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Submitted on June 15, 2006
Accepted on December 18, 2006
Laboratory of Reproductive Biology, National Institute for Basic Biology, Okazaki 444-8585, Japan; Core Research for Evolutional Science and Technology (CREST), Kawaguchi, Saitama 332-0012, Japan; Department of Molecular Biomechanics, Graduate University for Advanced Studies, Okazaki 444-8585, Japan; School of Life Science, Southwest University, 400715, Chongqing, P.R. China; National Research Institute of Aquaculture, Tamaki, Mie 516-0423, Japan; Laboratory of Sex Differentiation, National Institute for Basic Biology, Okazaki 444-8585, Japan
* To whom correspondence should be addressed. E-mail: nagahama{at}nibb.ac.jp.
Increasing evidence suggests the crucial role of estrogen in ovarian differentiation of non-mammalian vertebrates including fish. The present study has investigated the plausible role of Foxl2 in ovarian differentiation through transcriptional regulation of aromatase gene, using mono-sex fry of tilapia. Foxl2 expression is sexually dimorphic, like Cyp19a1, co-localizing with Cyp19a1 and Ad4BP/Sf-1 in the stromal cells and interstitial cells in gonads of normal XX and sex-reversed XY fish, before the occurrence of morphological sex differentiation. Under in vitro conditions, Foxl2 binds to the sequence, ACAAATA in the promoter region of the Cyp19a1 gene directly through its forkhead domain (FH), and activates the transcription of Cyp19a1 with its C-terminus. Foxl2 can also interact through the FH with the ligand binding domain (LBD) of Ad4BP/SF-1 to form a heterodimer and enhance the Ad4BP/SF-1 mediated Cyp19a1 transcription. Disruption of endogenous Foxl2 in XX tilapia by overexpression of its dominant negative mutant (M3) induces varying degrees of testicular development with occasional sex reversal from ovary to testis. Such fish display reduced expression of Cyp19a1 as well as a drop in the serum levels of estradiol-17
(E2) and 11-ketotestosterone (11-KT). Although the XY fish with wild type tilapia Foxl2 (tFoxl2) overexpression never exhibited a complete sex reversal, there were significant structural changes, such as tissue degeneration, somatic cell proliferation and induction of aromatase, with increased serum levels of E2 and 11-KT. Altogether, these results suggest that Foxl2 plays a decisive role in the ovarian differentiation of the Nile tilapia by regulating aromatase expression and possibly the entire steroidogenic pathway.
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