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Originally published In Press as doi:10.1074/jbc.M201829200 on May 1, 2002

J. Biol. Chem., Vol. 277, Issue 27, 24353-24360, July 5, 2002
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Opposing Action of Estrogen Receptors alpha  and beta  on Cyclin D1 Gene Expression*

Meng-Min LiuDagger , Chris Albanese§, Carol M. Anderson, Kristin Hilty, Paul Webb, Rosalie M. UhtDagger ||, Richard H. Price Jr.Dagger , Richard G. Pestell§, and Peter J. KushnerDagger **

From the Dagger  Department of Medicine, University of California, San Francisco, California 94112-1640, the § Albert Einstein Cancer Center, Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, Bronx, New York 10461, and the  Metabolic Research Unit, University of California, San Francisco, California 94143

Induction of cyclin D1 gene transcription by estrogen receptor alpha  (ERalpha ) plays an important role in estrogen-mediated proliferation. There is no classical estrogen response element in the cyclin D1 promoter, and induction by ERalpha has been mapped to an alternative response element, a cyclic AMP-response element at -57, with possible participation of an activating protein-1 site at -954. The action of ERbeta at the cyclin D1 promoter is unknown, although evidence suggests that ERbeta may inhibit the proliferative action of ERalpha . We examined the response of cyclin D1 promoter constructs by luciferase assay and the response of the endogenous protein by Western blot in HeLa cells transiently expressing ERalpha , ERalpha K206A (a derivative that is superactive at alternative response elements), or ERbeta . In each case, ER activation at the cyclin D1 promoter is mediated by both the cyclic AMP-response element and the activating protein-1 site, which play partly redundant roles. The activation by ERbeta occurs only with antiestrogens. Estrogens, which activate cyclin D1 gene expression with ERalpha , inhibit expression with ERbeta . Strikingly, the presence of ERbeta completely inhibits cyclin D1 gene activation by estrogen and ERalpha or even by estrogen and the superactive ERalpha K206A. The observation of the opposing action and dominance of ERbeta over ERalpha in activation of cyclin D1 gene expression has implications for the postulated role of ERbeta as a modulator of the proliferative effects of estrogen.

* This work was supported by National Institutes of Health Grant R01 CA80210 (to P. J. K.) and R01 CA70896, R01 CA75503, R01 CA86072, the Breast Cancer Alliance Inc., The Susan Komen Breast Cancer Foundation (to R. G. P.).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.

|| Present address: Depts. of Pathology and Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, VA 22908-0214.

** Consultant, Director, and holder of significant financial interests in KaroBio AB, a Swedish company that develops pharmaceuticals that target nuclear receptors. To whom correspondence should be addressed: Dept. of Medicine, 2200 Post St., Rm. C442, University of California, San Francisco, CA 94112-1640. Tel.: 415-476-6790; Fax: 415-885-7724; E-mail: kushner@itsa.ucsf.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.


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