90.
100. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 1996; 93:5925–5930.
101. Kumar R, Zakharov MN, Khan SH, Miki R, Jang H, Toraldo G, Singh R, Bhasin S, Jasuja R. The dynamic structure of the estrogen receptor. J Amino Acids 2012;2011:812540.
102. Kushner PJ, Agard DA, Greene GL, Scanlan TS, Shiau AK, Uht RM, Webb P. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 2000;74:311–317.
103. Labrie F. All sex steroids are made intracellularly in peripheral tissues by the mechanisms of intracrinology after menopause. J Steroid Biochem Mol Biol 2014; 2014:06.001.
104. Lacey JV Jr, Ioffe OB, Ronnett BM, Rush BB, Richesson DA, Chatterjee N, Langholz B, Glass AG, Sherman ME. Endometrial carcinoma risk among women diagnosed with endometrial hyperplasia: the 34-year experience in a large health plan. Br J Cancer 2007;98:45 – 53.
105. Lash GE, Robson SC, Bulmer JN. Review: functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta 2010;31(Suppl.):S87 – S92.
106. Lecce G, Meduri G, Ancelin M, Bergeron C, Perrot-Applanat M. Presence of estrogen receptor beta in the human endometrium through the cycle: expression in glandular, stromal, and vascular cells. J Clin Endocrinol Metab 2001;86:1379 – 1386.
107. Lewandowski S, Kalita K, Kaczmarek L. Estrogen receptor beta. Potential functional significance of a variety of mRNA isoforms. FEBS Lett 2002;524:1–5.
108. Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Hum Reprod 2002;17:2725–2736.
109. Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Hum Reprod 2008;17:2725–2736.
110. Leygue E, Dotzlaw H, Lu B, Glor C, Watson PH, Murphy LC. Estrogen receptor beta: mine is longer than yours? J Clin Endocrinol Metab 1998;83:3754–3755.
111. Li XC, Song WJ. Endometrial Intraepithelial Neoplasia (EIN) in endometrial biopsy specimens categorized by the 1994 World Health Organization classification for endometrial hyperplasia. Asian Pac J Cancer Prev 2013;14:5935–5939.
112. Lubahn DB, Moyer JS, Smithies O, Golding TS, Couse JF, Korach KS. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 1993; 90:11162–11166.
113. Maliqueo M, Clementi M, Gabler F, Johnson MC, Palomino A, Sir-Petermann T, Vega M. Expression of steroid receptors and proteins related to apoptosis in endometria of women with polycystic ovary syndrome. Fertil Steril 2003;80:812 – 819.
114. Maret A, Coudert JD, Garidou L, Foucras G, Gourdy P, Krust A, Dupont S, Chambon P, Druet P, Bayard F et al. Estradiol enhances primary antigen-specific CD4T cell responses and Th1 development in vivo. Essential role of estrogen receptor alpha expression in hematopoietic cells. Eur J Immunol 2003;33:512 – 521.
115. Marshall RJ, Jones DB. An immunohistochemical study of lymphoid tissue in human endometrium. Int J Gynecol Pathol 1988;7:225–235.
116. Masuda H, Kalka C, Takahashi T, Yoshida M, Wada M, Kobori M, Itoh R, Iwaguro H, Eguchi M, Iwami Y et al. Estrogen-mediated endothelial progenitor cell biology and kinetics for physiological postnatal vasculogenesis. Circ Res 2007;101:598–606.
117. Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, Arase T, Oda H, Uchida H, Asada H et al. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One 2010;5:e10387.
118. Matsuzaki S, Fukaya T, Suzuki T, Murakami T, Sasano H, Yajima A. Estrogen receptor alpha and beta mRNA expression in human endometrium throughout the menstrual cycle. Mol Hum Reprod 1999;5:559–564.
119. Matsuzaki S, Uehara S, Murakami T, Fujiwara J, Funato T, Okamura K. Quantitative analysis of estrogen receptor alpha and beta messenger ribonucleic acid levels in normal endometrium and ovarian endometriotic cysts using a real-time reverse transcription-polymerase chain reaction assay. Fertil Steril 2000;74:753–759.
