Herrera-Perez R Marisol, Cupo Christian, Allan Cole, Dagle Alicia B, Kasza Karen E
Department of Mechanical Engineering, Columbia University, New York, New York, 10027, USA.
PRX Life. 2023 Jul-Sep;1(1). doi: 10.1103/prxlife.1.013004. Epub 2023 Jul 25.
Rapid epithelial tissue flows are essential to building and shaping developing embryos. However, the mechanical properties of embryonic epithelial tissues and the factors that control these properties are not well understood. Actomyosin generates contractile tensions and contributes to the mechanical properties of cells and cytoskeletal networks , but it remains unclear how the levels and patterns of actomyosin activity contribute to embryonic epithelial tissue mechanics . To dissect the roles of cell-generated tensions in the mechanics of flowing epithelial tissues, we use optogenetic tools to manipulate actomyosin contractility with spatiotemporal precision in the germband epithelium, which rapidly flows during body axis elongation. We find that manipulating actomyosin-dependent tensions by either optogenetic activation or deactivation of actomyosin alters the solid-fluid mechanical properties of the germband epithelium, leading to changes in cell rearrangements and tissue-level flows. Optogenetically activating actomyosin leads to increases in the overall level but decreases in the anisotropy of tension in the tissue, whereas optogenetically deactivating actomyosin leads to decreases in both the level and anisotropy of tension compared to in wild-type embryos. We find that optogenetically activating actomyosin results in more solid-like (less fluid-like) tissue properties, which is associated with reduced cell rearrangements and tissue flow compared to in wild-type embryos. Optogenetically deactivating actomyosin also results in more solid-like properties than in wild-type embryos but less solid-like properties compared to optogenetically activating actomyosin. Together, these findings indicate that increasing the overall tension level is associated with more solid-like properties in tissues that are relatively isotropic, whereas high tension anisotropy fluidizes the tissue. Our results reveal that epithelial tissue flows in developing embryos involve the coordinated actomyosin-dependent regulation of the mechanical properties of tissues and the tensions driving them to flow in order to achieve rapid tissue remodeling.
快速的上皮组织流动对于发育中胚胎的构建和塑形至关重要。然而,胚胎上皮组织的力学特性以及控制这些特性的因素尚未得到充分了解。肌动球蛋白产生收缩张力,并对细胞和细胞骨架网络的力学特性有贡献,但目前尚不清楚肌动球蛋白活性的水平和模式如何影响胚胎上皮组织的力学性能。为了剖析细胞产生的张力在流动上皮组织力学中的作用,我们使用光遗传学工具在胚带上皮中以时空精确性操纵肌动球蛋白的收缩性,胚带上皮在体轴伸长期间快速流动。我们发现,通过光遗传学激活或失活肌动球蛋白来操纵依赖于肌动球蛋白的张力,会改变胚带上皮的固液力学特性,导致细胞重排和组织水平流动的变化。光遗传学激活肌动球蛋白会导致组织中张力的总体水平增加,但各向异性降低,而与野生型胚胎相比,光遗传学失活肌动球蛋白会导致张力的水平和各向异性均降低。我们发现,光遗传学激活肌动球蛋白会导致组织具有更类似固体(更少类似液体)的特性,与野生型胚胎相比,这与细胞重排和组织流动减少有关。光遗传学失活肌动球蛋白也会导致组织具有比野生型胚胎更类似固体的特性,但与光遗传学激活肌动球蛋白相比,类似固体的特性更少。总之,这些发现表明,在相对各向同性的组织中,增加总体张力水平与更类似固体的特性相关,而高张力各向异性会使组织流化。我们的结果表明,发育中胚胎的上皮组织流动涉及肌动球蛋白依赖性对组织力学特性以及驱动它们流动的张力的协调调节,以实现快速的组织重塑。