Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.

Regulation of cell growth and cell division has a fundamental role in tissue formation, organ development, and cancer progression. Remarkable similarities in the topological distributions were found in a variety of proliferating epithelia in both animals and plants. At the same time, there are speci...

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Main Authors: Yingzi Li, Hammad Naveed, Sema Kachalo, Lisa X Xu, Jie Liang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3422310?pdf=render
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spelling doaj-35dcf88ba24945969106c91de1a0c45a2020-11-24T22:06:49ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0178e4310810.1371/journal.pone.0043108Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.Yingzi LiHammad NaveedSema KachaloLisa X XuJie LiangRegulation of cell growth and cell division has a fundamental role in tissue formation, organ development, and cancer progression. Remarkable similarities in the topological distributions were found in a variety of proliferating epithelia in both animals and plants. At the same time, there are species with significantly varied frequency of hexagonal cells. Moreover, local topology has been shown to be disturbed on the boundary between proliferating and quiescent cells, where cells have fewer sides than natural proliferating epithelia. The mechanisms of regulating these topological changes remain poorly understood. In this study, we use a mechanical model to examine the effects of orientation of division plane, differential proliferation, and mechanical forces on animal epithelial cells. We find that regardless of orientation of division plane, our model can reproduce the commonly observed topological distributions of cells in natural proliferating animal epithelia with the consideration of cell rearrangements. In addition, with different schemes of division plane, we are able to generate different frequency of hexagonal cells, which is consistent with experimental observations. In proliferating cells interfacing quiescent cells, our results show that differential proliferation alone is insufficient to reproduce the local changes in cell topology. Rather, increased tension on the boundary, in conjunction with differential proliferation, can reproduce the observed topological changes. We conclude that both division plane orientation and mechanical forces play important roles in cell topology in animal proliferating epithelia. Moreover, cell memory is also essential for generating specific topological distributions.http://europepmc.org/articles/PMC3422310?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yingzi Li
Hammad Naveed
Sema Kachalo
Lisa X Xu
Jie Liang
spellingShingle Yingzi Li
Hammad Naveed
Sema Kachalo
Lisa X Xu
Jie Liang
Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
PLoS ONE
author_facet Yingzi Li
Hammad Naveed
Sema Kachalo
Lisa X Xu
Jie Liang
author_sort Yingzi Li
title Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
title_short Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
title_full Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
title_fullStr Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
title_full_unstemmed Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
title_sort mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
description Regulation of cell growth and cell division has a fundamental role in tissue formation, organ development, and cancer progression. Remarkable similarities in the topological distributions were found in a variety of proliferating epithelia in both animals and plants. At the same time, there are species with significantly varied frequency of hexagonal cells. Moreover, local topology has been shown to be disturbed on the boundary between proliferating and quiescent cells, where cells have fewer sides than natural proliferating epithelia. The mechanisms of regulating these topological changes remain poorly understood. In this study, we use a mechanical model to examine the effects of orientation of division plane, differential proliferation, and mechanical forces on animal epithelial cells. We find that regardless of orientation of division plane, our model can reproduce the commonly observed topological distributions of cells in natural proliferating animal epithelia with the consideration of cell rearrangements. In addition, with different schemes of division plane, we are able to generate different frequency of hexagonal cells, which is consistent with experimental observations. In proliferating cells interfacing quiescent cells, our results show that differential proliferation alone is insufficient to reproduce the local changes in cell topology. Rather, increased tension on the boundary, in conjunction with differential proliferation, can reproduce the observed topological changes. We conclude that both division plane orientation and mechanical forces play important roles in cell topology in animal proliferating epithelia. Moreover, cell memory is also essential for generating specific topological distributions.
url http://europepmc.org/articles/PMC3422310?pdf=render
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