The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.

Previous studies have addressed why and how mono-stratified epithelia adopt a polygonal topology. One major additional, and yet unanswered question is how the frequency of different cell shapes is achieved and whether the same distribution applies between non-proliferative and proliferative epitheli...

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Main Authors: Karim Azzag, Yoann Chelin, François Rousset, Emilie Le Goff, Camille Martinand-Mari, Anne-Marie Martinez, Bernard Maurin, Martine Daujat-Chavanieu, Nelly Godefroy, Julien Averseng, Paul Mangeat, Stephen Baghdiguian
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4441440?pdf=render
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spelling doaj-b2114752291e43f1b76fb99f4eeae7c92020-11-24T21:58:38ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01105e012634110.1371/journal.pone.0126341The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.Karim AzzagYoann ChelinFrançois RoussetEmilie Le GoffCamille Martinand-MariAnne-Marie MartinezBernard MaurinMartine Daujat-ChavanieuNelly GodefroyJulien AversengPaul MangeatStephen BaghdiguianPrevious studies have addressed why and how mono-stratified epithelia adopt a polygonal topology. One major additional, and yet unanswered question is how the frequency of different cell shapes is achieved and whether the same distribution applies between non-proliferative and proliferative epithelia. We compared different proliferative and non-proliferative epithelia from a range of organisms as well as Drosophila melanogaster mutants, deficient for apoptosis or hyperproliferative. We show that the distribution of cell shapes in non-proliferative epithelia (follicular cells of five species of tunicates) is distinctly, and more stringently organized than proliferative ones (cultured epithelial cells and Drosophila melanogaster imaginal discs). The discrepancy is not supported by geometrical constraints (spherical versus flat monolayers), number of cells, or apoptosis events. We have developed a theoretical model of epithelial morphogenesis, based on the physics of divided media, that takes into account biological parameters such as cell-cell contact adhesions and tensions, cell and tissue growth, and which reproduces the effects of proliferation by increasing the topological heterogeneity observed experimentally. We therefore present a model for the morphogenesis of epithelia where, in a proliferative context, an extended distribution of cell shapes (range of 4 to 10 neighbors per cell) contrasts with the narrower range of 5-7 neighbors per cell that characterizes non proliferative epithelia.http://europepmc.org/articles/PMC4441440?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Karim Azzag
Yoann Chelin
François Rousset
Emilie Le Goff
Camille Martinand-Mari
Anne-Marie Martinez
Bernard Maurin
Martine Daujat-Chavanieu
Nelly Godefroy
Julien Averseng
Paul Mangeat
Stephen Baghdiguian
spellingShingle Karim Azzag
Yoann Chelin
François Rousset
Emilie Le Goff
Camille Martinand-Mari
Anne-Marie Martinez
Bernard Maurin
Martine Daujat-Chavanieu
Nelly Godefroy
Julien Averseng
Paul Mangeat
Stephen Baghdiguian
The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
PLoS ONE
author_facet Karim Azzag
Yoann Chelin
François Rousset
Emilie Le Goff
Camille Martinand-Mari
Anne-Marie Martinez
Bernard Maurin
Martine Daujat-Chavanieu
Nelly Godefroy
Julien Averseng
Paul Mangeat
Stephen Baghdiguian
author_sort Karim Azzag
title The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
title_short The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
title_full The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
title_fullStr The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
title_full_unstemmed The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
title_sort non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Previous studies have addressed why and how mono-stratified epithelia adopt a polygonal topology. One major additional, and yet unanswered question is how the frequency of different cell shapes is achieved and whether the same distribution applies between non-proliferative and proliferative epithelia. We compared different proliferative and non-proliferative epithelia from a range of organisms as well as Drosophila melanogaster mutants, deficient for apoptosis or hyperproliferative. We show that the distribution of cell shapes in non-proliferative epithelia (follicular cells of five species of tunicates) is distinctly, and more stringently organized than proliferative ones (cultured epithelial cells and Drosophila melanogaster imaginal discs). The discrepancy is not supported by geometrical constraints (spherical versus flat monolayers), number of cells, or apoptosis events. We have developed a theoretical model of epithelial morphogenesis, based on the physics of divided media, that takes into account biological parameters such as cell-cell contact adhesions and tensions, cell and tissue growth, and which reproduces the effects of proliferation by increasing the topological heterogeneity observed experimentally. We therefore present a model for the morphogenesis of epithelia where, in a proliferative context, an extended distribution of cell shapes (range of 4 to 10 neighbors per cell) contrasts with the narrower range of 5-7 neighbors per cell that characterizes non proliferative epithelia.
url http://europepmc.org/articles/PMC4441440?pdf=render
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