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

Author:

Booth Alexander JR1ORCID,Yue Zuojun1,Eykelenboom John K1ORCID,Stiff Tom2,Luxton GW Gant3ORCID,Hochegger Helfrid2ORCID,Tanaka Tomoyuki U1ORCID

Affiliation:

1. Centre for Gene Regulation and Expression, School of Life Sciences, University of Dundee, Dundee, United Kingdom

2. Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom

3. College of Biological Sciences, University of Minnesota, Minneapolis, United States

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.

Funder

Wellcome

Cancer Research UK

Medical Research Council

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference30 articles.

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3. Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading;Gauthier;PNAS,2011

4. Nuclear envelope breakdown in mammalian cells involves stepwise Lamina disassembly and microtubule-drive deformation of the nuclear membrane;Georgatos;Journal of Cell Science,1997

5. Regulation of kinetochore-microtubule attachments through homeostatic control during mitosis;Godek;Nature Reviews Molecular Cell Biology,2015

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