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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Main Authors: Jochen Kursawe, Pavel A Brodskiy, Jeremiah J Zartman, Ruth E Baker, Alexander G Fletcher
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-12-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1004679
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spelling doaj-01ae5eef01db4482a9e0ddf43154a4412021-04-21T14:58:49ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-12-011112e100467910.1371/journal.pcbi.1004679Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces.Jochen KursawePavel A BrodskiyJeremiah J ZartmanRuth E BakerAlexander G FletcherEmbryogenesis 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.https://doi.org/10.1371/journal.pcbi.1004679
collection DOAJ
language English
format Article
sources DOAJ
author Jochen Kursawe
Pavel A Brodskiy
Jeremiah J Zartman
Ruth E Baker
Alexander G Fletcher
spellingShingle Jochen Kursawe
Pavel A Brodskiy
Jeremiah J Zartman
Ruth E Baker
Alexander G Fletcher
Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces.
PLoS Computational Biology
author_facet Jochen Kursawe
Pavel A Brodskiy
Jeremiah J Zartman
Ruth E Baker
Alexander G Fletcher
author_sort Jochen Kursawe
title 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_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_sort capabilities and limitations of tissue size control through passive mechanical forces.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2015-12-01
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.
url https://doi.org/10.1371/journal.pcbi.1004679
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