Shear-induced damped oscillations in an epithelium depend on actomyosin contraction and E-cadherin cell adhesion

Elife. 2018 Nov 14:7:e39640. doi: 10.7554/eLife.39640.

Abstract

Shear forces between cells occur during global changes in multicellular organization during morphogenesis and tissue growth, yet how cells sense shear forces and propagate a response across a tissue is unknown. We found that applying exogenous shear at the midline of an epithelium induced a local, short-term deformation near the shear plane, and a long-term collective oscillatory movement across the epithelium that spread from the shear-plane and gradually dampened. Inhibiting actomyosin contraction or E-cadherin trans-cell adhesion blocked oscillations, whereas stabilizing actin filaments prolonged oscillations. Combining these data with a model of epithelium mechanics supports a mechanism involving the generation of a shear-induced mechanical event at the shear plane which is then relayed across the epithelium by actomyosin contraction linked through E-cadherin. This causes an imbalance of forces in the epithelium, which is gradually dissipated through oscillatory cell movements and actin filament turnover to restore the force balance across the epithelium.

Keywords: MDCK; cell biology; cell mechanics; collective cell behavior; developmental biology; epithelial cells; microfabrication; tissue mechanics.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Actomyosin / metabolism*
  • Animals
  • Cadherins / metabolism*
  • Cell Adhesion / drug effects
  • Cell Count
  • Cell Movement / drug effects
  • Depsipeptides / pharmacology
  • Dogs
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelium / metabolism*
  • Heterocyclic Compounds, 4 or More Rings / pharmacology
  • Madin Darby Canine Kidney Cells
  • Rheology
  • Stress, Mechanical*

Substances

  • Actins
  • Cadherins
  • Depsipeptides
  • Heterocyclic Compounds, 4 or More Rings
  • jasplakinolide
  • blebbistatin
  • Actomyosin