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Molecular Endocrinology, Vol 9, 1441-1454, Copyright © 1995 by Endocrine Society

ARTICLES

Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene

JF Couse, SW Curtis, TF Washburn, J Lindzey, TS Golding, DB Lubahn, O Smithies and KS Korach
Receptor Biology Section, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, North Carolina 27709, USA.

We employed homologous recombination in mouse embryonic stem cells to disrupt the estrogen receptor (ER) gene. Subsequently generated mice that are homozygous for the gene disruption, termed ERKO, possess no demonstrable wild-type ER by Western blot analysis. However, the presence of residual high affinity binding, as detected by [3H]estradiol binding assays and sucrose gradients in uterine extracts from ERKO females prompted further investigation of transcription and translation products from the disrupted ER gene. Analysis of ERKO uterine messenger RNA (mRNA) by reverse transcriptase-polymerase chain reaction demonstrated that although no full-length wild-type ER mRNA was present, two smaller transcripts, labeled E1 and E2, were identified and partially sequenced. Both ERKO transcripts are splicing variants that result in the disrupting NEO sequence being partially or completely removed from the mRNA. In the ERKO-E2 variant, this results in a frame shift and the creation of at least two stop codons downstream. In the ERKO-E1 variant, the ER reading frame is preserved and encodes for a smaller mutant ER that could be the source of the residual estradiol binding. When this mutant form is overexpressed and characterized in vitro, it results in a smaller protein of the predicted size that possesses significantly reduced estrogen-dependent transcriptional activity compared with that of the wild-type ER. Despite residual amounts of an impaired ER variant, estrogen insensitivity in the female ERKOs was confirmed by the failure of estrogen treatment to induce known uterine markers of estrogen action, such as increased DNA synthesis, and transcription of the progesterone receptor, lactoferrin, and glucose-6-phosphate dehydrogenase genes. Furthermore, serum levels of estradiol in the ERKO female are more than 10-fold higher than those in the wild type, consistent with a syndrome of hormone insensitivity.


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S. Nilsson, S. Makela, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner, and J.-A. Gustafsson
Mechanisms of Estrogen Action
Physiol Rev, October 1, 2001; 81(4): 1535 - 1565.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. H. Karas, H. Schulten, G. Pare, M. J. Aronovitz, C. Ohlsson, J.-A. Gustafsson, and M. E. Mendelsohn
Effects of Estrogen on the Vascular Injury Response in Estrogen Receptor {alpha},{beta} (Double) Knockout Mice
Circ. Res., September 14, 2001; 89(6): 534 - 539.
[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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 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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 Proc. Natl. Acad. Sci. USAHome page
D. B. Dubal, H. Zhu, J. Yu, S. W. Rau, P. J. Shughrue, I. Merchenthaler, M. S. Kindy, and P. M. Wise
Estrogen receptor alpha , not beta , is a critical link in estradiol-mediated protection against brain injury
PNAS, February 1, 2001; (2001) 41483198.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
T. Kurita, K.-j. Lee, P. T.K. Saunders, P. S. Cooke, J. A. Taylor, D. B. Lubahn, C. Zhao, S. Mäkelä, J.-A. Gustafsson, R. Dahiya, et al.
Regulation of Progesterone Receptors and Decidualization in Uterine Stroma of the Estrogen Receptor-{{alpha}} Knockout Mouse
Biol Reprod, January 1, 2001; 64(1): 272 - 283.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
H. Wang, H. Eriksson, and L. Sahlin
Estrogen Receptors {alpha} and {beta} in the Female Reproductive Tract of the Rat During the Estrous Cycle
Biol Reprod, November 1, 2000; 63(5): 1331 - 1340.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
M. K. Österlund, J.-A. Gustafsson, E. Keller, and Y. L. Hurd
Estrogen Receptor {beta} (ER{beta}) Messenger Ribonucleic Acid (mRNA) Expression within the Human Forebrain: Distinct Distribution Pattern to ER{alpha} mRNA
J. Clin. Endocrinol. Metab., October 1, 2000; 85(10): 3840 - 3846.
[Abstract] [Full Text]

