Molecular Characterization of Estrogen Receptors 1, 2a, and 2b and Their Tissue and Ontogenic Expression Profiles in Fathead Minnow (Pimephales promelas)1

Abstract There are two estrogen receptor (ER) subtypes in fish, Esr1 and Esr2 (formerly ERα and ERβ), and in some species the Esr2 subtype has two forms, Esr2b (formerly ERβ1) and Esr2a (formerly ERβ2 or ERγ). There is little information, however, on the different characteristics and functional significance of the two receptor subtypes in fish, and this is especially relevant for understanding the disruption of ER signaling by chemicals with estrogenic activity. In this study, the full-length cDNAs for esr1 (3167 base pairs [bp]) and esr2b (2318 bp), and a partial-length (267 bp) cDNA for esr2a, were cloned and characterized in fathead minnow (fhm; Pimephales promelas), and their patterns of expression established during development and in adults. Real-time polymerase chain reaction revealed some clear distinctions in the ontogenic and tissue expression of fhm esr1, esr2b, and esr2a, suggesting different functions for each ER subtype. Fhm ERs were expressed in brain, pituitary, liver, gonad, intestine, and gill of male and female fish, esr2b and esr2a were also expressed in muscle. Fhm esr1 and esr2b were expressed predominantly in the liver, whereas fhm esr2a was expressed predominantly in intestine and was lowest expressed in liver. Responses of the different hepatic ERs in male fathead minnow exposed to 100 ng estradiol/L differed, with a significant induction (5-fold) of fhm esr1 but no effect on esr2b or esr2a expression, suggesting different mechanisms of regulation for the different ERs. The detailed characterization of ERs in fathead minnow provides the foundation for understanding the molecular basis of estrogenic disruption in fish.

[1]  F. Pakdel,et al.  In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout , 1991, Molecular and Cellular Endocrinology.

[2]  M. Lazar,et al.  The CoRNR motif controls the recruitment of corepressors by nuclear hormone receptors , 1999, Nature.

[3]  K. Yamauchi,et al.  Molecular cloning and characterization of Japanese eel estrogen receptor cDNA , 1996, Molecular and Cellular Endocrinology.

[4]  P. Argos,et al.  Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A , 1986, Nature.

[5]  J. Jameson,et al.  Estrogen Receptor Binding to DNA Is Not Required for Its Activity through the Nonclassical AP1 Pathway* , 2001, The Journal of Biological Chemistry.

[6]  E. Simpson,et al.  Estrogen and spermatogenesis. , 2001, Endocrine reviews.

[7]  K. Dong,et al.  cDNA cloning and expression of a novel estrogen receptor beta-subtype in goldfish (Carassius auratus). , 2000, Biochimica et biophysica acta.

[8]  L. Densmore,et al.  Cloning, in vitro expression, and novel phylogenetic classification of a channel catfish estrogen receptor. , 1999, General and comparative endocrinology.

[9]  J. Sumpter.  Feminized responses in fish to environmental estrogens. , 1995, Toxicology letters.

[10]  S. Cowley,et al.  A comparison of transcriptional activation by ER alpha and ER beta. , 1999, The Journal of steroid biochemistry and molecular biology.

[11]  P. Shughrue,et al.  Comparative distribution of estrogen receptor‐α and ‐β mRNA in the rat central nervous system , 1997, The Journal of comparative neurology.

[12]  S. Inoue,et al.  Expression and Cellular Localization of Estrogen Receptors α and β in the Human Fetus1 , 2001 .

[13]  S. Cowley,et al.  A comparison of transcriptional activation by ERα and ERβ , 1999, The Journal of Steroid Biochemistry and Molecular Biology.

[14]  J. Sumpter,et al.  Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. , 1995, Environmental health perspectives.

[15]  K. Davis,et al.  Localization of Estrogen Receptor α and β RNA in Germinal and Nongerminal Epithelia of the Channel Catfish Testis , 2001 .

[16]  N. Copeland,et al.  Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. , 1997, Molecular endocrinology.

