Cell ingression and apical shape oscillations during dorsal closure in Drosophila

Biophys J. 2012 Mar 7;102(5):969-79. doi: 10.1016/j.bpj.2012.01.027. Epub 2012 Mar 6.

Abstract

Programmed patterns of gene expression, cell-cell signaling, and cellular forces cause morphogenic movements during dorsal closure. We investigated the apical cell-shape changes that characterize amnioserosa cells during dorsal closure in Drosophila embryos with in vivo imaging of green-fluorescent-protein-labeled DE-cadherin. Time-lapsed, confocal images were assessed with a novel segmentation algorithm, Fourier analysis, and kinematic and dynamical modeling. We found two generic processes, reversible oscillations in apical cross-sectional area and cell ingression characterized by persistent loss of apical area. We quantified a time-dependent, spatially-averaged sum of intracellular and intercellular forces acting on each cell's apical belt of DE-cadherin. We observed that a substantial fraction of amnioserosa cells ingress near the leading edges of lateral epidermis, consistent with the view that ingression can be regulated by leading-edge cells. This is in addition to previously observed ingression processes associated with zipping and apoptosis. Although there is cell-to-cell variability in the maximum rate for decreasing apical area (0.3-9.5 μm(2)/min), the rate for completing ingression is remarkably constant (0.83 cells/min, r(2) > 0.99). We propose that this constant ingression rate contributes to the spatiotemporal regularity of mechanical stress exerted by the amnioserosa on each leading edge during closure.

Publication types

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

MeSH terms

  • Animals
  • Cadherins / metabolism
  • Cell Polarity
  • Cell Shape*
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / embryology*
  • Embryo, Nonmammalian / cytology*
  • Embryo, Nonmammalian / metabolism
  • Embryonic Development*
  • Models, Biological*
  • Time Factors

Substances

  • Cadherins