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Molecular Endocrinology, Vol 7, 743-752, Copyright © 1993 by Endocrine Society

ARTICLES

Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I

SM Aronica and BS Katzenellenbogen
Department of Physiology and Biophysics, University of Illinois, Urbana 61801.

We have shown previously that exposure of rat uterine cells in primary culture to estradiol (E2), insulin-like growth factor-I (IGF-I), or agents which alter intracellular cAMP levels, such as cholera toxin plus isobutylmethylxanthine (CT + IBMX) and 8-Br-cAMP, results in the up-regulation of cellular levels of the progesterone receptor, an effect believed to be mediated through the activation of estrogen receptor (ER) and phosphorylation pathways. We have therefore undertaken studies using transient transfection of these uterine cell cultures with a simple estrogen-responsive reporter gene in order to determine the ability of these agents to stimulate ER-mediated gene transcription directly. We also compared the ability of these same agents to alter the phosphorylation state of the endogenous uterine ER protein. Plasmid DNA containing two tandem estrogen responsive elements and a TATA box linked to the chloramphenicol acetyl transferase (CAT) gene was introduced into immature rat uterine cells grown in primary culture. Treatment of transfected cells with 10(-9) M E2, CT (1 micrograms/ml) + IBMX (10(-4) M), 8-Br-cAMP (10(-4) M), or IGF-I (20 ng/ml) resulted in an 8- to 10-fold induction of CAT activity. CAT activity stimulated by all agents was nearly completely suppressed by coincubation with the antiestrogen ICI 164,384 (ICI) or the protein kinase (PK) inhibitor H8. CAT activity induced by 8-Br-cAMP was more readily suppressed by ICI than that induced by E2, indicating that ER in cells exposed to 8-Br-cAMP is either unoccupied or minimally occupied by ligand. The level of ER phosphorylation in uterine cells was increased 3- to 5-fold upon exposure to E2, CT + IBMX, 8-Br-cAMP, or IGF-I. Of interest, the antiestrogen ICI also elicited a similar increase in overall ER phosphorylation. The PK inhibitors H8 and PKI suppressed the increase in overall ER phosphorylation stimulated by these agents by 50-75%. The results of our study indicate that E2, IGF- I, and agents which raise intracellular cAMP are able to stimulate ER- mediated trans-activation and ER phosphorylation. The fact that antiestrogen (ICI) evokes a similar increase in ER phosphorylation without a similar increase in transcription activation indicates that an increase in overall ER phosphorylation does not necessarily result in increased transcriptional activity.(ABSTRACT TRUNCATED AT 400 WORDS)


