Muscle and intestine innexins with muscle DEG/ENaC channels promote muscle coordination and embryo elongation in C. elegans.

IF 3.6 2区 生物学 Q1 DEVELOPMENTAL BIOLOGY Development Pub Date : 2025-04-15 Epub Date: 2025-04-28 DOI:10.1242/dev.204242
Flora Llense, Teresa Ferraro, Xinyi Yang, Hanla Song, Michel Labouesse
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Abstract

Body axis elongation represents a fundamental morphogenetic process in development, which involves cell shape changes powered by mechanical forces. How mechanically interconnected tissues coordinate during organismal development remains largely unexplored. During Caenorhabditis elegans elongation, cyclic forces generated by muscle contractions induce remodeling of adherens junctions and the actin cytoskeleton in the epidermis, facilitating gradual embryo lengthening. Although previous studies have identified key players in epidermal cells, understanding how muscle cells coordinate their activity for proper embryo elongation remains unsolved. Using a calcium sensor to monitor muscle activity during elongation, we identified two cells in each muscle quadrant with a leader cell function that orchestrate muscle activity within their respective quadrants. Strikingly, ablation of these cells halted muscle contractions and delayed elongation. A targeted RNA interference screen focusing on communication channels identified two innexins and two DEG/ENaC channels regulating muscle activity, which proved to be required for normal embryonic elongation. Interestingly, one innexin exhibited specific expression in intestinal cells. Our findings provide insights into how embryonic body wall muscles coordinate their activity and how interconnected tissues ensure proper morphogenesis.

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具有肌Deg/Enac通道的肌内蛋白和肠内蛋白促进肌肉协调和胚胎伸长。
体轴伸长是发育过程中的一个基本形态发生过程,涉及由机械力驱动的细胞形状变化。在生物体的发育过程中,机械相互连接的组织是如何协调的,这在很大程度上仍未得到探索。在秀丽隐杆线虫的伸长过程中,肌肉收缩产生的循环力会诱导表皮中粘连接头和肌动蛋白细胞骨架的重塑,从而促进胚胎的逐渐延长。虽然先前的研究已经确定了表皮细胞中的关键参与者,但对肌肉细胞如何协调其活动以实现适当的胚胎伸长的了解仍未解决。利用钙传感器监测伸长过程中的肌肉活动,我们在每个肌肉象限发现了两个具有领导细胞功能的细胞,它们协调各自象限内的肌肉活动。令人震惊的是,消减这些细胞会停止肌肉收缩并延迟伸长。以通讯通道为重点的定向 RNAi 筛选发现了两种内联蛋白和两种调节肌肉活动的 Deg 通道,它们被证明是正常胚胎伸长所必需的。有趣的是,其中一种内联蛋白在肠细胞中有特异性表达。我们的研究结果为了解胚胎体壁肌肉如何协调其活动以及相互连接的组织如何确保正常的形态发生提供了新的见解。
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来源期刊
Development
Development 生物-发育生物学
CiteScore
6.70
自引率
4.30%
发文量
433
审稿时长
3 months
期刊介绍: Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.
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