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Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles

In many asymmetrically dividing cells, the microtubule-organizing centers (MTOCs; mammalian centrosome and yeast spindle pole body [SPB]) nucleate more astral microtubules on one of the two spindle poles than the other. This differential activity generally correlates with the age of MTOCs and contri...

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Autores principales: Lengefeld, Jette, Yen, Eric, Chen, Xiuzhen, Leary, Allen, Vogel, Jackie, Barral, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5746063/
https://www.ncbi.nlm.nih.gov/pubmed/29142076
http://dx.doi.org/10.1091/mbc.E16-10-0725
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author Lengefeld, Jette
Yen, Eric
Chen, Xiuzhen
Leary, Allen
Vogel, Jackie
Barral, Yves
author_facet Lengefeld, Jette
Yen, Eric
Chen, Xiuzhen
Leary, Allen
Vogel, Jackie
Barral, Yves
author_sort Lengefeld, Jette
collection PubMed
description In many asymmetrically dividing cells, the microtubule-organizing centers (MTOCs; mammalian centrosome and yeast spindle pole body [SPB]) nucleate more astral microtubules on one of the two spindle poles than the other. This differential activity generally correlates with the age of MTOCs and contributes to orienting the mitotic spindle within the cell. The asymmetry might result from the two MTOCs being in distinctive maturation states. We investigated this model in budding yeast. Using fluorophores with different maturation kinetics to label the outer plaque components of the SPB, we found that the Cnm67 protein is mobile, whereas Spc72 is not. However, these two proteins were rapidly as abundant on both SPBs, indicating that SPBs mature more rapidly than anticipated. Superresolution microscopy confirmed this finding for Spc72 and for the γ-tubulin complex. Moreover, astral microtubule number and length correlated with the subcellular localization of SPBs rather than their age. Kar9-dependent orientation of the spindle drove the differential activity of the SPBs in astral microtubule organization rather than intrinsic differences between the spindle poles. Together, our data establish that Kar9 and spatial cues, rather than the kinetics of SPB maturation, control the asymmetry of astral microtubule organization between the preexisting and new SPBs.
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spelling pubmed-57460632018-03-16 Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles Lengefeld, Jette Yen, Eric Chen, Xiuzhen Leary, Allen Vogel, Jackie Barral, Yves Mol Biol Cell Articles In many asymmetrically dividing cells, the microtubule-organizing centers (MTOCs; mammalian centrosome and yeast spindle pole body [SPB]) nucleate more astral microtubules on one of the two spindle poles than the other. This differential activity generally correlates with the age of MTOCs and contributes to orienting the mitotic spindle within the cell. The asymmetry might result from the two MTOCs being in distinctive maturation states. We investigated this model in budding yeast. Using fluorophores with different maturation kinetics to label the outer plaque components of the SPB, we found that the Cnm67 protein is mobile, whereas Spc72 is not. However, these two proteins were rapidly as abundant on both SPBs, indicating that SPBs mature more rapidly than anticipated. Superresolution microscopy confirmed this finding for Spc72 and for the γ-tubulin complex. Moreover, astral microtubule number and length correlated with the subcellular localization of SPBs rather than their age. Kar9-dependent orientation of the spindle drove the differential activity of the SPBs in astral microtubule organization rather than intrinsic differences between the spindle poles. Together, our data establish that Kar9 and spatial cues, rather than the kinetics of SPB maturation, control the asymmetry of astral microtubule organization between the preexisting and new SPBs. The American Society for Cell Biology 2018-01-01 /pmc/articles/PMC5746063/ /pubmed/29142076 http://dx.doi.org/10.1091/mbc.E16-10-0725 Text en © 2018 Lengefeld, Yen, 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
Lengefeld, Jette
Yen, Eric
Chen, Xiuzhen
Leary, Allen
Vogel, Jackie
Barral, Yves
Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title_full Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title_fullStr Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title_full_unstemmed Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title_short Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
title_sort spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5746063/
https://www.ncbi.nlm.nih.gov/pubmed/29142076
http://dx.doi.org/10.1091/mbc.E16-10-0725
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