Theory of epithelial sheet morphology in three dimensions

Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):27-32. doi: 10.1073/pnas.1312076111. Epub 2013 Dec 23.

Abstract

Morphogenesis during embryo development requires the coordination of mechanical forces to generate the macroscopic shapes of organs. We propose a minimal theoretical model, based on cell adhesion and actomyosin contractility, which describes the various shapes of epithelial cells and the bending and buckling of epithelial sheets, as well as the relative stability of cellular tubes and spheres. We show that, to understand these processes, a full 3D description of the cells is needed, but that simple scaling laws can still be derived. The morphologies observed in vivo can be understood as stable points of mechanical equations and the transitions between them are either continuous or discontinuous. We then focus on epithelial sheet bending, a ubiquitous morphogenetic process. We calculate the curvature of an epithelium as a function of actin belt tension as well as of cell-cell and and cell-substrate tension. The model allows for a comparison of the relative stabilities of spherical or cylindrical cellular structures (acini or tubes). Finally, we propose a unique type of buckling instability of epithelia, driven by a flattening of individual cell shapes, and discuss experimental tests to verify our predictions.

Keywords: active foams; biophysics; mathematical modeling.

MeSH terms

  • Actins / chemistry
  • Actomyosin / chemistry
  • Actomyosin / metabolism
  • Animals
  • Apoptosis
  • Cell Adhesion
  • Cell Communication
  • Cell Shape
  • Drosophila
  • Elasticity
  • Epithelial Cells / cytology*
  • Epithelium / growth & development*
  • Imaging, Three-Dimensional
  • Models, Theoretical
  • Morphogenesis
  • Wings, Animal / pathology
  • Xenopus

Substances

  • Actins
  • Actomyosin