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Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling

Directed cell migration arises from cells following a microenvironmental gradient (e.g. of a chemokine) or polarizing feature (e.g. a linear structure). However cells not only follow, but in many cases, also generate directionality cues by modifying their microenvironment. This bi-directional relati...

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Autores principales: Pamonag, Michael, Hinson, Abigail, Burton, Elisha J., Jafari, Nojan, Sales, Dominic, Babcock, Sarah, Basha, Rozlan, Hu, Xiaofeng, Kubow, Kristopher E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956187/
https://www.ncbi.nlm.nih.gov/pubmed/35333902
http://dx.doi.org/10.1371/journal.pone.0265403
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author Pamonag, Michael
Hinson, Abigail
Burton, Elisha J.
Jafari, Nojan
Sales, Dominic
Babcock, Sarah
Basha, Rozlan
Hu, Xiaofeng
Kubow, Kristopher E.
author_facet Pamonag, Michael
Hinson, Abigail
Burton, Elisha J.
Jafari, Nojan
Sales, Dominic
Babcock, Sarah
Basha, Rozlan
Hu, Xiaofeng
Kubow, Kristopher E.
author_sort Pamonag, Michael
collection PubMed
description Directed cell migration arises from cells following a microenvironmental gradient (e.g. of a chemokine) or polarizing feature (e.g. a linear structure). However cells not only follow, but in many cases, also generate directionality cues by modifying their microenvironment. This bi-directional relationship is seen in the alignment of extracellular matrix (ECM) fibers ahead of invading cell masses. The forces generated by many migrating cells cause fiber alignment, which in turn promotes further migration in the direction of fiber alignment via contact guidance and durotaxis. While this positive-feedback relationship has been widely described for cells invading en masse, single cells are also able to align ECM fibers, as well as respond to contact guidance and durotaxis cues, and should therefore exhibit the same relationship. In this study, we directly tested this hypothesis by studying the migration persistence of individual HT-1080 fibrosarcoma cells migrating in photocrosslinked collagen matrices with limited remodeling potential. Our results demonstrate that this positive-feedback relationship is indeed a fundamental aspect of cell migration in fibrillar environments. We observed that the cells’ inability to align and condense fibers resulted in a decrease in persistence relative to cells in native collagen matrices and even relative to isotropic (glass) substrates. Further experiments involving 2D collagen and electrospun polymer scaffolds suggest that substrates composed of rigid, randomly oriented fibers reduce cells’ ability to follow another directionality cue by forcing them to meander to follow the available adhesive area (i.e. fibers). Finally, our results demonstrate that the bi-directional relationship between cell remodeling and migration is not a “dimensionality” effect, but a fundamental effect of fibrous substrate structure.
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spelling pubmed-89561872022-03-26 Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling Pamonag, Michael Hinson, Abigail Burton, Elisha J. Jafari, Nojan Sales, Dominic Babcock, Sarah Basha, Rozlan Hu, Xiaofeng Kubow, Kristopher E. PLoS One Research Article Directed cell migration arises from cells following a microenvironmental gradient (e.g. of a chemokine) or polarizing feature (e.g. a linear structure). However cells not only follow, but in many cases, also generate directionality cues by modifying their microenvironment. This bi-directional relationship is seen in the alignment of extracellular matrix (ECM) fibers ahead of invading cell masses. The forces generated by many migrating cells cause fiber alignment, which in turn promotes further migration in the direction of fiber alignment via contact guidance and durotaxis. While this positive-feedback relationship has been widely described for cells invading en masse, single cells are also able to align ECM fibers, as well as respond to contact guidance and durotaxis cues, and should therefore exhibit the same relationship. In this study, we directly tested this hypothesis by studying the migration persistence of individual HT-1080 fibrosarcoma cells migrating in photocrosslinked collagen matrices with limited remodeling potential. Our results demonstrate that this positive-feedback relationship is indeed a fundamental aspect of cell migration in fibrillar environments. We observed that the cells’ inability to align and condense fibers resulted in a decrease in persistence relative to cells in native collagen matrices and even relative to isotropic (glass) substrates. Further experiments involving 2D collagen and electrospun polymer scaffolds suggest that substrates composed of rigid, randomly oriented fibers reduce cells’ ability to follow another directionality cue by forcing them to meander to follow the available adhesive area (i.e. fibers). Finally, our results demonstrate that the bi-directional relationship between cell remodeling and migration is not a “dimensionality” effect, but a fundamental effect of fibrous substrate structure. Public Library of Science 2022-03-25 /pmc/articles/PMC8956187/ /pubmed/35333902 http://dx.doi.org/10.1371/journal.pone.0265403 Text en © 2022 Pamonag 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
Pamonag, Michael
Hinson, Abigail
Burton, Elisha J.
Jafari, Nojan
Sales, Dominic
Babcock, Sarah
Basha, Rozlan
Hu, Xiaofeng
Kubow, Kristopher E.
Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title_full Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title_fullStr Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title_full_unstemmed Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title_short Individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
title_sort individual cells generate their own self-reinforcing contact guidance cues through local matrix fiber remodeling
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956187/
https://www.ncbi.nlm.nih.gov/pubmed/35333902
http://dx.doi.org/10.1371/journal.pone.0265403
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