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Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces

Embryogenesis is an extraordinarily robust process, exhibiting the ability to control tissue size and repair patterning defects in the face of environmental and genetic perturbations. The size and shape of a developing tissue is a function of the number and size of its constituent cells as well as t...

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Autores principales: Kursawe, Jochen, Brodskiy, Pavel A., Zartman, Jeremiah J., Baker, Ruth E., Fletcher, Alexander G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4703071/
https://www.ncbi.nlm.nih.gov/pubmed/26713738
http://dx.doi.org/10.1371/journal.pcbi.1004679
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author Kursawe, Jochen
Brodskiy, Pavel A.
Zartman, Jeremiah J.
Baker, Ruth E.
Fletcher, Alexander G.
author_facet Kursawe, Jochen
Brodskiy, Pavel A.
Zartman, Jeremiah J.
Baker, Ruth E.
Fletcher, Alexander G.
author_sort Kursawe, Jochen
collection PubMed
description Embryogenesis is an extraordinarily robust process, exhibiting the ability to control tissue size and repair patterning defects in the face of environmental and genetic perturbations. The size and shape of a developing tissue is a function of the number and size of its constituent cells as well as their geometric packing. How these cellular properties are coordinated at the tissue level to ensure developmental robustness remains a mystery; understanding this process requires studying multiple concurrent processes that make up morphogenesis, including the spatial patterning of cell fates and apoptosis, as well as cell intercalations. In this work, we develop a computational model that aims to understand aspects of the robust pattern repair mechanisms of the Drosophila embryonic epidermal tissues. Size control in this system has previously been shown to rely on the regulation of apoptosis rather than proliferation; however, to date little work has been done to understand the role of cellular mechanics in this process. We employ a vertex model of an embryonic segment to test hypotheses about the emergence of this size control. Comparing the model to previously published data across wild type and genetic perturbations, we show that passive mechanical forces suffice to explain the observed size control in the posterior (P) compartment of a segment. However, observed asymmetries in cell death frequencies across the segment are demonstrated to require patterning of cellular properties in the model. Finally, we show that distinct forms of mechanical regulation in the model may be distinguished by differences in cell shapes in the P compartment, as quantified through experimentally accessible summary statistics, as well as by the tissue recoil after laser ablation experiments.
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spelling pubmed-47030712016-01-14 Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces Kursawe, Jochen Brodskiy, Pavel A. Zartman, Jeremiah J. Baker, Ruth E. Fletcher, Alexander G. PLoS Comput Biol Research Article Embryogenesis is an extraordinarily robust process, exhibiting the ability to control tissue size and repair patterning defects in the face of environmental and genetic perturbations. The size and shape of a developing tissue is a function of the number and size of its constituent cells as well as their geometric packing. How these cellular properties are coordinated at the tissue level to ensure developmental robustness remains a mystery; understanding this process requires studying multiple concurrent processes that make up morphogenesis, including the spatial patterning of cell fates and apoptosis, as well as cell intercalations. In this work, we develop a computational model that aims to understand aspects of the robust pattern repair mechanisms of the Drosophila embryonic epidermal tissues. Size control in this system has previously been shown to rely on the regulation of apoptosis rather than proliferation; however, to date little work has been done to understand the role of cellular mechanics in this process. We employ a vertex model of an embryonic segment to test hypotheses about the emergence of this size control. Comparing the model to previously published data across wild type and genetic perturbations, we show that passive mechanical forces suffice to explain the observed size control in the posterior (P) compartment of a segment. However, observed asymmetries in cell death frequencies across the segment are demonstrated to require patterning of cellular properties in the model. Finally, we show that distinct forms of mechanical regulation in the model may be distinguished by differences in cell shapes in the P compartment, as quantified through experimentally accessible summary statistics, as well as by the tissue recoil after laser ablation experiments. Public Library of Science 2015-12-29 /pmc/articles/PMC4703071/ /pubmed/26713738 http://dx.doi.org/10.1371/journal.pcbi.1004679 Text en © 2015 Kursawe 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
Kursawe, Jochen
Brodskiy, Pavel A.
Zartman, Jeremiah J.
Baker, Ruth E.
Fletcher, Alexander G.
Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title_full Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title_fullStr Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title_full_unstemmed Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title_short Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces
title_sort capabilities and limitations of tissue size control through passive mechanical forces
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4703071/
https://www.ncbi.nlm.nih.gov/pubmed/26713738
http://dx.doi.org/10.1371/journal.pcbi.1004679
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