TY - JOUR
T1 - The non-proliferative nature of ascidian folliculogenesis as a model of highly ordered cellular topology distinct from proliferative epithelia
AU - Azzag, Karim
AU - Chelin, Yoann
AU - Rousset, François
AU - Le Goff, Emilie
AU - Martinand-Mari, Camille
AU - Martinez, Anne Marie
AU - Maurin, Bernard
AU - Daujat-Chavanieu, Martine
AU - Godefroy, Nelly
AU - Averseng, Julien
AU - Mangeat, Paul
AU - Baghdiguian, Stephen
N1 - Publisher Copyright:
© 2015 Azzag et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2015/5/22
Y1 - 2015/5/22
N2 - 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.
AB - 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.
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U2 - 10.1371/journal.pone.0126341
DO - 10.1371/journal.pone.0126341
M3 - Article
C2 - 26000769
AN - SCOPUS:84930625455
SN - 1932-6203
VL - 10
JO - PLoS One
JF - PLoS One
IS - 5
M1 - e0126341
ER -