Cell Ingression and Apical Shape Oscillations during Dorsal Closure in Drosophila

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 μm2/min), the rate for completing ingression is remarkably constant (0.83 cells/min, r2 > 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.