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Endocrinology Vol. 138, No. 11 4613-4621
Copyright © 1997 by The Endocrine Society

ARTICLES

Tissue Distribution and Quantitative Analysis of Estrogen Receptor-{alpha} (ER{alpha}) and Estrogen Receptor-ß (ERß) Messenger Ribonucleic Acid in the Wild-Type and ER{alpha}-Knockout Mouse

John F. Couse, Jonathan Lindzey, Kaj Grandien, Jan-Åke Gustafsson and Kenneth S. Korach

Receptor Biology Section (J.F.C., J.L., K.S.K.), Laboratory of Reproductive and Developmental Toxicology, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, North Carolina 27709; and the Department of Medical Nutrition (K.G., J.-A.G.), Karolinska Institute, NOVUM, S-14186, Huddinge, Sweden

Address all correspondence and requests for reprints to: Dr. Kenneth S. Korach, Receptor Biology Section, Laboratory of Reproductive and Developmental Toxicology, National Institute of Environmental Health Sciences, National Institutes of Health, MD B3–02, P.O. Box 12233, Research Triangle Park, North Carolina 27709.

Until recently, only a single type of estrogen receptor (ER) was thought to exist and mediate the genomic effects of the hormone 17ß-estradiol in mammalian tissues. However, the cloning of a gene encoding a second type of ER, termed ERß, from the mouse, rat, and human has prompted a reevaluation of the estrogen signaling system. Based on in vitro studies, the ERß protein binds estradiol with an affinity similar to that of the classical ER (now referred to as ER{alpha}) and is able to mediate the effects of estradiol in transfected mammalian cell lines. Essential to further investigations of the possible physiological roles of ERß, and its possible interactions with ER{alpha}, are data on the tissue distribution of the two ER types. Herein, we have described the optimization and use of an RNase protection assay able to detect and distinguish messenger RNA (mRNA) transcripts from both the ER{alpha} and ERß genes in the mouse. Because this assay is directly quantitative, a comparison of the levels of expression within various tissues was possible. In addition, the effect of disruption of the ER{alpha} gene on the expression of the ERß gene was also investigated using the ER{alpha}-knockout (ERKO) mouse. Transcripts encoding ER{alpha} were detected in all the wild-type tissues assayed from both sexes. In the female reproductive tract, the highest expression of ERß mRNA was observed in the ovary and showed great variation among individual animals; detectable levels were observed in the uterus and oviduct, whereas mammary tissue was negative. In the male reproductive tract, significant expression of ERß was seen in the prostate and epididymis, whereas the testes were negative. In other tissues of both sexes, the hypothalamus and lung were clearly positive for both ER{alpha} and ERß mRNA. The ERKO mice demonstrated slightly reduced levels of ERß mRNA in the ovary, prostate, and epididymis. These data, in combination with the several described phenotypes in both sexes of the ERKO mouse, suggest that the biological functions of the ERß protein may be dependent on the presence of ER{alpha} in certain cell types and tissues. Further characterization of the physiological phenotypes in the ERKO mice may elucidate possible ERß specific actions.




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M. Marino, F. Acconcia, and A. Trentalance
Biphasic Estradiol-induced AKT Phosphorylation Is Modulated by PTEN via MAP Kinase in HepG2 Cells
Mol. Biol. Cell, June 1, 2003; 14(6): 2583 - 2591.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
G.-J. Shim, L. Wang, S. Andersson, N. Nagy, L. L. Kis, Q. Zhang, S. Makela, M. Warner, and J.-A. Gustafsson
Disruption of the estrogen receptor {beta} gene in mice causes myeloproliferative disease resembling chronic myeloid leukemia with lymphoid blast crisis
PNAS, May 27, 2003; 100(11): 6694 - 6699.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
J. M. Naciff, G. J. Overmann, S. M. Torontali, G. J. Carr, J. P. Tiesman, B. D. Richardson, and G. P. Daston
Gene Expression Profile Induced by 17{alpha}-Ethynyl Estradiol in the Prepubertal Female Reproductive System of the Rat
Toxicol. Sci., April 1, 2003; 72(2): 314 - 330.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. O. Mueller, J. M. Hall, D. L. Swope, L. C. Pedersen, and K. S. Korach
Molecular Determinants of the Stereoselectivity of Agonist Activity of Estrogen Receptors (ER) alpha and beta
J. Biol. Chem., March 28, 2003; 278(14): 12255 - 12262.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
F. Amant, E. Huys, A. Geurts-Moespot, B. G. Lindeque, I. Vergote, F. Sweep, and E. F. P. M. Schoenmakers
Ethnic Variations in Uterine Leiomyoma Biology Are Not Caused By Differences in Myometrial Estrogen Receptor Alpha Levels
Reproductive Sciences, February 1, 2003; 10(2): 105 - 109.
[Abstract] [PDF]

