A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms

Abstract Collective migration is commonly observed in groups of migrating cells, in the form of swarms or aggregates. Mechanistic models have proven very useful in understanding collective cell migration. Such models, either explicitly consider the forces involved in the interaction and movement of...

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Main Authors: Arnab Barua, Josue M. Nava-Sedeño, Michael Meyer-Hermann, Haralampos Hatzikirou
Format: Article
Language:English
Published: Nature Publishing Group 2020-12-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-79119-y
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spelling doaj-f5f2cb54edcf44459797384d4bb068d92020-12-27T12:17:53ZengNature Publishing GroupScientific Reports2045-23222020-12-0110111310.1038/s41598-020-79119-yA least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanismsArnab Barua0Josue M. Nava-Sedeño1Michael Meyer-Hermann2Haralampos Hatzikirou3Department of Systems Immunology and Braunschweig Integrated Centre of Systems Biology, Helmholtz Centre for Infection ResearchCenter for Information Services and High Performance Computing, Technische Univesität DresdenDepartment of Systems Immunology and Braunschweig Integrated Centre of Systems Biology, Helmholtz Centre for Infection ResearchDepartment of Systems Immunology and Braunschweig Integrated Centre of Systems Biology, Helmholtz Centre for Infection ResearchAbstract Collective migration is commonly observed in groups of migrating cells, in the form of swarms or aggregates. Mechanistic models have proven very useful in understanding collective cell migration. Such models, either explicitly consider the forces involved in the interaction and movement of individuals or phenomenologically define rules which mimic the observed behavior of cells. However, mechanisms leading to collective migration are varied and specific to the type of cells involved. Additionally, the precise and complete dynamics of many important chemomechanical factors influencing cell movement, from signalling pathways to substrate sensing, are typically either too complex or largely unknown. The question is how to make quantitative/qualitative predictions of collective behavior without exact mechanistic knowledge. Here we propose the least microenvironmental uncertainty principle (LEUP) that may serve as a generative model of collective migration without precise incorporation of full mechanistic details. Using statistical physics tools, we show that the famous Vicsek model is a special case of LEUP. Finally, to test the biological applicability of our theory, we apply LEUP to construct a model of the collective behavior of spherical Serratia marcescens bacteria, where the underlying migration mechanisms remain elusive.https://doi.org/10.1038/s41598-020-79119-y
collection DOAJ
language English
format Article
sources DOAJ
author Arnab Barua
Josue M. Nava-Sedeño
Michael Meyer-Hermann
Haralampos Hatzikirou
spellingShingle Arnab Barua
Josue M. Nava-Sedeño
Michael Meyer-Hermann
Haralampos Hatzikirou
A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
Scientific Reports
author_facet Arnab Barua
Josue M. Nava-Sedeño
Michael Meyer-Hermann
Haralampos Hatzikirou
author_sort Arnab Barua
title A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
title_short A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
title_full A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
title_fullStr A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
title_full_unstemmed A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms
title_sort least microenvironmental uncertainty principle (leup) as a generative model of collective cell migration mechanisms
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2020-12-01
description Abstract Collective migration is commonly observed in groups of migrating cells, in the form of swarms or aggregates. Mechanistic models have proven very useful in understanding collective cell migration. Such models, either explicitly consider the forces involved in the interaction and movement of individuals or phenomenologically define rules which mimic the observed behavior of cells. However, mechanisms leading to collective migration are varied and specific to the type of cells involved. Additionally, the precise and complete dynamics of many important chemomechanical factors influencing cell movement, from signalling pathways to substrate sensing, are typically either too complex or largely unknown. The question is how to make quantitative/qualitative predictions of collective behavior without exact mechanistic knowledge. Here we propose the least microenvironmental uncertainty principle (LEUP) that may serve as a generative model of collective migration without precise incorporation of full mechanistic details. Using statistical physics tools, we show that the famous Vicsek model is a special case of LEUP. Finally, to test the biological applicability of our theory, we apply LEUP to construct a model of the collective behavior of spherical Serratia marcescens bacteria, where the underlying migration mechanisms remain elusive.
url https://doi.org/10.1038/s41598-020-79119-y
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