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...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2019-12-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/49249 |
id |
doaj-dc7ad15b2e494f039193f5433ed8fe41 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT kendalljlough telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT kevinmbyrd telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT carlospdescovich telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT daniellecspitzer telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT abbyjbergman telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT gerardmjbeaudoiniii telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT louisfreichardt telophasecorrectionrefinesdivisionorientationinstratifiedepithelia AT scottewilliams telophasecorrectionrefinesdivisionorientationinstratifiedepithelia |
_version_ |
1721458792541978624 |