Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation.

Formation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. In our recent paper we observed that apical constrictions during the initial phase of ventral furrow formation produce elongated patterns of cellular constriction chains prior to invagination and argued that these are indicative of tensile stress feedback. Here, we quantitatively analyze the constriction patterns preceding ventral furrow formation and find that they are consistent with the predictions of our active-granular-fluid model of a monolayer of mechanically coupled stress-sensitive constricting particles. Our model shows that tensile feedback causes constriction chains to develop along underlying precursor tensile stress chains that gradually strengthen with subsequent cellular constrictions. As seen in both our model and available optogenetic experiments, this mechanism allows constriction chains to penetrate or circumvent zones of reduced cell contractility, thus increasing the robustness of ventral furrow formation to spatial variation of cell contractility by rescuing cellular constrictions in the disrupted regions. Author summary: Invagination of epithelial tissues is a common means by which living organisms generate their form and structure. Using the ventral furrow in the Drosophila embryo, our study addresses the fundamental question of how individual cells coordinate their activities to produce well-organized and robust invagination. Ventral furrow formation, the best studied example of epithelial invagination during early embryonic development, is initiated by constrictions of the apical (outer) surfaces of some of the cells in the epithelial cell layer to produce bending forces that cause tissue buckling. We find that these apical constrictions follow a pattern based on underlying stress chains that run along the axis of invagination. Our analysis of the experimentally observed and numerically simulated constriction patterns shows that tensile stress prompts cells to constrict, and that constrictions strengthen the stress chains. This two-way interaction allows cells to coordinate their constrictions via mechanical feedback. Reduction of regional cellular contractility by both experimental and computational perturbations shows that stress chains penetrate the affected tissue, giving rise to cell constrictions. Thus, stress feedback increases the robustness of tissue invagination. Our study elucidates how cell communication via mechanical forces helps to achieve robust structure formation. [ABSTRACT FROM AUTHOR]