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 EndocrinologyHome page
D. M. Klotz, S. C. Hewitt, K. S. Korach, and R. P. Diaugustine
Activation of a Uterine Insulin-Like Growth Factor I Signaling Pathway by Clinical and Environmental Estrogens: Requirement of Estrogen Receptor-{alpha}
Endocrinology, September 1, 2000; 141(9): 3430 - 3439.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
W. P. Bocchinfuso, J. K. Lindzey, S. C. Hewitt, J. A. Clark, P. H. Myers, R. Cooper, and K. S. Korach
Induction of Mammary Gland Development in Estrogen Receptor-{alpha} Knockout Mice
Endocrinology, August 1, 2000; 141(8): 2982 - 2994.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. S. Thurmond, F. G. Murante, J. E. Staples, A. E. Silverstone, K. S. Korach, and T. A. Gasiewicz
Role of Estrogen Receptor {alpha} in Hematopoietic Stem Cell Development and B Lymphocyte Maturation in the Male Mouse
Endocrinology, July 1, 2000; 141(7): 2309 - 2318.
[Abstract] [Full Text] [PDF]

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 J Natl Cancer Inst MonogrHome page
R. B. Dickson and G. M. Stancel
Chapter 8: Estrogen Receptor-Mediated Processes in Normal and Cancer Cells
J Natl Cancer Inst Monographs, July 1, 2000; 2000(27): 135 - 145.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
S. R. Wersinger and E. F. Rissman
Dopamine Activates Masculine Sexual Behavior Independent of the Estrogen Receptor alpha
J. Neurosci., June 1, 2000; 20(11): 4248 - 4254.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
O. Vidal, M. K. Lindberg, K. Hollberg, D. J. Baylink, G. Andersson, D. B. Lubahn, S. Mohan, J.-A. Gustafsson, and C. Ohlsson
Estrogen receptor specificity in the regulation of skeletal growth and maturation in male mice
PNAS, May 9, 2000; 97(10): 5474 - 5479.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
T. Kurita, K.-j. Lee, P. S. Cooke, J. A. Taylor, D. B. Lubahn, and G. R. Cunha
Paracrine Regulation of Epithelial Progesterone Receptor by Estradiol in the Mouse Female Reproductive Tract
Biol Reprod, April 1, 2000; 62(4): 821 - 830.
[Abstract] [Full Text]

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 Toxicol PatholHome page
A. Yoshida, R. R. Newbold, and D. Dixon
Abnormal Cell Differentiation and p21 Expression of Endometrial Epithelial Cells Following Developmental Exposure to Diethylstilbestrol (DES)
Toxicol Pathol, March 1, 2000; 28(2): 237 - 245.
[Abstract] [PDF]

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 Biol. Reprod.Home page
L. Zhao, C. S. Samuel, G. W. Tregear, F. Beck, and E. M. Wintour
Collagen Studies in Late Pregnant Relaxin Null Mice
Biol Reprod, March 1, 2000; 63(3): 697 - 703.
[Abstract] [Full Text]

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 DevelopmentHome page
S Dupont, A Krust, A Gansmuller, A Dierich, P Chambon, and M Mark
Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes
Development, January 10, 2000; 127(19): 4277 - 4291.
[Abstract] [PDF]

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 EndocrinologyHome page
J. F. Couse, D. O. Bunch, J. Lindzey, D. W. Schomberg, and K. S. Korach
Prevention of the Polycystic Ovarian Phenotype and Characterization of Ovulatory Capacity in the Estrogen Receptor-{alpha} Knockout Mouse
Endocrinology, December 1, 1999; 140(12): 5855 - 5865.
[Abstract] [Full Text]

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 EndocrinologyHome page
J. Tan, B. C. Paria, S. K. Dey, and S. K. Das
Differential Uterine Expression of Estrogen and Progesterone Receptors Correlates with Uterine Preparation for Implantation and Decidualization in the Mouse
Endocrinology, November 1, 1999; 140(11): 5310 - 5321.
[Abstract] [Full Text]

