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Review Articles

Multiple receptors shape the estrogen response pathway and are critical considerations for the future of in vitro-based risk assessment efforts

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Pages 570-586 | Received 15 Jul 2016, Accepted 26 Jan 2017, Published online: 04 Jul 2017

References

  • Acconcia F, Ascenzi P, Fabozzi G, Visca P, Marino M. 2004. S-palmitoylation modulates human estrogen receptor-alpha functions. Biochem Biophys Res Commun. 316:878–883.
  • Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Ando S, Maggiolini M. 2007. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 67:1859–1866.
  • Arao Y, Hamilton KJ, Ray MK, Scott G, Mishina Y, Korach KS. 2011. Estrogen receptor α AF-2 mutation results in antagonist reversal and reveals tissue selective function of estrogen receptor modulators. Proc Natl Acad Sci. 2011108:14986–14991.
  • Autrup H, Barile FA, Blaauboer BJ, Degen GH, Dekant W, Dietrich D, Domingo JL, Gori GB, Greim H, Hengstler JG, et al. 2015. Principles of pharmacology and toxicology also govern effects of chemicals on the endocrine system. Toxicol Sci. 146:11–15.
  • Babiker FA, De Windt LJ, van Eickels M, Grohe C, Meyer R, Doevendans PA. 2002. Estrogenic hormone action in the heart: regulatory network and function. Cardiovasc Res. 53:709–719.
  • Barakat RR. 1995. The effect of tamoxifen on the endometrium. Oncology (Williston Park, N.Y.)). 9:129–134. Discussion 139–140, 142.
  • Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S. 1998. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol. 54:105–112.
  • Block GE, Jensen EV, Polley TZ. 1975. The prediction of hormonal dependency of mammary cancer. Ann Surg. 182:342–352.
  • Bologa CG, Revankar CM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA, et al. 2006. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol. 2:207–212.
  • Browne P, Judson RS, Casey WM, Kleinstreuer NC, Thomas RS. 2015. Screening chemicals for estrogen receptor bioactivity using a computational model. Environ Sci Technol. 49:8804–8814.
  • Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. 2001. Phosphatidylinositol 3-Kinase/AKT-mediated activation of estrogen receptor α: a new model For Anti-Estrogen Resistance. J Biol Chem. 276:9817–9824.
  • Carmeci C, Thompson DA, Ring HZ, Francke U, Weigel RJ. 1997. Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics. 45:607–617.
  • Castles CG, Oesterreich S, Hansen R, Fuqua SA. 1997. Auto-regulation of the estrogen receptor promoter. J Steroid Biochem Mol Biol. 62:155–163.
  • Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RG, Shaul PW. 2000. Estrogen receptor alpha and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ Res. 87:E44–E52.
  • Chang EC, Frasor J, Komm B, Katzenellenbogen BS. 2006. Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology. 147:4831–4842.
  • Charn TH, Liu ET, Chang EC, Lee YK, Katzenellenbogen JA, Katzenellenbogen BS. 2010. Genome-wide dynamics of chromatin binding of estrogen receptors alpha and beta: mutual restriction and competitive site selection. Mol Endocrinol (Baltimore, Md). 24:47–59.
  • Chen DB, Bird IM, Zheng J, Magness RR. 2004. Membrane estrogen receptor-dependent extracellular signal-regulated kinase pathway mediates acute activation of endothelial nitric oxide synthase by estrogen in uterine artery endothelial cells. Endocrinology. 145:113–125.
  • Cowley SM, Parker MG. 1999. A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol. 69:165–175.
  • Critchley HO, Henderson TA, Kelly RW, Scobie GS, Evans LR, Groome NP, Saunders PT. 2002. 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. 87:5265–5273.
  • deGraffenried LA, Hopp TA, Valente AJ, Clark RA, Fuqua SA. 2004. Regulation of the estrogen receptor alpha minimal promoter by Sp1, USF-1 and ERalpha. Breast Cancer Res Treat. 85:111–120.
  • Denger S, Reid G, Brand H, Kos M, Gannon F. 2001. Tissue-specific expression of human ERalpha and ERbeta in the male. Mol Cell Endocrinol. 178:155–160.
  • Diel P. 2002. Tissue-specific estrogenic response and molecular mechanisms. Toxicol Lett. 127:217–224.