[17]  A. D. Vethaak,et al.  A Novel in Vivo Bioassay for (Xeno-)estrogens Using Transgenic Zebrafish , 2000 .

[18]  F. Pakdel,et al.  The analysis of chimeric human/rainbow trout estrogen receptors reveals amino acid residues outside of P- and D-boxes important for the transactivation function. , 2000, Nucleic acids research.

[19]  R. Lesage,et al.  Androgen and estrogen binding in rat skeletal and perineal muscles. , 1976, Canadian journal of biochemistry.

[20]  J. Corton,et al.  Interaction of Estrogenic Chemicals and Phytoestrogens with Estrogen Receptor β. , 1998, Endocrinology.

[21]  J. Sumpter,et al.  Endocrine disruption in wildlife: a critical review of the evidence. , 1998, Critical reviews in toxicology.

[22]  K. Skjoedt,et al.  Molecular cloning, characterisation, and tissue distribution of oestrogen receptor alpha in eelpout (Zoarces viviparus). , 2003, General and comparative endocrinology.

[23]  A. Elizur,et al.  Regulation of fish gonadotropins. , 2003, International review of cytology.

[24]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[25]  J. Sumpter,et al.  Differential Effects of Xenoestrogens on Coactivator Recruitment by Estrogen Receptor (ER) α and ERβ* , 2000, The Journal of Biological Chemistry.

[26]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[27]  H. Everaus,et al.  Nongenomic effects of 17β-estradiol—diversity of membrane binding sites , 2004, The Journal of Steroid Biochemistry and Molecular Biology.

[28]  D. B. Montagnani,et al.  Environmentally Persistent Oestrogen‐like Substances in UK River Systems , 1996 .

[29]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[30]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[31]  K. Korach,et al.  Postnatal Sex Reversal of the Ovaries in Mice Lacking Estrogen Receptors α and β , 1999 .

[32]  Alec G. Maule,et al.  Interaction of xenobiotics with estrogen receptors α and β and a putative plasma sex hormone-binding globulin from channel catfish (Ictalurus punctatus) , 2004 .

[33]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[34]  I. Merchenthaler,et al.  Evidence for the colocalization of estrogen receptor-beta mRNA and estrogen receptor-alpha immunoreactivity in neurons of the rat forebrain. , 1998, Endocrinology.

[35]  B. Katzenellenbogen,et al.  Identification of Amino Acids in the Hormone Binding Domain of the Human Estrogen Receptor Important in Estrogen Binding* , 1996, The Journal of Biological Chemistry.

[36]  J. Polman,et al.  ER beta: identification and characterization of a novel human estrogen receptor. , 1996, FEBS letters.

[37]  Y. Valotaire,et al.  Caractérisation de récepteurs spécifiques à l'œstradiol, induction de la vitellogénine et de son mRNA dans le foie de truite arc-en-ciel (Salmo gairdnerii) , 1985 .

[38]  Y. Valotaire,et al.  [Characterization of specific receptors for estradiol, induction of vitellogenin and its mRNA in the liver of rainbow trout (Salmo gairdnerii)]. , 1985, Biochimie.

[39]  F. Pakdel,et al.  Identification and estrogen induction of two estrogen receptors (ER) messenger ribonucleic acids in the rainbow trout liver: sequence homology with other ERs. , 1989, Molecular endocrinology.

[40]  G. Chalepakis,et al.  Gene regulation by steroid hormones. , 1989, Cell.

[41]  G. Sweeney,et al.  Cloning of the Atlantic salmon (Salmo salar) estrogen receptor-alpha gene. , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[42]  R. Sharpe.  Reproductive biology: Do males rely on female hormones? , 1997, Nature.

[43]  J. Richards.  Hormonal control of gene expression in the ovary. , 1994, Endocrine reviews.

[44]  J. Gustafsson,et al.  Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. , 1998, Molecular pharmacology.

[45]  K. Korach,et al.  The Multifaceted Mechanisms of Estradiol and Estrogen Receptor Signaling* , 2001, The Journal of Biological Chemistry.

