Fujiwara Motohiro, Akiyama-Oda Yasuko, Oda Hiroki
Laboratory of Evolutionary Cell and Developmental Biology, JT Biohistory Research Hall, Takatsuki, Japan.
PRESTO, Japan Science and Technology Agency (JST), Kawaguchi, Japan.
Front Cell Dev Biol. 2022 Aug 12;10:932814. doi: 10.3389/fcell.2022.932814. eCollection 2022.
Remodeling of multicellular architecture is a critical developmental process for shaping the axis of a bilaterally symmetric animal body and involves coordinated cell-cell interactions and cell rearrangement. In arthropods, the early embryonic process that leads to the segmented body axis varies at the cellular and molecular levels depending on the species. Developmental studies using insect and spider model species have provided specific examples of these diversified mechanisms that regulate axis formation and segmentation in arthropod embryos. However, there are few theoretical models for how diversity in the early embryonic process occurred during evolution, in part because of a limited computational infrastructure. We developed a virtual spherical-shaped multicellular platform to reproduce body axis-forming processes. Each virtual cell behaves according to the cell vertex model, with the computational program organized in a hierarchical order from cells and tissues to whole embryos. Using an initial set of two different mechanical states for cell differentiation and global directional signals that are linked to the planar polarity of each cell, the virtual cell assembly exhibited morphogenetic processes similar to those observed in spider embryos. We found that the development of an elongating body axis is achieved through implementation of an interactive cell polarity parameter associated with edge tension at the cell-cell adhesion interface, with no local control of the cell division rate and direction. We also showed that modifying the settings can cause variation in morphogenetic processes. This platform also can embed a gene network that generates waves of gene expression in a virtual dynamic multicellular field. This study provides a computational platform for testing the development and evolution of animal body patterns.
多细胞结构的重塑是塑造两侧对称动物体轴的关键发育过程，涉及协调的细胞间相互作用和细胞重排。在节肢动物中，导致分节体轴形成的早期胚胎过程在细胞和分子水平上因物种而异。使用昆虫和蜘蛛模型物种进行的发育研究提供了这些多样化机制的具体例子，这些机制调节节肢动物胚胎中的轴形成和分节。然而，关于早期胚胎过程中的多样性在进化过程中是如何产生的，理论模型很少，部分原因是计算基础设施有限。我们开发了一个虚拟球形多细胞平台来重现体轴形成过程。每个虚拟细胞根据细胞顶点模型运行，计算程序从细胞、组织到整个胚胎按层次顺序组织。利用一组初始的两种不同的细胞分化机械状态和与每个细胞的平面极性相关的全局方向信号，虚拟细胞组装展示出与蜘蛛胚胎中观察到的相似的形态发生过程。我们发现，通过实施与细胞 - 细胞粘附界面处边缘张力相关的交互式细胞极性参数，可以实现伸长体轴的发育，而无需局部控制细胞分裂速率和方向。我们还表明，修改设置会导致形态发生过程的变化。这个平台还可以嵌入一个基因网络，该网络在虚拟动态多细胞场中产生基因表达波。这项研究为测试动物体型模式的发育和进化提供了一个计算平台。
