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Molecular Endocrinology 13 (10): 1672-1685
Copyright © 1999 by The Endocrine Society

The Estrogen Receptor Enhances AP-1 Activity by Two Distinct Mechanisms with Different Requirements for Receptor Transactivation Functions

Paul Webb, Phuong Nguyen, Cathleen Valentine, Gabriela N. Lopez, Grace R. Kwok, Eileen McInerney, Benita S. Katzenellenbogen, Eva Enmark, Jan-Åke Gustafsson, Stefan Nilsson and Peter J. Kushner

Metabolic Research Unit (P.W., P.N., C.V., G.N.L., G.R.K., P.J.K.) University of California School of Medicine San Francisco, California 94143
Department of Molecular and Integrative Physiology (E.M., B.S.K.) University of Illinois Urbana, Illinois 61801
KaroBio AB (S.N.) Novum Huddinge, Sweden S-14157
Department of Medical Nutrition and Biosciences (E.E., J.-A.G.) Karolinska Institute Huddinge, Sweden S-14186

Estrogen receptors (ERs {alpha} and ß) enhance transcription in response to estrogens by binding to estrogen response elements (EREs) within target genes and utilizing transactivation functions (AF-1 and AF-2) to recruit p160 coactivator proteins. The ERs also enhance transcription in response to estrogens and antiestrogens by modulating the activity of the AP-1 protein complex. Here, we examine the role of AF-1 and AF-2 in ER action at AP-1 sites. Estrogen responses at AP-1 sites require the integrity of the ER{alpha} AF-1 and AF-2 activation surfaces and the complementary surfaces on the p160 coactivator GRIP1 (glucocorticoid receptor interacting protein 1), the NID/AF-1 region, and NR boxes. Thus, estrogen-liganded ER{alpha} utilizes the same protein-protein contacts to transactivate at EREs and AP-1 sites. In contrast, antiestrogen responses are strongly inhibited by ER{alpha} AF-1 and weakly inhibited by AF-2. Indeed, ER{alpha} truncations that lack AF-1 enhance AP-1 activity in the presence of antiestrogens, but not estrogens. This phenotype resembles ERß, which naturally lacks constitutive AF-1 activity. We conclude that the ERs enhance AP-1 responsive transcription by distinct mechanisms with different requirements for ER transactivation functions. We suggest that estrogen-liganded ER enhances AP-1 activity via interactions with p160s and speculate that antiestrogen-liganded ER enhances AP-1 activity via interactions with corepressors.




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M. J. Chisamore, Y. Ahmed, D. J. Bentrem, V. C. Jordan, and D. A. Tonetti
Novel Antitumor Effect of Estradiol in Athymic Mice Injected with a T47D Breast Cancer Cell Line Overexpressing Protein Kinase C{alpha}
Clin. Cancer Res., October 1, 2001; 7(10): 3156 - 3165.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
G. Lazennec, D. Bresson, A. Lucas, C. Chauveau, and F. Vignon
ER{beta} Inhibits Proliferation and Invasion of Breast Cancer Cells
Endocrinology, September 1, 2001; 142(9): 4120 - 4130.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
C. M. Klinge
Estrogen receptor interaction with estrogen response elements
Nucleic Acids Res., July 15, 2001; 29(14): 2905 - 2919.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
R. Yu, V. Hebbar, D. W. Kim, S. Mandlekar, J. M. Pezzuto, and A.-N. T. Kong
Resveratrol Inhibits Phorbol Ester and UV-Induced Activator Protein 1 Activation by Interfering with Mitogen-Activated Protein Kinase Pathways
Mol. Pharmacol., July 1, 2001; 60(1): 217 - 224.
[Abstract] [Full Text]

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 EndocrinologyHome page
R. H. Price Jr., C. A. Butler, P. Webb, R. Uht, P. Kushner, and R. J. Handa
A Splice Variant of Estrogen Receptor {beta} Missing Exon 3 Displays Altered Subnuclear Localization and Capacity for Transcriptional Activation
Endocrinology, May 1, 2001; 142(5): 2039 - 2049.
[Abstract] [Full Text]

