Stephanie Cheung, Danila Bredikhin, Tobias Gerber, Petrus J. Steenbergen, Soham Basu, Richard Bailleul, Pauline Hansen, Alexandre Paix, Matthew A. Benton, Hendrik C. Korswagen, Detlev Arendt, Oliver Stegle, Aissam Ikmi
{"title":"Systemic coordination of whole-body tissue remodeling during local regeneration in sea anemones","authors":"Stephanie Cheung, Danila Bredikhin, Tobias Gerber, Petrus J. Steenbergen, Soham Basu, Richard Bailleul, Pauline Hansen, Alexandre Paix, Matthew A. Benton, Hendrik C. Korswagen, Detlev Arendt, Oliver Stegle, Aissam Ikmi","doi":"10.1016/j.devcel.2024.11.001","DOIUrl":null,"url":null,"abstract":"The complexity of regeneration extends beyond local wound responses, eliciting systemic processes across the entire organism. However, the functional relevance and coordination of distant molecular processes remain unclear. In the cnidarian <em>Nematostella vectensis</em>, we show that local regeneration triggers a systemic homeostatic response, leading to coordinated whole-body remodeling. Leveraging spatial transcriptomics, endogenous protein tagging, and live imaging, we comprehensively dissect this systemic response at the organismal scale. We identify proteolysis as a critical process driven by both local and systemic upregulation of metalloproteases. We show that metalloproteinase expression levels and activity scale with the extent of tissue loss. This proportional response drives long-range tissue and extracellular matrix movement. Our findings demonstrate the adaptive nature of the systematic response in regeneration, enabling the organism to maintain shape homeostasis while coping with a wide range of injuries.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"195 1","pages":""},"PeriodicalIF":10.7000,"publicationDate":"2024-11-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Developmental cell","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.devcel.2024.11.001","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CELL BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The complexity of regeneration extends beyond local wound responses, eliciting systemic processes across the entire organism. However, the functional relevance and coordination of distant molecular processes remain unclear. In the cnidarian Nematostella vectensis, we show that local regeneration triggers a systemic homeostatic response, leading to coordinated whole-body remodeling. Leveraging spatial transcriptomics, endogenous protein tagging, and live imaging, we comprehensively dissect this systemic response at the organismal scale. We identify proteolysis as a critical process driven by both local and systemic upregulation of metalloproteases. We show that metalloproteinase expression levels and activity scale with the extent of tissue loss. This proportional response drives long-range tissue and extracellular matrix movement. Our findings demonstrate the adaptive nature of the systematic response in regeneration, enabling the organism to maintain shape homeostasis while coping with a wide range of injuries.
期刊介绍:
Developmental Cell, established in 2001, is a comprehensive journal that explores a wide range of topics in cell and developmental biology. Our publication encompasses work across various disciplines within biology, with a particular emphasis on investigating the intersections between cell biology, developmental biology, and other related fields. Our primary objective is to present research conducted through a cell biological perspective, addressing the essential mechanisms governing cell function, cellular interactions, and responses to the environment. Moreover, we focus on understanding the collective behavior of cells, culminating in the formation of tissues, organs, and whole organisms, while also investigating the consequences of any malfunctions in these intricate processes.