folded gastrulation, cell shape change and the control of myosin localization

Development. 2005 Sep;132(18):4165-78. doi: 10.1242/dev.01938.

Abstract

The global cell movements that shape an embryo are driven by intricate changes to the cytoarchitecture of individual cells. In a developing embryo, these changes are controlled by patterning genes that confer cell identity. However, little is known about how patterning genes influence cytoarchitecture to drive changes in cell shape. In this paper, we analyze the function of the folded gastrulation gene (fog), a known target of the patterning gene twist. Our analysis of fog function therefore illuminates a molecular pathway spanning all the way from patterning gene to physical change in cell shape. We show that secretion of Fog protein is apically polarized, making this the earliest polarized component of a pathway that ultimately drives myosin to the apical side of the cell. We demonstrate that fog is both necessary and sufficient to drive apical myosin localization through a mechanism involving activation of myosin contractility with actin. We determine that this contractility driven form of localization involves RhoGEF2 and the downstream effector Rho kinase. This distinguishes apical myosin localization from basal myosin localization, which we find not to require actinomyosin contractility or FOG/RhoGEF2/Rho-kinase signaling. Furthermore, we demonstrate that once localized apically, myosin continues to contract. The force generated by continued myosin contraction is translated into a flattening and constriction of the cell surface through a tethering of the actinomyosin cytoskeleton to the apical adherens junctions. Our analysis of fog function therefore provides a direct link from patterning to cell shape change.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Adherens Junctions / physiology
  • Animals
  • Body Patterning / physiology*
  • Cell Cycle Proteins
  • Cell Polarity / physiology
  • Cell Shape / physiology*
  • Drosophila / embryology*
  • Drosophila / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Embryo, Nonmammalian / physiology
  • Green Fluorescent Proteins
  • Models, Biological*
  • Myosins / metabolism*
  • Myosins / physiology
  • Signal Transduction / physiology*
  • Twist-Related Protein 1 / genetics
  • Twist-Related Protein 1 / metabolism*
  • rho GTP-Binding Proteins / metabolism

Substances

  • Actins
  • Cell Cycle Proteins
  • Drosophila Proteins
  • FOG protein, Drosophila
  • Twi protein, Drosophila
  • Twist-Related Protein 1
  • sav protein, Drosophila
  • Green Fluorescent Proteins
  • Myosins
  • rho GTP-Binding Proteins