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Physiol. Rev. 81: 1535-1565, 2001;
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Physiological Reviews, Vol. 81, No. 4, October 2001, pp. 1535-1565
Copyright ©2001 by the American Physiological Society

Mechanisms of Estrogen Action

Stefan Nilsson, Sari Mäkelä, Eckardt Treuter, Michel Tujague, Jane Thomsen, Göran Andersson, Eva Enmark, Katarina Pettersson, Margaret Warner, and Jan-Åke Gustafsson

KaroBio AB and Departments of Biosciences and of Medical Nutrition, Karolinska Institute, NOVUM; Department of Pathology, Huddinge Hospital, Huddinge, Sweden; and Institute of Biomedicin Department of Anatomy, University of Turku, Turku, Finland

Nilsson, Stefan, Sari Mäkelä, Eckardt Treuter, Michel Tujague, Jane Thomsen, Göran Andersson, Eva Enmark, Katarina Pettersson, Margaret Warner, and Jan-Åke Gustafsson. Mechanisms of Estrogen Action. Physiol. Rev. 81: 1535-1565, 2001.Our appreciation of the physiological functions of estrogens and the mechanisms through which estrogens bring about these functions has changed during the past decade. Just as transgenic mice were produced in which estrogen receptors had been inactivated and we thought that we were about to understand the role of estrogen receptors in physiology and pathology, it was found that there was not one but two distinct and functional estrogen receptors, now called ERalpha and ERbeta . Transgenic mice in which each of the receptors or both the receptors are inactive have revealed a much broader role for estrogens in the body than was previously thought. This decade also saw the description of a male patient who had no functional ERalpha and whose continued bone growth clearly revealed an important function of estrogen in men. The importance of estrogen in both males and females was also demonstrated in the laboratory in transgenic mice in which the aromatase gene was inactivated. Finally, crystal structures of the estrogen receptors with agonists and antagonists have revealed much about how ligand binding influences receptor conformation and how this conformation influences interaction of the receptor with coactivators or corepressors and hence determines cellular response to ligands.




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T. J. Peterson, S. Karmakar, M. C. Pace, T. Gao, and C. L. Smith
The Silencing Mediator of Retinoic Acid and Thyroid Hormone Receptor (SMRT) Corepressor Is Required for Full Estrogen Receptor {alpha} Transcriptional Activity
Mol. Cell. Biol., September 1, 2007; 27(17): 5933 - 5948.
[Abstract] [Full Text] [PDF]

Home page
 Toxicol SciHome page
M. Heneweer, R. Houtman, J. Poortman, M. Groot, C. Maliepaard, and A. Peijnenburg
Estrogenic Effects in the Immature Rat Uterus after Dietary Exposure to Ethinylestradiol and Zearalenone Using a Systems Biology Approach
Toxicol. Sci., September 1, 2007; 99(1): 303 - 314.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. Sayeed, S. D. Konduri, W. Liu, S. Bansal, F. Li, and G. M. Das
Estrogen Receptor {alpha} Inhibits p53-Mediated Transcriptional Repression: Implications for the Regulation of Apoptosis
Cancer Res., August 15, 2007; 67(16): 7746 - 7755.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. M. Gowri, S. Sengupta, S. Bertera, and B. S. Katzenellenbogen
Lipin1 Regulation by Estrogen in Uterus and Liver: Implications for Diabetes and Fertility
Endocrinology, August 1, 2007; 148(8): 3685 - 3693.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
M. Kininis, B. S. Chen, A. G. Diehl, G. D. Isaacs, T. Zhang, A. C. Siepel, A. G. Clark, and W. L. Kraus
Genomic Analyses of Transcription Factor Binding, Histone Acetylation, and Gene Expression Reveal Mechanistically Distinct Classes of Estrogen-Regulated Promoters
Mol. Cell. Biol., July 15, 2007; 27(14): 5090 - 5104.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
N. Heldring, A. Pike, S. Andersson, J. Matthews, G. Cheng, J. Hartman, M. Tujague, A. Strom, E. Treuter, M. Warner, et al.
Estrogen Receptors: How Do They Signal and What Are Their Targets
Physiol Rev, July 1, 2007; 87(3): 905 - 931.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. M. Silva and M. A. Shupnik
Integration of Steroid and Growth Factor Pathways in Breast Cancer: Focus on Signal Transducers and Activators of Transcription and Their Potential Role in Resistance
Mol. Endocrinol., July 1, 2007; 21(7): 1499 - 1512.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
A. M. Trauernicht, S. J. Kim, N. H. Kim, and T. G. Boyer
Modulation of Estrogen Receptor {alpha} Protein Level and Survival Function by DBC-1
Mol. Endocrinol., July 1, 2007; 21(7): 1526 - 1536.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
B. C. Trainor, S. Lin, M. S. Finy*, M. R. Rowland, and R. J. Nelson
Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways
PNAS, June 5, 2007; 104(23): 9840 - 9845.
[Abstract] [Full Text] [PDF]

