Circadian Clock Gene Regulation of Steroidogenic Acute Regulatory Protein Gene Expression in Preovulatory Ovarian Follicles

Apr 14, 2007Endocrinology

Circadian clock genes controlling hormone-making protein in egg follicles before ovulation

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Abstract

The expression of clock genes in preovulatory follicles of laying quail shows diurnal changes that may influence ovulation timing.

Circadian clocks are present in both the central pacemaker and peripheral organs, including the ovary in poultry.
The largest preovulatory follicle (F1) exhibits diurnal variations in clock genes Per2 and Per3, while smaller follicles do not.
The steroidogenic acute regulatory protein (StAR) gene, which is involved in progesterone synthesis, shows 24-hour expression changes in the F1 follicle aligned with Per2.
The StAR gene's expression is linked to the circadian clock, evidenced by the presence of E-box enhancers that interact with CLOCK/BMAL1 to promote transcription.
LH administration enhances the activity of the StAR gene promoter, suggesting the LH-responsive F1 follicular clock plays a role in regulating progesterone release.

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It is now known that circadian clocks are localized not only in the central pacemaker but also in peripheral organs. An example of a clock-dependent peripheral organ is the ovary of domestic poultry in which ovulation is induced by the positive feedback action of ovarian progesterone on the neuroendocrine system to generate a preovulatory release of LH during a daily 6-10 h "open period" of the ovulatory cycle. It has been assumed previously that the timing of ovulation in poultry is controlled solely by a clock-dependent mechanism within the neuroendocrine system. Here, we question this assumption by demonstrating the expression of the clock genes, Per2 (Period 2) and Per3, Clock, and Bmal1 (brain and muscle Arnt-like protein 1), in preovulatory follicles in laying quail. Diurnal changes in Per2 and Per3 expression were seen in the largest preovulatory follicle (F1) but not in smaller follicles. We next sought to identify clock-driven genes in preovulatory follicles focusing on those involved in the synthesis of progesterone. One such gene was identified, encoding steroidogenic acute regulatory protein (StAR), which showed 24-h changes in expression in the F1 follicle coinciding with those of Per2. Evidence that StAR gene expression is clock driven was obtained by showing that its 5' flanking region contains E-box enhancers that bind to CLOCK/BMAL1 heterodimers to activate gene transcription. We also showed that LH administration increased the promoter activity of chicken StAR. We therefore suggest that the timing of ovulation in poultry involves an LH-responsive F1 follicular clock that is involved in the timing of the preovulatory release of progesterone.

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Circadian Clock Gene Regulation of Steroidogenic Acute Regulatory Protein Gene Expression in Preovulatory Ovarian Follicles

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