Enucleated cells reveal differential roles of the nucleus in cell migration, polarity, and mechanotransduction

David M Graham; Tomas Andersen; Lisa Sharek; Gunes Uzer; Katheryn Rothenberg; Brenton D Hoffman; Janet Rubin; Martial Balland; James E Bear; Keith Burridge

doi:10.1083/jcb.201706097

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Enucleated cells reveal differential roles of the nucleus in cell migration, polarity, and mechanotransduction

Journal article

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Enucleated cells reveal differential roles of the nucleus in cell migration, polarity, and mechanotransduction

David M Graham, Tomas Andersen, Lisa Sharek, Gunes Uzer, Katheryn Rothenberg, Brenton D Hoffman, Janet Rubin, Martial Balland, James E Bear and Keith Burridge

The Journal of cell biology, Vol.217(3), pp.895-914

03/05/2018

DOI: 10.1083/jcb.201706097

PMCID: PMC5839789

PMID: 29351995

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Abstract

The nucleus has long been postulated to play a critical physical role during cell polarization and migration, but that role has not been defined or rigorously tested. Here, we enucleated cells to test the physical necessity of the nucleus during cell polarization and directed migration. Using enucleated mammalian cells (cytoplasts), we found that polarity establishment and cell migration in one dimension (1D) and two dimensions (2D) occur without the nucleus. Cytoplasts directionally migrate toward soluble (chemotaxis) and surface-bound (haptotaxis) extracellular cues and migrate collectively in scratch-wound assays. Consistent with previous studies, migration in 3D environments was dependent on the nucleus. In part, this likely reflects the decreased force exerted by cytoplasts on mechanically compliant substrates. This response is mimicked both in cells with nucleocytoskeletal defects and upon inhibition of actomyosin-based contractility. Together, our observations reveal that the nucleus is dispensable for polarization and migration in 1D and 2D but critical for proper cell mechanical responses.

Cell Nucleus - metabolism

Cell Polarity - physiology

Chemotaxis - physiology

Cytoplasm - metabolism

Human Umbilical Vein Endothelial Cells - cytology

Human Umbilical Vein Endothelial Cells - metabolism

Humans

Details

Title: Subtitle: Enucleated cells reveal differential roles of the nucleus in cell migration, polarity, and mechanotransduction
Creators: David M Graham - University of North Carolina at Chapel Hill
Tomas Andersen - Laboratoire Interdisciplinaire de Physique
Lisa Sharek - University of North Carolina at Chapel Hill
Gunes Uzer - Boise State University
Katheryn Rothenberg - Duke University
Brenton D Hoffman - Duke University
Janet Rubin - University of North Carolina at Chapel Hill
Martial Balland - Université Paris Cité
James E Bear - University of North Carolina at Chapel Hill
Keith Burridge - University of North Carolina at Chapel Hill
Resource Type: Journal article
Publication Details: The Journal of cell biology, Vol.217(3), pp.895-914
DOI: 10.1083/jcb.201706097
PMID: 29351995
PMCID: PMC5839789
NLM abbreviation: J Cell Biol
ISSN: 0021-9525
eISSN: 1540-8140
Grant note: R01 AR066616 / NIAMS NIH HHS R01 GM029860 / NIGMS NIH HHS R01 GM110155 / NIGMS NIH HHS P20 GM109095 / NIGMS NIH HHS P01 GM103723 / NIGMS NIH HHS R35 GM130312 / NIGMS NIH HHS P30 CA016086 / NCI NIH HHS R01 GM111557 / NIGMS NIH HHS
Language: English
Date published: 03/05/2018
Academic Unit: Biology
Record Identifier: 9984696717802771

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