  • Dixon RA. 2004. Phytoestrogens. Annu Rev Plant Biol. 55:225–261.
  • Edwards DP, Boonyaratanakornkit V. 2003. Rapid extranuclear signaling by the estrogen receptor (ER): MNAR couples ER and Src to the MAP kinase signaling pathway. Mol Interv. 3:12–15.
  • Ellison-Zelski SJ, Solodin NM, Alarid ET. 2009. Repression of ESR1 through actions of estrogen receptor alpha and Sin3A at the proximal promoter. Mol Cell Biol. 29:4949–4958.
  • Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjold M, Gustafsson JA. 1997. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 82:4258–4265.
  • Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. 2000. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol (Baltimore, Md). 14:1649–1660.
  • Filardo EJ, Quinn JA, Frackelton AR Jr, Bland KI. 2002. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol (Baltimore, Md). 16:70–84.
  • Flouriot G, Brand H, Denger S, Metivier R, Kos M, Reid G, Sonntag-Buck V, Gannon F. 2000. Identification of a new isoform of the human estrogen receptor-alpha (hER-α) that is encoded by distinct transcripts and that is able to repress hER-α activation function 1. EMBO J. 19:4688–4700.
  • Ford CH, Al-Bader M, Al-Ayadhi B, Francis I. 2011. Reassessment of estrogen receptor expression in human breast cancer cell lines. Anticancer Res. 31:521–527.
  • Fujimoto J, Hirose R, Sakaguchi H, Tamaya T. 1999. Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata. Mol Hum Reprod. 5:742–747.
  • Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, Chambon P. 1986. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 320:134–139..
  • Greene GL, Gilna P, Waterfield M, Baker A, Hort Y, Shine J. 1986. Sequence and expression of human estrogen receptor complementary DNA. Science. 231:1150–1154.
  • Grober OMV, Mutarelli M, Giurato G, Ravo M, Cicatiello L, De Filippo MR, Ferraro L, Nassa G, Papa MF, Paris O, 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. 12:36–36.
  • Gu Y, Chen T, Lopez E, Wu W, Wang X, Cao J, Teng L. 2014. The therapeutic target of estrogen receptor-alpha36 in estrogen-dependent tumors. J Transl Med. 12:16.
  • Habib AA, Chatterjee S, Park S-K, Ratan RR, Lefebvre S, Vartanian T. 2001. The epidermal growth factor receptor engages receptor interacting protein and nuclear factor-κB (NF-κB)-inducing kinase to activate NF-κB: identification of a novel receptor-tyrosine kinase signalosome. J Biol Chem. 276:8865–8874.
  • Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS. 2003. Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol. 206:13–22.
  • Hernandez-Sotomayor SM, Carpenter G. 1992. Epidermal growth factor receptor: elements of intracellular communication. J Membr Biol. 128:81–89.
  • Hervouet E, Cartron PF, Jouvenot M, Delage-Mourroux R. 2013. Epigenetic regulation of estrogen signaling in breast cancer. Epigenetics. 8:237–245.
  • Hiroi H, Inoue S, Watanabe T, Goto W, Orimo A, Momoeda M, Tsutsumi O, Taketani Y, Muramatsu M. 1999. Differential immunolocalization of estrogen receptor alpha and beta in rat ovary and uterus. J Mol Endocrinol. 22:37–44.
  • Irsik DL, Carmines PK, Lane PH. 2013. Classical estrogen receptors and ERα splice variants in the mouse. PLoS One. 8:e70926.
  • Jensen EV, Block GE, Smith S, Kyser K, DeSombre ER. 1971. Estrogen receptors and breast cancer response to adrenalectomy. Natl Cancer Inst Monogr. 34:55–70.
  • Jiang Y, Liu YE, Lu A, Gupta A, Goldberg ID, Liu J, Shi YE. 2003. Stimulation of estrogen receptor signaling by gamma synuclein. Cancer Res. 63:3899–3903.
  • Judson R, Richard A, Dix DJ, Houck K, Martin M, Kavlock R, Dellarco V, Henry T, Holderman T, Sayre P, et al. 2009. The toxicity data landscape for environmental chemicals. Environ Health Perspect. 117:685–695.