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 J Mol EndocrinolHome page
L. A. Gilad and B. Schwartz
Association of estrogen receptor {beta} with plasma-membrane caveola components: implication in control of vitamin D receptor
J. Mol. Endocrinol., June 1, 2007; 38(6): 603 - 618.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
V. Duong, N. Boulle, S. Daujat, J. Chauvet, S. Bonnet, H. Neel, and V. Cavailles
Differential Regulation of Estrogen Receptor {alpha} Turnover and Transactivation by Mdm2 and Stress-Inducing Agents
Cancer Res., June 1, 2007; 67(11): 5513 - 5521.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
R. O'Lone, K. Knorr, I. Z. Jaffe, M. E. Schaffer, P. G. V. Martini, R. H. Karas, J. Bienkowska, M. E. Mendelsohn, and U. Hansen
Estrogen Receptors {alpha} and {beta} Mediate Distinct Pathways of Vascular Gene Expression, Including Genes Involved in Mitochondrial Electron Transport and Generation of Reactive Oxygen Species
Mol. Endocrinol., June 1, 2007; 21(6): 1281 - 1296.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
J. M. Naciff, G. J. Overmann, S. M. Torontali, G. J. Carr, Z. S. Khambatta, J. P. Tiesman, B. D. Richardson, and G. P. Daston
Uterine Temporal Response to Acute Exposure to 17{alpha}-Ethinyl Estradiol in the Immature Rat
Toxicol. Sci., June 1, 2007; 97(2): 467 - 490.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Pharmacol.Home page
L. Penolazzi, M. Zennaro, E. Lambertini, E. Tavanti, E. Torreggiani, R. Gambari, and R. Piva
Induction of Estrogen Receptor {alpha} Expression with Decoy Oligonucleotide Targeted to NFATc1 Binding Sites in Osteoblasts
Mol. Pharmacol., June 1, 2007; 71(6): 1457 - 1462.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. Lupien, M. Jeyakumar, E. Hebert, K. Hilmi, D. Cotnoir-White, C. Loch, A. Auger, G. Dayan, G.-A. Pinard, J.-M. Wurtz, et al.
Raloxifene and ICI182,780 Increase Estrogen Receptor-{alpha} Association with a Nuclear Compartment via Overlapping Sets of Hydrophobic Amino Acids in Activation Function 2 Helix 12
Mol. Endocrinol., April 1, 2007; 21(4): 797 - 816.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
J. Yan, Y.-S. Kim, X.-P. Yang, M. Albers, M. Koegl, and A. M. Jetten
Ubiquitin-interaction motifs of RAP80 are critical in its regulation of estrogen receptor {alpha}
Nucleic Acids Res., March 12, 2007; 35(5): 1673 - 1686.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
Y. Lu, A. Amleh, J. Sun, X. Jin, S. D. McCullough, R. Baer, D. Ren, R. Li, and Y. Hu
Ubiquitination and Proteasome-Mediated Degradation of BRCA1 and BARD1 during Steroidogenesis in Human Ovarian Granulosa Cells
Mol. Endocrinol., March 1, 2007; 21(3): 651 - 663.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
N. Vasudevan and D. W. Pfaff
Membrane-Initiated Actions of Estrogens in Neuroendocrinology: Emerging Principles
Endocr. Rev., February 1, 2007; 28(1): 1 - 19.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. H. Al-Dhaheri and B. G. Rowan
Protein Kinase A Exhibits Selective Modulation of Estradiol-Dependent Transcription in Breast Cancer Cells that Is Associated with Decreased Ligand Binding, Altered Estrogen Receptor {alpha} Promoter Interaction, and Changes in Receptor Phosphorylation
Mol. Endocrinol., February 1, 2007; 21(2): 439 - 456.
[Abstract] [Full Text] [PDF]

