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Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells

Endothelial cell migration is critical for vascular angiogenesis and is compromised to facilitate tumor metastasis. The migratory process requires the coordinated assembly and disassembly of focal adhesions (FA), actin, and microtubules (MT). MT dynamics at FAs deliver vesicular cargoes and enhance...

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Autores principales: Merenich, Daniel, Nakos, Konstantinos, Pompan, Taylor, Donovan, Samantha J., Gill, Amrik, Patel, Pranav, Spiliotis, Elias T., Myers, Kenneth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282018/
https://www.ncbi.nlm.nih.gov/pubmed/35274967
http://dx.doi.org/10.1091/mbc.E21-06-0334
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author Merenich, Daniel
Nakos, Konstantinos
Pompan, Taylor
Donovan, Samantha J.
Gill, Amrik
Patel, Pranav
Spiliotis, Elias T.
Myers, Kenneth A.
author_facet Merenich, Daniel
Nakos, Konstantinos
Pompan, Taylor
Donovan, Samantha J.
Gill, Amrik
Patel, Pranav
Spiliotis, Elias T.
Myers, Kenneth A.
author_sort Merenich, Daniel
collection PubMed
description Endothelial cell migration is critical for vascular angiogenesis and is compromised to facilitate tumor metastasis. The migratory process requires the coordinated assembly and disassembly of focal adhesions (FA), actin, and microtubules (MT). MT dynamics at FAs deliver vesicular cargoes and enhance actomyosin contractility to promote FA turnover and facilitate cell advance. Noncentrosomal (NC) MTs regulate FA dynamics and are sufficient to drive cell polarity, but how NC MTs target FAs to control FA turnover is not understood. Here, we show that Rac1 induces the assembly of FA-proximal septin filaments that promote NC MT growth into FAs and inhibit mitotic centromere-associated kinesin (MCAK)-associated MT disassembly, thereby maintaining intact MT plus ends proximal to FAs. Septin-associated MT rescue is coupled with accumulation of Aurora-A kinase and cytoplasmic linker-associated protein (CLASP) localization to the MT between septin and FAs. In this way, NC MTs are strategically positioned to undergo MCAK- and CLASP-regulated bouts of assembly and disassembly into FAs, thereby regulating FA turnover and cell migration.
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spelling pubmed-92820182022-07-15 Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells Merenich, Daniel Nakos, Konstantinos Pompan, Taylor Donovan, Samantha J. Gill, Amrik Patel, Pranav Spiliotis, Elias T. Myers, Kenneth A. Mol Biol Cell Articles Endothelial cell migration is critical for vascular angiogenesis and is compromised to facilitate tumor metastasis. The migratory process requires the coordinated assembly and disassembly of focal adhesions (FA), actin, and microtubules (MT). MT dynamics at FAs deliver vesicular cargoes and enhance actomyosin contractility to promote FA turnover and facilitate cell advance. Noncentrosomal (NC) MTs regulate FA dynamics and are sufficient to drive cell polarity, but how NC MTs target FAs to control FA turnover is not understood. Here, we show that Rac1 induces the assembly of FA-proximal septin filaments that promote NC MT growth into FAs and inhibit mitotic centromere-associated kinesin (MCAK)-associated MT disassembly, thereby maintaining intact MT plus ends proximal to FAs. Septin-associated MT rescue is coupled with accumulation of Aurora-A kinase and cytoplasmic linker-associated protein (CLASP) localization to the MT between septin and FAs. In this way, NC MTs are strategically positioned to undergo MCAK- and CLASP-regulated bouts of assembly and disassembly into FAs, thereby regulating FA turnover and cell migration. The American Society for Cell Biology 2022-04-28 /pmc/articles/PMC9282018/ /pubmed/35274967 http://dx.doi.org/10.1091/mbc.E21-06-0334 Text en © 2022 Merenich et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial-Share Alike 4.0 International Creative Commons License.
spellingShingle Articles
Merenich, Daniel
Nakos, Konstantinos
Pompan, Taylor
Donovan, Samantha J.
Gill, Amrik
Patel, Pranav
Spiliotis, Elias T.
Myers, Kenneth A.
Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title_full Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title_fullStr Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title_full_unstemmed Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title_short Septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
title_sort septins guide noncentrosomal microtubules to promote focal adhesion disassembly in migrating cells
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282018/
https://www.ncbi.nlm.nih.gov/pubmed/35274967
http://dx.doi.org/10.1091/mbc.E21-06-0334
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