[46]  G. Stancel,et al.  Interaction of human estrogen receptors α and β with the same naturally occurring estrogen response elements , 1999 .

[47]  K. Korach,et al.  Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[48]  K. Pau,et al.  Putative estrogen receptor β and α mRNA expression in male and female rhesus macaques , 1998, Molecular and Cellular Endocrinology.

[49]  D. Leitman,et al.  Estrogen Receptor β-Selective Transcriptional Activity and Recruitment of Coregulators by Phytoestrogens* , 2001, The Journal of Biological Chemistry.

[50]  G. Martínez‐Rodríguez,et al.  Cloning, characterisation, and expression of three oestrogen receptors (ERα, ERβ1 and ERβ2) in the European sea bass, Dicentrarchus labrax , 2004, Molecular and Cellular Endocrinology.

[51]  X. Xu,et al.  The presence of functional estrogen receptors in intestinal epithelial cells. , 1993, Endocrinology.

[52]  K. Aida,et al.  Effects of sex steroids on the smoltification of masu salmon, Oncorhynchus masou. , 1987, General and comparative endocrinology.

[53]  T. Zacharewski,et al.  Reciprocal mutagenesis between human α(L349, M528) and rainbow trout (M317, I496) estrogen receptor residues demonstrates their importance in ligand binding and gene expression at different temperatures , 2001, Molecular and Cellular Endocrinology.

[54]  S. Fawell,et al.  Identification of residues in the estrogen receptor that confer differential sensitivity to estrogen and hydroxytamoxifen. , 1993, Molecular endocrinology.

[55]  P Argos,et al.  The chicken oestrogen receptor sequence: homology with v‐erbA and the human oestrogen and glucocorticoid receptors. , 1986, The EMBO journal.

[56]  S. Madsen,et al.  Effects of 17β-estradiol and 4-nonylphenol on smoltification and vitellogenesis in Atlantic salmon (Salmo salar) , 1997, Fish Physiology and Biochemistry.

[57]  M. Hawkins,et al.  The unusual binding properties of the third distinct teleost estrogen receptor subtype ERbetaa are accompanied by highly conserved amino acid changes in the ligand binding domain. , 2004, Endocrinology.

[58]  S. Miwa,et al.  Inhibitory effects of 17α-methyltestosterone and estradiol-17β on smoltification of sterilized amago salmon (Oncorhynchus rhodurus) , 1985 .

[59]  L. Cohen,et al.  Specific cytosol binding of diethylstilbestrol in rat skeletal muscle , 1982, Steroids.

[60]  B. O’Malley,et al.  Molecular mechanisms of action of steroid/thyroid receptor superfamily members. , 1994, Annual review of biochemistry.

[61]  O. Kah,et al.  Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ER (cid:1) , ER (cid:2) 1 and ER (cid:2) 2 , 2004 .

[62]  J. Thornton,et al.  Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[63]  H. Habibi,et al.  Molecular cloning of estrogen receptor α and expression pattern of estrogen receptor subtypes in male and female goldfish , 2003, Molecular and Cellular Endocrinology.

[64]  E. Verdu,et al.  Modulatory effects of estrogen in two murine models of experimental colitis. , 2002, American journal of physiology. Gastrointestinal and liver physiology.

[65]  S. Inoue,et al.  Expression and cellular localization of estrogen receptors alpha and beta in the human fetus. , 2001, The Journal of clinical endocrinology and metabolism.

[66]  Gerald T Ankley,et al.  Cloning and in vitro expression and characterization of the androgen receptor and isolation of estrogen receptor alpha from the fathead Minnow (Pimephales promelas). , 2004, Environmental science & technology.

[67]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[68]  I. Merchenthaler,et al.  Evidence of the Colocalization of Estrogen Receptor-β mRNA and Estrogen Receptor-α Immunoreactivity in Neurons of the Rat Forebrain. , 1998, Endocrinology.

[69]  D. Langenau,et al.  Phylogenetic sequence analysis, recombinant expression, and tissue distribution of a channel catfish estrogen receptor beta. , 2000, General and comparative endocrinology.