  • Kanda N, Watanabe S. 2003. 17beta-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J Invest Dermatol. 121:1500–1509.
  • Kang JS, Lee BJ, Ahn B, Kim DJ, Nam SY, Yun YW, Nam KT, Choi M, Kim HS, Jang DD, et al. 2003. Expression of estrogen receptor alpha and beta in the uterus and vagina of immature rats treated with 17-ethinyl estradiol. J Vet Med Sci/Jpn Soc Veterinary Sci. 65:1293–1297.
  • Kang L, Zhang X, Xie Y, Tu Y, Wang D, Liu Z, Wang Z-Y. 2010. Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling. Mol Endocrinol. 24:709–721.
  • Katzenellenbogen BS, Choi I, Delage-Mourroux R, Ediger TR, Martini PGV, Montano M, Sun J, Weis K, Katzenellenbogen JA. 2000. Molecular mechanisms of estrogen action: selective ligands and receptor pharmacology. J Steroid Biochem Mol Biol. 74:279–285.
  • Kelly MJ, Levin ER. 2001. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol Metab. 12:152–156.
  • Kim HP, Lee JY, Jeong JK, Bae SW, Lee HK, Jo I. 1999. Nongenomic stimulation of nitric oxide release by estrogen is mediated by estrogen receptor alpha localized in caveolae. Biochem Biophys Res Commun. 263:257–262.
  • Kim KH, Toomre D, Bender JR. 2011. Splice isoform estrogen receptors as integral transmembrane proteins. Mol Biol Cell. 22:4415–4423.
  • Kininis M, Kraus WL. 2008. A global view of transcriptional regulation by nuclear receptors: gene expression, factor localization, and DNA sequence analysis. Nucl Recept Signal. 6:e005.
  • Klinge CM. 2000. Estrogen receptor interaction with co-activators and co-repressors⋆. Steroids. 65:227–251.
  • Klinge CM, Riggs KA, Wickramasinghe NS, Emberts CG, McConda DB, Barry PN, Magnusen JE. 2010. Estrogen receptor alpha 46 is reduced in tamoxifen resistant breast cancer cells and re-expression inhibits cell proliferation and estrogen receptor alpha 66-regulated target gene transcription. Mol Cell Endocrinol. 323:268–276.
  • Knapp P, Chabowski A, Blachnio-Zabielska A, Walentowicz-Sadlecka M, Grabiec M, Knapp PA. 2013. Expression of estrogen receptors (alpha, beta), cyclooxygenase-2 and aromatase in normal endometrium and endometrioid cancer of uterus. Adv Med Sci. 58:96–103.
  • Kolkova Z, Noskova V, Ehinger A, Hansson S, Casslén B. 2010. G protein-coupled estrogen receptor 1 (GPER, GPR 30) in normal human endometrium and early pregnancy decidua. Mol Hum Reprod. 16:743–751.
  • Krewski D, Acosta D Jr, Andersen M, Anderson H, Bailar JC III, Boekelheide K, Brent R, Charnley G, Cheung VG, Green S Jr, et al. 2010. Toxicity testing in the 21st century: a vision and a strategy. J Toxicol Environ Health Part B Crit Rev. 13:51–138.
  • Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D. 1993. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology. 132:2279–2286.
  • Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. 1996. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA. 93:5925–5930.
  • Kushner PJ, Agard DA, Greene GL, Scanlan TS, Shiau AK, Uht RM, Webb P. 2000. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol. 74:311–317.
  • Lambertini E, Penolazzi L, Giordano S, Del Senno L, Piva R. 2003. Expression of the human oestrogen receptor-alpha gene is regulated by promoter F in MG-63 osteoblastic cells. Biochem J. 372:831–839.
  • Lee LM, Cao J, Deng H, Chen P, Gatalica Z, Wang ZY. 2008. ER-alpha36, a novel variant of ER-alpha, is expressed in ER-positive and-negative human breast carcinomas. Anticancer Res. 28:479–483.
  • Leung YK, Mak P, Hassan S, Ho SM. 2006. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc Natl Acad Sci USA. 103:13162–13167.
  • Levin ER. 2005. Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol (Baltimore, Md). 19:1951–1959.
