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Originally published In Press as doi:10.1074/jbc.M212312200 on January 31, 2003

J. Biol. Chem., Vol. 278, Issue 15, 12834-12845, April 11, 2003
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Mechanistic Differences in the Activation of Estrogen Receptor-alpha (ERalpha )- and ERbeta -dependent Gene Expression by cAMP Signaling Pathway(s)*

Kevin M. ColemanDagger , Martin DutertreDagger , Abeer El-Gharbawy§, Brian G. Rowan§, Nancy L. WeigelDagger , and Carolyn L. SmithDagger

From the Dagger  Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030-3498 and the § Department of Biochemistry and Molecular Biology, Medical College of Ohio, Toledo, Ohio 43614-5804

Although increases in intracellular cAMP can stimulate estrogen receptor-alpha (ERalpha ) activity in the absence of exogenous hormone, no studies have addressed whether ERbeta can be similarly regulated. In transient transfections, forskolin plus 3-isobutyl-1-methylxanthine (IBMX), which increases intracellular cAMP, stimulated the transcriptional activities of both ERalpha and ERbeta . This effect was blocked by the protein kinase A inhibitor H89 (N-(2-(p-bromocinnamylamino)-ethyl)-5-isoquinolinesulfonamide) and was dependent on an estrogen response element. A 12-O-tetradecanoylphorbol-13-acetate response element (TRE) located 5' to the estrogen response element was necessary for cAMP-dependent activation of gene expression by ERbeta but not ERalpha , indicating that the former subtype requires a functional interaction with TRE-interacting factor(s) to stimulate transcription. Both p160 and CREB-binding protein coactivators stimulated cAMP-induced ERalpha and ERbeta transcriptional activity. However, mutation of the two cAMP-inducible SRC-1 phosphorylation sites important for cAMP activation of chicken progesterone receptor or all seven known SRC-1 phosphorylation sites did not specifically impair cAMP activation of ERalpha . The E/F domains of ERalpha are sufficient for activation by forskolin/IBMX, and this is accompanied by an increase in receptor phosphorylation. In contrast, cAMP signaling reduces the phosphorylation of the corresponding region of ERbeta , and this correlates with the lack of forskolin/IBMX stimulated transcriptional activity. Our data suggest that cAMP activation of ERalpha transcriptional activity is associated with receptor instead of SRC-1 phosphorylation. Moreover, differences in the cofactor requirements, domains of ERalpha and ERbeta sufficient for forskolin/IBMX activation, and the effect of cAMP on receptor phosphorylation indicate that this signaling pathway utilizes distinct mechanisms to stimulate ERalpha and ERbeta transcriptional activity.

* This work was supported by a UNCF/Merck fellowship and National Institutes of Health Training Fellowship HD07165 (to K. M. C.), Department of Defense Breast Cancer Research Program Fellowship DAMD17-00-1-0136 (to M. D.), Department of Defense Breast Cancer Research Program Awards DAMD17-02-1-0531 and DAMD17-02-1-0530 (to B. G. R.), and Department of Defense Grant DAMD17-98-1-8282 and National Institutes of Health Grant DK53002 (to C. L. S.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. Molecular and Cellular Biology, One Baylor Plaza, Houston, TX 77030. Tel.: 713-798-6235; Fax: 713-790-1275; E-mail: carolyns@bcm.tmc.edu.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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