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Centrosome centering and decentering by microtubule network rearrangement

The centrosome is positioned at the cell center by pushing and pulling forces transmitted by microtubules (MTs). Centrosome decentering is often considered to result from asymmetric, cortical pulling forces exerted in particular by molecular motors on MTs and controlled by external cues affecting th...

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Autores principales: Letort, Gaëlle, Nedelec, Francois, Blanchoin, Laurent, Théry, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5025270/
https://www.ncbi.nlm.nih.gov/pubmed/27440925
http://dx.doi.org/10.1091/mbc.E16-06-0395
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author Letort, Gaëlle
Nedelec, Francois
Blanchoin, Laurent
Théry, Manuel
author_facet Letort, Gaëlle
Nedelec, Francois
Blanchoin, Laurent
Théry, Manuel
author_sort Letort, Gaëlle
collection PubMed
description The centrosome is positioned at the cell center by pushing and pulling forces transmitted by microtubules (MTs). Centrosome decentering is often considered to result from asymmetric, cortical pulling forces exerted in particular by molecular motors on MTs and controlled by external cues affecting the cell cortex locally. Here we used numerical simulations to investigate the possibility that it could equally result from the redistribution of pushing forces due to a reorientation of MTs. We first showed that MT gliding along cell edges and pivoting around the centrosome regulate MT rearrangement and thereby direct the spatial distribution of pushing forces, whereas the number, dynamics, and stiffness of MTs determine the magnitude of these forces. By modulating these parameters, we identified different regimes, involving both pushing and pulling forces, characterized by robust centrosome centering, robust off-centering, or “reactive” positioning. In the last-named conditions, weak asymmetric cues can induce a misbalance of pushing and pulling forces, resulting in an abrupt transition from a centered to an off-centered position. Taken together, these results point to the central role played by the configuration of the MTs on the distribution of pushing forces that position the centrosome. We suggest that asymmetric external cues should not be seen as direct driver of centrosome decentering and cell polarization but instead as inducers of an effective reorganization of the MT network, fostering centrosome motion to the cell periphery.
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spelling pubmed-50252702016-11-30 Centrosome centering and decentering by microtubule network rearrangement Letort, Gaëlle Nedelec, Francois Blanchoin, Laurent Théry, Manuel Mol Biol Cell Articles The centrosome is positioned at the cell center by pushing and pulling forces transmitted by microtubules (MTs). Centrosome decentering is often considered to result from asymmetric, cortical pulling forces exerted in particular by molecular motors on MTs and controlled by external cues affecting the cell cortex locally. Here we used numerical simulations to investigate the possibility that it could equally result from the redistribution of pushing forces due to a reorientation of MTs. We first showed that MT gliding along cell edges and pivoting around the centrosome regulate MT rearrangement and thereby direct the spatial distribution of pushing forces, whereas the number, dynamics, and stiffness of MTs determine the magnitude of these forces. By modulating these parameters, we identified different regimes, involving both pushing and pulling forces, characterized by robust centrosome centering, robust off-centering, or “reactive” positioning. In the last-named conditions, weak asymmetric cues can induce a misbalance of pushing and pulling forces, resulting in an abrupt transition from a centered to an off-centered position. Taken together, these results point to the central role played by the configuration of the MTs on the distribution of pushing forces that position the centrosome. We suggest that asymmetric external cues should not be seen as direct driver of centrosome decentering and cell polarization but instead as inducers of an effective reorganization of the MT network, fostering centrosome motion to the cell periphery. The American Society for Cell Biology 2016-09-15 /pmc/articles/PMC5025270/ /pubmed/27440925 http://dx.doi.org/10.1091/mbc.E16-06-0395 Text en © 2016 Letort et al. 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 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Letort, Gaëlle
Nedelec, Francois
Blanchoin, Laurent
Théry, Manuel
Centrosome centering and decentering by microtubule network rearrangement
title Centrosome centering and decentering by microtubule network rearrangement
title_full Centrosome centering and decentering by microtubule network rearrangement
title_fullStr Centrosome centering and decentering by microtubule network rearrangement
title_full_unstemmed Centrosome centering and decentering by microtubule network rearrangement
title_short Centrosome centering and decentering by microtubule network rearrangement
title_sort centrosome centering and decentering by microtubule network rearrangement
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5025270/
https://www.ncbi.nlm.nih.gov/pubmed/27440925
http://dx.doi.org/10.1091/mbc.E16-06-0395
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