  • Leygue E, Dotzlaw H, Lu B, Glor C, Watson PH, Murphy LC. 1998. Estrogen receptor beta: mine is longer than yours? J Clin Endocrinol Metab. 83:3754–3755.
  • Li L, Haynes MP, Bender JR. 2003. Plasma membrane localization and function of the estrogen receptor alpha variant (ER46) in human endothelial cells. Proc Natl Acad Sci USA. 100:4807–4812.
  • Lin AHY, Li RWS, Ho EYW, Leung GPH, Leung SWS, Vanhoutte PM, Man RYK. 2013. Differential ligand binding affinities of human estrogen receptor-α isoforms. PLoS One. 8:e63199.
  • Lin CY, Strom A, Li Kong S, Kietz S, Thomsen JS, Tee JB, Vega VB, Miller LD, Smeds J, Bergh J, 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:R25.
  • Lin SL, Yan LY, Liang XW, Wang ZB, Wang ZY, Qiao J, Schatten H, Sun QY. 2009. A novel variant of ER-alpha, ER-alpha36 mediates testosterone-stimulated ERK and Akt activation in endometrial cancer Hec1A cells. Reprod Biol Endocrinol: RB&E. 7:102.
  • Liu MM, Albanese C, Anderson CM, Hilty K, Webb P, Uht RM, Price RH Jr, Pestell RG, Kushner PJ. 2002. Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J Biol Chem. 277:24353–24360.
  • MacGregor JI, Jordan VC. 1998. Basic guide to the mechanisms of antiestrogen action. Pharmacol Rev. 50:151–196.
  • Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, Katzenellenbogen BS. 2008. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol Endocrinol (Baltimore, Md). 22:2116–2127.
  • Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Ando S. 2004. The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells.J Biol Chem. 279:27008–27016.
  • Martin LA, Farmer I, Johnston SR, Ali S, Dowsett M. 2005. Elevated ERK1/ERK2/estrogen receptor cross-talk enhances estrogen-mediated signaling during long-term estrogen deprivation. Endocr Relat Cancer. 12 Suppl 1:S75–S84.
  • McMullen PD, Bhattacharya S, Woods CG, Sun B, Yarborough K, Ross SM, Miller ME, McBride MT, LeCluyse EL, Clewell RA, Andersen ME. 2014. A map of the PPARalpha transcription regulatory network for primary human hepatocytes. Chem Biol Interact. 209:14–24.
  • Mermelstein PG, Micevych PE. 2008. Nervous system physiology regulated by membrane estrogen receptors. Rev Neurosci. 19:413–424.
  • Metivier R, Penot G, Carmouche RP, Hubner MR, Reid G, Denger S, Manu D, Brand H, Kos M, Benes V, Gannon F. 2004. Transcriptional complexes engaged by apo-estrogen receptor-alpha isoforms have divergent outcomes. EMBO J. 23:3653–3666.
  • Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M, Auricchio F. 1998. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 17:2008–2018.
  • Miller VM, Duckles SP. 2008. Vascular actions of estrogens: functional implications. Pharmacol Rev. 60:210–241.
  • Moore JT, McKee DD, Slentz-Kesler K, Moore LB, Jones SA, Horne EL, Su J-L, Kliewer SA, Lehmann JM, Willson TM. 1998. Cloning and characterization of human estrogen receptor β isoforms. Biochem Biophys Res Commun. 247:75–78.
  • Mukherjee R, Jow L, Noonan D, McDonnell DP. 1994. Human and rat peroxisome proliferator activated receptors (PPARs) demonstrate similar tissue distribution but different responsiveness to PPAR activators. J Steroid Biochem Mol Biol. 51:157–166.
  • Murphy AJ, Guyre PM, Wira CR, Pioli PA. 2009. Estradiol regulates expression of estrogen receptor ERalpha46 in human macrophages. PLoS One. 4:e5539.
  • Mylonas I, Jeschke U, Shabani N, Kuhn C, Balle A, Kriegel S, Kupka MS, Friese K. 2004. Immunohistochemical analysis of estrogen receptor alpha, estrogen receptor beta and progesterone receptor in normal human endometrium. Acta Histochem. 106:245–252.
  • Mylonas I, Jeschke U, Shabani N, Kuhn C, Kriegel S, Kupka MS, Friese K. 2005. Normal and malignant human endometrium express immunohistochemically Estrogen Receptor Alpha (ER-α), Estrogen Receptor Beta (ER-β) and Progesterone Receptor (PR). Anticancer Res. 25:1679–1686.