[70]  G. Callard,et al.  Molecular cloning of an estrogen receptor beta subtype from the goldfish, Carassius auratus. , 1999, General and comparative endocrinology.

[71]  P. Thomas,et al.  Effects of Estrogens and Xenoestrogens on Androgen Production by Atlantic Croaker Testes In Vitro: Evidence for a Nongenomic Action Mediated by an Estrogen Membrane Receptor1 , 2000, Biology of reproduction.

[72]  J. Gustafsson,et al.  Differential Recruitment of the Mammalian Mediator Subunit TRAP220 by Estrogen Receptors ERα and ERβ* , 2001, The Journal of Biological Chemistry.

[73]  Chunfa Wu,et al.  Novel transcripts of the estrogen receptor α gene in channel catfish , 2000 .

[74]  J. Gustafsson,et al.  Cloning of a novel receptor expressed in rat prostate and ovary. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  J. Corton,et al.  Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. , 1998, Endocrinology.

[76]  E. Jensen,et al.  Estrogen receptor (ER) , a modulator of ER in the uterus , 2000 .

[77]  B. Katzenellenbogen,et al.  Novel Ligands that Function as Selective Estrogens or Antiestrogens for Estrogen Receptor-α or Estrogen Receptor-β. , 1999, Endocrinology.

[78]  J. Gustafsson,et al.  Estrogen receptor (ER) b, a modulator of ERa in the uterus , 2000 .

[79]  C. Tyler,et al.  An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin , 1999 .

[80]  D. Agard,et al.  Estrogen receptor pathways to AP-1 , 2000, The Journal of Steroid Biochemistry and Molecular Biology.

[81]  J. Gustafsson,et al.  Structural determinants of DNA-binding specificity by steroid receptors. , 1995, Molecular endocrinology.

[82]  Carl T. Wittwer,et al.  Rapid Cycle Real-Time PCR — Methods and Applications , 2002, Springer Berlin Heidelberg.

[83]  J. Sumpter,et al.  Toxicology of Aquatic Pollution: Oestrogenic substances in the aquatic environment and their potential impact on animals, particularly fish , 1996 .

[84]  R. Evans,et al.  The steroid and thyroid hormone receptor superfamily. , 1988, Science.

[85]  R. J. Smith.  Seasonal changes in the histology of the gonads and dorsal skin of the fathead minnow, Pimephales promelas , 1978 .

[86]  J. Raelson,et al.  Up-regulation of estrogen receptor mRNA and estrogen receptor activity by estradiol in liver of rainbow trout and other teleostean fish. , 1996, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[87]  J. Lees,et al.  Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors. , 1992, The EMBO journal.

[88]  V. Laudet,et al.  Molecular Characterization of Three Estrogen Receptor Forms in Zebrafish: Binding Characteristics, Transactivation Properties, and Tissue Distributions1 , 2002, Biology of reproduction.

[89]  J. Gustafsson,et al.  Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. , 1997, Science.

[90]  S. Fawell,et al.  Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor , 1990, Cell.

[91]  K. Korach,et al.  Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements. , 2002, Molecular endocrinology.

[92]  S. Shany,et al.  The protective effect of estrogen against chemically induced murine colon carcinogenesis is associated with decreased CpG island methylation and increased mRNA and protein expression of the colonic vitamin D receptor. , 1999, Oncology research.

[93]  T. Iwanaga,et al.  Developmental changes of the oestrogen receptor-alpha and -beta mRNAs in the female reproductive organ of the rat--an analysis by in situ hybridization. , 2000, The Journal of endocrinology.

[94]  J. Schwabe,et al.  Solution structure of the DNA-binding domain of the oestrogen receptor. , 1990, Nature.

[95]  T. Runnalls,et al.  Ontogeny of gonadal sex development relative to growth in fathead minnow , 2004 .

[96]  K. Korach,et al.  Analysis of the Molecular Mechanisms of Human Estrogen Receptors α and β Reveals Differential Specificity in Target Promoter Regulation by Xenoestrogens* , 2002, The Journal of Biological Chemistry.

