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Segment-Specific Adhesion as a Driver of Convergent Extension

Convergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback...

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Autores principales: Vroomans, Renske M. A., Hogeweg, Paulien, ten Tusscher, Kirsten H. W. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4338282/
https://www.ncbi.nlm.nih.gov/pubmed/25706823
http://dx.doi.org/10.1371/journal.pcbi.1004092
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author Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
author_facet Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
author_sort Vroomans, Renske M. A.
collection PubMed
description Convergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback mechanisms. Computational modelling studies play an important role in unravelling the multiscale feedbacks underlying convergent extension. Convergent extension usually operates in tissue which has been patterned or is currently being patterned into distinct domains of gene expression. How such tissue patterns are maintained during the large scale tissue movements of convergent extension has thus far not been investigated. Intriguingly, experimental data indicate that in certain cases these tissue patterns may drive convergent extension rather than requiring safeguarding against convergent extension. Here we use a 2D Cellular Potts Model (CPM) of a tissue prepatterned into segments, to show that convergent extension tends to disrupt this pre-existing segmental pattern. However, when cells preferentially adhere to cells of the same segment type, segment integrity is maintained without any reduction in tissue extension. Strikingly, we demonstrate that this segment-specific adhesion is by itself sufficient to drive convergent extension. Convergent extension is enhanced when we endow our in silico cells with persistence of motion, which in vivo would naturally follow from cytoskeletal dynamics. Finally, we extend our model to confirm the generality of our results. We demonstrate a similar effect of differential adhesion on convergent extension in tissues that can only extend in a single direction (as often occurs due to the inertia of the head region of the embryo), and in tissues prepatterned into a sequence of domains resulting in two opposing adhesive gradients, rather than alternating segments.
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spelling pubmed-43382822015-03-04 Segment-Specific Adhesion as a Driver of Convergent Extension Vroomans, Renske M. A. Hogeweg, Paulien ten Tusscher, Kirsten H. W. J. PLoS Comput Biol Research Article Convergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback mechanisms. Computational modelling studies play an important role in unravelling the multiscale feedbacks underlying convergent extension. Convergent extension usually operates in tissue which has been patterned or is currently being patterned into distinct domains of gene expression. How such tissue patterns are maintained during the large scale tissue movements of convergent extension has thus far not been investigated. Intriguingly, experimental data indicate that in certain cases these tissue patterns may drive convergent extension rather than requiring safeguarding against convergent extension. Here we use a 2D Cellular Potts Model (CPM) of a tissue prepatterned into segments, to show that convergent extension tends to disrupt this pre-existing segmental pattern. However, when cells preferentially adhere to cells of the same segment type, segment integrity is maintained without any reduction in tissue extension. Strikingly, we demonstrate that this segment-specific adhesion is by itself sufficient to drive convergent extension. Convergent extension is enhanced when we endow our in silico cells with persistence of motion, which in vivo would naturally follow from cytoskeletal dynamics. Finally, we extend our model to confirm the generality of our results. We demonstrate a similar effect of differential adhesion on convergent extension in tissues that can only extend in a single direction (as often occurs due to the inertia of the head region of the embryo), and in tissues prepatterned into a sequence of domains resulting in two opposing adhesive gradients, rather than alternating segments. Public Library of Science 2015-02-23 /pmc/articles/PMC4338282/ /pubmed/25706823 http://dx.doi.org/10.1371/journal.pcbi.1004092 Text en © 2015 Vroomans 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
Segment-Specific Adhesion as a Driver of Convergent Extension
title Segment-Specific Adhesion as a Driver of Convergent Extension
title_full Segment-Specific Adhesion as a Driver of Convergent Extension
title_fullStr Segment-Specific Adhesion as a Driver of Convergent Extension
title_full_unstemmed Segment-Specific Adhesion as a Driver of Convergent Extension
title_short Segment-Specific Adhesion as a Driver of Convergent Extension
title_sort segment-specific adhesion as a driver of convergent extension
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4338282/
https://www.ncbi.nlm.nih.gov/pubmed/25706823
http://dx.doi.org/10.1371/journal.pcbi.1004092
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