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Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure

Coordination of actomyosin contraction and cell-cell junctions generates forces that can lead to tissue morphogenetic processes like the formation of neural tube (NT), however, its molecular mechanisms responsible for regulating and coupling this contractile network to cadherin adhesion remain to be...

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Autores principales: Karpińska, Kamila, Cao, Christine, Yamamoto, Vicky, Gielata, Mateusz, Kobielak, Agnieszka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7089943/
https://www.ncbi.nlm.nih.gov/pubmed/32258033
http://dx.doi.org/10.3389/fcell.2020.00154
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author Karpińska, Kamila
Cao, Christine
Yamamoto, Vicky
Gielata, Mateusz
Kobielak, Agnieszka
author_facet Karpińska, Kamila
Cao, Christine
Yamamoto, Vicky
Gielata, Mateusz
Kobielak, Agnieszka
author_sort Karpińska, Kamila
collection PubMed
description Coordination of actomyosin contraction and cell-cell junctions generates forces that can lead to tissue morphogenetic processes like the formation of neural tube (NT), however, its molecular mechanisms responsible for regulating and coupling this contractile network to cadherin adhesion remain to be fully elucidated. Here, using a gene trapping technology, we unveil the new player in this process, α-catulin, which shares sequence homology with vinculin and α-catenin. Ablation of α-catulin in mouse causes defective NT closure due to impairment of apical constriction, concomitant with apical actin and P-Mlc2 accumulation. Using a 3D culture model system, we showed that α-catulin localizes to the apical membrane and its removal alters the distribution of active RhoA and polarization. Actin cytoskeleton and P-Mlc2, downstream targets of RhoA, are not properly organized, with limited accumulation at the junctions, indicating a loss of junction stabilization. Our data suggest that α-catulin plays an important role during NT closure by acting as a scaffold for RhoA distribution, resulting in proper spatial activation of myosin to influence actin-myosin dynamics and tension at cell-cell adhesion.
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spelling pubmed-70899432020-03-31 Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure Karpińska, Kamila Cao, Christine Yamamoto, Vicky Gielata, Mateusz Kobielak, Agnieszka Front Cell Dev Biol Cell and Developmental Biology Coordination of actomyosin contraction and cell-cell junctions generates forces that can lead to tissue morphogenetic processes like the formation of neural tube (NT), however, its molecular mechanisms responsible for regulating and coupling this contractile network to cadherin adhesion remain to be fully elucidated. Here, using a gene trapping technology, we unveil the new player in this process, α-catulin, which shares sequence homology with vinculin and α-catenin. Ablation of α-catulin in mouse causes defective NT closure due to impairment of apical constriction, concomitant with apical actin and P-Mlc2 accumulation. Using a 3D culture model system, we showed that α-catulin localizes to the apical membrane and its removal alters the distribution of active RhoA and polarization. Actin cytoskeleton and P-Mlc2, downstream targets of RhoA, are not properly organized, with limited accumulation at the junctions, indicating a loss of junction stabilization. Our data suggest that α-catulin plays an important role during NT closure by acting as a scaffold for RhoA distribution, resulting in proper spatial activation of myosin to influence actin-myosin dynamics and tension at cell-cell adhesion. Frontiers Media S.A. 2020-03-17 /pmc/articles/PMC7089943/ /pubmed/32258033 http://dx.doi.org/10.3389/fcell.2020.00154 Text en Copyright © 2020 Karpińska, Cao, Yamamoto, Gielata and Kobielak. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Karpińska, Kamila
Cao, Christine
Yamamoto, Vicky
Gielata, Mateusz
Kobielak, Agnieszka
Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title_full Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title_fullStr Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title_full_unstemmed Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title_short Alpha-Catulin, a New Player in a Rho Dependent Apical Constriction That Contributes to the Mouse Neural Tube Closure
title_sort alpha-catulin, a new player in a rho dependent apical constriction that contributes to the mouse neural tube closure
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7089943/
https://www.ncbi.nlm.nih.gov/pubmed/32258033
http://dx.doi.org/10.3389/fcell.2020.00154
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