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Molecular Endocrinology 11 (2): 172-182
Copyright © 1997 by The Endocrine Society

Estrogen Receptor-ß mRNA Expression in Rat Ovary: Down-Regulation by Gonadotropins

Michael Byers, George G. J. M. Kuiper, Jan-Åke Gustafsson and Ok-Kyong Park-Sarge

Department of Physiology (M.B., O-K.P-S.) University of Kentucky Lexington, Kentucky 40536
Center for Biotechnology (G.G.J.M.K.) and Department of Medical Nutrition (J-Å.G.) Karolinska Institute S-14186 Huddinge, Sweden

We have examined the expression and regulation of the two estrogen receptor (ER{alpha} and ERß) genes in the rat ovary, using Northern blotting, RT-PCR, and in situ hybridization histochemistry. Northern blotting results show that the ovary expresses both ER{alpha} and ERß genes as single (~6.5-kb) and multiple (ranging from ~1.0-kb to ~10.0-kb) transcripts, respectively. ER{alpha} mRNA is expressed at a level lower than ERß mRNA in immature rat ovaries. This relationship appears unchanged between sexually mature adult rats and immature rats. In sexually mature adult rats undergoing endogenous hormonal changes, whole ovarian content of ERß mRNA, as determined by RT-PCR, remained more or less constant with the exception of the evening of proestrus when ERß mRNA levels were decreased. Examination of ERß mRNA expression at the cellular level, by in situ hybridization, showed that ERß mRNA is expressed preferentially in granulosa cells of small, growing, and preovulatory follicles, although weak expression of ERß mRNA was observed in a subset of corpora lutea, and that the decrease in ERß mRNA during proestrous evening is attributable, at least in part, to down-regulation of ERß mRNA in the preovulatory follicles. This type of expression and regulation was not typical for ER{alpha} mRNA in the ovary. Although whole ovarian content of ER{alpha} mRNA was clearly detected by RT-PCR, no apparent modulation of ER{alpha} mRNA levels was observed during the estrous cycle. Examination of ER{alpha} mRNA expression at the cellular level, by in situ hybridization, showed that ER{alpha} mRNA is expressed at a low level throughout the ovary with no particular cellular localization.

To further examine the potential role of the preovulatory pituitary gonadotropins in regulating ERß mRNA expression in the ovary, we used immature rats treated with gonadotropins. In rats undergoing exogenous hormonal challenges, whole ovarian content of ERß mRNA, as determined by RT-PCR, remained more or less unchanged after an injection of PMSG. In contrast, a subsequent injection of human CG (hCG) resulted in a substantial decrease in whole ovarian content of ERß mRNA. In situ hybridization for ERß mRNA shows that small, growing, and preovulatory follicles express ERß mRNA in the granulosa cells. The preovulatory follicles contain ERß mRNA at a level lower than that observed for small and growing follicles. In addition, there is an abrupt decrease in ERß mRNA expression in the preovulatory follicles after hCG injection. The inhibitory effect of hCG on ERß mRNA expression was also observed in cultured granulosa cells. Moreover, agents stimulating LH/CG receptor-associated intracellular signaling pathways (forskolin and a phorbol ester) readily mimicked the effect of hCG in down-regulating ERß mRNA in cultured granulosa cells.

Taken together, our results demonstrate that 1) the ovary expresses both ER{alpha} and ERß genes, although ERß is the predominant form of estrogen receptor in the ovary, 2) ERß mRNA is localized predominantly to the granulosa cells of small, growing, and preovulatory follicles, and 3) the preovulatory LH surge down-regulates ERß mRNA. These results clearly implicate the physiological importance of ERß in female reproductive functions.




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D. W. Schomberg, J. F. Couse, A. Mukherjee, D. B. Lubahn, M. Sar, K. E. Mayo, and K. S. Korach
Targeted Disruption of the Estrogen Receptor-{alpha} Gene in Female Mice: Characterization of Ovarian Responses and Phenotype in the Adult
Endocrinology, June 1, 1999; 140(6): 2733 - 2744.
[Abstract] [Full Text]

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 EndocrinologyHome page
Q. Zhang, X. Wang, and D. J. Wolgemuth
Developmentally Regulated Expression of Cyclin D3 and Its Potential in Vivo Interacting Proteins during Murine Gametogenesis
Endocrinology, June 1, 1999; 140(6): 2790 - 2800.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
K.-M. Lau, S. C. Mok, and S.-M. Ho
Expression of human estrogen receptor-alpha and -beta , progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells
PNAS, May 11, 1999; 96(10): 5722 - 5727.
[Abstract] [Full Text] [PDF]

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T. S. Sperry and P. Thomas
Characterization of Two Nuclear Androgen Receptors in Atlantic Croaker: Comparison of Their Biochemical Properties and Binding Specificities
Endocrinology, April 1, 1999; 140(4): 1602 - 1611.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
C. S. Rosenfeld, X. Yuan, M. Manikkam, M. D. Calder, H. A. Garverick, and D. B. Lubahn
Cloning, Sequencing, and Localization of Bovine Estrogen Receptor-ß within the Ovarian Follicle
Biol Reprod, March 1, 1999; 60(3): 691 - 697.
[Abstract] [Full Text]

