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. Recently [J Phys Condens Matter. 2016;28(41):414021], 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.

果蝇（Drosophila）胚胎腹沟（ventral furrow）的形成依赖于腹侧区域细胞的顶膜收缩（apical constriction）产生弯曲力，以驱动组织内陷（tissue invagination）。近期我们在《物理：凝聚态物质》[J Phys Condens Matter, 2016; 28(41): 414021]的研究中观察到，在腹沟形成的初始阶段，顶膜收缩会在组织内陷前形成拉长的细胞收缩链模式，并认为此类模式是拉伸应力反馈（tensile stress feedback）的体现。本文我们对腹沟形成前的收缩模式开展定量分析，发现其与我们提出的由机械耦合应力敏感收缩颗粒构成的单层活性颗粒流体模型（active-granular-fluid model）的预测结果相符。该模型表明，拉伸反馈会使收缩链沿着前驱拉伸应力链发育，而前驱拉伸应力链会随后续的细胞收缩过程逐渐增强。正如模型与现有光遗传学实验（optogenetic experiments）所观测到的，这一机制可使收缩链穿透或绕过细胞收缩力降低的区域，通过拯救受损区域的细胞收缩过程，提升腹沟形成过程对细胞收缩力空间变异的鲁棒性。