Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.

Geometric and mechanical properties of individual cells and interactions among neighboring cells are the basis of formation of tissue patterns. Understanding the complex interplay of cells is essential for gaining insight into embryogenesis, tissue development, and other emerging behavior. Here we d...

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Main Authors: Sëma Kachalo, Hammad Naveed, Youfang Cao, Jieling Zhao, Jie Liang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4431879?pdf=render
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spelling doaj-a75bfed0ba414dc18a12bc9546e73cec2020-11-24T21:35:49ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01105e012648410.1371/journal.pone.0126484Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.Sëma KachaloHammad NaveedYoufang CaoJieling ZhaoJie LiangGeometric and mechanical properties of individual cells and interactions among neighboring cells are the basis of formation of tissue patterns. Understanding the complex interplay of cells is essential for gaining insight into embryogenesis, tissue development, and other emerging behavior. Here we describe a cell model and an efficient geometric algorithm for studying the dynamic process of tissue formation in 2D (e.g. epithelial tissues). Our approach improves upon previous methods by incorporating properties of individual cells as well as detailed description of the dynamic growth process, with all topological changes accounted for. Cell size, shape, and division plane orientation are modeled realistically. In addition, cell birth, cell growth, cell shrinkage, cell death, cell division, cell collision, and cell rearrangements are now fully accounted for. Different models of cell-cell interactions, such as lateral inhibition during the process of growth, can be studied in detail. Cellular pattern formation for monolayered tissues from arbitrary initial conditions, including that of a single cell, can also be studied in detail. Computational efficiency is achieved through the employment of a special data structure that ensures access to neighboring cells in constant time, without additional space requirement. We have successfully generated tissues consisting of more than 20,000 cells starting from 2 cells within 1 hour. We show that our model can be used to study embryogenesis, tissue fusion, and cell apoptosis. We give detailed study of the classical developmental process of bristle formation on the epidermis of D. melanogaster and the fundamental problem of homeostatic size control in epithelial tissues. Simulation results reveal significant roles of solubility of secreted factors in both the bristle formation and the homeostatic control of tissue size. Our method can be used to study broad problems in monolayered tissue formation. Our software is publicly available.http://europepmc.org/articles/PMC4431879?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sëma Kachalo
Hammad Naveed
Youfang Cao
Jieling Zhao
Jie Liang
spellingShingle Sëma Kachalo
Hammad Naveed
Youfang Cao
Jieling Zhao
Jie Liang
Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
PLoS ONE
author_facet Sëma Kachalo
Hammad Naveed
Youfang Cao
Jieling Zhao
Jie Liang
author_sort Sëma Kachalo
title Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
title_short Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
title_full Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
title_fullStr Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
title_full_unstemmed Mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
title_sort mechanical model of geometric cell and topological algorithm for cell dynamics from single-cell to formation of monolayered tissues with pattern.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Geometric and mechanical properties of individual cells and interactions among neighboring cells are the basis of formation of tissue patterns. Understanding the complex interplay of cells is essential for gaining insight into embryogenesis, tissue development, and other emerging behavior. Here we describe a cell model and an efficient geometric algorithm for studying the dynamic process of tissue formation in 2D (e.g. epithelial tissues). Our approach improves upon previous methods by incorporating properties of individual cells as well as detailed description of the dynamic growth process, with all topological changes accounted for. Cell size, shape, and division plane orientation are modeled realistically. In addition, cell birth, cell growth, cell shrinkage, cell death, cell division, cell collision, and cell rearrangements are now fully accounted for. Different models of cell-cell interactions, such as lateral inhibition during the process of growth, can be studied in detail. Cellular pattern formation for monolayered tissues from arbitrary initial conditions, including that of a single cell, can also be studied in detail. Computational efficiency is achieved through the employment of a special data structure that ensures access to neighboring cells in constant time, without additional space requirement. We have successfully generated tissues consisting of more than 20,000 cells starting from 2 cells within 1 hour. We show that our model can be used to study embryogenesis, tissue fusion, and cell apoptosis. We give detailed study of the classical developmental process of bristle formation on the epidermis of D. melanogaster and the fundamental problem of homeostatic size control in epithelial tissues. Simulation results reveal significant roles of solubility of secreted factors in both the bristle formation and the homeostatic control of tissue size. Our method can be used to study broad problems in monolayered tissue formation. Our software is publicly available.
url http://europepmc.org/articles/PMC4431879?pdf=render
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