Chiral cell sliding drives left-right asymmetric organ twisting

Elife. 2018 Jun 12:7:e32506. doi: 10.7554/eLife.32506.

Abstract

Polarized epithelial morphogenesis is an essential process in animal development. While this process is mostly attributed to directional cell intercalation, it can also be induced by other mechanisms. Using live-imaging analysis and a three-dimensional vertex model, we identified 'cell sliding,' a novel mechanism driving epithelial morphogenesis, in which cells directionally change their position relative to their subjacent (posterior) neighbors by sliding in one direction. In Drosophila embryonic hindgut, an initial left-right (LR) asymmetry of the cell shape (cell chirality in three dimensions), which occurs intrinsically before tissue deformation, is converted through LR asymmetric cell sliding into a directional axial twisting of the epithelial tube. In a Drosophila inversion mutant showing inverted cell chirality and hindgut rotation, cell sliding occurs in the opposite direction to that in wild-type. Unlike directional cell intercalation, cell sliding does not require junctional remodeling. Cell sliding may also be involved in other cases of LR-polarized epithelial morphogenesis.

Keywords: Cell chirality; Cell sliding; D. melanogaster; Epithelial morphogenesis; Left-right asymmetry; developmental biology; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Biomarkers / metabolism
  • Biomechanical Phenomena
  • Body Patterning / physiology*
  • Cell Culture Techniques
  • Cell Movement
  • Cell Polarity
  • Cell Shape
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Embryo, Nonmammalian
  • Epithelial Cells / cytology*
  • Epithelial Cells / metabolism
  • Gastrointestinal Tract / cytology*
  • Gastrointestinal Tract / metabolism
  • Gene Expression
  • Myosin Type I / genetics
  • Myosin Type I / metabolism
  • Time-Lapse Imaging

Substances

  • Biomarkers
  • Drosophila Proteins
  • Myo31DF protein, Drosophila
  • Myosin Type I

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.