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Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments

Proper kinetochore-microtubule attachments, mediated by the NDC80 complex, are required for error-free chromosome segregation. Erroneous attachments are corrected by the tension dependence of kinetochore-microtubule interactions. Here, we present a method, based on fluorescence lifetime imaging micr...

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Detalles Bibliográficos
Autores principales: Yoo, Tae Yeon, Choi, Jeong-Mo, Conway, William, Yu, Che-Hang, Pappu, Rohit V, Needleman, Daniel J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6089600/
https://www.ncbi.nlm.nih.gov/pubmed/30044223
http://dx.doi.org/10.7554/eLife.36392
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author Yoo, Tae Yeon
Choi, Jeong-Mo
Conway, William
Yu, Che-Hang
Pappu, Rohit V
Needleman, Daniel J
author_facet Yoo, Tae Yeon
Choi, Jeong-Mo
Conway, William
Yu, Che-Hang
Pappu, Rohit V
Needleman, Daniel J
author_sort Yoo, Tae Yeon
collection PubMed
description Proper kinetochore-microtubule attachments, mediated by the NDC80 complex, are required for error-free chromosome segregation. Erroneous attachments are corrected by the tension dependence of kinetochore-microtubule interactions. Here, we present a method, based on fluorescence lifetime imaging microscopy and Förster resonance energy transfer, to quantitatively measure the fraction of NDC80 complexes bound to microtubules at individual kinetochores in living human cells. We found that NDC80 binding is modulated in a chromosome autonomous fashion over prometaphase and metaphase, and is predominantly regulated by centromere tension. We show that this tension dependency requires phosphorylation of the N-terminal tail of Hec1, a component of the NDC80 complex, and the proper localization of Aurora B kinase, which modulates NDC80 binding. Our results lead to a mathematical model of the molecular basis of tension-dependent NDC80 binding to kinetochore microtubules in vivo.
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spelling pubmed-60896002018-08-15 Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments Yoo, Tae Yeon Choi, Jeong-Mo Conway, William Yu, Che-Hang Pappu, Rohit V Needleman, Daniel J eLife Cell Biology Proper kinetochore-microtubule attachments, mediated by the NDC80 complex, are required for error-free chromosome segregation. Erroneous attachments are corrected by the tension dependence of kinetochore-microtubule interactions. Here, we present a method, based on fluorescence lifetime imaging microscopy and Förster resonance energy transfer, to quantitatively measure the fraction of NDC80 complexes bound to microtubules at individual kinetochores in living human cells. We found that NDC80 binding is modulated in a chromosome autonomous fashion over prometaphase and metaphase, and is predominantly regulated by centromere tension. We show that this tension dependency requires phosphorylation of the N-terminal tail of Hec1, a component of the NDC80 complex, and the proper localization of Aurora B kinase, which modulates NDC80 binding. Our results lead to a mathematical model of the molecular basis of tension-dependent NDC80 binding to kinetochore microtubules in vivo. eLife Sciences Publications, Ltd 2018-07-25 /pmc/articles/PMC6089600/ /pubmed/30044223 http://dx.doi.org/10.7554/eLife.36392 Text en © 2018, Yoo et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Yoo, Tae Yeon
Choi, Jeong-Mo
Conway, William
Yu, Che-Hang
Pappu, Rohit V
Needleman, Daniel J
Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title_full Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title_fullStr Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title_full_unstemmed Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title_short Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
title_sort measuring ndc80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6089600/
https://www.ncbi.nlm.nih.gov/pubmed/30044223
http://dx.doi.org/10.7554/eLife.36392
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