  • Nalbandian G, Kovats S. 2005. Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol Res. 31:91–106.
  • National Research Council (NRC). 2007. Toxicity testing in the 21st century: a vision and a strategy. Washington (DC): The National Academies Press.
  • National Toxicology, P. 2010. Multigenerational reproductive toxicology study of ethinyl estradiol (CAS No. 57-63-6) in Sprague–Dawley rats. Natl Toxicol Program Tech Rep Ser. 547:1–312.
  • Noteboom WD, Gorski J. 1965. Stereospecific binding of estrogens in the rat uterus. Arch Biochem Biophys. 111:559–568.
  • O'Lone R, Frith MC, Karlsson EK, Hansen U. 2004. Genomic targets of nuclear estrogen receptors. Mol Endocrinol (Baltimore, Md). 18:1859–1875.
  • Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M. 1998. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor ofestrogen action in human. Nucleic Acids Res. 26:3505–3512.
  • Omoto Y, Eguchi H, Yamamoto-Yamaguchi Y, Hayashi S. 2003. Estrogen receptor (ER) beta1 and ERbetacx/beta2 inhibit ERalpha function differently in breast cancer cell line MCF7. Oncogene. 22:5011–5020.
  • Paech K, Webb P, Kuiper GGJM, Nilsson S, Gustafsson J-Å, Kushner PJ, Scanlan TS. 1997. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 277:1508–1510.
  • Pedram A, Razandi M, Levin ER. 2006. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol (Baltimore, Md). 20:1996–2009.
  • Pendse SN, Maertens A, Rosenberg M, Roy D, Fasani RA, Vantangoli MM, Madnick SJ, Boekelheide K, Fornace AJ, Yager JD, et al. 2017. Information-dependent enrichment analysis reveals time-dependent transcriptional regulation of the estrogen pathway of toxicity. Arch Toxicol. 91:1749–1762.
  • Penot G, Le Peron C, Merot Y, Grimaud-Fanouillere E, Ferriere F, Boujrad N, Kah O, Saligaut C, Ducouret B, Metivier R, Flouriot G. 2005. The human estrogen receptor-alpha isoform hERalpha46 antagonizes the proliferative influence of hERalpha66 in MCF7 breast cancer cells. Endocrinology. 146:5474–5484.
  • Petersen DN, Tkalcevic GT, Koza-Taylor PH, Turi TG, Brown TA. 1998. Identification of estrogen receptor beta2, a functional variant of estrogen receptor beta expressed in normal rat tissues. Endocrinology. 139:1082–1092.
  • Pike ACW, Brzozowski AM, Hubbard RE, Bonn T, Thorsell A-G, Engström O, Ljunggren J, Gustafsson J-Å, Carlquist M. 1999. Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO J. 18:4608–4618.
  • Plante BJ, Lessey BA, Taylor RN, Wang W, Bagchi MK, Yuan L, Scotchie J, Fritz MA, Young SL. 2012. G protein-coupled estrogen receptor (GPER) expression in normal and abnormal endometrium. Reprod Sci (Thousand Oaks, Calif). 19:684–693.
  • Razandi M, Oh P, Pedram A, Schnitzer J, Levin ER. 2002. ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions. Mol Endocrinol (Baltimore, Md). 16:100–115.
  • Razandi M, Pedram A, Greene GL, Levin ER. 1999. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol (Baltimore, Md). 13:307–319.
  • Reif DM, Martin MT, Tan SW, Houck KA, Judson RS, Richard AM, Knudsen TB, Dix DJ, Kavlock RJ. 2010. Endocrine profiling and prioritization of environmental chemicals using ToxCast data. Environ Health Perspect. 118:1714–1720.
  • Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. 2005. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 307:1625–1630.
  • Revelli A, Massobrio M, Tesarik J. 1998. Nongenomic actions of steroid hormones in reproductive tissues. Endocr Rev. 19:3–17.
  • Rotroff DM, Dix DJ, Houck KA, Knudsen TB, Martin MT, McLaurin KW, Reif DM, Crofton KM, Singh AV, Xia M, et al. 2013. Using in vitro high throughput screening assays to identify potential endocrine-disrupting chemicals. Environ Health Perspect. 121:7–14.