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 EndocrinologyHome page
B. T. Akingbemi, R. Ge, C. S. Rosenfeld, L. G. Newton, D. O. Hardy, J. F. Catterall, D. B. Lubahn, K. S. Korach, and M. P. Hardy
Estrogen Receptor-{alpha} Gene Deficiency Enhances Androgen Biosynthesis in the Mouse Leydig Cell
Endocrinology, January 1, 2003; 144(1): 84 - 93.
[Abstract] [Full Text] [PDF]

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 Drug Metab. Dispos.Home page
Y. Hu and D. Kupfer
Enantioselective Metabolism of the Endocrine Disruptor Pesticide Methoxychlor by Human Cytochromes P450 (P450s): Major Differences in Selective Enantiomer Formation by Various P450 Isoforms
Drug Metab. Dispos., December 1, 2002; 30(12): 1329 - 1336.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
Y. Miki, T. Nakata, T. Suzuki, A. D. Darnel, T. Moriya, C. Kaneko, K. Hidaka, Y. Shiotsu, H. Kusaka, and H. Sasano
Systemic Distribution of Steroid Sulfatase and Estrogen Sulfotransferase in Human Adult and Fetal Tissues
J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5760 - 5768.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. Rivas, J. S. Fisher, C. McKinnell, N. Atanassova, and R. M. Sharpe
Induction of Reproductive Tract Developmental Abnormalities in the Male Rat by Lowering Androgen Production or Action in Combination with a Low Dose of Diethylstilbestrol: Evidence for Importance of the Androgen-Estrogen Balance
Endocrinology, December 1, 2002; 143(12): 4797 - 4808.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
S. B. Pillai, J. M. Jones, and R. D. Koos
Treatment of Rats with 17{beta}-Estradiol or Relaxin Rapidly Inhibits Uterine Estrogen Receptor {beta}1 and {beta}2 Messenger Ribonucleic Acid Levels
Biol Reprod, December 1, 2002; 67(6): 1919 - 1926.
[Abstract] [Full Text] [PDF]

