Cell-to-cell heterogeneity in cortical tension specifies curvature of contact surfaces in Caenorhabditis elegans embryos

PLoS One. 2012;7(1):e30224. doi: 10.1371/journal.pone.0030224. Epub 2012 Jan 10.

Abstract

In the two-cell stage embryos of Caenorhabditis elegans, the contact surface of the two blastomeres forms a curve that bulges from the AB blastomere to the P₁ blastomere. This curve is a consequence of the high intracellular hydrostatic pressure of AB compared with that of P₁. However, the higher pressure in AB is intriguing because AB has a larger volume than P₁. In soap bubbles, which are a widely used model of cell shape, a larger bubble has lower pressure than a smaller bubble. Here, we reveal that the higher pressure in AB is mediated by its higher cortical tension. The cell fusion experiments confirmed that the curvature of the contact surface is related to the pressure difference between the cells. Chemical and genetic interferences showed that the pressure difference is mediated by actomyosin. Fluorescence imaging indicated that non-muscle myosin is enriched in the AB cortex. The cell killing experiments provided evidence that AB but not P₁ is responsible for the pressure difference. Computer simulation clarified that the cell-to-cell heterogeneity of cortical tensions is indispensable for explaining the pressure difference. This study demonstrates that heterogeneity in surface tension results in significant deviations of cell behavior compared to simple soap bubble models, and thus must be taken into consideration in understanding cell shape within embryos.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actin Cytoskeleton / radiation effects
  • Actomyosin / metabolism
  • Animals
  • Caenorhabditis elegans / cytology*
  • Caenorhabditis elegans / radiation effects
  • Cell Communication* / radiation effects
  • Cell Death / radiation effects
  • Cell Shape / radiation effects
  • Cell Size / radiation effects
  • Computer Simulation
  • Cytoplasm / metabolism
  • Cytoplasm / radiation effects
  • Embryo, Nonmammalian / cytology*
  • Embryo, Nonmammalian / radiation effects
  • Extracellular Space / metabolism
  • Extracellular Space / radiation effects
  • Lasers
  • Models, Biological
  • Muscles / metabolism
  • Muscles / radiation effects
  • Pressure
  • Surface Tension / radiation effects
  • Ultraviolet Rays

Substances

  • Actomyosin