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K. W. Braun, W. A. Tribley, M. D. Griswold, and K. H. Kim
Follicle-stimulating Hormone Inhibits All-trans-retinoic Acid-induced Retinoic Acid Receptor alpha Nuclear Localization and Transcriptional Activation in Mouse Sertoli Cell Lines
J. Biol. Chem., February 11, 2000; 275(6): 4145 - 4151.
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O. M. Conneely, J. P. Lydon, F. De Mayo, and B. W. O'Malley
Reproductive Functions of the Progesterone Receptor
Reproductive Sciences, January 1, 2000; 7(1_suppl): S25 - S32.
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D. Szapary, Y. Huang, and S. S. Simons Jr.
Opposing Effects of Corepressor and Coactivators in Determining the Dose-Response Curve of Agonists, and Residual Agonist Activity of Antagonists, for Glucocorticoid Receptor-Regulated Gene Expression
Mol. Endocrinol., December 1, 1999; 13(12): 2108 - 2121.
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J. M. Hall and D. P. McDonnell
The Estrogen Receptor {beta}-Isoform (ER{beta}) of the Human Estrogen Receptor Modulates ER{alpha} Transcriptional Activity and Is a Key Regulator of the Cellular Response to Estrogens and Antiestrogens
Endocrinology, December 1, 1999; 140(12): 5566 - 5578.
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S. C. Sharma, J. W. Clemens, M. D. Pisarska, and J. S. Richards
Expression and Function of Estrogen Receptor Subtypes in Granulosa Cells: Regulation by Estradiol and Forskolin
Endocrinology, September 1, 1999; 140(9): 4320 - 4334.
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H. Endoh, K. Maruyama, Y. Masuhiro, Y. Kobayashi, M. Goto, H. Tai, J. Yanagisawa, D. Metzger, S. Hashimoto, and S. Kato
Purification and Identification of p68 RNA Helicase Acting as a Transcriptional Coactivator Specific for the Activation Function 1 of Human Estrogen Receptor alpha
Mol. Cell. Biol., August 1, 1999; 19(8): 5363 - 5372.
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T. R. Ediger, W. L. Kraus, E. J. Weinman, and B. S. Katzenellenbogen
Estrogen Receptor Regulation of the Na+/H+ Exchanger Regulatory Factor
Endocrinology, July 1, 1999; 140(7): 2976 - 2982.
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J.L. Kornyei, Z. Vertes, A. Oszter, K.A. Kovacs, Ch.V. Rao, and M. Vertes
Opioid peptides inhibit the action of oestradiol on human myometrial cells in culture
Mol. Hum. Reprod., June 1, 1999; 5(6): 565 - 572.
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P. V. N. Bodine, H. A. Harris, and B. S. Komm
Suppression of Ligand-Dependent Estrogen Receptor Activity by Bone-Resorbing Cytokines in Human Osteoblasts
Endocrinology, June 1, 1999; 140(6): 2439 - 2451.
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J.R. Malayer, J. Cheng, and V.M. Woods
Estrogen Responses in Bovine Fetal Uterine Cells Involve Pathways Directed by Both Estrogen Response Element and Activator Protein-1
Biol Reprod, May 1, 1999; 60(5): 1204 - 1210.
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T. Improta-Brears, A. R. Whorton, F. Codazzi, J. D. York, T. Meyer, and D. P. McDonnell
Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium
PNAS, April 13, 1999; 96(8): 4686 - 4691.
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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.
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M. D. Sadar
Androgen-independent Induction of Prostate-specific Antigen Gene Expression via Cross-talk between the Androgen Receptor and Protein Kinase A Signal Transduction Pathways
J. Biol. Chem., March 19, 1999; 274(12): 7777 - 7783.
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D. Chen, P. E. Pace, R. C. Coombes, and S. Ali
Phosphorylation of Human Estrogen Receptor alpha  by Protein Kinase A Regulates Dimerization
Mol. Cell. Biol., February 1, 1999; 19(2): 1002 - 1015.
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D. Lee, P. Dong, D. Copolov, and A. T. Lim
D5 Dopamine Receptors Mediate Estrogen-Induced Stimulation of Hypothalamic Atrial Natriuretic Factor Neurons
Mol. Endocrinol., February 1, 1999; 13(2): 344 - 352.
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C. Patrone, E. Gianazza, S. Santagati, P. Agrati, and A. Maggi
Divergent Pathways Regulate Ligand-Independent Activation of ER{alpha} in SK-N-BE Neuroblastoma and COS-1 Renal Carcinoma Cells
Mol. Endocrinol., June 1, 1998; 12(6): 835 - 841.
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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.
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M. von Lindern, L. Boer, O. Wessely, M. Parker, and H. Beug
