Cell-cell and cell-extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Mol Biol Cell. 2017 May 15;28(10):1301-1310. doi: 10.1091/mbc.E17-01-0033. Epub 2017 Mar 22.

Abstract

Tissue morphogenesis relies on the coordinated action of actin networks, cell-cell adhesions, and cell-extracellular matrix (ECM) adhesions. Such coordination can be achieved through cross-talk between cell-cell and cell-ECM adhesions. Drosophila dorsal closure (DC), a morphogenetic process in which an extraembryonic tissue called the amnioserosa contracts and ingresses to close a discontinuity in the dorsal epidermis of the embryo, requires both cell-cell and cell-ECM adhesions. However, whether the functions of these two types of adhesions are coordinated during DC is not known. Here we analyzed possible interdependence between cell-cell and cell-ECM adhesions during DC and its effect on the actomyosin network. We find that loss of cell-ECM adhesion results in aberrant distributions of cadherin-mediated adhesions and actin networks in the amnioserosa and subsequent disruption of myosin recruitment and dynamics. Moreover, loss of cell-cell adhesion caused up-regulation of cell-ECM adhesion, leading to reduced cell deformation and force transmission across amnioserosa cells. Our results show how interdependence between cell-cell and cell-ECM adhesions is important in regulating cell behaviors, force generation, and force transmission critical for tissue morphogenesis.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism
  • Actomyosin / metabolism
  • Animals
  • Cadherins / metabolism
  • Cell Adhesion / physiology*
  • Cell Movement / physiology
  • Cell-Matrix Junctions / metabolism*
  • Drosophila / embryology
  • Drosophila / metabolism
  • Drosophila Proteins / metabolism
  • Embryonic Development / physiology
  • Epidermis / metabolism
  • Extracellular Matrix / metabolism
  • Myosins / metabolism

Substances

  • Actins
  • Cadherins
  • Drosophila Proteins
  • Actomyosin
  • Myosins