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A more recent version of this article appeared on September 8, 2006
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M601522200v1
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Papers In Press, published online ahead of print July 17, 2006
J. Biol. Chem, 10.1074/jbc.M601522200
Submitted on February 16, 2006
Revised on July 5, 2006
Accepted on July 17, 2006

Estrogen induced proliferation of uterine epithelial cells is independent of estrogen receptor alpha binding to classical estrogen response elements

Jeanne E. O'Brien, Theresa J. Peterson, Ming Han Tong, Eun-Jig Lee, Liza E. Pfaff, Sylvia C. Hewitt, Kenneth S. Korach, Jeffrey Weiss, and J. Larry Jameson

Endocrinology, Metabolism, and Molecular Medicine, Feinberg School of Medicine Northwestern University, Chicago, IL 60622

Corresponding Author: ljameson{at}northwestern.edu

Acting via the estrogen receptor (ER), estradiol exerts pleomorphic effects on the uterus, producing cyclical waves of cellular proliferation and differentiation in preparation for embryo implantation. In the classical pathway, the ER binds directly to an estrogen response element (ERE) to activate or repress gene expression. However, emerging evidence supports the existence of nonclassical pathways in which the activated ER alters gene expression through protein-protein tethering with transcription factors such as cfos/cjun B (AP-1) and Sp-1. In this report, we examined the relative roles of classical and nonclassical ER signaling in vivo by comparing the estrogen-dependent uterine response in mice that express wild-type ERalpha , a mutant ERalpha (E207A/G208A) that selectively lacks ERE binding, or ERalpha null. In the compound heterozygote (AA/-) female, the nonclassical allele (AA) was insufficient to mediate an acute uterotrophic response to estradiol (E2). The uterine epithelial proliferative response to E2 and 4-hydroxytamoxifen (4HT) was retained in the AA/- females and uterine luminal epithelial height increased commensurate with the extent of ERalpha signaling. This proliferative response was confirmed by BrdU incorporation. Microarray experiments identified Cdkn1A (p21) as a nonclassical pathway responsive gene and transient expression experiments using the Cdkn1A promoter confirmed transcriptional responses to the ERalpha (E207A/G208A) mutant. These results indicate that nonclassical ERalpha signaling is sufficient to restore luminal epithelial proliferation but not other estrogen-responsive events such as fluid accumulation and hyperemia. We conclude that nonclassical pathway signaling via ERalpha plays a critical physiologic role in the uterine response to estrogen.


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