120. Matsuzaki S, Murakami T, Uehara S, Canis M, Sasano H, Okamura K. Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis. Fertil Steril 2001;75:1198–1205.
121. Matthews J, Wihlen B, Tujague M, Wan J, Strom A, Gustafsson JA. 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 2006;20:534–543.
122. May FE. Novel drugs that target the estrogen-related receptor alpha: their therapeutic potential in breast cancer. Cancer Manag Res. 2014; 23:225 – 252.
123. Mccluggage WG. Benign Diseases of the Endometrium. In: Kurman R, Ellenson L, Ronnett B (eds). Pathology of Female Genetal Tract. Boston, USA: Springer, 2011, 305–358.
124. Mcdonnell DP, Norris JD. Connections and regulation of the human estrogen receptor. Science 2002;296:1642 – 1644.
125. Mehasseb MK, Panchal R, Taylor AH, Brown L, Bell SC, Habiba M. Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertil Steril 2011;95:2228–2235.
126. Menasce LP, White GR, Harrison CJ, Boyle JM. Localization of the estrogen receptor locus (ESR) to chromosome 6q25.1 by FISH and a simple post-FISH banding technique. Genomics 1993;17:263–265.
127. Milanesi L, Vasconsuelo A, De Boland AR, Boland R. Expression and subcellular distribution of native estrogen receptor beta in murine C2C12 cells and skeletal muscle tissue. Steroids 2009;74:489–497.
128. Moore JT, Mckee DD, Slentz-Kesler K, Moore LB, Jones SA, Horne EL, Su JL, Kliewer SA, Lehmann JM, Willson TM. Cloning and characterization of human estrogen receptor beta isoforms. Biochem Biophys Res Commun 1998;247:75–78.
129. Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 1996;392:49–53.
130. Murali R, Soslow RA, Weigelt B. Classification of endometrial carcinoma: more than two types. Lancet Oncol 2014;15:e268–e278.
131. Mylonas I, Jeschke U, Shabani N, Kuhn C, Kriegel S, Kupka MS, Friese K. Normal and malignant human endometrium express immunohistochemically estrogen receptor alpha (ER-alpha), estrogen receptor beta (ER-beta) and progesterone receptor (PR). Anticancer Res 2005;25:1679–1686.
132. Mylonas I, Jeschke U, Shabani N, Kuhn C, Kunze S, Dian D, Friedl C, Kupka MS, Friese K. Steroid receptors ERalpha, ERbeta, PR-A and PR-B are differentially expressed in normal and atrophic human endometrium. Histol Histopathol 2007;22:169 – 176.
133. Narkar M, Kholkute S, Chitlange S, Nandedkar T. Expression of steroid hormone receptors, proliferation and apoptotic markers in primate endometrium. Mol Cell Endocrinol 2006;246:107–113.
134. Nayak NR, Brenner RM. Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J Clin Endocrinol Metab 2002; 87:1845–1855.
135. Negoita M, Mihailovici MS. Expression of hormonal receptors (alpha-estrogen, beta-estrogen, progesteron), Ki-67 and P53 in endometrium of tamoxifen treated breast cancer patients. Rev Med Chir Soc Med Nat Iasi 2011;115:834–838.
136. Nguyen HP, Sprung CN, Gargett CE. Differential expression of Wnt signaling molecules between pre- and postmenopausal endometrial epithelial cells suggests a population of putative epithelial stem/progenitor cells reside in the basalis layer. Endocrinology 2012;153:2870 – 2883.
137. Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA. Mechanisms of estrogen action. Physiol Rev 2001;81:535–1565.
138. Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor ofestrogen action in human. Nucleic Acids Res 1998;26:3505 – 3512.
139. O’neill PA, Davies MPA, Shaaban AM, Innes H, Torevell A, Sibson DR, Foster CS. Wild-type estrogen receptor beta (ERbeta1) mRNA and protein expression in tamoxifen-treated post-menopausal breast cancers. Br J Cancer 2004; 91:1694–1702.