  • Rotroff DM, Martin MT, Dix DJ, Filer DL, Houck KA, Knudsen TB, Sipes NS, Reif DM, Xia M, Huang R, Judson RS. 2014. Predictive endocrine testing in the 21st century using in vitro assays of estrogen receptor signaling responses. Environ Sci Technol. 48:8706–8716.
  • Sabbah M, Courilleau D, Mester J, Redeuilh G. 1999. Estrogen induction of the cyclin D1 promoter: involvement of a cAMP response-like element. Proc Natl Acad Sci. 96:11217–11222.
  • Safe SH, Pallaroni L, Yoon K, Gaido K, Ross S, Saville B, McDonnellc D. 2001. Toxicology of environmental estrogens. Reprod Fertil Dev. 13:307–315.
  • Sanchez AM, Flamini MI, Baldacci C, Goglia L, Genazzani AR, Simoncini T. 2010. Estrogen receptor-alpha promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Mol Endocrinol (Baltimore, Md). 24:2114–2125.
  • Saville B, Wormke M, Wang F, Nguyen T, Enmark E, Kuiper G, Gustafsson J-Å, Safe S. 2000. Ligand-, ell-, and estrogen receptor subtype (α/β)-dependent activation at GC-rich (Sp1) promoter elements. J Biol Chem. 275:5379–5387.
  • Schultz JR, Petz LN, Nardulli AM. 2003. Estrogen receptor alpha and Sp1 regulate progesterone receptor gene expression. Mol Cell Endocrinol. 201:165–175.
  • Shao R, Egecioglu E, Weijdegård B, Kopchick JJ, Fernandez-Rodriguez J, Andersson N, Billig H. 2007. Dynamic regulation of estrogen receptor-α isoform expression in the mouse fallopian tube: mechanistic insight into estrogen-dependent production and secretion of insulin-like growth factors. Am J Physiol Endocrinol Metab. 293:E1430–E1442.
  • Shen C, Huang Y, Liu Y, Wang G, Zhao Y, Wang Z, Teng M, Wang Y, Flockhart DA, Skaar TC, et al. 2011. A modulated empirical Bayes model for identifying topological and temporal estrogen receptor alpha regulatory networks in breast cancer. BMC Syst Biol. 5:67.
  • Sluyser M, Van Nie R. 1974. Estrogen receptor content and hormone-responsive growth of mouse mammary tumors. Cancer Res. 34:3253–3257.
  • Smith K, LeJeune S, Harris AH, Rees MC. 1991. Epidermal growth factor receptor in human uterine tissues. Hum Reprod (Oxford, England). 6:619–622.
  • Soto AM, Justicia H, Wray JW, Sonnenschein C. 1991. p-Nonyl-phenol: an estrogenic xenobiotic released from “modified” polystyrene. Environ Health Perspect. 92:167–173.
  • Swedenborg E, Pongratz I. 2010. AhR and ARNT modulate ER signaling. Toxicology. 268:132–138.
  • Tamrazi A, Carlson KE, Daniels JR, Hurth KM, Katzenellenbogen JA. 2002. Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol Endocrinol (Baltimore, Md). 16:2706–2719.
  • Tapiero H, Nguyen Ba G, Tew KD. 2002. Estrogens and environmental estrogens. Biomed Pharmacother. 56:36–44.
  • Thomas P, Pang Y, Filardo EJ, Dong J. 2005. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology. 146:624–632.
  • Toft D, Gorski J. 1966. A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization. Proc Natl Acad Sci USA. 55:1574–1581.
  • Toft D, Shyamala G, Gorski J. 1967. A receptor molecule for estrogens: studies using a cell-free system. Proc Natl Acad Sci USA. 57:1740–1743.
  • Tong JS, Zhang QH, Wang ZB, Li S, Yang CR, Fu XQ, Hou Y, Wang ZY, Sheng J, Sun QY. 2010. ER-alpha36, a novel variant of ER-alpha, mediates estrogen-stimulated proliferation of endometrial carcinoma cells via the PKCdelta/ERK pathway. PLoS One. 5:e15408.