The Transactivation Domain AF-2 but Not the DNA-Binding Domain of the Estrogen Receptor Is Required to Inhibit Differentiation of Avian Erythroid Progenitors
Mol. Endocrinol., February 1, 1998; 12(2): 263 - 277.
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S. Kahmann, L. Vaßen, and L. Klein-Hitpass
Synergistic Enhancement of PRB-Mediated RU486 and R5020 Agonist Activities through Cyclic Adenosine 3',5'-Monophosphate Represents a Delayed Primary Response
Mol. Endocrinol., February 1, 1998; 12(2): 278 - 289.
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M. A. Razik, K. Lee, R. R. Price, M. R. Williams, R. R. Ongjoco, M. K. Dole, X. L. Rudner, M. M. Kwatra, and D. A. Schwinn
Transcriptional Regulation of the Human alpha 1a-Adrenergic Receptor Gene. CHARACTERIZATION OF THE 5'-REGULATORY AND PROMOTER REGION
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J. Tassignon and F. Haeseleer Abraham Borkowski
Natural Antiestrogen Receptor Autoantibodies in Man with Estrogenic Activity in Mammary Carcinoma Cell Culture: Study of their Mechanism of Action; Evidence for Involvement of Estrogen-Like Epitopes
J. Clin. Endocrinol. Metab., October 1, 1997; 82(10): 3464 - 3470.
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T. L. McCarthy, C. Ji, H. Shu, S. Casinghino, K. Crothers, P. Rotwein, and M. Centrella
17beta -Estradiol Potently Suppresses cAMP-induced Insulin-like Growth Factor-I Gene Activation in Primary Rat Osteoblast Cultures
J. Biol. Chem., July 18, 1997; 272(29): 18132 - 18139.
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C. L. Smith, Z. Nawaz, and B. W. O’Malley
Coactivator and Corepressor Regulation of the Agonist/Antagonist Activity of the Mixed Antiestrogen, 4-Hydroxytamoxifen
Mol. Endocrinol., June 1, 1997; 11(6): 657 - 666.
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Y. Zhang, C. A. Beck, A. Poletti, J. P. Clement IV, P. Prendergast, T.-T. Yip, T. W. Hutchens, D. P. Edwards, and N. L. Weigel
Phosphorylation of Human Progesterone Receptor by Cyclin-Dependent Kinase 2 on Three Sites That Are Authentic Basal Phosphorylation Sites In Vivo
Mol. Endocrinol., June 1, 1997; 11(6): 823 - 832.
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A. M. Nakhla, N. A. Romas, and W. Rosner
Estradiol Activates the Prostate Androgen Receptor and Prostate-specific Antigen Secretion through the Intermediacy of Sex Hormone-binding Globulin
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G. B. Tremblay, A. Tremblay, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, F. Labrie, and V. Giguère
Cloning, Chromosomal Localization, and Functional Analysis of the Murine Estrogen Receptor {beta}
Mol. Endocrinol., March 1, 1997; 11(3): 353 - 365.
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Y. Lee and J. Gorski
Estrogen-induced transcription of the progesterone receptor gene does not parallel estrogen receptor occupancy
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Insulin- and Mitogen-activated Protein Kinase-mediated Phosphorylation and Activation of Peroxisome Proliferator-activated Receptor gamma
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R. P. Matthews and G. S. McKnight
Characterization of the cAMP Response Element of the Cystic Fibrosis Transmembrane Conductance Regulator Gene Promoter
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D. Szapary, M. Xu, and S. S. Simons Jr.
Induction Properties of a Transiently Transfected Glucocorticoid-responsive Gene Vary with Glucocorticoid Receptor Concentration
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D. C. Leitman, C. H.R.M. Costa, H. Graf, J. D. Baxter, and R. C.J. Ribeiro
Thyroid Hormone Activation of Transcription Is Potentiated by Activators of cAMP-dependent Protein Kinase
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S. Kato, H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, et al.
Activation of the Estrogen Receptor Through Phosphorylation by Mitogen-Activated Protein Kinase
Science, December 1, 1995; 270(5241): 1491 - 1494.
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S. Mani, J. Allen, J. Clark, J. Blaustein, and B. O'Malley
Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior
Science, August 26, 1994; 265(5176): 1246 - 1249.
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S. K. Das, J. Tan, S. Raja, J. Halder, B. C. Paria, and S. K. Dey
Estrogen Targets Genes Involved in Protein Processing, Calcium Homeostasis, and Wnt Signaling in the Mouse Uterus Independent of Estrogen Receptor-alpha and -beta
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R. S. Piotrowicz, L. Ding, P. Maher, and E. G. Levin
Inhibition of Cell Migration by 24-kDa Fibroblast Growth Factor-2 Is Dependent upon the Estrogen Receptor
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