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Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation

Remodeling of multicellular architecture is a critical developmental process for shaping the axis of a bilaterally symmetric animal body and involves coordinated cell–cell interactions and cell rearrangement. In arthropods, the early embryonic process that leads to the segmented body axis varies at...

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Autores principales: Fujiwara, Motohiro, Akiyama-Oda, Yasuko, Oda, Hiroki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411422/
https://www.ncbi.nlm.nih.gov/pubmed/36036016
http://dx.doi.org/10.3389/fcell.2022.932814
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author Fujiwara, Motohiro
Akiyama-Oda, Yasuko
Oda, Hiroki
author_facet Fujiwara, Motohiro
Akiyama-Oda, Yasuko
Oda, Hiroki
author_sort Fujiwara, Motohiro
collection PubMed
description Remodeling of multicellular architecture is a critical developmental process for shaping the axis of a bilaterally symmetric animal body and involves coordinated cell–cell interactions and cell rearrangement. In arthropods, the early embryonic process that leads to the segmented body axis varies at the cellular and molecular levels depending on the species. Developmental studies using insect and spider model species have provided specific examples of these diversified mechanisms that regulate axis formation and segmentation in arthropod embryos. However, there are few theoretical models for how diversity in the early embryonic process occurred during evolution, in part because of a limited computational infrastructure. We developed a virtual spherical-shaped multicellular platform to reproduce body axis-forming processes. Each virtual cell behaves according to the cell vertex model, with the computational program organized in a hierarchical order from cells and tissues to whole embryos. Using an initial set of two different mechanical states for cell differentiation and global directional signals that are linked to the planar polarity of each cell, the virtual cell assembly exhibited morphogenetic processes similar to those observed in spider embryos. We found that the development of an elongating body axis is achieved through implementation of an interactive cell polarity parameter associated with edge tension at the cell–cell adhesion interface, with no local control of the cell division rate and direction. We also showed that modifying the settings can cause variation in morphogenetic processes. This platform also can embed a gene network that generates waves of gene expression in a virtual dynamic multicellular field. This study provides a computational platform for testing the development and evolution of animal body patterns.
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spelling pubmed-94114222022-08-27 Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation Fujiwara, Motohiro Akiyama-Oda, Yasuko Oda, Hiroki Front Cell Dev Biol Cell and Developmental Biology Remodeling of multicellular architecture is a critical developmental process for shaping the axis of a bilaterally symmetric animal body and involves coordinated cell–cell interactions and cell rearrangement. In arthropods, the early embryonic process that leads to the segmented body axis varies at the cellular and molecular levels depending on the species. Developmental studies using insect and spider model species have provided specific examples of these diversified mechanisms that regulate axis formation and segmentation in arthropod embryos. However, there are few theoretical models for how diversity in the early embryonic process occurred during evolution, in part because of a limited computational infrastructure. We developed a virtual spherical-shaped multicellular platform to reproduce body axis-forming processes. Each virtual cell behaves according to the cell vertex model, with the computational program organized in a hierarchical order from cells and tissues to whole embryos. Using an initial set of two different mechanical states for cell differentiation and global directional signals that are linked to the planar polarity of each cell, the virtual cell assembly exhibited morphogenetic processes similar to those observed in spider embryos. We found that the development of an elongating body axis is achieved through implementation of an interactive cell polarity parameter associated with edge tension at the cell–cell adhesion interface, with no local control of the cell division rate and direction. We also showed that modifying the settings can cause variation in morphogenetic processes. This platform also can embed a gene network that generates waves of gene expression in a virtual dynamic multicellular field. This study provides a computational platform for testing the development and evolution of animal body patterns. Frontiers Media S.A. 2022-08-12 /pmc/articles/PMC9411422/ /pubmed/36036016 http://dx.doi.org/10.3389/fcell.2022.932814 Text en Copyright © 2022 Fujiwara, Akiyama-Oda and Oda. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Fujiwara, Motohiro
Akiyama-Oda, Yasuko
Oda, Hiroki
Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title_full Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title_fullStr Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title_full_unstemmed Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title_short Virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
title_sort virtual spherical-shaped multicellular platform for simulating the morphogenetic processes of spider-like body axis formation
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411422/
https://www.ncbi.nlm.nih.gov/pubmed/36036016
http://dx.doi.org/10.3389/fcell.2022.932814
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