  • Tu BB, Lin SL, Yan LY, Wang ZY, Sun QY, Qiao J. 2011. ER-alpha36, a novel variant of estrogen receptor alpha, is involved in EGFR-related carcinogenesis in endometrial cancer. Am J Obstet Gynecol. 205:227e221–226.
  • Vaananen HK, Harkonen PL. 1996. Estrogen and bone metabolism. Maturitas. 23 Suppl:S65–S69.
  • van der Meer DL, Degenhardt T, Vaisanen S, de Groot PJ, Heinaniemi M, de Vries SC, Muller M, Carlberg C, Kersten S. 2010. Profiling of promoter occupancy by PPARalpha in human hepatoma cells via ChIP-chip analysis. Nucleic Acids Res. 38:2839–2850.
  • Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, et al. 2012. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 33:378–455.
  • Villalobo A, Ruano M, Palomo-Jiménez P, Li H, Martín-Nieto J. 2000. The epidermal growth factor receptor and the calcium signal. In: Calcium: the molecular basis of calcium action in biology and medicine. Netherlands: Springer; p. 287–303.
  • Wallacides A, Chesnel A, Ajj H, Chillet M, Flament S, Dumond H. 2012. Estrogens promote proliferation of the seminoma-like TCam-2 cell line through a GPER-dependent ERα36 induction. Mol Cell Endocrinol. 350:61–71.
  • Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, Deuel TF. 2005. Identification, cloning, and expression of human estrogen receptor-α36, a novel variant of human estrogen receptor-α66. Biochem Biophys Res Commun. 336:1023–1027.
  • Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, Deuel TF. 2006. A variant of estrogen receptor-{alpha}, hER-{alpha}36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signaling. Proc Natl Acad Sci USA. 103:9063–9068.
  • Yun SP, Ryu JM, Kim MO, Park JH, Han HJ. 2012. Rapid actions of plasma membrane estrogen receptors regulate motility of mouse embryonic stem cells through a profilin-1/cofilin-1-directed kinase signaling pathway. Mol Endocrinol (Baltimore, Md). 26:1291–1303.
  • Zhang H, McElrath T, Tong W, Pollard JW. 2005. The molecular basis of tamoxifen induction of mouse uterine epithelial cell proliferation. J Endocrinol. 184:129–140.
  • Zhang Q, Bhattacharya S, Conolly RB, Clewell HJ, Kaminski NE, Andersen ME. 2014. Molecular signaling network motifs provide a mechanistic basis for cellular threshold responses. Environ Health Perspect. 122:1261–1270.
  • Zhang XT, Kang LG, Ding L, Vranic S, Gatalica Z, Wang ZY. 2011. A positive feedback loop of ER-α36/EGFR promotes malignant growth of ER-negative breast cancer cells. Oncogene. 30:770–780.
  • Zhang Z, Maier B, Santen RJ, Song RX. 2002. Membrane association of estrogen receptor alpha mediates estrogen effect on MAPK activation. Biochem Biophys Res Commun. 294:926–933.
  • Zhao C, Gao H, Liu Y, Papoutsi Z, Jaffrey S, Gustafsson JA, Dahlman-Wright K. 2010. Genome-wide mapping of estrogen receptor-beta-binding regions reveals extensive cross-talk with transcription factor activator protein-1. Cancer Res. 70:5174–5183.
  • Zhao C, Putnik M, Gustafsson JA, Dahlman-Wright K. 2009. Microarray analysis of altered gene expression in ERbeta-overexpressing HEK293 cells. Endocrine. 36:224–232.
  • Zhao C, Dahlman-Wright K, Gustafsson JA. 2010. Estrogen signaling via estrogen receptor {beta}. J Biol Chem. 285:39575–39579.
  • Zheng Y, Zhang J, Xu ZZ, Sheng JM, Zhang XC, Wang HH, Teng XD, Liu XJ, Cao J, Teng LS. 2010. Quantitative profiles of the mRNAs of ER-alpha and its novel variant ER-alpha36 in breast cancers and matched normal tissues. J Zhejiang Univ Sci B. 11:144–150.
  • Zou Y, Ding L, Coleman M, Wang Z. 2009. Estrogen receptor-alpha (ER-alpha) suppresses expression of its variant ER-alpha 36. FEBS Lett. 583:1368–1374.