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Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction

Convergent extension (CE) is an evolutionarily conserved collective cell movement that elongates several organ systems during development. Studies have revealed two distinct cellular mechanisms, one based on cell crawling and the other on junction contraction. Whether these two behaviors collaborate...

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Detalles Bibliográficos
Autores principales: Weng, Shinuo, Huebner, Robert J., Wallingford, John B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9119128/
https://www.ncbi.nlm.nih.gov/pubmed/35476988
http://dx.doi.org/10.1016/j.celrep.2022.110666
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author Weng, Shinuo
Huebner, Robert J.
Wallingford, John B.
author_facet Weng, Shinuo
Huebner, Robert J.
Wallingford, John B.
author_sort Weng, Shinuo
collection PubMed
description Convergent extension (CE) is an evolutionarily conserved collective cell movement that elongates several organ systems during development. Studies have revealed two distinct cellular mechanisms, one based on cell crawling and the other on junction contraction. Whether these two behaviors collaborate is unclear. Here, using live-cell imaging, we show that crawling and contraction act both independently and jointly but that CE is more effective when they are integrated via mechano-reciprocity. We thus developed a computational model considering both crawling and contraction. This model recapitulates the biomechanical efficacy of integrating the two modes and further clarifies how the two modes and their integration are influenced by cell adhesion. Finally, we use these insights to understand the function of an understudied catenin, Arvcf, during CE. These data are significant for providing interesting biomechanical and cell biological insights into a fundamental morphogenetic process that is implicated in human neural tube defects and skeletal dysplasias.
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spelling pubmed-91191282022-05-19 Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction Weng, Shinuo Huebner, Robert J. Wallingford, John B. Cell Rep Article Convergent extension (CE) is an evolutionarily conserved collective cell movement that elongates several organ systems during development. Studies have revealed two distinct cellular mechanisms, one based on cell crawling and the other on junction contraction. Whether these two behaviors collaborate is unclear. Here, using live-cell imaging, we show that crawling and contraction act both independently and jointly but that CE is more effective when they are integrated via mechano-reciprocity. We thus developed a computational model considering both crawling and contraction. This model recapitulates the biomechanical efficacy of integrating the two modes and further clarifies how the two modes and their integration are influenced by cell adhesion. Finally, we use these insights to understand the function of an understudied catenin, Arvcf, during CE. These data are significant for providing interesting biomechanical and cell biological insights into a fundamental morphogenetic process that is implicated in human neural tube defects and skeletal dysplasias. 2022-04-26 /pmc/articles/PMC9119128/ /pubmed/35476988 http://dx.doi.org/10.1016/j.celrep.2022.110666 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) ).
spellingShingle Article
Weng, Shinuo
Huebner, Robert J.
Wallingford, John B.
Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title_full Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title_fullStr Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title_full_unstemmed Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title_short Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
title_sort convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9119128/
https://www.ncbi.nlm.nih.gov/pubmed/35476988
http://dx.doi.org/10.1016/j.celrep.2022.110666
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