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...
Main Authors: | , , , , , , , , , , , |
---|---|
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 |
id |
doaj-b2114752291e43f1b76fb99f4eeae7c9 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT karimazzag thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT yoannchelin thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT francoisrousset thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT emilielegoff thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT camillemartinandmari thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT annemariemartinez thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT bernardmaurin thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT martinedaujatchavanieu thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT nellygodefroy thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT julienaverseng thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT paulmangeat thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT stephenbaghdiguian thenonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT karimazzag nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT yoannchelin nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT francoisrousset nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT emilielegoff nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT camillemartinandmari nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT annemariemartinez nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT bernardmaurin nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT martinedaujatchavanieu nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT nellygodefroy nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT julienaverseng nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT paulmangeat nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia AT stephenbaghdiguian nonproliferativenatureofascidianfolliculogenesisasamodelofhighlyorderedcellulartopologydistinctfromproliferativeepithelia |
_version_ |
1725851059833798656 |