Actomyosin controls planarity and folding of epithelia in response to compression

Nat Mater. 2020 Jan;19(1):109-117. doi: 10.1038/s41563-019-0461-x. Epub 2019 Aug 26.

Abstract

Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression over shorter timescales. Here, using suspended epithelia, we uncover the immediate response of epithelial tissues to the application of in-plane compressive strains (5-80%). We show that fast compression induces tissue buckling followed by actomyosin-dependent tissue flattening that erases the buckle within tens of seconds, in both mono- and multi-layered epithelia. Strikingly, we identify a well-defined limit to this response, so that stable folds form in the tissue when compressive strains exceed a 'buckling threshold' of ~35%. A combination of experiment and modelling shows that this behaviour is orchestrated by adaptation of the actomyosin cytoskeleton as it re-establishes tissue tension following compression. Thus, tissue pre-tension allows epithelia to both buffer against deformation and sets their ability to form and retain folds during morphogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actomyosin / chemistry*
  • Animals
  • Cadherins / physiology
  • Compressive Strength
  • Cytoskeleton
  • Dogs
  • Elasticity
  • Epithelial Cells / cytology
  • Epithelium / embryology
  • Epithelium / physiology*
  • Green Fluorescent Proteins
  • Madin Darby Canine Kidney Cells
  • Microscopy, Confocal
  • Models, Biological
  • Morphogenesis
  • Stress, Mechanical
  • Viscosity

Substances

  • Cadherins
  • Green Fluorescent Proteins
  • Actomyosin