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...

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Bibliographic Details
Published in:eLife 2018-06, Vol.7
Main Authors: McKinley, Kara L, Stuurman, Nico, Royer, Loic A, Schartner, Christoph, Castillo-Azofeifa, David, Delling, Markus, Klein, Ophir D, Vale, Ronald D
Format: Article
Language:English
Subjects:
Animals
Body Patterning - physiology
Cell Biology
Cell division
Cell Division - physiology
Cell Lineage - physiology
Cytokinesis
Cytokinesis - physiology
Cytoskeleton
Daughters
Developmental Biology
Embryo, Mammalian - cytology
Embryo, Mammalian - embryology
Epithelial Cells - cytology
Epithelial Cells - metabolism
Epithelial Cells - physiology
epithelium
Epithelium - embryology
Epithelium - physiology
Female
Interphase
intestine
light sheet microscopy
Male
Mammals - embryology
Mammals - physiology
Mice, Inbred C57BL
Mice, Transgenic
Microscopy
Microscopy, Confocal
mitosis
Offspring
organoid
Organoids
Pattern formation
Small intestine
stem cell
Stem cells
Time-Lapse Imaging - methods
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Summary: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.
ISSN:2050-084X
2050-084X
DOI:10.7554/elife.36739