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 J. Histochem. Cytochem.Home page
G. Pelletier
Effects of Estradiol on Prostate Epithelial Cells in the Castrated Rat
J. Histochem. Cytochem., November 1, 2002; 50(11): 1517 - 1524.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. A. Schreihofer, D. F. Rowe, E. F. Rissman, E. M. Scordalakes, J.-a. Gustafsson, and M. A. Shupnik
Estrogen Receptor-{alpha} (ER{alpha}), But Not ER{beta}, Modulates Estrogen Stimulation of the ER{alpha}-Truncated Variant, TERP-1
Endocrinology, November 1, 2002; 143(11): 4196 - 4202.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
W. N. Jefferson, J. F. Couse, E. Padilla-Banks, K. S. Korach, and R. R. Newbold
Neonatal Exposure to Genistein Induces Estrogen Receptor (ER){alpha} Expression and Multioocyte Follicles in the Maturing Mouse Ovary: Evidence for ER{beta}-Mediated and Nonestrogenic Actions
Biol Reprod, October 1, 2002; 67(4): 1285 - 1296.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. T. Kim, B. C. Kim, I. Y. Kim, M. Mamura, D. H. Seong, J.-J. Jang, and S.-J. Kim
Raloxifene, a Mixed Estrogen Agonist/Antagonist, Induces Apoptosis through Cleavage of BAD in TSU-PR1 Human Cancer Cells
J. Biol. Chem., August 30, 2002; 277(36): 32510 - 32515.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. M. Robertson, L. O'Donnell, E. R. Simpson, and M. E. E. Jones
The Phenotype of the Aromatase Knockout Mouse Reveals Dietary Phytoestrogens Impact Significantly on Testis Function
Endocrinology, August 1, 2002; 143(8): 2913 - 2921.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
J. M. Naciff, M. L. Jump, S. M. Torontali, G. J. Carr, J. P. Tiesman, G. J. Overmann, and G. P. Daston
Gene Expression Profile Induced by 17{alpha}-Ethynyl Estradiol, Bisphenol A, and Genistein in the Developing Female Reproductive System of the Rat
Toxicol. Sci., July 1, 2002; 68(1): 184 - 199.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. G. Geisler, W. Zawalich, K. Zawalich, J. R.T. Lakey, H. Stukenbrok, A. J. Milici, and W. C. Soeller
Estrogen Can Prevent or Reverse Obesity and Diabetes in Mice Expressing Human Islet Amyloid Polypeptide
Diabetes, July 1, 2002; 51(7): 2158 - 2169.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. Lopez, M. D. Sanchez, W. Shea-Eaton, and M. P. McLean
Estrogen Activates the High-Density Lipoprotein Receptor Gene via Binding to Estrogen Response Elements and Interaction with Sterol Regulatory Element Binding Protein-1A
Endocrinology, June 1, 2002; 143(6): 2155 - 2168.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C.-R. Shyr, Y.-C. Hu, E. Kim, and C. Chang
Modulation of Estrogen Receptor-mediated Transactivation by Orphan Receptor TR4 in MCF-7 Cells
J. Biol. Chem., April 19, 2002; 277(17): 14622 - 14628.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Raghow, M. Z. Hooshdaran, S. Katiyar, and M. S. Steiner
Toremifene Prevents Prostate Cancer in the Transgenic Adenocarcinoma of Mouse Prostate Model
Cancer Res., March 1, 2002; 62(5): 1370 - 1376.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. R. Schultz, M. A. Loven, V. M. S. Melvin, D. P. Edwards, and A. M. Nardulli
Differential Modulation of DNA Conformation by Estrogen Receptors alpha and beta
J. Biol. Chem., March 1, 2002; 277(10): 8702 - 8707.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
I. E. Messinis, S. Milingos, E. Alexandris, I. Mademtzis, G. Kollios, and K. Seferiadis
Evidence of differential control of FSH and LH responses to GnRH by ovarian steroids in the luteal phase of the cycle
Hum. Reprod., February 1, 2002; 17(2): 299 - 303.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
N. Ben-Jonathan and R. Hnasko
Dopamine as a Prolactin (PRL) Inhibitor
Endocr. Rev., December 1, 2001; 22(6): 724 - 763.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
E. R. Levin
Genome and Hormones: Gender Differences in Physiology: Invited Review: Cell localization, physiology, and nongenomic actions of estrogen receptors
J Appl Physiol, October 1, 2001; 91(4): 1860 - 1867.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
K. M. Waters, S. Safe, and K. W. Gaido
Differential Gene Expression in Response to Methoxychlor and Estradiol through ER{alpha}, ER{beta}, and AR in Reproductive Tissues of Female Mice
Toxicol. Sci., September 1, 2001; 63(1): 47 - 56.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. Larrea, R. Garcia-Becerra, A. E. Lemus, G. A. Garcia, G. Perez-Palacios, K. J. Jackson, K. M. Coleman, R. Dace, C. L. Smith, and A. J. Cooney
A-Ring Reduced Metabolites of 19-nor Synthetic Progestins as Subtype Selective Agonists for ER{alpha}
Endocrinology, September 1, 2001; 142(9): 3791 - 3799.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Wang, D. Sudilovsky, B. Zhang, P. C. Haughney, M. A. Rosen, D. S. Wu, T. J. Cunha, R. Dahiya, G. R. Cunha, and S. W. Hayward
A Human Prostatic Epithelial Model of Hormonal Carcinogenesis
Cancer Res., August 1, 2001; 61(16): 6064 - 6072.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
G. S. Prins, L. Birch, J. F. Couse, I. Choi, B. Katzenellenbogen, and K. S. Korach
Estrogen Imprinting of the Developing Prostate Gland Is Mediated through Stromal Estrogen Receptor {alpha}: Studies with {alpha}ERKO and {beta}ERKO Mice
Cancer Res., August 1, 2001; 61(16): 6089 - 6097.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
P. Ciana, G. Di Luccio, S. Belcredito, G. Pollio, E. Vegeto, L. Tatangelo, C. Tiveron, and A. Maggi
Engineering of a Mouse for the in Vivo Profiling of Estrogen Receptor Activity
Mol. Endocrinol., July 1, 2001; 15(7): 1104 - 1113.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
L. O'Donnell, K. M. Robertson, M. E. Jones, and E. R. Simpson
Estrogen and Spermatogenesis
Endocr. Rev., June 1, 2001; 22(3): 289 - 318.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. F. Palter, A. B. Tavares, A. Hourvitz, J. D. Veldhuis, and E. Y. Adashi
Are Estrogens of Import to Primate/Human Ovarian Folliculogenesis?
Endocr. Rev., June 1, 2001; 22(3): 389 - 424.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
M. M. Mansour, M. R. Machen, B. J. Tarleton, A. A. Wiley, J. Wower, F. F. Bartol, and H. O. Goyal
Expression and Molecular Characterization of Estrogen Receptor Alpha Messenger RNA in Male Reproductive Organs of Adult Goats
Biol Reprod, May 1, 2001; 64(5): 1432 - 1438.
[Abstract] [Full Text]

