Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Lough, Kendall J, Byrd, Kevin M, Descovich, Carlos P, Spitzer, Danielle C, Bergman, Abby J, Beaudoin, Gerard MJ, Reichardt, Louis F, Williams, Scott E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959978/
https://www.ncbi.nlm.nih.gov/pubmed/31833472
http://dx.doi.org/10.7554/eLife.49249
_version_ 1783487691623497728
author Lough, Kendall J
Byrd, Kevin M
Descovich, Carlos P
Spitzer, Danielle C
Bergman, Abby J
Beaudoin, Gerard MJ
Reichardt, Louis F
Williams, Scott E
author_facet Lough, Kendall J
Byrd, Kevin M
Descovich, Carlos P
Spitzer, Danielle C
Bergman, Abby J
Beaudoin, Gerard MJ
Reichardt, Louis F
Williams, Scott E
author_sort Lough, Kendall J
collection PubMed
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.
format Online
Article
Text
id pubmed-6959978
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-69599782020-01-15 Telophase correction refines division orientation in stratified epithelia Lough, Kendall J Byrd, Kevin M Descovich, Carlos P Spitzer, Danielle C Bergman, Abby J Beaudoin, Gerard MJ Reichardt, Louis F Williams, Scott E eLife Cell Biology 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. eLife Sciences Publications, Ltd 2019-12-13 /pmc/articles/PMC6959978/ /pubmed/31833472 http://dx.doi.org/10.7554/eLife.49249 Text en © 2019, Lough et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Lough, Kendall J
Byrd, Kevin M
Descovich, Carlos P
Spitzer, Danielle C
Bergman, Abby J
Beaudoin, Gerard MJ
Reichardt, Louis F
Williams, Scott E
Telophase correction refines division orientation in stratified epithelia
title 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_short Telophase correction refines division orientation in stratified epithelia
title_sort telophase correction refines division orientation in stratified epithelia
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6959978/
https://www.ncbi.nlm.nih.gov/pubmed/31833472
http://dx.doi.org/10.7554/eLife.49249
work_keys_str_mv AT loughkendallj telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT byrdkevinm telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT descovichcarlosp telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT spitzerdaniellec telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT bergmanabbyj telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT beaudoingerardmj telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT reichardtlouisf telophasecorrectionrefinesdivisionorientationinstratifiedepithelia
AT williamsscotte telophasecorrectionrefinesdivisionorientationinstratifiedepithelia