140. Ordi J, Bergeron C, Hardisson D, Mccluggage WG, Hollema H, Felix A, Soslow RA, Oliva E, Tavassoli FA, Alvarado-Cabrero I et al. Reproducibility of current classifications of endometrial endometrioid glandular proliferations: further evidence supporting a simplified classification. Histopathology 2013;64:284–292.
141. Owings RA, Quick CM. Endometrial intraepithelial neoplasia. Arch Pathol Lab Med 2014; 138:484 – 491.
142. Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S. Human estrogen receptor beta binds DNA in a manner similar to and dimerizes with estrogen receptor alpha. J Biol Chem 1997;272:25832 – 25838.
143. Padykula HA, Coles LG, Mccracken JA, King NW, Longcope C, Kaiserman-Abramof I. A zonal pattern of cell proliferation and differentiation in the rhesus endometrium during the estrogen surge. Biol Reprod 1984;31:1103 – 1118.
144. Padykula HA, Coles LG, Okulicz WC, Rapaport SI, Mc Cracken JA, King NW Jr, Longcope C, Kaiserman-Abramof I. The basalis of the primate endometrium: a bifunctional germinal compartment. Biol Reprod 1989;40:681–690.
145. Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, Scanlan TS. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 1997;277:1508–1510.
146. Park JC, Lim SY, Jang TK, Bae JG, Kim JI, Rhee JH. Endometrial histology and predictable clinical factors for endometrial disease in women with polycystic ovary syndrome. Clin Exp Reprod Med 2011;38:42 – 46.
147. Paruthiyil S, Parmar H, Kerekatte V, Cunha GR, Firestone GL, Leitman DC. Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res 2004;64:423–428.
148. Pastore MB, Jobe SO, Ramadoss J, Magness RR. Estrogen receptor-alpha and estrogen receptor-beta in the uterine vascular endothelium during pregnancy: functional implications for regulating uterine blood flow. Semin Reprod Med 2012;30:46 – 61.
149. Paul M, Chotewa K, Mazurek U, Witek A, Wilezok T. Estrogen receptor bD6 (ERbD6) isoform in human endometrial hyperplasia and adenocarcinoma. Cancer Invest 2004; 22:211 – 218.
150. Pettersen BG. Osteopontin—an important downstream effector of S100A4-mediated invasion and metastasis. Int J Cancer 2011;129:780 – 790.
151. Prakansamut N, Sirayapiwat P, Triratanachat S. The percentages of endometrial hyperplasia and endometrial cancer among polycystic ovary syndrome (PCOS) patients presenting with abnormal menstrual pattern. J Med Assoc Thai 2014; 97:159–164.
152. Prianishnikov VA. A functional model of the structure of the epithelium of normal, hyperplastic and malignant human endometrium: a review. Gynecol Oncol 1978; 6:420–428.
153. Prossnitz ER, Barton M. Estrogen biology: new insights into GPER function and clinical opportunities. Mol Cell Endocrinol 2014;389:71–83.
154. Ramsey TL, Risinger KE, Jernigan SC, Mattingly KA, Klinge CM. Estrogen receptor beta isoforms exhibit differences in ligand-activated transcriptional activity in an estrogen response element sequence-dependent manner. Endocrinology 2004; 145:149–160.
155. Rees MC, Bicknell R. Angiogenesis in the endometrium. Angiogenesis 1998;2:29–35.
156. Rider V, Li X, Peterson G, Dawson J, Kimler BF, Abdou NI. Differential expression of estrogen receptors in women with systemic lupus erythematosus. J Rheumatol 2006;33:1093–1101.
157. Rizza P, Barone I, Zito D, Giordano F, Lanzino M, De Amicis F, Mauro L, Sisci D, Catalano S, Wright KD et al. Estrogen receptor beta as a novel target of androgen receptor action in breast cancer cell lines. Breast Cancer Res 2014;16:R21.
158. Robson A, Harris LK, Innes BA, Lash GE, Aljunaidy MM, Aplin JD, Baker PN, Robson SC, Bulmer JN. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J 2012;26:4876–4885.
