Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.

<h4>Background</h4>Migrating leukocytes normally have a polarized morphology with an actin-rich lamellipodium at the front and a uropod at the rear. Microtubules (MTs) are required for persistent migration and chemotaxis, but how they affect cell polarity is not known.<h4>Methodolo...

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Main Authors: Aya Takesono, Sarah J Heasman, Beata Wojciak-Stothard, Ritu Garg, Anne J Ridley
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0008774&type=printable
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author Aya Takesono
Sarah J Heasman
Beata Wojciak-Stothard
Ritu Garg
Anne J Ridley
author_facet Aya Takesono
Sarah J Heasman
Beata Wojciak-Stothard
Ritu Garg
Anne J Ridley
author_sort Aya Takesono
collection DOAJ
description <h4>Background</h4>Migrating leukocytes normally have a polarized morphology with an actin-rich lamellipodium at the front and a uropod at the rear. Microtubules (MTs) are required for persistent migration and chemotaxis, but how they affect cell polarity is not known.<h4>Methodology/principal findings</h4>Here we report that T cells treated with nocodazole to disrupt MTs are unable to form a stable uropod or lamellipodium, and instead often move by membrane blebbing with reduced migratory persistence. However, uropod-localized receptors and ezrin/radixin/moesin proteins still cluster in nocodazole-treated cells, indicating that MTs are required specifically for uropod stability. Nocodazole stimulates RhoA activity, and inhibition of the RhoA target ROCK allows nocodazole-treated cells to re-establish lamellipodia and uropods and persistent migratory polarity. ROCK inhibition decreases nocodazole-induced membrane blebbing and stabilizes MTs. The myosin inhibitor blebbistatin also stabilizes MTs, indicating that RhoA/ROCK act through myosin II to destabilize MTs.<h4>Conclusions/significance</h4>Our results indicate that RhoA/ROCK signaling normally contributes to migration by affecting both actomyosin contractility and MT stability. We propose that regulation of MT stability and RhoA/ROCK activity is a mechanism to alter T-cell migratory behavior from lamellipodium-based persistent migration to bleb-based migration with frequent turning.
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spelling doaj-art-c6bea63751a044e9aa9b0da3bef0d2b02025-08-20T02:31:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032010-01-0151e877410.1371/journal.pone.0008774Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.Aya TakesonoSarah J HeasmanBeata Wojciak-StothardRitu GargAnne J Ridley<h4>Background</h4>Migrating leukocytes normally have a polarized morphology with an actin-rich lamellipodium at the front and a uropod at the rear. Microtubules (MTs) are required for persistent migration and chemotaxis, but how they affect cell polarity is not known.<h4>Methodology/principal findings</h4>Here we report that T cells treated with nocodazole to disrupt MTs are unable to form a stable uropod or lamellipodium, and instead often move by membrane blebbing with reduced migratory persistence. However, uropod-localized receptors and ezrin/radixin/moesin proteins still cluster in nocodazole-treated cells, indicating that MTs are required specifically for uropod stability. Nocodazole stimulates RhoA activity, and inhibition of the RhoA target ROCK allows nocodazole-treated cells to re-establish lamellipodia and uropods and persistent migratory polarity. ROCK inhibition decreases nocodazole-induced membrane blebbing and stabilizes MTs. The myosin inhibitor blebbistatin also stabilizes MTs, indicating that RhoA/ROCK act through myosin II to destabilize MTs.<h4>Conclusions/significance</h4>Our results indicate that RhoA/ROCK signaling normally contributes to migration by affecting both actomyosin contractility and MT stability. We propose that regulation of MT stability and RhoA/ROCK activity is a mechanism to alter T-cell migratory behavior from lamellipodium-based persistent migration to bleb-based migration with frequent turning.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0008774&type=printable
spellingShingle Aya Takesono
Sarah J Heasman
Beata Wojciak-Stothard
Ritu Garg
Anne J Ridley
Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
PLoS ONE
title Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
title_full Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
title_fullStr Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
title_full_unstemmed Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
title_short Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells.
title_sort microtubules regulate migratory polarity through rho rock signaling in t cells
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0008774&type=printable
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AT beatawojciakstothard microtubulesregulatemigratorypolaritythroughrhorocksignalingintcells
AT ritugarg microtubulesregulatemigratorypolaritythroughrhorocksignalingintcells
AT annejridley microtubulesregulatemigratorypolaritythroughrhorocksignalingintcells