Starvation induces FoxO-dependent mitotic-to-endocycle switch pausing during Drosophila oogenesis

Development. 2014 Aug;141(15):3013-21. doi: 10.1242/dev.108399. Epub 2014 Jul 3.

Abstract

When exposed to nutrient challenge, organisms have to adapt their physiology in order to balance reproduction with adult fitness. In mammals, ovarian follicles enter a massive growth phase during which they become highly dependent on gonadotrophic factors and nutrients. Somatic tissues play a crucial role in integrating these signals, controlling ovarian follicle atresia and eventually leading to the selection of a single follicle for ovulation. We used Drosophila follicles as a model to study the effect of starvation on follicle maturation. Upon starvation, Drosophila vitellogenic follicles adopt an 'atresia-like' behavior, in which some slow down their development whereas others enter degeneration. The mitotic-to-endocycle (M/E) transition is a critical step during Drosophila oogenesis, allowing the entry of egg chambers into vitellogenesis. Here, we describe a specific and transient phase during M/E switching that is paused upon starvation. The Insulin pathway induces the pausing of the M/E switch, blocking the entry of egg chambers into vitellogenesis. Pausing of the M/E switch involves a previously unknown crosstalk between FoxO, Cut and Notch that ensures full reversion of the process and rapid resumption of oogenesis upon refeeding. Our work reveals a novel genetic mechanism controlling the extent of the M/E switch upon starvation, thus integrating metabolic cues with development, growth and reproduction.

Keywords: Drosophila; Follicle; M/E switch; Oogenesis; dFoxO.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle
  • Cytoplasm / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster / physiology*
  • Female
  • Food Deprivation*
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / physiology*
  • Gene Expression Regulation
  • Green Fluorescent Proteins / metabolism
  • Mitosis*
  • Oocytes / cytology
  • Oogenesis / physiology*
  • Ovarian Follicle / metabolism
  • Ovulation
  • Ploidies
  • Receptors, Notch / metabolism
  • Signal Transduction
  • Vitellogenesis

Substances

  • Drosophila Proteins
  • FOXO protein, Drosophila
  • Forkhead Transcription Factors
  • Receptors, Notch
  • Green Fluorescent Proteins