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Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly

BACKGROUND: At the beginning of mitosis, the cell forms a spindle made of microtubules and associated proteins to segregate chromosomes. An important part of spindle architecture is a set of antiparallel microtubule bundles connecting the spindle poles. A key question is how microtubules extending a...

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Autores principales: Winters, Lora, Ban, Ivana, Prelogović, Marcel, Kalinina, Iana, Pavin, Nenad, Tolić, Iva M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6533735/
https://www.ncbi.nlm.nih.gov/pubmed/31122217
http://dx.doi.org/10.1186/s12915-019-0656-2
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author Winters, Lora
Ban, Ivana
Prelogović, Marcel
Kalinina, Iana
Pavin, Nenad
Tolić, Iva M.
author_facet Winters, Lora
Ban, Ivana
Prelogović, Marcel
Kalinina, Iana
Pavin, Nenad
Tolić, Iva M.
author_sort Winters, Lora
collection PubMed
description BACKGROUND: At the beginning of mitosis, the cell forms a spindle made of microtubules and associated proteins to segregate chromosomes. An important part of spindle architecture is a set of antiparallel microtubule bundles connecting the spindle poles. A key question is how microtubules extending at arbitrary angles form an antiparallel interpolar bundle. RESULTS: Here, we show in fission yeast that microtubules meet at an oblique angle and subsequently rotate into antiparallel alignment. Our live-cell imaging approach provides a direct observation of interpolar bundle formation. By combining experiments with theory, we show that microtubules from each pole search for those from the opposite pole by performing random angular movement. Upon contact, two microtubules slide sideways along each other in a directed manner towards the antiparallel configuration. We introduce the contour length of microtubules as a measure of activity of motors that drive microtubule sliding, which we used together with observation of Cut7/kinesin-5 motors and our theory to reveal the minus-end-directed motility of this motor in vivo. CONCLUSION: Random rotational motion helps microtubules from the opposite poles to find each other and subsequent accumulation of motors allows them to generate forces that drive interpolar bundle formation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0656-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-65337352019-05-28 Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly Winters, Lora Ban, Ivana Prelogović, Marcel Kalinina, Iana Pavin, Nenad Tolić, Iva M. BMC Biol Research Article BACKGROUND: At the beginning of mitosis, the cell forms a spindle made of microtubules and associated proteins to segregate chromosomes. An important part of spindle architecture is a set of antiparallel microtubule bundles connecting the spindle poles. A key question is how microtubules extending at arbitrary angles form an antiparallel interpolar bundle. RESULTS: Here, we show in fission yeast that microtubules meet at an oblique angle and subsequently rotate into antiparallel alignment. Our live-cell imaging approach provides a direct observation of interpolar bundle formation. By combining experiments with theory, we show that microtubules from each pole search for those from the opposite pole by performing random angular movement. Upon contact, two microtubules slide sideways along each other in a directed manner towards the antiparallel configuration. We introduce the contour length of microtubules as a measure of activity of motors that drive microtubule sliding, which we used together with observation of Cut7/kinesin-5 motors and our theory to reveal the minus-end-directed motility of this motor in vivo. CONCLUSION: Random rotational motion helps microtubules from the opposite poles to find each other and subsequent accumulation of motors allows them to generate forces that drive interpolar bundle formation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0656-2) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-23 /pmc/articles/PMC6533735/ /pubmed/31122217 http://dx.doi.org/10.1186/s12915-019-0656-2 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Winters, Lora
Ban, Ivana
Prelogović, Marcel
Kalinina, Iana
Pavin, Nenad
Tolić, Iva M.
Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title_full Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title_fullStr Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title_full_unstemmed Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title_short Pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
title_sort pivoting of microtubules driven by minus-end-directed motors leads to spindle assembly
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6533735/
https://www.ncbi.nlm.nih.gov/pubmed/31122217
http://dx.doi.org/10.1186/s12915-019-0656-2
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