Kinetochore-independent chromosome segregation driven by lateral microtubule bundles

During cell division, chromosomes attach to spindle microtubules at sites called kinetochores, and force generated at the kinetochore-microtubule interface is the main driver of chromosome movement. Surprisingly, kinetochores are not required for chromosome segregation on acentrosomal spindles in Ca...

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Main Authors: Christina C Muscat, Keila M Torre-Santiago, Michael V Tran, James A Powers, Sarah M Wignall
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/06462
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author Christina C Muscat
Keila M Torre-Santiago
Michael V Tran
James A Powers
Sarah M Wignall
author_facet Christina C Muscat
Keila M Torre-Santiago
Michael V Tran
James A Powers
Sarah M Wignall
author_sort Christina C Muscat
collection DOAJ
description During cell division, chromosomes attach to spindle microtubules at sites called kinetochores, and force generated at the kinetochore-microtubule interface is the main driver of chromosome movement. Surprisingly, kinetochores are not required for chromosome segregation on acentrosomal spindles in Caenorhabditis elegans oocytes, but the mechanism driving chromosomes apart in their absence is not understood. In this study, we show that lateral microtubule–chromosome associations established during prometaphase remain intact during anaphase to facilitate separation, defining a novel form of kinetochore-independent segregation. Chromosome dynamics during congression and segregation are controlled by opposing forces; plus-end directed forces are mediated by a protein complex that forms a ring around the chromosome center and dynein on chromosome arms provides a minus-end force. At anaphase onset, ring removal shifts the balance between these forces, triggering poleward movement along lateral microtubule bundles. This represents an elegant strategy for controlling chromosomal movements during cell division distinct from the canonical kinetochore-driven mechanism.
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spelling doaj.art-c4229fd7714e4e4dbb40a5ab82e965602022-12-22T04:29:21ZengeLife Sciences Publications LtdeLife2050-084X2015-05-01410.7554/eLife.06462Kinetochore-independent chromosome segregation driven by lateral microtubule bundlesChristina C Muscat0Keila M Torre-Santiago1Michael V Tran2James A Powers3Sarah M Wignall4Department of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesLight Microscopy Imaging Center, Indiana University, Bloomington, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDuring cell division, chromosomes attach to spindle microtubules at sites called kinetochores, and force generated at the kinetochore-microtubule interface is the main driver of chromosome movement. Surprisingly, kinetochores are not required for chromosome segregation on acentrosomal spindles in Caenorhabditis elegans oocytes, but the mechanism driving chromosomes apart in their absence is not understood. In this study, we show that lateral microtubule–chromosome associations established during prometaphase remain intact during anaphase to facilitate separation, defining a novel form of kinetochore-independent segregation. Chromosome dynamics during congression and segregation are controlled by opposing forces; plus-end directed forces are mediated by a protein complex that forms a ring around the chromosome center and dynein on chromosome arms provides a minus-end force. At anaphase onset, ring removal shifts the balance between these forces, triggering poleward movement along lateral microtubule bundles. This represents an elegant strategy for controlling chromosomal movements during cell division distinct from the canonical kinetochore-driven mechanism.https://elifesciences.org/articles/06462mitosismeiosisoocytespindlemicrotubulecytoskeleton
spellingShingle Christina C Muscat
Keila M Torre-Santiago
Michael V Tran
James A Powers
Sarah M Wignall
Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
eLife
mitosis
meiosis
oocyte
spindle
microtubule
cytoskeleton
title Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
title_full Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
title_fullStr Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
title_full_unstemmed Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
title_short Kinetochore-independent chromosome segregation driven by lateral microtubule bundles
title_sort kinetochore independent chromosome segregation driven by lateral microtubule bundles
topic mitosis
meiosis
oocyte
spindle
microtubule
cytoskeleton
url https://elifesciences.org/articles/06462
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AT keilamtorresantiago kinetochoreindependentchromosomesegregationdrivenbylateralmicrotubulebundles
AT michaelvtran kinetochoreindependentchromosomesegregationdrivenbylateralmicrotubulebundles
AT jamesapowers kinetochoreindependentchromosomesegregationdrivenbylateralmicrotubulebundles
AT sarahmwignall kinetochoreindependentchromosomesegregationdrivenbylateralmicrotubulebundles