Increased lateral tension is sufficient for epithelial folding in Drosophila

Development. 2020 Dec 4;147(23):dev194316. doi: 10.1242/dev.194316.

Abstract

The folding of epithelial sheets is important for tissues, organs and embryos to attain their proper shapes. Epithelial folding requires subcellular modulations of mechanical forces in cells. Fold formation has mainly been attributed to mechanical force generation at apical cell sides, but several studies indicate a role of mechanical tension at lateral cell sides in this process. However, whether lateral tension increase is sufficient to drive epithelial folding remains unclear. Here, we have used optogenetics to locally increase mechanical force generation at apical, lateral or basal sides of epithelial Drosophila wing disc cells, an important model for studying morphogenesis. We show that optogenetic recruitment of RhoGEF2 to apical, lateral or basal cell sides leads to local accumulation of F-actin and increase in mechanical tension. Increased lateral tension, but not increased apical or basal tension, results in sizeable fold formation. Our results stress the diversification of folding mechanisms between different tissues and highlight the importance of lateral tension increase for epithelial folding.

Keywords: Drosophila; Epithelial folding; Mechanical tension; Optogenetics; RhoGEF2; Wing disc.

MeSH terms

  • Actins / genetics
  • Animals
  • Biomechanical Phenomena / genetics*
  • Body Patterning / genetics*
  • Cell Cycle Proteins / genetics*
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Epithelial Cells / metabolism
  • Epithelial Cells / ultrastructure
  • Gene Expression Regulation, Developmental / genetics
  • Morphogenesis / genetics*
  • Stress, Mechanical
  • Wings, Animal / growth & development
  • Wings, Animal / ultrastructure

Substances

  • Actins
  • Cell Cycle Proteins
  • Drosophila Proteins
  • sav protein, Drosophila