Pulsed contractions of an actin–myosin network drive apical constriction

Abstract

During development, changes in individual cell shape drive the overall organization of organs and tissues. Now a study of the dynamics of cell behaviour during fruit fly development reveals a previously unknown ratchet-like mechanism that drives cell shape change. Gastrulation in the Drosophila embryo involves the apical constriction of ventral cells, which induces a ventral furrow and invagination of the mesoderm. This new work shows that the apical constriction of ventral cells is pulsed: repeated constrictions are interrupted by pauses in which the constricted state of the cells in maintained. These pulses are powered by actin–myosin contractions and are dependent on the expression of a transcription factor Snail, whereas the constricted state is stabilized by another transcription factor, Twist. During gastrulation in Drosophila embryo, there is apical constriction of ventral cells, which results in formation of a ventral furrow and invagination of the mesoderm. This study reports a mechanism for this process and shows that apical constriction of ventral cells is pulsed. These pulses are powered by the actin–myosin contractions and are dependent on the expression of a transcription factor, Snail, whereas the constricted state is stabilized by the transcription factor Twist. Apical constriction facilitates epithelial sheet bending and invagination during morphogenesis1,2. Apical constriction is conventionally thought to be driven by the continuous purse-string-like contraction of a circumferential actin and non-muscle myosin-II (myosin) belt underlying adherens junctions3,4,5,6,7. However, it is unclear whether other force-generating mechanisms can drive this process. Here we show, with the use of real-time imaging and quantitative image analysis of Drosophila gastrulation, that the apical constriction of ventral furrow cells is pulsed. Repeated constrictions, which are asynchronous between neighbouring cells, are interrupted by pauses in which the constricted state of the cell apex is maintained. In contrast to the purse-string model, constriction pulses are powered by actin–myosin network contractions that occur at the medial apical cortex and pull discrete adherens junction sites inwards. The transcription factors Twist and Snail differentially regulate pulsed constriction. Expression of snail initiates actin–myosin network contractions, whereas expression of twist stabilizes the constricted state of the cell apex. Our results suggest a new model for apical constriction in which a cortical actin–myosin cytoskeleton functions as a developmentally controlled subcellular ratchet to reduce apical area incrementally.