{"title":"Dynamics of positional information in the vertebrate neural tube.","authors":"Anđela Marković, James Briscoe, Karen M Page","doi":"10.1098/rsif.2024.0414","DOIUrl":null,"url":null,"abstract":"<p><p>In developing embryos, cells acquire distinct identities depending on their position in a tissue. Secreted signalling molecules, known as morphogens, act as long-range cues to provide the spatial information that controls these cell fate decisions. In several tissues, both the level and the duration of morphogen signalling appear to be important for determining cell fates. This is the case in the forming vertebrate nervous system where antiparallel morphogen gradients pattern the dorsal-ventral axis by partitioning the tissue into sharply delineated domains of molecularly distinct neural progenitors. How information in the gradients is decoded to generate precisely positioned boundaries of gene expression remains an open question. Here, we adopt tools from information theory to quantify the positional information in the neural tube and investigate how temporal changes in signalling could influence positional precision. The results reveal that the use of signalling dynamics, as well as the signalling level, substantially increases the precision possible for the estimation of position from morphogen gradients. This analysis links the dynamics of opposing morphogen gradients with precise pattern formation and provides an explanation for why time is used to impart positional information.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 221","pages":"20240414"},"PeriodicalIF":3.7000,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11631457/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of The Royal Society Interface","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1098/rsif.2024.0414","RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/12/11 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
In developing embryos, cells acquire distinct identities depending on their position in a tissue. Secreted signalling molecules, known as morphogens, act as long-range cues to provide the spatial information that controls these cell fate decisions. In several tissues, both the level and the duration of morphogen signalling appear to be important for determining cell fates. This is the case in the forming vertebrate nervous system where antiparallel morphogen gradients pattern the dorsal-ventral axis by partitioning the tissue into sharply delineated domains of molecularly distinct neural progenitors. How information in the gradients is decoded to generate precisely positioned boundaries of gene expression remains an open question. Here, we adopt tools from information theory to quantify the positional information in the neural tube and investigate how temporal changes in signalling could influence positional precision. The results reveal that the use of signalling dynamics, as well as the signalling level, substantially increases the precision possible for the estimation of position from morphogen gradients. This analysis links the dynamics of opposing morphogen gradients with precise pattern formation and provides an explanation for why time is used to impart positional information.
期刊介绍:
J. R. Soc. Interface welcomes articles of high quality research at the interface of the physical and life sciences. It provides a high-quality forum to publish rapidly and interact across this boundary in two main ways: J. R. Soc. Interface publishes research applying chemistry, engineering, materials science, mathematics and physics to the biological and medical sciences; it also highlights discoveries in the life sciences of relevance to the physical sciences. Both sides of the interface are considered equally and it is one of the only journals to cover this exciting new territory. J. R. Soc. Interface welcomes contributions on a diverse range of topics, including but not limited to; biocomplexity, bioengineering, bioinformatics, biomaterials, biomechanics, bionanoscience, biophysics, chemical biology, computer science (as applied to the life sciences), medical physics, synthetic biology, systems biology, theoretical biology and tissue engineering.