Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis

Alexander J. R. Booth, Zuojun Yue, John K. Eykelenboom, Tom Stiff, G. W. Gant Luxton, Helfrid Hochegger, Tomoyuki Tanaka (Lead / Corresponding author)

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Abstract

To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome interaction with the spindle can be influenced by how widely chromosomes are scattered in space. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced soon after nuclear envelope breakdown (NEBD) in human cells. The CSV reduction occurs primarily independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on nuclear envelope remnants soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates timely chromosome congression and correct segregation. Thus, we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient and correct chromosome-spindle interactions.

Original languageEnglish
Article numbere46902
JournaleLife
Volume8
Early online date2 Jul 2019
DOIs
Publication statusPublished - 3 Jul 2019

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pioglitazone
Nuclear Envelope
Human Chromosomes
Myosins
Chromosomes
Mitosis
Scattering
Microtubules
Myosin Type II
Spindle Apparatus

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@article{92427de518b643138e66537721d13f30,
title = "Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis",
abstract = "To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome interaction with the spindle can be influenced by how widely chromosomes are scattered in space. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced soon after nuclear envelope breakdown (NEBD) in human cells. The CSV reduction occurs primarily independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on nuclear envelope remnants soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates timely chromosome congression and correct segregation. Thus, we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient and correct chromosome-spindle interactions.",
author = "Booth, {Alexander J. R.} and Zuojun Yue and Eykelenboom, {John K.} and Tom Stiff and Luxton, {G. W. Gant} and Helfrid Hochegger and Tomoyuki Tanaka",
note = "This work was supported by the Wellcome Trust (096535/Z/11/Z, 097945/Z/11/Z, 208401/Z/17/Z), Cancer Research UK (C28206/A114499) and Medical Research Council (MR/K015869/1). T.U.T. is a Wellcome Trust Principal Research Fellow.",
year = "2019",
month = "7",
day = "3",
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language = "English",
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journal = "eLife",
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Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis. / Booth, Alexander J. R.; Yue, Zuojun; Eykelenboom, John K.; Stiff, Tom; Luxton, G. W. Gant; Hochegger, Helfrid; Tanaka, Tomoyuki (Lead / Corresponding author).

In: eLife, Vol. 8, e46902, 03.07.2019.

Research output: Contribution to journalArticle

TY - JOUR

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AU - Booth, Alexander J. R.

AU - Yue, Zuojun

AU - Eykelenboom, John K.

AU - Stiff, Tom

AU - Luxton, G. W. Gant

AU - Hochegger, Helfrid

AU - Tanaka, Tomoyuki

N1 - This work was supported by the Wellcome Trust (096535/Z/11/Z, 097945/Z/11/Z, 208401/Z/17/Z), Cancer Research UK (C28206/A114499) and Medical Research Council (MR/K015869/1). T.U.T. is a Wellcome Trust Principal Research Fellow.

PY - 2019/7/3

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N2 - To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome interaction with the spindle can be influenced by how widely chromosomes are scattered in space. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced soon after nuclear envelope breakdown (NEBD) in human cells. The CSV reduction occurs primarily independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on nuclear envelope remnants soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates timely chromosome congression and correct segregation. Thus, we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient and correct chromosome-spindle interactions.

AB - To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome interaction with the spindle can be influenced by how widely chromosomes are scattered in space. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced soon after nuclear envelope breakdown (NEBD) in human cells. The CSV reduction occurs primarily independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on nuclear envelope remnants soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates timely chromosome congression and correct segregation. Thus, we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient and correct chromosome-spindle interactions.

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