159. Rody A, Holtrich U, Solbach C, Kourtis K, Von Minckwitz G, Engels K, Kissler S, Gatje R, Karn T, Kaufmann M. Methylation of estrogen receptor beta promoter correlates with loss of ER-beta expression in mammary carcinoma and is an early indication marker in premalignant lesions. Endocr Relat Cancer 2005; 12:903–916.
160. Saegusa M, Okayasu I. Changes in expression of estrogen receptors alpha and beta in relation to progesterone receptor and pS2 status in normal and malignant endometrium. Jpn J Cancer Res 2000;91:510–518.
161. Saha P, Saraswat G, Chakraborty P, Banerjee S, Pal BC, Kabir SN. Puerarin, a selective estrogen receptor modulator, disrupts pregnancy in rats at pre-implantation stage. Reproduction 2012;144:633–645.
162. Sakaguchi H, Fujimoto J, Aoki I, Toyoki H, Khatun S, Tamaya T. Expression of estrogen receptor alpha and beta in uterine endometrial and ovarian cancers. Eur J Cancer 2002;38(Suppl. 6):S74 – S75.
163. Sastre-Serra J, Nadal-Serrano M, Pons DG, Valle A, Garau I, Garcia-Bonafe M, Oliver J, Roca P. The oxidative stress in breast tumors of postmenopausal women is ERalpha/ ERbeta ratio dependent. Free Radic Biol Med 2013;61C:11 – 17.
164. Saxon LK, Turner CH. Estrogen receptor beta: the antimechanostat? Bone 2005; 36:185–192.
165. Setiawan VW, Pike MC, Karageorgi S, Deming SL, Anderson K, Bernstein L, Brinton LA, Cai H, Cerhan JR, Cozen W et al. Age at Last Birth in Relation to Risk of Endometrial Cancer: Pooled Analysis in the Epidemiology of Endometrial Cancer Consortium. USA: Oxford University Press, 2012, 269 – 278.
166. Shao R, Wang X, Feng Y, Billig H, Cao S. The elusive and controversial roles of estrogen and progesterone receptors in human endometriosis. Am J Transl Res 2014; 6:104 – 113.
167. Silvestri A, Fraser HM. Estrogen and progesterone receptors in the marmoset endometrium: changes during the ovulatory cycle, early pregnancy and after inhibition of vascular endothelial growth factor, GnRH or ovariectomy. Reproduction 2007;134:341–353.
168. Skrzypczak M, Bieche I, Szymczak S, Tozlu S, Lewandowski S, Girault I, Radwanska K, Szczylik C, Jakowicki JA, Lidereau R et al. Evaluation of mRNA expression of estrogen receptor beta and its isoforms in human normal and neoplastic endometrium. Int J Cancer 2004;110:783 – 787.
169. Slayden D, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol 2004;67:393–409.
170. Smith LH, Coats SR, Qin H, Petrie MS, Covington JW, Su M, Eren M, Vaughan DE. Differential and opposing regulation of PAI-1 promoter activity by estrogen receptor alpha and estrogen receptor beta in endothelial cells. Circ Res 2004; 95:269–275.
171. Šmuc T, Rižner TL. Aberrant pre-receptor regulation of estrogen and progesterone action in endometrial cancer. Mol Cell Endocrinol 2009;301:74–82.
172. Sourial S, Tempest N, Hapangama D. Theories on the pathogenesis of endometriosis. Int J Reprod Med 2014;2014:179515.
173. Spencer TE, Dunlap KA, Filant J. Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption. Mol Cell Endocrinol 2011; 354:34–53.
174. Takama F, Kanuma T, Wang D, Kagami I, Mizunuma H. Estrogen receptor b expression and depth of myometrial invasion in human endometrial cancer. Br J Cancer 2001; 84:545–549.
175. Tan NS, Frecer V, Lam TJ, Ding JL. Temperature dependence of estrogen binding: importance of a subzone in the ligand binding domain of a novel piscine estrogen receptor. Biochim Biophys Acta 1999;1452:103–120.
176. Taylor AH, Al-Azzawi F. Immunolocalisation of estrogen receptor beta in human tissues. J Mol Endocrinol 2000;24:145–155.
