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A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development

Patterning and growth are linked during early development and have to be tightly controlled to result in a functional tissue or organ. During the development of the Drosophila eye, this linkage is particularly clear: the growth of the eye primordium mainly results from proliferating cells ahead of t...

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Autores principales: Fried, Patrick, Sánchez-Aragón, Máximo, Aguilar-Hidalgo, Daniel, Lehtinen, Birgitta, Casares, Fernando, Iber, Dagmar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5023109/
https://www.ncbi.nlm.nih.gov/pubmed/27626238
http://dx.doi.org/10.1371/journal.pcbi.1005052
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author Fried, Patrick
Sánchez-Aragón, Máximo
Aguilar-Hidalgo, Daniel
Lehtinen, Birgitta
Casares, Fernando
Iber, Dagmar
author_facet Fried, Patrick
Sánchez-Aragón, Máximo
Aguilar-Hidalgo, Daniel
Lehtinen, Birgitta
Casares, Fernando
Iber, Dagmar
author_sort Fried, Patrick
collection PubMed
description Patterning and growth are linked during early development and have to be tightly controlled to result in a functional tissue or organ. During the development of the Drosophila eye, this linkage is particularly clear: the growth of the eye primordium mainly results from proliferating cells ahead of the morphogenetic furrow (MF), a moving signaling wave that sweeps across the tissue from the posterior to the anterior side, that induces proliferating cells anterior to it to differentiate and become cell cycle quiescent in its wake. Therefore, final eye disc size depends on the proliferation rate of undifferentiated cells and on the speed with which the MF sweeps across the eye disc. We developed a spatio-temporal model of the growing eye disc based on the regulatory interactions controlled by the signals Decapentaplegic (Dpp), Hedgehog (Hh) and the transcription factor Homothorax (Hth) and explored how the signaling patterns affect the movement of the MF and impact on eye disc growth. We used published and new quantitative data to parameterize the model. In particular, two crucial parameter values, the degradation rate of Hth and the diffusion coefficient of Hh, were measured. The model is able to reproduce the linear movement of the MF and the termination of growth of the primordium. We further show that the model can explain several mutant phenotypes, but fails to reproduce the previously observed scaling of the Dpp gradient in the anterior compartment.
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spelling pubmed-50231092016-09-27 A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development Fried, Patrick Sánchez-Aragón, Máximo Aguilar-Hidalgo, Daniel Lehtinen, Birgitta Casares, Fernando Iber, Dagmar PLoS Comput Biol Research Article Patterning and growth are linked during early development and have to be tightly controlled to result in a functional tissue or organ. During the development of the Drosophila eye, this linkage is particularly clear: the growth of the eye primordium mainly results from proliferating cells ahead of the morphogenetic furrow (MF), a moving signaling wave that sweeps across the tissue from the posterior to the anterior side, that induces proliferating cells anterior to it to differentiate and become cell cycle quiescent in its wake. Therefore, final eye disc size depends on the proliferation rate of undifferentiated cells and on the speed with which the MF sweeps across the eye disc. We developed a spatio-temporal model of the growing eye disc based on the regulatory interactions controlled by the signals Decapentaplegic (Dpp), Hedgehog (Hh) and the transcription factor Homothorax (Hth) and explored how the signaling patterns affect the movement of the MF and impact on eye disc growth. We used published and new quantitative data to parameterize the model. In particular, two crucial parameter values, the degradation rate of Hth and the diffusion coefficient of Hh, were measured. The model is able to reproduce the linear movement of the MF and the termination of growth of the primordium. We further show that the model can explain several mutant phenotypes, but fails to reproduce the previously observed scaling of the Dpp gradient in the anterior compartment. Public Library of Science 2016-09-14 /pmc/articles/PMC5023109/ /pubmed/27626238 http://dx.doi.org/10.1371/journal.pcbi.1005052 Text en © 2016 Fried et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fried, Patrick
Sánchez-Aragón, Máximo
Aguilar-Hidalgo, Daniel
Lehtinen, Birgitta
Casares, Fernando
Iber, Dagmar
A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title_full A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title_fullStr A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title_full_unstemmed A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title_short A Model of the Spatio-temporal Dynamics of Drosophila Eye Disc Development
title_sort model of the spatio-temporal dynamics of drosophila eye disc development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5023109/
https://www.ncbi.nlm.nih.gov/pubmed/27626238
http://dx.doi.org/10.1371/journal.pcbi.1005052
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