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Interpreting T-cell search “strategies” in the light of evolution under constraints

Two decades of in vivo imaging have revealed how diverse T-cell motion patterns can be. Such recordings have sparked the notion of search “strategies”: T cells may have evolved ways to search for antigen efficiently depending on the task at hand. Mathematical models have indeed confirmed that severa...

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Autores principales: Wortel, Inge M. N., Textor, Johannes
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9997883/
https://www.ncbi.nlm.nih.gov/pubmed/36848395
http://dx.doi.org/10.1371/journal.pcbi.1010918
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author Wortel, Inge M. N.
Textor, Johannes
author_facet Wortel, Inge M. N.
Textor, Johannes
author_sort Wortel, Inge M. N.
collection PubMed
description Two decades of in vivo imaging have revealed how diverse T-cell motion patterns can be. Such recordings have sparked the notion of search “strategies”: T cells may have evolved ways to search for antigen efficiently depending on the task at hand. Mathematical models have indeed confirmed that several observed T-cell migration patterns resemble a theoretical optimum; for example, frequent turning, stop-and-go motion, or alternating short and long motile runs have all been interpreted as deliberately tuned behaviours, optimising the cell’s chance of finding antigen. But the same behaviours could also arise simply because T cells cannot follow a straight, regular path through the tight spaces they navigate. Even if T cells do follow a theoretically optimal pattern, the question remains: which parts of that pattern have truly been evolved for search, and which merely reflect constraints from the cell’s migration machinery and surroundings? We here employ an approach from the field of evolutionary biology to examine how cells might evolve search strategies under realistic constraints. Using a cellular Potts model (CPM), where motion arises from intracellular dynamics interacting with cell shape and a constraining environment, we simulate evolutionary optimization of a simple task: explore as much area as possible. We find that our simulated cells indeed evolve their motility patterns. But the evolved behaviors are not shaped solely by what is functionally optimal; importantly, they also reflect mechanistic constraints. Cells in our model evolve several motility characteristics previously attributed to search optimisation—even though these features are not beneficial for the task given here. Our results stress that search patterns may evolve for other reasons than being “optimal”. In part, they may be the inevitable side effects of interactions between cell shape, intracellular dynamics, and the diverse environments T cells face in vivo.
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spelling pubmed-99978832023-03-10 Interpreting T-cell search “strategies” in the light of evolution under constraints Wortel, Inge M. N. Textor, Johannes PLoS Comput Biol Research Article Two decades of in vivo imaging have revealed how diverse T-cell motion patterns can be. Such recordings have sparked the notion of search “strategies”: T cells may have evolved ways to search for antigen efficiently depending on the task at hand. Mathematical models have indeed confirmed that several observed T-cell migration patterns resemble a theoretical optimum; for example, frequent turning, stop-and-go motion, or alternating short and long motile runs have all been interpreted as deliberately tuned behaviours, optimising the cell’s chance of finding antigen. But the same behaviours could also arise simply because T cells cannot follow a straight, regular path through the tight spaces they navigate. Even if T cells do follow a theoretically optimal pattern, the question remains: which parts of that pattern have truly been evolved for search, and which merely reflect constraints from the cell’s migration machinery and surroundings? We here employ an approach from the field of evolutionary biology to examine how cells might evolve search strategies under realistic constraints. Using a cellular Potts model (CPM), where motion arises from intracellular dynamics interacting with cell shape and a constraining environment, we simulate evolutionary optimization of a simple task: explore as much area as possible. We find that our simulated cells indeed evolve their motility patterns. But the evolved behaviors are not shaped solely by what is functionally optimal; importantly, they also reflect mechanistic constraints. Cells in our model evolve several motility characteristics previously attributed to search optimisation—even though these features are not beneficial for the task given here. Our results stress that search patterns may evolve for other reasons than being “optimal”. In part, they may be the inevitable side effects of interactions between cell shape, intracellular dynamics, and the diverse environments T cells face in vivo. Public Library of Science 2023-02-27 /pmc/articles/PMC9997883/ /pubmed/36848395 http://dx.doi.org/10.1371/journal.pcbi.1010918 Text en © 2023 Wortel, Textor 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
Wortel, Inge M. N.
Textor, Johannes
Interpreting T-cell search “strategies” in the light of evolution under constraints
title Interpreting T-cell search “strategies” in the light of evolution under constraints
title_full Interpreting T-cell search “strategies” in the light of evolution under constraints
title_fullStr Interpreting T-cell search “strategies” in the light of evolution under constraints
title_full_unstemmed Interpreting T-cell search “strategies” in the light of evolution under constraints
title_short Interpreting T-cell search “strategies” in the light of evolution under constraints
title_sort interpreting t-cell search “strategies” in the light of evolution under constraints
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9997883/
https://www.ncbi.nlm.nih.gov/pubmed/36848395
http://dx.doi.org/10.1371/journal.pcbi.1010918
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