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 EndocrinologyHome page
M. Sar and F. Welsch
Differential Expression of Estrogen Receptor-{beta} and Estrogen Receptor-{alpha} in the Rat Ovary
Endocrinology, February 1, 1999; 140(2): 963 - 971.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
R. Misao, Y. Nakanishi, W.S. Sun, J. Fujimoto, S. Iwagaki, R. Hirose, and T. Tamaya
Expression of oestrogen receptor {alpha} and ß mRNA in corpus luteum of human subjects
Mol. Hum. Reprod., January 1, 1999; 5(1): 17 - 21.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. H. Krege, J. B. Hodgin, J. F. Couse, E. Enmark, M. Warner, J. F. Mahler, M. Sar, K. S. Korach, J.-A. Gustafsson, and O. Smithies
Generation and reproductive phenotypes of mice lacking estrogen receptor beta
PNAS, December 22, 1998; 95(26): 15677 - 15682.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
G. Flouriot, C. Griffin, M. Kenealy, V. Sonntag-Buck, and F. Gannon
Differentially Expressed Messenger RNA Isoforms of the Human Estrogen Receptor-{alpha} Gene Are Generated by Alternative Splicing and Promoter Usage
Mol. Endocrinol., December 1, 1998; 12(12): 1939 - 1954.
[Abstract] [Full Text]

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C. Griffin, G. Flouriot, V. Sonntag-Buck, P. Nestor, and F. Gannon
Identification of Novel Chicken Estrogen Receptor-{alpha} Messenger Ribonucleic Acid Isoforms Generated by Alternative Splicing and Promoter Usage
Endocrinology, November 1, 1998; 139(11): 4614 - 4625.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
N. A. Mitchner, C. Garlick, and N. Ben-Jonathan
Cellular Distribution and Gene Regulation of Estrogen Receptors {alpha} and {beta} in the Rat Pituitary Gland
Endocrinology, September 1, 1998; 139(9): 3976 - 3983.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J. W. Clemens, R. L. Robker, W. L. Kraus, B. S. Katzenellenbogen, and J. S. Richards
Hormone Induction of Progesterone Receptor (PR) Messenger Ribonucleic Acid and Activation of PR Promoter Regions in Ovarian Granulosa Cells: Evidence for a Role of Cyclic Adenosine 3',5'-Monophosphate but Not Estradiol
Mol. Endocrinol., August 1, 1998; 12(8): 1201 - 1214.
[Abstract] [Full Text]

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 Circ. Res.Home page
V. Lindner, S. K. Kim, R. H. Karas, G. G. J. M. Kuiper, J.-A. Gustafsson, and M. E. Mendelsohn
Increased Expression of Estrogen Receptor-ß mRNA in Male Blood Vessels After Vascular Injury
Circ. Res., July 27, 1998; 83(2): 224 - 229.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
V. Kusec, A. S. Virdi, R. Prince, and J. T. Triffitt
Localization of Estrogen Receptor-{alpha} in Human and Rabbit Skeletal Tissues
J. Clin. Endocrinol. Metab., July 1, 1998; 83(7): 2421 - 2428.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
R. L. Robker and J. S. Richards
Hormonal Control of the Cell Cycle in Ovarian Cells: Proliferation Versus Differentiation
Biol Reprod, July 1, 1998; 59(3): 476 - 482.
[Full Text]

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 EndocrinologyHome page
C. M. Telleria, L. Zhong, S. Deb, R. K. Srivastava, K. S. Park, N. Sugino, O.-K. Park-Sarge, and G. Gibori
Differential Expression of the Estrogen Receptors {alpha} and {beta} in the Rat Corpus Luteum of Pregnancy: Regulation by Prolactin and Placental Lactogens
Endocrinology, May 1, 1998; 139(5): 2432 - 2442.
[Abstract] [Full Text] [PDF]

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N. Sugino, M. Zilberstein, R. K. Srivastava, C. M. Telleria, S. E. Nelson, M. Risk, J. Y. Chou, and G. Gibori
Establishment and Characterization of a Simian Virus 40-Transformed Temperature-Sensitive Rat Luteal Cell Line
Endocrinology, April 1, 1998; 139(4): 1936 - 1942.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. A. K. Srivastava, N. Srivastava, M. Averna, R. C. Lin, K. S. Korach, D. B. Lubahn, and G. Schonfeld
Estrogen Up-regulates Apolipoprotein E (ApoE) Gene Expression by Increasing ApoE mRNA in the Translating Pool via the Estrogen Receptor alpha -Mediated Pathway
J. Biol. Chem., December 26, 1997; 272(52): 33360 - 33366.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. K. Das, J. A. Taylor, K. S. Korach, B. C. Paria, S. K. Dey, and D. B. Lubahn
Estrogenic responses in estrogen receptor-alpha deficient mice reveal a distinct estrogen signaling pathway
PNAS, November 25, 1997; 94(24): 12786 - 12791.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. F. Couse, J. Lindzey, K. Grandien, J.-A. Gustafsson, and K. S. Korach
Tissue Distribution and Quantitative Analysis of Estrogen Receptor-{alpha} (ER{alpha}) and Estrogen Receptor-{beta} (ER{beta}) Messenger Ribonucleic Acid in the Wild-Type and ER{alpha}-Knockout Mouse
Endocrinology, November 1, 1997; 138(11): 4613 - 4621.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
K. Pettersson, K. Grandien, G. G. J. M. Kuiper, and J.-A. Gustafsson
Mouse Estrogen Receptor {beta} Forms Estrogen Response Element-Binding Heterodimers with Estrogen Receptor {alpha}
Mol. Endocrinol., September 1, 1997; 11(10): 1486 - 1496.
[Abstract] [Full Text]


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