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Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts

Mesenchymal cell migration relies on the coordinated regulation of the actin and microtubule networks that participate in polarized cell protrusion, adhesion, and contraction. During collective migration, most of the traction forces are generated by the acto-myosin network linked to focal adhesions...

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Autores principales: De Pascalis, Chiara, Pérez-González, Carlos, Seetharaman, Shailaja, Boëda, Batiste, Vianay, Benoit, Burute, Mithila, Leduc, Cécile, Borghi, Nicolas, Trepat, Xavier, Etienne-Manneville, Sandrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6122997/
https://www.ncbi.nlm.nih.gov/pubmed/29980627
http://dx.doi.org/10.1083/jcb.201801162
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author De Pascalis, Chiara
Pérez-González, Carlos
Seetharaman, Shailaja
Boëda, Batiste
Vianay, Benoit
Burute, Mithila
Leduc, Cécile
Borghi, Nicolas
Trepat, Xavier
Etienne-Manneville, Sandrine
author_facet De Pascalis, Chiara
Pérez-González, Carlos
Seetharaman, Shailaja
Boëda, Batiste
Vianay, Benoit
Burute, Mithila
Leduc, Cécile
Borghi, Nicolas
Trepat, Xavier
Etienne-Manneville, Sandrine
author_sort De Pascalis, Chiara
collection PubMed
description Mesenchymal cell migration relies on the coordinated regulation of the actin and microtubule networks that participate in polarized cell protrusion, adhesion, and contraction. During collective migration, most of the traction forces are generated by the acto-myosin network linked to focal adhesions at the front of leader cells, which transmit these pulling forces to the followers. Here, using an in vitro wound healing assay to induce polarization and collective directed migration of primary astrocytes, we show that the intermediate filament (IF) network composed of vimentin, glial fibrillary acidic protein, and nestin contributes to directed collective movement by controlling the distribution of forces in the migrating cell monolayer. Together with the cytoskeletal linker plectin, these IFs control the organization and dynamics of the acto-myosin network, promoting the actin-driven treadmilling of adherens junctions, thereby facilitating the polarization of leader cells. Independently of their effect on adherens junctions, IFs influence the dynamics and localization of focal adhesions and limit their mechanical coupling to the acto-myosin network. We thus conclude that IFs promote collective directed migration in astrocytes by restricting the generation of traction forces to the front of leader cells, preventing aberrant tractions in the followers, and by contributing to the maintenance of lateral cell–cell interactions.
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spelling pubmed-61229972019-03-03 Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts De Pascalis, Chiara Pérez-González, Carlos Seetharaman, Shailaja Boëda, Batiste Vianay, Benoit Burute, Mithila Leduc, Cécile Borghi, Nicolas Trepat, Xavier Etienne-Manneville, Sandrine J Cell Biol Research Articles Mesenchymal cell migration relies on the coordinated regulation of the actin and microtubule networks that participate in polarized cell protrusion, adhesion, and contraction. During collective migration, most of the traction forces are generated by the acto-myosin network linked to focal adhesions at the front of leader cells, which transmit these pulling forces to the followers. Here, using an in vitro wound healing assay to induce polarization and collective directed migration of primary astrocytes, we show that the intermediate filament (IF) network composed of vimentin, glial fibrillary acidic protein, and nestin contributes to directed collective movement by controlling the distribution of forces in the migrating cell monolayer. Together with the cytoskeletal linker plectin, these IFs control the organization and dynamics of the acto-myosin network, promoting the actin-driven treadmilling of adherens junctions, thereby facilitating the polarization of leader cells. Independently of their effect on adherens junctions, IFs influence the dynamics and localization of focal adhesions and limit their mechanical coupling to the acto-myosin network. We thus conclude that IFs promote collective directed migration in astrocytes by restricting the generation of traction forces to the front of leader cells, preventing aberrant tractions in the followers, and by contributing to the maintenance of lateral cell–cell interactions. Rockefeller University Press 2018-09-03 /pmc/articles/PMC6122997/ /pubmed/29980627 http://dx.doi.org/10.1083/jcb.201801162 Text en © 2018 De Pascalis et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
De Pascalis, Chiara
Pérez-González, Carlos
Seetharaman, Shailaja
Boëda, Batiste
Vianay, Benoit
Burute, Mithila
Leduc, Cécile
Borghi, Nicolas
Trepat, Xavier
Etienne-Manneville, Sandrine
Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title_full Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title_fullStr Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title_full_unstemmed Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title_short Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
title_sort intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6122997/
https://www.ncbi.nlm.nih.gov/pubmed/29980627
http://dx.doi.org/10.1083/jcb.201801162
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