Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis

PLoS Biol. 2020 Nov 30;18(11):e3000940. doi: 10.1371/journal.pbio.3000940. eCollection 2020 Nov.

Abstract

It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, in which a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells grow, the overlying epithelial cells flatten in a wave that begins in the anterior. Here, we demonstrate that an anterior to posterior gradient of decreasing cytoplasmic pressure is present across the nurse cells and that this gradient acts through TGFβ to control both the triggering and the progression of the wave of epithelial cell flattening. Our data indicate that intrinsic nurse cell growth is important to control proper nurse cell pressure. Finally, we reveal that nurse cell pressure and subsequent TGFβ activity in the stretched cells combine to increase follicle elongation in the anterior, which is crucial for allowing nurse cell growth and pressure control. More generally, our results reveal that during development, inner cytoplasmic pressure in individual cells has an important role in shaping their neighbors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomechanical Phenomena
  • Cell Differentiation
  • Cell Polarity
  • Cell Shape
  • Cytoplasm / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / metabolism*
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Female
  • Microscopy, Atomic Force
  • Models, Biological
  • Oocytes / cytology
  • Oocytes / metabolism
  • Oogenesis
  • Ovarian Follicle / cytology*
  • Ovarian Follicle / metabolism*
  • Pressure
  • Signal Transduction
  • Transforming Growth Factor beta / metabolism

Substances

  • Drosophila Proteins
  • Transforming Growth Factor beta

Grant support

This work received supported by the Agence Nationale de la recherche (Blanc 12-SVSE-0023-01, MechInMorph to AB and MG) (https://anr.fr), the Centre National pour la Recherche Scientifique (https://www.cnrs.fr), and the Ecole Normale Supérieure of Lyon (http://www.ens-lyon.fr). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.