[97]  K. Korach.  Insights from the study of animals lacking functional estrogen receptor. , 1994, Science.

[98]  G. Martínez‐Rodríguez,et al.  Cloning, characterisation, and expression of three oestrogen receptors (ERalpha, ERbeta1 and ERbeta2) in the European sea bass, Dicentrarchus labrax. , 2004, Molecular and cellular endocrinology.

[99]  H. Habibi,et al.  Molecular characterization of LH-β and FSH-β subunits and their regulation by estrogen in the goldfish pituitary , 2002, Molecular and Cellular Endocrinology.

[100]  E. Dahlberg.  Characterization of the cytosolic estrogen receptor in rat skeletal muscle. , 1982, Biochimica et biophysica acta.

[101]  J. Gustafsson,et al.  Generation and reproductive phenotypes of mice lacking estrogen receptor beta. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[102]  D. Power,et al.  Two estrogen receptors expressed in the teleost fish, Sparus aurata: cDNA cloning, characterization and tissue distribution. , 2000, The Journal of endocrinology.

[103]  I. Merchenthaler,et al.  Comparative distribution of estrogen receptor-alpha (ER-alpha) and beta (ER-beta) mRNA in the rat pituitary, gonad, and reproductive tract. , 1998, Steroids.

[104]  J. Bogerd,et al.  Cloning and expression of a functional estrogen receptor-alpha from African catfish (Clarias gariepinus) pituitary. , 2003, Journal of molecular endocrinology.

[105]  Y. Le Dréan,et al.  Regulation of gene expression and biological activity of rainbow trout estrogen receptor , 1997, Fish Physiology and Biochemistry.

[106]  I. Merchenthaler,et al.  Comparative distribution of estrogen receptor-α (ER-α) and β (ER-β) mRNA in the rat pituitary, gonad, and reproductive tract , 1998, Steroids.

[107]  S. Fawell,et al.  A 22-amino-acid peptide restores DNA-binding activity to dimerization-defective mutants of the estrogen receptor , 1990, Molecular and cellular biology.

[108]  S. Masushige,et al.  Tissue-specific response of estrogen receptor gene expression to estrogen in chick. , 1992, Biochemical and biophysical research communications.

[109]  M. Wilson,et al.  Estrogen Receptor- b Messenger Ribonucleic Acid Expression in the Pituitary Gland* , 1998 .

[110]  K. Yu,et al.  cDNA cloning and expression of a novel estrogen receptor β-subtype in goldfish (Carassius auratus) , 2000 .

[111]  R. Métivier,et al.  Two Estrogen Receptor (ER) Isoforms with Different Estrogen Dependencies Are Generated from the Trout ER Gene1. , 2000, Endocrinology.

[112]  J. Gustafsson,et al.  Differential Response of Estrogen Receptor a and Estrogen Receptor b to Partial Estrogen Agonists/Antagonists , 1998 .

[113]  J. Gustafsson,et al.  The Estrogen Receptor β Subtype: A Novel Mediator of Estrogen Action in Neuroendocrine Systems , 1998, Frontiers in Neuroendocrinology.

[114]  L. Andersson,et al.  A role for estrogen receptor β in the regulation of growth of the ventral prostate , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[115]  K. Davis,et al.  Localization of estrogen receptor alpha and beta RNA in germinal and nongerminal epithelia of the channel catfish testis. , 2001, General and comparative endocrinology.

[116]  S. Petersen,et al.  Direct and Indirect Regulation of Gonadotropin-Releasing Hormone Neurons by Estradiol1 , 2003, Biology of reproduction.

[117]  J. Gustafsson,et al.  Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. , 2000, The Journal of biological chemistry.

[118]  M Carlquist,et al.  Structure of the ligand‐binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist , 1999, The EMBO journal.

[119]  J. Sumpter,et al.  Wild Intersex Roach (Rutilus rutilus) Have Reduced Fertility1 , 2002, Biology of reproduction.