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 J. Clin. Pathol.Home page
H. Grans, M. Nilsson, K. Dahlman-Wright, and B. Evengard
Reduced levels of oestrogen receptor {beta} mRNA in Swedish patients with chronic fatigue syndrome
J. Clin. Pathol., February 1, 2007; 60(2): 195 - 198.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
H. A. Harris
Estrogen Receptor-{beta}: Recent Lessons from in Vivo Studies
Mol. Endocrinol., January 1, 2007; 21(1): 1 - 13.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
X. Fan, M. Warner, and J.-A. Gustafsson
Estrogen receptor beta expression in the embryonic brain regulates development of calretinin-immunoreactive GABAergic interneurons
PNAS, December 19, 2006; 103(51): 19338 - 19343.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
B. M. Jaber, T. Gao, L. Huang, S. Karmakar, and C. L. Smith
The Pure Estrogen Receptor Antagonist ICI 182,780 Promotes a Novel Interaction of Estrogen Receptor-{alpha} with the 3',5'-Cyclic Adenosine Monophosphate Response Element-Binding Protein-Binding Protein/p300 Coactivators
Mol. Endocrinol., November 1, 2006; 20(11): 2695 - 2710.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. Lu, D. Chen, Z. Lin, S. Reierstad, A. M. Trauernicht, T. G. Boyer, and S. E. Bulun
BRCA1 Negatively Regulates the Cancer-Associated Aromatase Promoters I.3 and II in Breast Adipose Fibroblasts and Malignant Epithelial Cells
J. Clin. Endocrinol. Metab., November 1, 2006; 91(11): 4514 - 4519.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
K. Ohshiro, S. K. Rayala, M. D. Williams, R. Kumar, and A. K. El-Naggar
Biological Role of Estrogen Receptor {beta} in Salivary Gland Adenocarcinoma Cells.
Clin. Cancer Res., October 15, 2006; 12(20): 5994 - 5999.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
A. R. Thomsen, K. Almstrup, J. E. Nielsen, I. K. Sorensen, O. W. Petersen, H. Leffers, and V. M. Breinholt
Estrogenic Effect of Soy Isoflavones on Mammary Gland Morphogenesis and Gene Expression Profile
Toxicol. Sci., October 1, 2006; 93(2): 357 - 368.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. C. Chang, J. Frasor, B. Komm, and B. S. Katzenellenbogen
Impact of Estrogen Receptor {beta} on Gene Networks Regulated by Estrogen Receptor {alpha} in Breast Cancer Cells
Endocrinology, October 1, 2006; 147(10): 4831 - 4842.
[Abstract] [Full Text] [PDF]

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 J EndocrinolHome page
B. A S Reyes, H. Tsukamura, H. I'Anson, M. A. C Estacio, K. Hirunagi, and K.-I. Maeda
Temporal expression of estrogen receptor {alpha} in the hypothalamus and medulla oblongata during fasting: a role of noradrenergic neurons.
J. Endocrinol., September 1, 2006; 190(3): 593 - 600.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
B. N. Duong, S. Elliott, D. E. Frigo, L. I. Melnik, L. Vanhoy, S. Tomchuck, H. P. Lebeau, O. David, B. S. Beckman, J. Alam, et al.
AKT Regulation of Estrogen Receptor {beta} Transcriptional Activity in Breast Cancer.
Cancer Res., September 1, 2006; 66(17): 8373 - 8381.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
J. R. Schultz-Norton, W. H. McDonald, J. R. Yates, and A. M. Nardulli
Protein Disulfide Isomerase Serves as a Molecular Chaperone to Maintain Estrogen Receptor {alpha} Structure and Function
Mol. Endocrinol., September 1, 2006; 20(9): 1982 - 1995.
[Abstract] [Full Text] [PDF]

Home page
 EndocrinologyHome page
B. T. Zhu, G.-Z. Han, J.-Y. Shim, Y. Wen, and X.-R. Jiang
Quantitative Structure-Activity Relationship of Various Endogenous Estrogen Metabolites for Human Estrogen Receptor {alpha} and {beta} Subtypes: Insights into the Structural Determinants Favoring a Differential Subtype Binding
Endocrinology, September 1, 2006; 147(9): 4132 - 4150.
[Abstract] [Full Text] [PDF]

Home page
 EndocrinologyHome page
Y.-H. Chen, M.-J. Lee, H.-H. Chang, P.-F. Hung, and Y.-H. Kao
17{beta}-Estradiol Stimulates Resistin Gene Expression in 3T3-L1 Adipocytes via the Estrogen Receptor, Extracellularly Regulated Kinase, and CCAAT/Enhancer Binding Protein-{alpha} Pathways
Endocrinology, September 1, 2006; 147(9): 4496 - 4504.
[Abstract] [Full Text] [PDF]

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 Eur J EndocrinolHome page
S. Naessen, K. Carlstrom, R. Glant, H. Jacobsson, and A. L. Hirschberg
Bone mineral density in bulimic women - influence of endocrine factors and previous anorexia.
Eur. J. Endocrinol., August 1, 2006; 155(2): 245 - 251.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
Z. Zhang, K. Chen, J. C. Shih, and C. T. Teng
Estrogen-Related Receptors-Stimulated Monoamine Oxidase B Promoter Activity Is Down-Regulated by Estrogen Receptors
Mol. Endocrinol., July 1, 2006; 20(7): 1547 - 1561.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. Y. Kim, E. M. Woo, Y. T. E. Chong, D. R. Homenko, and W. L. Kraus
Acetylation of Estrogen Receptor {alpha} by p300 at Lysines 266 and 268 Enhances the Deoxyribonucleic Acid Binding and Transactivation Activities of the Receptor
Mol. Endocrinol., July 1, 2006; 20(7): 1479 - 1493.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
F. A. Babiker, D. Lips, R. Meyer, E. Delvaux, P. Zandberg, B. Janssen, G. van Eys, C. Grohe, and P. A. Doevendans
Estrogen Receptor {beta} Protects the Murine Heart Against Left Ventricular Hypertrophy
Arterioscler Thromb Vasc Biol, July 1, 2006; 26(7): 1524 - 1530.
[Abstract] [Full Text] [PDF]


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