Steroid signaling in mature follicles is important for Drosophila ovulation
Significance Ovulation is thought to be divergent from insects to mammals. In the latter case, ovulation is regulated by luteinizing hormone and the steroid hormone progesterone, neither of which is found in insects so far. This paper reports a role of ecdysteroids in Drosophila ovulation. Similar to the action of progesterone in mammals, 20-hydroxyecdysone produced in Drosophila follicle cells activates one of its receptors, EcR.B2, to allow proper activation of matrix metalloproteinase and follicle rupture. The conservation of steroid signaling in ovulation makes Drosophila a simple model to define the mechanism of steroid action in ovulation. Although ecdysteroid signaling regulates multiple steps in oogenesis, it is not known whether it regulates Drosophila ovulation, a process involving a matrix metalloproteinase-dependent follicle rupture. In this study, we demonstrated that ecdysteroid signaling is operating in mature follicle cells to control ovulation. Moreover, knocking down shade ( shd ), encoding the monooxygenase that converts ecdysone (E) to the more active 20-hydroxyecdysone (20E), specifically in mature follicle cells, blocked follicle rupture, which was rescued by ectopic expression of shd or exogenous 20E. In addition, disruption of the Ecdysone receptor ( EcR ) in mature follicle cells mimicked shd -knockdown defects, which were reversed by ectopic expression of EcR.B2 but not by EcR.A or EcR.B1 isoforms. Furthermore, we showed that ecdysteroid signaling is essential for the proper activation of matrix metalloproteinase 2 (Mmp2) for follicle rupture. Our data strongly suggest that 20E produced in follicle cells before ovulation activates EcR.B2 to prime mature follicles to be responsive to neuronal ovulatory stimuli, thus providing mechanistic insights into steroid signaling in Drosophila ovulation.
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