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 Exp. Biol. Med.Home page
D. A. Jacob, J. L. Temple, H. B. Patisaul, L. J. Young, and E. F. Rissman
Coumestrol Antagonizes Neuroendocrine Actions of Estrogen via the Estrogen Receptor {{alpha}}
Experimental Biology and Medicine, April 1, 2001; 226(4): 301 - 306.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
G. LECCE, G. MEDURI, M. ANCELIN, C. BERGERON, and M. PERROT-APPLANAT
Presence of Estrogen Receptor {beta} in the Human Endometrium through the Cycle: Expression in Glandular, Stromal, and Vascular Cells
J. Clin. Endocrinol. Metab., March 1, 2001; 86(3): 1379 - 1386.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
H.O. Goyal, T.D. Braden, M. Mansour, C.S. Williams, A. Kamaleldin, and K.K. Srivastava
Diethylstilbestrol-Treated Adult Rats with Altered Epididymal Sperm Numbers and Sperm Motility Parameters, but Without Alterations in Sperm Production and Sperm Morphology
Biol Reprod, March 1, 2001; 64(3): 927 - 934.
[Abstract] [Full Text]

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 EndocrinologyHome page
H. A. Harris, R. A. Henderson, R. A. Bhat, and B. S. Komm
Regulation of Metallothionein II Messenger Ribonucleic Acid Measures Exogenous Estrogen Receptor-{beta} Activity in SAOS-2 and LNCaPLN3 Cells
Endocrinology, February 1, 2001; 142(2): 645 - 652.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
N. Atanassova, C. McKinnell, K. Williams, K. J. Turner, J. S. Fisher, P. T. K. Saunders, M. R. Millar, and R. M. Sharpe
Age-, Cell- and Region-Specific Immunoexpression of Estrogen Receptor {{alpha}} (But Not Estrogen Receptor {beta}) during Postnatal Development of the Epididymis and Vas Deferens of the Rat and Disruption of This Pattern by Neonatal Treatment with Diethylstilbestrol
Endocrinology, February 1, 2001; 142(2): 874 - 886.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. S. Krumenacker, S. M. Hyder, and F. Murad
Estradiol rapidly inhibits soluble guanylyl cyclase expression in rat uterus
PNAS, January 16, 2001; 98(2): 717 - 722.
[Abstract] [Full Text] [PDF]


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