[120]  K. Korach,et al.  Estrogen receptor null mice: what have we learned and where will they lead us? , 1999, Endocrine reviews.

[121]  J. Gustafsson,et al.  Expression of estrogen receptor alpha and beta during mouse embryogenesis , 1999, Mechanisms of Development.

[122]  K. Korach,et al.  Reproductive phenotypes in the estrogen receptor-alpha knockout mouse. , 1999, Annales d'endocrinologie.

[123]  S. Madsen,et al.  17-β estradiol and 4-nonylphenol delay smolt development and downstream migration in Atlantic salmon, Salmo salar , 2004 .

[124]  K. Grandien,et al.  Printed in U.S.A. Copyright © 1997 by The Endocrine Society Comparison of the Ligand Binding Specificity and Transcript Tissue Distribution of Estrogen Receptors � and � , 2022 .

[125]  E. Calabrese,et al.  Detection of an estrogen receptor in two nematode species and inhibition of binding and development by environmental chemicals. , 2000, Ecotoxicology and environmental safety.

[126]  J. E. Rall,et al.  Steroid/thyroid hormone receptor genes in Caenorhabditis elegans. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[127]  T. Sabo-Attwood,et al.  Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol , 2004, Molecular and Cellular Endocrinology.

[128]  R. Sharpe.  The Roles of Oestrogen in the Male , 1998, Trends in Endocrinology & Metabolism.

[129]  J. Gustafsson,et al.  Differential recruitment of the mammalian mediator subunit TRAP220 by estrogen receptors ERalpha and ERbeta. , 2001, The Journal of biological chemistry.

[130]  J. Dorrington,et al.  Interactions between FSH, estradiol-17 beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. , 1993, The Journal of steroid biochemistry and molecular biology.

[131]  R. Rasmussen.  Quantification on the LightCycler , 2001 .

[132]  J. Kim,et al.  Regulation of Xenopus laevis estrogen receptor gene expression is mediated by an estrogen response element in the protein coding region. , 1995, DNA and cell biology.

[133]  D. Herbert,et al.  Evidence for estrogen receptor-linked calcium transport in the intestine. , 1993, Bone and mineral.

[134]  John W. R. Schwabe,et al.  The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: How receptors discriminate between their response elements , 1993, Cell.

[135]  J. Gustafsson,et al.  Transcriptional targets shared by estrogen receptor- related receptors (ERRs) and estrogen receptor (ER) alpha, but not by ERbeta. , 1999, The EMBO journal.

[136]  J. Nagler,et al.  Estrogen Receptor-α Protein Localization in the Testis of the Rainbow Trout (Oncorhynchus mykiss) During Different Stages of the Reproductive Cycle1 , 2001, Biology of reproduction.

[137]  G. Stancel,et al.  Interaction of human estrogen receptors alpha and beta with the same naturally occurring estrogen response elements. , 1999, Biochemical pharmacology.

[138]  Shafiq A. Khan,et al.  Interactions between FSH, estradiol-17β and transforming growth factor-β regulate growth and differentiation in the rat gonad , 1993, The Journal of Steroid Biochemistry and Molecular Biology.

[139]  Y. Hishikawa,et al.  Identification and localization of estrogen receptor alpha- and beta-positive cells in adult male and female mouse intestine at various estrogen levels. , 2004, Histochemistry and cell biology.

[140]  J. Gustafsson,et al.  Transcriptional targets shared by estrogen receptor‐related receptors (ERRs) and estrogen receptor (ER) α, but not by ERβ , 1999 .

[141]  J. Sumpter,et al.  Altered Sexual Maturation and Gamete Production in Wild Roach (Rutilus rutilus) Living in Rivers That Receive Treated Sewage Effluents1 , 2002, Biology of reproduction.

[142]  E. Laws,et al.  Estrogen receptor expression in human pituitary: correlation with immunohistochemistry in normal tissue, and immunohistochemistry and morphology in macroadenomas. , 1994, The Journal of clinical endocrinology and metabolism.