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Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study
From gastrulation to late organogenesis animal development involves many genetic and bio-mechanical interactions between epithelial and mesenchymal tissues. Ectodermal organs, such as hairs, feathers and teeth are well studied examples of organs whose development is based on epithelial-mesenchymal i...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5843354/ https://www.ncbi.nlm.nih.gov/pubmed/29481561 http://dx.doi.org/10.1371/journal.pcbi.1005981 |
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author | Marin-Riera, Miquel Moustakas-Verho, Jacqueline Savriama, Yoland Jernvall, Jukka Salazar-Ciudad, Isaac |
author_facet | Marin-Riera, Miquel Moustakas-Verho, Jacqueline Savriama, Yoland Jernvall, Jukka Salazar-Ciudad, Isaac |
author_sort | Marin-Riera, Miquel |
collection | PubMed |
description | From gastrulation to late organogenesis animal development involves many genetic and bio-mechanical interactions between epithelial and mesenchymal tissues. Ectodermal organs, such as hairs, feathers and teeth are well studied examples of organs whose development is based on epithelial-mesenchymal interactions. These develop from a similar primordium through an epithelial folding and its interaction with the mesenchyme. Despite extensive knowledge on the molecular pathways involved, little is known about the role of bio-mechanical processes in the morphogenesis of these organs. We propose a simple computational model for the biomechanics of one such organ, the tooth, and contrast its predictions against cell-tracking experiments, mechanical relaxation experiments and the observed tooth shape changes over developmental time. We found that two biomechanical processes, differential tissue growth and differential cell adhesion, were enough, in the model, for the development of the 3D morphology of the early tooth germ. This was largely determined by the length and direction of growth of the cervical loops, lateral folds of the enamel epithelium. The formation of these cervical loops was found to require accelerated epithelial growth relative to other tissues and their direction of growth depended on specific differential adhesion between the three tooth tissues. These two processes and geometrical constraints in early tooth bud also explained the shape asymmetry between the lateral cervical loops and those forming in the anterior and posterior of the tooth. By performing mechanical perturbations ex vivo and in silico we inferred the distribution and direction of tensile stresses in the mesenchyme that restricted cervical loop lateral growth and forced them to grow downwards. Overall our study suggests detailed quantitative explanations for how bio-mechanical processes lead to specific morphological 3D changes over developmental time. |
format | Online Article Text |
id | pubmed-5843354 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-58433542018-03-23 Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study Marin-Riera, Miquel Moustakas-Verho, Jacqueline Savriama, Yoland Jernvall, Jukka Salazar-Ciudad, Isaac PLoS Comput Biol Research Article From gastrulation to late organogenesis animal development involves many genetic and bio-mechanical interactions between epithelial and mesenchymal tissues. Ectodermal organs, such as hairs, feathers and teeth are well studied examples of organs whose development is based on epithelial-mesenchymal interactions. These develop from a similar primordium through an epithelial folding and its interaction with the mesenchyme. Despite extensive knowledge on the molecular pathways involved, little is known about the role of bio-mechanical processes in the morphogenesis of these organs. We propose a simple computational model for the biomechanics of one such organ, the tooth, and contrast its predictions against cell-tracking experiments, mechanical relaxation experiments and the observed tooth shape changes over developmental time. We found that two biomechanical processes, differential tissue growth and differential cell adhesion, were enough, in the model, for the development of the 3D morphology of the early tooth germ. This was largely determined by the length and direction of growth of the cervical loops, lateral folds of the enamel epithelium. The formation of these cervical loops was found to require accelerated epithelial growth relative to other tissues and their direction of growth depended on specific differential adhesion between the three tooth tissues. These two processes and geometrical constraints in early tooth bud also explained the shape asymmetry between the lateral cervical loops and those forming in the anterior and posterior of the tooth. By performing mechanical perturbations ex vivo and in silico we inferred the distribution and direction of tensile stresses in the mesenchyme that restricted cervical loop lateral growth and forced them to grow downwards. Overall our study suggests detailed quantitative explanations for how bio-mechanical processes lead to specific morphological 3D changes over developmental time. Public Library of Science 2018-02-26 /pmc/articles/PMC5843354/ /pubmed/29481561 http://dx.doi.org/10.1371/journal.pcbi.1005981 Text en © 2018 Marin-Riera 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 Marin-Riera, Miquel Moustakas-Verho, Jacqueline Savriama, Yoland Jernvall, Jukka Salazar-Ciudad, Isaac Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title | Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title_full | Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title_fullStr | Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title_full_unstemmed | Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title_short | Differential tissue growth and cell adhesion alone drive early tooth morphogenesis: An ex vivo and in silico study |
title_sort | differential tissue growth and cell adhesion alone drive early tooth morphogenesis: an ex vivo and in silico study |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5843354/ https://www.ncbi.nlm.nih.gov/pubmed/29481561 http://dx.doi.org/10.1371/journal.pcbi.1005981 |
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