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Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics

Lymphocytes have been described to perform different motility patterns such as Brownian random walks, persistent random walks, and Lévy walks. Depending on the conditions, such as confinement or the distribution of target cells, either Brownian or Lévy walks lead to more efficient interaction with t...

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Autores principales: van Steijn, Leonie, Wortel, Inge M. N., Sire, Clément, Dupré, Loïc, Theraulaz, Guy, Merks, Roeland M. H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8880896/
https://www.ncbi.nlm.nih.gov/pubmed/35157694
http://dx.doi.org/10.1371/journal.pcbi.1009156
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author van Steijn, Leonie
Wortel, Inge M. N.
Sire, Clément
Dupré, Loïc
Theraulaz, Guy
Merks, Roeland M. H.
author_facet van Steijn, Leonie
Wortel, Inge M. N.
Sire, Clément
Dupré, Loïc
Theraulaz, Guy
Merks, Roeland M. H.
author_sort van Steijn, Leonie
collection PubMed
description Lymphocytes have been described to perform different motility patterns such as Brownian random walks, persistent random walks, and Lévy walks. Depending on the conditions, such as confinement or the distribution of target cells, either Brownian or Lévy walks lead to more efficient interaction with the targets. The diversity of these motility patterns may be explained by an adaptive response to the surrounding extracellular matrix (ECM). Indeed, depending on the ECM composition, lymphocytes either display a floating motility without attaching to the ECM, or sliding and stepping motility with respectively continuous or discontinuous attachment to the ECM, or pivoting behaviour with sustained attachment to the ECM. Moreover, on the long term, lymphocytes either perform a persistent random walk or a Brownian-like movement depending on the ECM composition. How the ECM affects cell motility is still incompletely understood. Here, we integrate essential mechanistic details of the lymphocyte-matrix adhesions and lymphocyte intrinsic cytoskeletal induced cell propulsion into a Cellular Potts model (CPM). We show that the combination of de novo cell-matrix adhesion formation, adhesion growth and shrinkage, adhesion rupture, and feedback of adhesions onto cell propulsion recapitulates multiple lymphocyte behaviours, for different lymphocyte subsets and various substrates. With an increasing attachment area and increased adhesion strength, the cells’ speed and persistence decreases. Additionally, the model predicts random walks with short-term persistent but long-term subdiffusive properties resulting in a pivoting type of motility. For small adhesion areas, the spatial distribution of adhesions emerges as a key factor influencing cell motility. Small adhesions at the front allow for more persistent motility than larger clusters at the back, despite a similar total adhesion area. In conclusion, we present an integrated framework to simulate the effects of ECM proteins on cell-matrix adhesion dynamics. The model reveals a sufficient set of principles explaining the plasticity of lymphocyte motility.
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spelling pubmed-88808962022-02-26 Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics van Steijn, Leonie Wortel, Inge M. N. Sire, Clément Dupré, Loïc Theraulaz, Guy Merks, Roeland M. H. PLoS Comput Biol Research Article Lymphocytes have been described to perform different motility patterns such as Brownian random walks, persistent random walks, and Lévy walks. Depending on the conditions, such as confinement or the distribution of target cells, either Brownian or Lévy walks lead to more efficient interaction with the targets. The diversity of these motility patterns may be explained by an adaptive response to the surrounding extracellular matrix (ECM). Indeed, depending on the ECM composition, lymphocytes either display a floating motility without attaching to the ECM, or sliding and stepping motility with respectively continuous or discontinuous attachment to the ECM, or pivoting behaviour with sustained attachment to the ECM. Moreover, on the long term, lymphocytes either perform a persistent random walk or a Brownian-like movement depending on the ECM composition. How the ECM affects cell motility is still incompletely understood. Here, we integrate essential mechanistic details of the lymphocyte-matrix adhesions and lymphocyte intrinsic cytoskeletal induced cell propulsion into a Cellular Potts model (CPM). We show that the combination of de novo cell-matrix adhesion formation, adhesion growth and shrinkage, adhesion rupture, and feedback of adhesions onto cell propulsion recapitulates multiple lymphocyte behaviours, for different lymphocyte subsets and various substrates. With an increasing attachment area and increased adhesion strength, the cells’ speed and persistence decreases. Additionally, the model predicts random walks with short-term persistent but long-term subdiffusive properties resulting in a pivoting type of motility. For small adhesion areas, the spatial distribution of adhesions emerges as a key factor influencing cell motility. Small adhesions at the front allow for more persistent motility than larger clusters at the back, despite a similar total adhesion area. In conclusion, we present an integrated framework to simulate the effects of ECM proteins on cell-matrix adhesion dynamics. The model reveals a sufficient set of principles explaining the plasticity of lymphocyte motility. Public Library of Science 2022-02-14 /pmc/articles/PMC8880896/ /pubmed/35157694 http://dx.doi.org/10.1371/journal.pcbi.1009156 Text en © 2022 van Steijn et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
van Steijn, Leonie
Wortel, Inge M. N.
Sire, Clément
Dupré, Loïc
Theraulaz, Guy
Merks, Roeland M. H.
Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title_full Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title_fullStr Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title_full_unstemmed Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title_short Computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
title_sort computational modelling of cell motility modes emerging from cell-matrix adhesion dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8880896/
https://www.ncbi.nlm.nih.gov/pubmed/35157694
http://dx.doi.org/10.1371/journal.pcbi.1009156
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