Department of Physics and Astronomy, Texas Tech University, Lubbock, Texas, United States of America.
Department of Mathematical and Systems Engineering, Shizuoka University, Hamamatsu, Japan.
PLoS Comput Biol. 2021 Jul 6;17(7):e1009173. doi: 10.1371/journal.pcbi.1009173. eCollection 2021 Jul.
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.
果蝇胚胎腹侧沟的形成依赖于腹侧区域细胞的顶端收缩,产生弯曲力,驱动组织内陷。在我们最近的论文中,我们观察到在腹侧沟形成的初始阶段,顶端收缩在组织内陷之前产生了拉长的细胞收缩链模式,并认为这表明存在张力反馈。在这里,我们定量分析了腹侧沟形成之前的收缩模式,发现它们与我们的单层机械偶联的应力敏感收缩颗粒的主动颗粒状流模型的预测一致。我们的模型表明,张力反馈导致收缩链沿着逐渐增强的基础前导张力链发展,随着后续的细胞收缩而增强。正如我们的模型和现有的光遗传学实验所看到的,这种机制允许收缩链穿透或绕过细胞收缩能力降低的区域,从而通过在中断区域挽救细胞收缩,增加腹侧沟形成对细胞收缩性空间变化的鲁棒性。