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 J. Immunol.Home page
J. E. Staples, T. A. Gasiewicz, N. C. Fiore, D. B. Lubahn, K. S. Korach, and A. E. Silverstone
Estrogen Receptor {alpha} Is Necessary in Thymic Development and Estradiol-Induced Thymic Alterations
J. Immunol., October 15, 1999; 163(8): 4168 - 4174.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
H. Wang, B. Masironi, H. Eriksson, and L. Sahlin
A Comparative Study of Estrogen Receptors {alpha} and {beta} in the Rat Uterus
Biol Reprod, October 1, 1999; 61(4): 955 - 964.
[Abstract] [Full Text]

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 EndocrinologyHome page
D. Ghosh, J. A. Taylor, J. A. Green, and D. B. Lubahn
Methoxychlor Stimulates Estrogen-Responsive Messenger Ribonucleic Acids in Mouse Uterus through a Non-Estrogen Receptor (Non-ER){alpha} and Non-ER{beta} Mechanism
Endocrinology, August 1, 1999; 140(8): 3526 - 3533.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
J. F. Couse and K. S. Korach
Estrogen Receptor Null Mice: What Have We Learned and Where Will They Lead Us?
Endocr. Rev., June 1, 1999; 20(3): 358 - 417.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
D. Chen, P. Ganapathy, L.-J. Zhu, X. Xu, Q. Li, I. C. Bagchi, and M. K. Bagchi
Potential Regulation of Membrane Trafficking by Estrogen Receptor {alpha} via Induction of Rab11 in Uterine Glands during Implantation
Mol. Endocrinol., June 1, 1999; 13(6): 993 - 1004.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
S. Matsuzaki, T. Fukaya, T. Suzuki, T. Murakami, H. Sasano, and A. Yajima
Oestrogen receptor {alpha} and ß mRNA expression in human endometrium throughout the menstrual cycle
Mol. Hum. Reprod., June 1, 1999; 5(6): 559 - 564.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. J. Shughrue, M. V. Lane, and I. Merchenthaler
Biologically Active Estrogen Receptor-{beta}: Evidence from in Vivo Autoradiographic Studies with Estrogen Receptor {alpha}-Knockout Mice
Endocrinology, June 1, 1999; 140(6): 2613 - 2620.
[Abstract] [Full Text]

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 EndocrinologyHome page
B. C. Paria, J. Tan, D. B. Lubahn, S. K. Dey, and S. K. Das
Uterine Decidual Response Occurs in Estrogen Receptor-{alpha}-Deficient Mice
Endocrinology, June 1, 1999; 140(6): 2704 - 2710.
[Abstract] [Full Text]

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 EndocrinologyHome page
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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 Cancer Res.Home page
W. P. Bocchinfuso, W. P. Hively, J. F. Couse, H. E. Varmus, and K. S. Korach
A Mouse Mammary Tumor Virus-Wnt-1 Transgene Induces Mammary Gland Hyperplasia and Tumorigenesis in Mice Lacking Estrogen Receptor-{{alpha}}
Cancer Res., April 1, 1999; 59(8): 1869 - 1876.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. W. Curtis, J. Clark, P. Myers, and K. S. Korach
Disruption of estrogen signaling does not prevent progesterone action in the estrogen receptor alpha  knockout mouse uterus
PNAS, March 30, 1999; 96(7): 3646 - 3651.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. Razandi, A. Pedram, G. L. Greene, and E. R. Levin
Cell Membrane and Nuclear Estrogen Receptors (ERs) Originate from a Single Transcript: Studies of ER{alpha} and ER{beta} Expressed in Chinese Hamster Ovary Cells
Mol. Endocrinol., February 1, 1999; 13(2): 307 - 319.
[Abstract] [Full Text]

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 EndocrinologyHome page
Q. Gu, K. S. Korach, and R. L. Moss
Rapid Action of 17{beta}-Estradiol on Kainate-Induced Currents in Hippocampal Neurons Lacking Intracellular Estrogen Receptors
Endocrinology, February 1, 1999; 140(2): 660 - 666.
[Abstract] [Full Text]

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 EndocrinologyHome page
D. L. Buchanan, T. Setiawan, D. B. Lubahn, J. A. Taylor, T. Kurita, G. R. Cunha, and P. S. Cooke
Tissue Compartment-Specific Estrogen Receptor-{alpha} Participation in the Mouse Uterine Epithelial Secretory Response
Endocrinology, January 1, 1999; 140(1): 484 - 491.
[Abstract] [Full Text]


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