Wnt/Frizzled Signaling Controls C. Elegans Gastrulation by Activating Actomyosin Contractility

Curr Biol. 2006 Oct 24;16(20):1986-97. doi: 10.1016/j.cub.2006.08.090.

Abstract

Background: Embryonic patterning mechanisms regulate the cytoskeletal machinery that drives morphogenesis, but there are few cases where links between patterning mechanisms and morphogenesis are well understood. We have used a combination of genetics, in vivo imaging, and cell manipulations to identify such links in C. elegans gastrulation. Gastrulation in C. elegans begins with the internalization of endodermal precursor cells in a process that depends on apical constriction of ingressing cells.

Results: We show that ingression of the endodermal precursor cells is regulated by pathways, including a Wnt-Frizzled signaling pathway, that specify endodermal cell fate. We find that Wnt signaling has a role in gastrulation in addition to its earlier roles in regulating endodermal cell fate and cell-cycle timing. In the absence of Wnt signaling, endodermal precursor cells polarize and enrich myosin II apically but fail to contract their apical surfaces. We show that a regulatory myosin light chain normally becomes phosphorylated on the apical side of ingressing cells at a conserved site that can lead to myosin-filament formation and contraction of actomyosin networks and that this phosphorylation depends on Wnt signaling.

Conclusions: We conclude that Wnt signaling regulates C. elegans gastrulation through regulatory myosin light-chain phosphorylation, which results in the contraction of the apical surface of ingressing cells. These findings forge new links between cell-fate specification and morphogenesis, and they represent a novel mechanism by which Wnt signaling can regulate morphogenesis.

Publication types

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

MeSH terms

  • Actomyosin / physiology*
  • Animals
  • Caenorhabditis elegans / embryology*
  • Frizzled Receptors / metabolism*
  • Gastrula / physiology*
  • Microscopy, Fluorescence
  • Models, Biological
  • Morphogenesis / physiology*
  • Phosphorylation
  • RNA Interference
  • Signal Transduction / physiology*
  • Wnt Proteins / metabolism*

Substances

  • Frizzled Receptors
  • Wnt Proteins
  • Actomyosin