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Cadherin preserves cohesion across involuting tissues during C. elegans neurulation

The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show...

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Autores principales: Barnes, Kristopher M, Fan, Li, Moyle, Mark W, Brittin, Christopher A, Xu, Yichi, Colón-Ramos, Daniel A, Santella, Anthony, Bao, Zhirong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7544503/
https://www.ncbi.nlm.nih.gov/pubmed/33030428
http://dx.doi.org/10.7554/eLife.58626
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author Barnes, Kristopher M
Fan, Li
Moyle, Mark W
Brittin, Christopher A
Xu, Yichi
Colón-Ramos, Daniel A
Santella, Anthony
Bao, Zhirong
author_facet Barnes, Kristopher M
Fan, Li
Moyle, Mark W
Brittin, Christopher A
Xu, Yichi
Colón-Ramos, Daniel A
Santella, Anthony
Bao, Zhirong
author_sort Barnes, Kristopher M
collection PubMed
description The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show that in C. elegans morphogenesis, apical constriction in the retracting pharynx drives involution of the adjacent neuroectoderm. HMR-1/cadherin mediates this process via inter-tissue attachment, as well as cohesion within the neuroectoderm. Our results demonstrate that HMR-1 is capable of mediating embryo-wide reorganization driven by a centrally located force generator, and indicate a non-canonical use of cadherin on the basal side of an epithelium that may apply to vertebrate neurulation. Additionally, we highlight shared morphology and gene expression in tissues driving involution, which suggests that neuroectoderm involution in C. elegans is potentially homologous with vertebrate neurulation and thus may help elucidate the evolutionary origin of the brain.
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spelling pubmed-75445032020-10-09 Cadherin preserves cohesion across involuting tissues during C. elegans neurulation Barnes, Kristopher M Fan, Li Moyle, Mark W Brittin, Christopher A Xu, Yichi Colón-Ramos, Daniel A Santella, Anthony Bao, Zhirong eLife Neuroscience The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show that in C. elegans morphogenesis, apical constriction in the retracting pharynx drives involution of the adjacent neuroectoderm. HMR-1/cadherin mediates this process via inter-tissue attachment, as well as cohesion within the neuroectoderm. Our results demonstrate that HMR-1 is capable of mediating embryo-wide reorganization driven by a centrally located force generator, and indicate a non-canonical use of cadherin on the basal side of an epithelium that may apply to vertebrate neurulation. Additionally, we highlight shared morphology and gene expression in tissues driving involution, which suggests that neuroectoderm involution in C. elegans is potentially homologous with vertebrate neurulation and thus may help elucidate the evolutionary origin of the brain. eLife Sciences Publications, Ltd 2020-10-08 /pmc/articles/PMC7544503/ /pubmed/33030428 http://dx.doi.org/10.7554/eLife.58626 Text en © 2020, Barnes et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Barnes, Kristopher M
Fan, Li
Moyle, Mark W
Brittin, Christopher A
Xu, Yichi
Colón-Ramos, Daniel A
Santella, Anthony
Bao, Zhirong
Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title_full Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title_fullStr Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title_full_unstemmed Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title_short Cadherin preserves cohesion across involuting tissues during C. elegans neurulation
title_sort cadherin preserves cohesion across involuting tissues during c. elegans neurulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7544503/
https://www.ncbi.nlm.nih.gov/pubmed/33030428
http://dx.doi.org/10.7554/eLife.58626
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