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 Learn. Mem.Home page
R. D. Brinton
Cellular and Molecular Mechanisms of Estrogen Regulation of Memory Function and Neuroprotection Against Alzheimer's Disease: Recent Insights and Remaining Challenges
Learn. Mem., May 1, 2001; 8(3): 121 - 133.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
E. Vegeto, C. Bonincontro, G. Pollio, A. Sala, S. Viappiani, F. Nardi, A. Brusadelli, B. Viviani, P. Ciana, and A. Maggi
Estrogen Prevents the Lipopolysaccharide-Induced Inflammatory Response in Microglia
J. Neurosci., March 15, 2001; 21(6): 1809 - 1818.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
I. Samudio, C. Vyhlidal, F. Wang, M. Stoner, I. Chen, M. Kladde, R. Barhoumi, R. Burghardt, and S. Safe
Transcriptional Activation of Deoxyribonucleic Acid Polymerase {{alpha}} Gene Expression in MCF-7 Cells by 17{{beta}}-Estradiol
Endocrinology, March 1, 2001; 142(3): 1000 - 1008.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. E. Quaedackers, C. E. Van Den Brink, S. Wissink, R. H. M. M. Schreurs, J.-A. Gustafsson, P. T. Van Der Saag, and B. Van Der Burg
4-Hydroxytamoxifen Trans-Represses Nuclear Factor-{{kappa}}B Activity in Human Osteoblastic U2-OS Cells through Estrogen Receptor (ER){{alpha}}, and Not through ER{{beta}}
Endocrinology, March 1, 2001; 142(3): 1156 - 1166.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. Lu and V. Giguere
Requirement of Ras-Dependent Pathways for Activation of the Transforming Growth Factor {beta}3 Promoter by Estradiol
Endocrinology, February 1, 2001; 142(2): 751 - 759.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
W. Feng, P. Webb, P. Nguyen, X. Liu, J. Li, M. Karin, and P. J. Kushner
Potentiation of Estrogen Receptor Activation Function 1 (AF-1) by Src/JNK through a Serine 118-Independent Pathway
Mol. Endocrinol., January 1, 2001; 15(1): 32 - 45.
[Abstract] [Full Text]

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 JNCI J Natl Cancer InstHome page
R. Schiff, P. Reddy, M. Ahotupa, E. Coronado-Heinsohn, M. Grim, S. G. Hilsenbeck, R. Lawrence, S. Deneke, R. Herrera, G. C. Chamness, et al.
Oxidative Stress and AP-1 Activity in Tamoxifen-Resistant Breast Tumors In Vivo
J Natl Cancer Inst, December 6, 2000; 92(23): 1926 - 1934.
[Abstract] [Full Text] [PDF]

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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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 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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 Clin. Cancer Res.Home page
K. Yao, E.-S. Lee, D. J. Bentrem, G. England, J. I. M. Schafer, R. M. O'Regan, and V. C. Jordan
Antitumor Action of Physiological Estradiol on Tamoxifen-stimulated Breast Tumors Grown in Athymic Mice
Clin. Cancer Res., May 1, 2000; 6(5): 2028 - 2036.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. J. Scheidegger, B. Cenni, D. Picard, and P. Delafontaine
Estradiol Decreases IGF-1 and IGF-1 Receptor Expression in Rat Aortic Smooth Muscle Cells. MECHANISMS FOR ITS ATHEROPROTECTIVE EFFECTS
J. Biol. Chem., December 1, 2000; 275(49): 38921 - 38928.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. V. Weatherman and T. S. Scanlan
Unique Protein Determinants of the Subtype-selective Ligand Responses of the Estrogen Receptors (ERalpha and ERbeta ) at AP-1 Sites
J. Biol. Chem., February 2, 2001; 276(6): 3827 - 3832.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. Webb, P. Nguyen, C. Valentine, R. V. Weatherman, T. S. Scanlan, and P. J. Kushner
An Antiestrogen-responsive Estrogen Receptor-alpha Mutant (D351Y) Shows Weak AF-2 Activity in the Presence of Tamoxifen
J. Biol. Chem., November 22, 2000; 275(48): 37552 - 37558.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Jakacka, M. Ito, J. Weiss, P.-Y. Chien, B. D. Gehm, and J. L. Jameson
Estrogen Receptor Binding to DNA Is Not Required for Its Activity through the Nonclassical AP1 Pathway
J. Biol. Chem., April 20, 2001; 276(17): 13615 - 13621.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. An, C. Tzagarakis-Foster, T. C. Scharschmidt, N. Lomri, and D. C. Leitman
Estrogen Receptor beta -Selective Transcriptional Activity and Recruitment of Coregulators by Phytoestrogens
J. Biol. Chem., May 18, 2001; 276(21): 17808 - 17814.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Teyssier, K. Belguise, F. Galtier, and D. Chalbos
Characterization of the Physical Interaction between Estrogen Receptor alpha and JUN Proteins
J. Biol. Chem., September 21, 2001; 276(39): 36361 - 36369.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. R. Walters, M. Dutertre, and C. L. Smith
SKF-82958 Is a Subtype-selective Estrogen Receptor-alpha (ERalpha ) Agonist That Induces Functional Interactions between ERalpha and AP-1
J. Biol. Chem., January 11, 2002; 277(3): 1669 - 1679.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Kahlert, S. Nuedling, M. van Eickels, H. Vetter, R. Meyer, and C. Grohe
Estrogen Receptor alpha Rapidly Activates the IGF-1 Receptor Pathway
J. Biol. Chem., June 9, 2000; 275(24): 18447 - 18453.
[Abstract] [Full Text] [PDF]


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