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Endocrinology Vol. 140, No. 1 484-491
Copyright © 1999 by The Endocrine Society

ARTICLES

Tissue Compartment-Specific Estrogen Receptor-{alpha} Participation in the Mouse Uterine Epithelial Secretory Response1

David L. Buchanan, Tommy Setiawan, Dennis B. Lubahn, Julia A. Taylor, Takeshi Kurita, Gerald R. Cunha and Paul S. Cooke

Department of Veterinary Biosciences, University of Illinois (D.L.B., T.S., P.S.C.), Urbana, Illinois 61802; the Department of Anatomy, University of California (T.K., G.R.C.), San Francisco, California 94143; and the Departments of Biochemistry and Child Health, University of Missouri (J.A.T., D.B.L.), Columbia, Missouri 65211

Address all correspondence and requests for reprints to: Dr. Paul Cooke, Department of Veterinary Biosciences, University of Illinois, 2001 South Lincoln Avenue, Urbana, Illinois 61802. E-mail: p-cooke{at}uiuc.edu

17ß-Estradiol (E2) acts through the estrogen receptor (ER) to regulate uterine epithelial cell growth, proliferation, differentiation, and secretory protein production. We have previously shown that E2-induced uterine epithelial proliferation is mediated indirectly by ER{alpha}-positive stroma; epithelial ER{alpha} is neither necessary nor sufficient for E2-induced uterine epithelial mitogenesis. In the present study, we addressed the question of whether production of uterine epithelial secretory proteins and their messenger RNAs (mRNAs) requires ER{alpha} in stroma, epithelium, or both by analyzing tissue recombinations composed of uterine tissue from adult ER{alpha} knockout (ko) and neonatal BALB/c (wt) mice. Stroma (S) and epithelium (E) were separated by trypsinization, and four types of uterine tissue recombinants were prepared: wt-S + wt-E, wt-S + ko-E, ko-S + wt-E, and ko-S + ko-E. These tissue recombinants were grown as subrenal capsule grafts in intact female nude mice for 4 weeks, at which time the hosts were ovariectomized. To assess the production of secretory proteins and their mRNAs, 1 week after ovariectomy the hosts were given three daily injections of oil or E2 (100 ng), and then 24 h later the grafts were recovered and used for either ER or lactoferrin (LF) immunohistochemistry. To assess steady state mRNA levels by Northern blotting, hosts received one injection of oil or E2 24 h before harvest. ER immunohistochemistry was used to monitor the completeness of tissue separation. In wt-S + wt-E tissue recombinants from E2-treated hosts, the epithelium stained intensely for LF (an abundant E2-dependent uterine secretory protein), whereas similar tissue recombinants from oil-treated hosts showed minimal immunostaining. Conversely, LF immunostaining was minimal in wt-S + ko-E grafts from both oil- and E2-treated hosts. LF staining was also minimal in ko-S + ko-E and ko-S + wt-E tissue recombinants regardless of hormone treatment. For Northern analyses, the epithelial content of the tissue recombinants was monitored using the reference epithelial transcript, E-cadherin. While all tissue recombinant groups expressed E-cadherin mRNA, wt-S + wt-E tissue recombinants from E2-treated hosts produced a strong, single 2.6-kb band of LF mRNA. LF transcripts were minimal or absent in all other tissue recombinant types. Northern blotting results identical to those seen for LF were also observed for the uterine secretory protein complement component C3. Our data demonstrate that both stromal and epithelial ER{alpha} are required for the production of LF protein and of LF or C3 mRNAs in response to E2. Thus, in contrast to E2-induced epithelial mitogenesis, which requires only stromal ER{alpha}, both epithelial and stromal ER{alpha} are necessary for the production of E2-dependent epithelial secretory proteins.




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