177. Thanapprapasr D, Thanapprapasr K. Molecular therapy as a future strategy in endometrial cancer. Asian Pac J Cancer Prev 2013;14:3419–3423.
178. Thomas C, Gustafsson J-Å. The different roles of ER subtypes in cancer biology and therapy. Nat Rev Cancer 2011;11:597–608.
179. Thornton JW. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci USA 2001;98:5671–5676.
180. Thornton JW, Need E, Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 2003;301:1714–1717.
181. Toft D, Gorski J. A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization. Proc Natl Acad Sci USA 1966;55:1574–1581.
182. Tokyol C, Aktepe F, Dilek FH, Sahin O, Arioz DT. Expression of cyclooxygenase-2 and matrix metalloproteinase-2 in adenomyosis and endometrial polyps and its correlation with angiogenesis. Int J Gynecol Pathol 2009;28:148 – 156.
183. Tremblay GB, Tremblay A, Labrie F, Giguere V. Dominant activity of activation function 1 (AF-1) and differential stoichiometric requirements for AF-1 and -2 in the estrogen receptor alpha–beta heterodimeric complex. Mol Cell Biol 1999; 19:1919–1927.
184. Trukhacheva E, Lin Z, Reierstad S, Cheng YH, Milad M, Bulun SE. Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J Clin Endocrinol Metab 2009;94:615–622.
185. Utsunomiya H, Suzuki T, Harada N, Ito K, Matsuzaki S, Konno R, Sato S, Yajima A, Sasano H. Analysis of estrogen receptor alpha and beta in endometrial carcinomas: correlation with ER beta and clinicopathologic findings in 45 cases. Int J Gynecol Pathol 2000;19:335–341.
186. Valentijn AJ, Palial K, Al-Lamee H, Tempest N, Drury J, Hapangama DK, Murray P, Von Zglinicki T, Saretzki G, Gargett CE. SSEA-1 isolates human endometrial basal glandular epithelial cells: phenotypic and functional characterization and implications in the pathogenesis of endometriosis. Hum Reprod 2013; 28:2695 – 2708.
187. Van Bogaert LJ. Clinicopathologic findings in endometrial polyps. Obstet Gynecol 1988; 71:771–773.
188. Vani S, Critchley HO, Fraser IS, Hickey M. Endometrial expression of steroid receptors in postmenopausal hormone replacement therapy users: relationship to bleeding patterns. J Fam Plann Reprod Health Care 2008;34:27 – 34.
189. Vassiliadou N, Bulmer JN. Quantitative analysis of T lymphocyte subsets in pregnant and nonpregnant human endometrium. Biol Reprod 1996;55:1017–1022.
190. Villavicencio A, Bacallao K, Avellaira C, Gabler F, Fuentes A, Vega M. Androgen and estrogen receptors and co-regulators levels in endometria from patients with polycystic ovarian syndrome with and without endometrial hyperplasia. Gynecol Oncol 2006;103:307–314.
191. ′-diindolylmethane. Endocrinology 2010;151:1662–1667.
192. Wada-Hiraike O, Hiraike H, Okinaga H, Imamov O, Barros RP, Morani A, Omoto Y, Warner M, Gustafsson JA. Role of estrogen receptor beta in uterine stroma and epithelium: insights from estrogen receptor beta2/2 mice. Proc Natl Acad Sci USA 2006;103:18350–18355.
193. Walter P, Green S, Greene G, Krust A, Bornert JM, Jeltsch JM, Staub A, Jensen E, Scrace G, Waterfield M et al. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci USA 1985;82:7889–7893.
194. Wang H, Isaksson E, Von Schoultz B, Cline JM, Sahlin L. The effect of long-term treatment with steroid hormones or tamoxifen on estrogen receptors (alpha and beta) in the endometrium of ovariectomized cynomolgus macaques. J Endocrinol 2002;175:673–681.
195. Wang A, Ji L, Shang W, Li M, Chen L, White RE, Han G. Expression of GPR30, ERalpha and ERbeta in endometrium during window of implantation in patients with polycystic ovary syndrome: a pilot study. Gynecol Endocrinol 2011; 27:251–255.
