Telophase correction refines division orientation in stratified epithelia

During organogenesis, precise control of spindle orientation balances proliferation and differentiation. In the developing murine epidermis, planar and perpendicular divisions yield symmetric and asymmetric fate outcomes, respectively. Classically, division axis specification involves centrosome mig...

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Main Authors: Kendall J Lough, Kevin M Byrd, Carlos P Descovich, Danielle C Spitzer, Abby J Bergman, Gerard MJ Beaudoin III, Louis F Reichardt, Scott E Williams
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49249
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spelling doaj-dc7ad15b2e494f039193f5433ed8fe412021-05-05T18:11:08ZengeLife Sciences Publications LtdeLife2050-084X2019-12-01810.7554/eLife.49249Telophase correction refines division orientation in stratified epitheliaKendall J Lough0https://orcid.org/0000-0001-9663-6983Kevin M Byrd1https://orcid.org/0000-0002-5565-0524Carlos P Descovich2https://orcid.org/0000-0002-6366-5195Danielle C Spitzer3https://orcid.org/0000-0003-4827-1857Abby J Bergman4Gerard MJ Beaudoin III5Louis F Reichardt6Scott E Williams7https://orcid.org/0000-0001-9975-7334Department of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United StatesDepartment of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United States; Department of Oral & Craniofacial Health Sciences, The University of North Carolina School of Dentistry, Chapel Hill, United StatesDepartment of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United StatesDepartment of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United StatesDepartment of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United States; Department of Physiology, University of California, San Francisco, San Francisco, United StatesDepartment of Pathology and Laboratory Medicine, Lineberger Comprehensive Cancer Center, The University of North Carolina, Chapel Hill, United States; Department of Biology, Lineberger Comprehensive Cancer Centre, The University of North Carolina, Chapel Hill, United StatesDuring organogenesis, precise control of spindle orientation balances proliferation and differentiation. In the developing murine epidermis, planar and perpendicular divisions yield symmetric and asymmetric fate outcomes, respectively. Classically, division axis specification involves centrosome migration and spindle rotation, events occurring early in mitosis. Here, we identify a novel orientation mechanism which corrects erroneous anaphase orientations during telophase. The directionality of reorientation correlates with the maintenance or loss of basal contact by the apical daughter. While the scaffolding protein LGN is known to determine initial spindle positioning, we show that LGN also functions during telophase to reorient oblique divisions toward perpendicular. The fidelity of telophase correction also relies on the tension-sensitive adherens junction proteins vinculin, α-E-catenin, and afadin. Failure of this corrective mechanism impacts tissue architecture, as persistent oblique divisions induce precocious, sustained differentiation. The division orientation plasticity provided by telophase correction may enable progenitors to adapt to local tissue needs.https://elifesciences.org/articles/49249oriented cell divisionspindle orientationasymmetric cell divisionepidermal differentiationadherens junctioncell-cell adhesion
collection DOAJ
language English
format Article
sources DOAJ
author Kendall J Lough
Kevin M Byrd
Carlos P Descovich
Danielle C Spitzer
Abby J Bergman
Gerard MJ Beaudoin III
Louis F Reichardt
Scott E Williams
spellingShingle Kendall J Lough
Kevin M Byrd
Carlos P Descovich
Danielle C Spitzer
Abby J Bergman
Gerard MJ Beaudoin III
Louis F Reichardt
Scott E Williams
Telophase correction refines division orientation in stratified epithelia
eLife
oriented cell division
spindle orientation
asymmetric cell division
epidermal differentiation
adherens junction
cell-cell adhesion
author_facet Kendall J Lough
Kevin M Byrd
Carlos P Descovich
Danielle C Spitzer
Abby J Bergman
Gerard MJ Beaudoin III
Louis F Reichardt
Scott E Williams
author_sort Kendall J Lough
title Telophase correction refines division orientation in stratified epithelia
title_short Telophase correction refines division orientation in stratified epithelia
title_full Telophase correction refines division orientation in stratified epithelia
title_fullStr Telophase correction refines division orientation in stratified epithelia
title_full_unstemmed Telophase correction refines division orientation in stratified epithelia
title_sort telophase correction refines division orientation in stratified epithelia
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-12-01
description During organogenesis, precise control of spindle orientation balances proliferation and differentiation. In the developing murine epidermis, planar and perpendicular divisions yield symmetric and asymmetric fate outcomes, respectively. Classically, division axis specification involves centrosome migration and spindle rotation, events occurring early in mitosis. Here, we identify a novel orientation mechanism which corrects erroneous anaphase orientations during telophase. The directionality of reorientation correlates with the maintenance or loss of basal contact by the apical daughter. While the scaffolding protein LGN is known to determine initial spindle positioning, we show that LGN also functions during telophase to reorient oblique divisions toward perpendicular. The fidelity of telophase correction also relies on the tension-sensitive adherens junction proteins vinculin, α-E-catenin, and afadin. Failure of this corrective mechanism impacts tissue architecture, as persistent oblique divisions induce precocious, sustained differentiation. The division orientation plasticity provided by telophase correction may enable progenitors to adapt to local tissue needs.
topic oriented cell division
spindle orientation
asymmetric cell division
epidermal differentiation
adherens junction
cell-cell adhesion
url https://elifesciences.org/articles/49249
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