Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia

Cell division is essential to expand, shape, and replenish epithelia. In the adult small intestine, cells from a common progenitor intermix with other lineages, whereas cell progeny in many other epithelia form contiguous patches. The mechanisms that generate these distinct patterns of progeny are p...

Full description

Bibliographic Details
Main Authors: Kara L McKinley, Nico Stuurman, Loic A Royer, Christoph Schartner, David Castillo-Azofeifa, Markus Delling, Ophir D Klein, Ronald D Vale
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/36739
id doaj-1ecc5bf280c04ae08f3035b81a637af0
record_format Article
spelling doaj-1ecc5bf280c04ae08f3035b81a637af02021-05-05T15:55:28ZengeLife Sciences Publications LtdeLife2050-084X2018-06-01710.7554/eLife.36739Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epitheliaKara L McKinley0https://orcid.org/0000-0001-6283-9168Nico Stuurman1https://orcid.org/0000-0002-6179-8613Loic A Royer2Christoph Schartner3https://orcid.org/0000-0003-0599-3956David Castillo-Azofeifa4Markus Delling5Ophir D Klein6https://orcid.org/0000-0002-6254-7082Ronald D Vale7https://orcid.org/0000-0003-3460-2758Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesChan Zuckerberg Biohub, San Francisco, United StatesDepartment of Physiology, University of California, San Francisco, San Francisco, United StatesDepartment of Orofacial Sciences, University of California, San Francisco, San Francisco, United States; Program in Craniofacial Biology, University of California, San Francisco, San Francisco, United StatesDepartment of Physiology, University of California, San Francisco, San Francisco, United StatesDepartment of Orofacial Sciences, University of California, San Francisco, San Francisco, United States; Program in Craniofacial Biology, University of California, San Francisco, San Francisco, United States; Department of Pediatrics, University of California, San Francisco, San Francisco, United States; Institute for Human Genetics, University of California, San Francisco, San Francisco, United StatesDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, United States; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesCell division is essential to expand, shape, and replenish epithelia. In the adult small intestine, cells from a common progenitor intermix with other lineages, whereas cell progeny in many other epithelia form contiguous patches. The mechanisms that generate these distinct patterns of progeny are poorly understood. Using light sheet and confocal imaging of intestinal organoids, we show that lineages intersperse during cytokinesis, when elongated interphase cells insert between apically displaced daughters. Reducing the cellular aspect ratio to minimize the height difference between interphase and mitotic cells disrupts interspersion, producing contiguous patches. Cellular aspect ratio is similarly a key parameter for division-coupled interspersion in the early mouse embryo, suggesting that this physical mechanism for patterning progeny may pertain to many mammalian epithelia. Our results reveal that the process of cytokinesis in elongated mammalian epithelia allows lineages to intermix and that cellular aspect ratio is a critical modulator of the progeny pattern.https://elifesciences.org/articles/36739organoidlight sheet microscopyepitheliummitosisintestinestem cell
collection DOAJ
language English
format Article
sources DOAJ
author Kara L McKinley
Nico Stuurman
Loic A Royer
Christoph Schartner
David Castillo-Azofeifa
Markus Delling
Ophir D Klein
Ronald D Vale
spellingShingle Kara L McKinley
Nico Stuurman
Loic A Royer
Christoph Schartner
David Castillo-Azofeifa
Markus Delling
Ophir D Klein
Ronald D Vale
Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
eLife
organoid
light sheet microscopy
epithelium
mitosis
intestine
stem cell
author_facet Kara L McKinley
Nico Stuurman
Loic A Royer
Christoph Schartner
David Castillo-Azofeifa
Markus Delling
Ophir D Klein
Ronald D Vale
author_sort Kara L McKinley
title Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
title_short Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
title_full Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
title_fullStr Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
title_full_unstemmed Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
title_sort cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-06-01
description Cell division is essential to expand, shape, and replenish epithelia. In the adult small intestine, cells from a common progenitor intermix with other lineages, whereas cell progeny in many other epithelia form contiguous patches. The mechanisms that generate these distinct patterns of progeny are poorly understood. Using light sheet and confocal imaging of intestinal organoids, we show that lineages intersperse during cytokinesis, when elongated interphase cells insert between apically displaced daughters. Reducing the cellular aspect ratio to minimize the height difference between interphase and mitotic cells disrupts interspersion, producing contiguous patches. Cellular aspect ratio is similarly a key parameter for division-coupled interspersion in the early mouse embryo, suggesting that this physical mechanism for patterning progeny may pertain to many mammalian epithelia. Our results reveal that the process of cytokinesis in elongated mammalian epithelia allows lineages to intermix and that cellular aspect ratio is a critical modulator of the progeny pattern.
topic organoid
light sheet microscopy
epithelium
mitosis
intestine
stem cell
url https://elifesciences.org/articles/36739
work_keys_str_mv AT karalmckinley cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT nicostuurman cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT loicaroyer cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT christophschartner cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT davidcastilloazofeifa cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT markusdelling cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT ophirdklein cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
AT ronalddvale cellularaspectratioandcelldivisionmechanicsunderliethepatterningofcellprogenyindiversemammalianepithelia
_version_ 1721459639673946112