196. Weihua Z, Saji S, Mäkinen S, Cheng G, Jensen EV, Warner M, Gustafsson J-Å. Estrogen receptor (ER) b, a modulator of ERa in the uterus. Proc Natl Acad Sci USA 2000; 97:5936 – 5941.
197. Weiser MJ, Foradori CD, Handa RJ. Estrogen receptor beta in the brain: from form to function. Brain Res Rev 2008;57:309–320.
198. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS. Uterine epithelial estrogen receptor alpha is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci USA 2010; 107:19272–19277.
199. Witek A, Mazurek U, Paul M, Bierzynska-Macyszyn G, Wilczok T. Quantitative analysis of estrogen receptor-alpha and -beta and exon 5 splicing variant mRNA in endometrial hyperplasia in perimenopausal women. Folia Histochem Cytobiol 2001; 39:119–121.
200. Wu KH, Tobias ML, Thornton JW, Kelley DB. Estrogen receptors in Xenopus: duplicate genes, splice variants, and tissue-specific expression. Gen Comp Endocrinol 2003;133:38–49.
201. Wu J, Wang C, Li X, Song Y, Wang W, Li C, Hu J, Zhu Z, Li J, Zhang W et al. Identification, characterization and application of a G-quadruplex structured DNA aptamer against cancer biomarker protein anterior gradient homolog 2. PLoS One 2012;7:1–9.
202. Wu WF, Tan XJ, Dai YB, Krishnan V, Warner M, Gustafsson JA. Targeting estrogen receptor beta in microglia and T cells to treat experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2013;110:3543–3548.
203. Wynn RM. Cyclic and gestational changes. In: Wynn, Jollie WP (eds). The Human Endometrium. New York, USA: Plenum Publishing Corp, 1989, 289–331.
204. Xue Q, Lin Z, Cheng YH, Huang CC, Marsh E, Yin P, Milad MP, Confino E, Reierstad S, Innes J et al. Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod 2007; 77:681–687.
205. Yang JH, Wu MY, Chen CD, Chen MJ, Yang YS, Ho HN. Altered apoptosis and proliferation in endometrial stromal cells of women with adenomyosis. Hum Reprod(Oxford, England) 2007;22:945–952.
206. Yang YF, Liao YY, Peng NF, Li LQ, Xie SR, Wang RB. Prediction of coexistent carcinomas risks by subjective EIN diagnosis and comparison with WHO classification in endometrial hyperplasias. Pathol Res Pract 2012;208:708–712.
207. Yasui T, Matsui S, Tani A, Kunimi K, Yamamoto S, Irahara M. Androgen in postmenopausal women. J Med Investig 2012;59:12–27.
208. Ye H, Xu XR, Liu YK, Liu ZH, Zhao AZ. Study on the relationship betwwen eastrogen receptor beta and etiology of human endometrial polyps. Zhonghua Fu Chan Ke Za Zhi 2006;41:814 – 816.
209. Zang H, Sahlin L, Masironi B, Hirschberg AL. Effects of testosterone and estrogen treatment on the distribution of sex hormone receptors in the endometrium of postmenopausal women. Menopause (New York, NY) 2008;15:233–239.
210. Zannoni GF, Monterossi G, De Stefano I, Gargini A, Salerno MG, Farulla I, Travaglia D, Vellone VG, Scambia G, Gallo D. The expression ratios of estrogen receptor alpha (ERalpha) to estrogen receptor beta1 (ERbeta1) and ERalpha to ERbeta2 identify poor clinical outcome in endometrioid endometrial cancer. Hum Pathol 2013;44:1047 – 1054.
211. Zhang D, Trudeau VL. Integration of membrane and nuclear estrogen receptor signaling. Comp Biochem Physiol A Mol Integr Physiol 2006;144:306–315.
212. Zhao C, Dahlman-Wright K, Gustafsson JA. Estrogen receptor beta: an overview and update. Nucl Receptor Signal 2008;6:e003.
213. Zitao L, Kuokkanen S, Pal L. Steroid hormone receptor profile of premenopausal endometrial polyps. Reprod Sci 2010;17:377–383.