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Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration

In animals, cells often move as collectives to shape organs, close wounds, or—in the case of disease—metastasize. To accomplish this, cells need to generate force to propel themselves forward. The motility of singly migrating cells is driven largely by an interplay between Rho GTPase signaling and t...

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Autores principales: Qian, Weiyi, Yamaguchi, Naoya, Lis, Patrycja, Cammer, Michael, Knaut, Holger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592895/
https://www.ncbi.nlm.nih.gov/pubmed/37873192
http://dx.doi.org/10.1101/2023.10.03.560679
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author Qian, Weiyi
Yamaguchi, Naoya
Lis, Patrycja
Cammer, Michael
Knaut, Holger
author_facet Qian, Weiyi
Yamaguchi, Naoya
Lis, Patrycja
Cammer, Michael
Knaut, Holger
author_sort Qian, Weiyi
collection PubMed
description In animals, cells often move as collectives to shape organs, close wounds, or—in the case of disease—metastasize. To accomplish this, cells need to generate force to propel themselves forward. The motility of singly migrating cells is driven largely by an interplay between Rho GTPase signaling and the actin network (Yamada and Sixt, 2019). Whether cells migrating as collectives use the same machinery for motility is unclear. Using the zebrafish posterior lateral line primordium as a model for collective cell migration, we find that active RhoA and myosin II cluster on the basal sides of the primordium cells and are required for primordium motility. Positive and negative feedbacks cause RhoA and myosin II activities to pulse. These pulses of RhoA signaling stimulate actin polymerization at the tip of the protrusions and myosin II-dependent actin flow and protrusion retraction at the base of the protrusions, and deform the basement membrane underneath the migrating primordium. This suggests that RhoA-induced actin flow on the basal sides of the cells constitutes the motor that pulls the primordium forward, a scenario that likely underlies collective migration in other—but not all (Bastock and Strutt, 2007; Lebreton and Casanova, 2013; Matthews et al., 2008)—contexts.
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spelling pubmed-105928952023-10-24 Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration Qian, Weiyi Yamaguchi, Naoya Lis, Patrycja Cammer, Michael Knaut, Holger bioRxiv Article In animals, cells often move as collectives to shape organs, close wounds, or—in the case of disease—metastasize. To accomplish this, cells need to generate force to propel themselves forward. The motility of singly migrating cells is driven largely by an interplay between Rho GTPase signaling and the actin network (Yamada and Sixt, 2019). Whether cells migrating as collectives use the same machinery for motility is unclear. Using the zebrafish posterior lateral line primordium as a model for collective cell migration, we find that active RhoA and myosin II cluster on the basal sides of the primordium cells and are required for primordium motility. Positive and negative feedbacks cause RhoA and myosin II activities to pulse. These pulses of RhoA signaling stimulate actin polymerization at the tip of the protrusions and myosin II-dependent actin flow and protrusion retraction at the base of the protrusions, and deform the basement membrane underneath the migrating primordium. This suggests that RhoA-induced actin flow on the basal sides of the cells constitutes the motor that pulls the primordium forward, a scenario that likely underlies collective migration in other—but not all (Bastock and Strutt, 2007; Lebreton and Casanova, 2013; Matthews et al., 2008)—contexts. Cold Spring Harbor Laboratory 2023-10-05 /pmc/articles/PMC10592895/ /pubmed/37873192 http://dx.doi.org/10.1101/2023.10.03.560679 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Qian, Weiyi
Yamaguchi, Naoya
Lis, Patrycja
Cammer, Michael
Knaut, Holger
Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title_full Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title_fullStr Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title_full_unstemmed Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title_short Pulses of RhoA Signaling Stimulate Actin Polymerization and Flow in Protrusions to Drive Collective Cell Migration
title_sort pulses of rhoa signaling stimulate actin polymerization and flow in protrusions to drive collective cell migration
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592895/
https://www.ncbi.nlm.nih.gov/pubmed/37873192
http://dx.doi.org/10.1101/2023.10.03.560679
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