Mira Zaher, Ronit Yelin, Alaa A Arraf, Julian Jadon, Manar Abboud Asleh, Sivan Goltzman, Lihi Shaulov, Dieter P Reinhardt, Thomas M Schultheiss
{"title":"Stored elastic bending tension as a mediator of embryonic body folding.","authors":"Mira Zaher, Ronit Yelin, Alaa A Arraf, Julian Jadon, Manar Abboud Asleh, Sivan Goltzman, Lihi Shaulov, Dieter P Reinhardt, Thomas M Schultheiss","doi":"10.1016/j.celrep.2024.115200","DOIUrl":null,"url":null,"abstract":"<p><p>During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that the flat stage is actually a poised balance of opposing dorsal and ventral elastic bending tensions. An intact extracellular matrix (ECM) is required for generating tension, as localized digestion of ECM dissipates tension, while removal of endoderm or ectoderm layers has no significant effect. As development proceeds, dorsal bending tension dissipates coincident with epithelial-mesenchymal transition in the dorsal LP while ventral tension is maintained, changing the balance of forces to promote ventral folding. Interference with the elastic ECM component fibrillin reduces ventral bending tension and perturbs body folding in vivo. A model is presented for the accumulation and harnessing of LP bending tension to drive body folding.</p>","PeriodicalId":9798,"journal":{"name":"Cell reports","volume":"44 1","pages":"115200"},"PeriodicalIF":7.5000,"publicationDate":"2025-01-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cell reports","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.celrep.2024.115200","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CELL BIOLOGY","Score":null,"Total":0}
Stored elastic bending tension as a mediator of embryonic body folding.
During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that the flat stage is actually a poised balance of opposing dorsal and ventral elastic bending tensions. An intact extracellular matrix (ECM) is required for generating tension, as localized digestion of ECM dissipates tension, while removal of endoderm or ectoderm layers has no significant effect. As development proceeds, dorsal bending tension dissipates coincident with epithelial-mesenchymal transition in the dorsal LP while ventral tension is maintained, changing the balance of forces to promote ventral folding. Interference with the elastic ECM component fibrillin reduces ventral bending tension and perturbs body folding in vivo. A model is presented for the accumulation and harnessing of LP bending tension to drive body folding.
期刊介绍:
Cell Reports publishes high-quality research across the life sciences and focuses on new biological insight as its primary criterion for publication. The journal offers three primary article types: Reports, which are shorter single-point articles, research articles, which are longer and provide deeper mechanistic insights, and resources, which highlight significant technical advances or major informational datasets that contribute to biological advances. Reviews covering recent literature in emerging and active fields are also accepted.
The Cell Reports Portfolio includes gold open-access journals that cover life, medical, and physical sciences, and its mission is to make cutting-edge research and methodologies available to a wide readership.
The journal's professional in-house editors work closely with authors, reviewers, and the scientific advisory board, which consists of current and future leaders in their respective fields. The advisory board guides the scope, content, and quality of the journal, but editorial decisions are independently made by the in-house scientific editors of Cell Reports.