Steroid signaling in mature follicles is important for Drosophila ovulation

Proc Natl Acad Sci U S A. 2017 Jan 24;114(4):699-704. doi: 10.1073/pnas.1614383114. Epub 2017 Jan 9.

Abstract

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.

Keywords: EcR isoforms; Shade; ecdysone; ovulation; steroid signaling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA-Binding Proteins / metabolism
  • Drosophila / metabolism*
  • Drosophila / physiology
  • Drosophila Proteins / metabolism
  • Ecdysone / metabolism
  • Ecdysterone / metabolism
  • Female
  • Genes, Insect / physiology
  • Matrix Metalloproteinase 2 / metabolism
  • Oogenesis / physiology
  • Ovarian Follicle / metabolism
  • Ovarian Follicle / physiology
  • Ovulation / metabolism*
  • Ovulation / physiology
  • Protein Isoforms / metabolism
  • Receptors, Steroid / metabolism
  • Signal Transduction / physiology*
  • Steroids / metabolism*

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Protein Isoforms
  • Receptors, Steroid
  • Steroids
  • ecdysone receptor
  • Ecdysone
  • Ecdysterone
  • Matrix Metalloproteinase 2