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Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems

Coordination of cell behaviour is key to a myriad of biological processes including tissue morphogenesis, wound healing, and tumour growth. As such, individual-based computational models, which explicitly describe inter-cellular interactions, are commonly used to model collective cell dynamics. Howe...

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Autores principales: Germano, Domenic P. J., Zanca, Adriana, Johnston, Stuart T., Flegg, Jennifer A., Osborne, James M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10560655/
https://www.ncbi.nlm.nih.gov/pubmed/37805982
http://dx.doi.org/10.1007/s11538-023-01214-8
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author Germano, Domenic P. J.
Zanca, Adriana
Johnston, Stuart T.
Flegg, Jennifer A.
Osborne, James M.
author_facet Germano, Domenic P. J.
Zanca, Adriana
Johnston, Stuart T.
Flegg, Jennifer A.
Osborne, James M.
author_sort Germano, Domenic P. J.
collection PubMed
description Coordination of cell behaviour is key to a myriad of biological processes including tissue morphogenesis, wound healing, and tumour growth. As such, individual-based computational models, which explicitly describe inter-cellular interactions, are commonly used to model collective cell dynamics. However, when using individual-based models, it is unclear how descriptions of cell boundaries affect overall population dynamics. In order to investigate this we define three cell boundary descriptions of varying complexities for each of three widely used off-lattice individual-based models: overlapping spheres, Voronoi tessellation, and vertex models. We apply our models to multiple biological scenarios to investigate how cell boundary description can influence tissue-scale behaviour. We find that the Voronoi tessellation model is most sensitive to changes in the cell boundary description with basic models being inappropriate in many cases. The timescale of tissue evolution when using an overlapping spheres model is coupled to the boundary description. The vertex model is demonstrated to be the most stable to changes in boundary description, though still exhibits timescale sensitivity. When using individual-based computational models one should carefully consider how cell boundaries are defined. To inform future work, we provide an exploration of common individual-based models and cell boundary descriptions in frequently studied biological scenarios and discuss their benefits and disadvantages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11538-023-01214-8.
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spelling pubmed-105606552023-10-10 Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems Germano, Domenic P. J. Zanca, Adriana Johnston, Stuart T. Flegg, Jennifer A. Osborne, James M. Bull Math Biol Original Article Coordination of cell behaviour is key to a myriad of biological processes including tissue morphogenesis, wound healing, and tumour growth. As such, individual-based computational models, which explicitly describe inter-cellular interactions, are commonly used to model collective cell dynamics. However, when using individual-based models, it is unclear how descriptions of cell boundaries affect overall population dynamics. In order to investigate this we define three cell boundary descriptions of varying complexities for each of three widely used off-lattice individual-based models: overlapping spheres, Voronoi tessellation, and vertex models. We apply our models to multiple biological scenarios to investigate how cell boundary description can influence tissue-scale behaviour. We find that the Voronoi tessellation model is most sensitive to changes in the cell boundary description with basic models being inappropriate in many cases. The timescale of tissue evolution when using an overlapping spheres model is coupled to the boundary description. The vertex model is demonstrated to be the most stable to changes in boundary description, though still exhibits timescale sensitivity. When using individual-based computational models one should carefully consider how cell boundaries are defined. To inform future work, we provide an exploration of common individual-based models and cell boundary descriptions in frequently studied biological scenarios and discuss their benefits and disadvantages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11538-023-01214-8. Springer US 2023-10-08 2023 /pmc/articles/PMC10560655/ /pubmed/37805982 http://dx.doi.org/10.1007/s11538-023-01214-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Germano, Domenic P. J.
Zanca, Adriana
Johnston, Stuart T.
Flegg, Jennifer A.
Osborne, James M.
Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title_full Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title_fullStr Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title_full_unstemmed Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title_short Free and Interfacial Boundaries in Individual-Based Models of Multicellular Biological systems
title_sort free and interfacial boundaries in individual-based models of multicellular biological systems
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10560655/
https://www.ncbi.nlm.nih.gov/pubmed/37805982
http://dx.doi.org/10.1007/s11538-023-01214-8
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