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Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics
The ability to program collective cell migration can allow us to control critical multicellular processes in development, regenerative medicine, and invasive disease. However, while various technologies exist to make individual cells migrate, translating these tools to control myriad, collectively i...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8962779/ https://www.ncbi.nlm.nih.gov/pubmed/35360553 http://dx.doi.org/10.1093/pnasnexus/pgac002 |
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author | Wolf, Abraham E Heinrich, Matthew A Breinyn, Isaac B Zajdel, Tom J Cohen, Daniel J |
author_facet | Wolf, Abraham E Heinrich, Matthew A Breinyn, Isaac B Zajdel, Tom J Cohen, Daniel J |
author_sort | Wolf, Abraham E |
collection | PubMed |
description | The ability to program collective cell migration can allow us to control critical multicellular processes in development, regenerative medicine, and invasive disease. However, while various technologies exist to make individual cells migrate, translating these tools to control myriad, collectively interacting cells within a single tissue poses many challenges. For instance, do cells within the same tissue interpret a global migration ‘command’ differently based on where they are in the tissue? Similarly, since no stimulus is permanent, what are the long-term effects of transient commands on collective cell dynamics? We investigate these questions by bioelectrically programming large epithelial tissues to globally migrate ‘rightward’ via electrotaxis. Tissues clearly developed distinct rear, middle, side, and front responses to a single global migration stimulus. Furthermore, at no point poststimulation did tissues return to their prestimulation behavior, instead equilibrating to a 3rd, new migratory state. These unique dynamics suggested that programmed migration resets tissue mechanical state, which was confirmed by transient chemical disruption of cell–cell junctions, analysis of strain wave propagation patterns, and quantification of cellular crowd dynamics. Overall, this work demonstrates how externally driving the collective migration of a tissue can reprogram baseline cell–cell interactions and collective dynamics, even well beyond the end of the global migratory cue, and emphasizes the importance of considering the supracellular context of tissues and other collectives when attempting to program crowd behaviors. |
format | Online Article Text |
id | pubmed-8962779 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-89627792022-03-29 Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics Wolf, Abraham E Heinrich, Matthew A Breinyn, Isaac B Zajdel, Tom J Cohen, Daniel J PNAS Nexus Physical Sciences and Engineering The ability to program collective cell migration can allow us to control critical multicellular processes in development, regenerative medicine, and invasive disease. However, while various technologies exist to make individual cells migrate, translating these tools to control myriad, collectively interacting cells within a single tissue poses many challenges. For instance, do cells within the same tissue interpret a global migration ‘command’ differently based on where they are in the tissue? Similarly, since no stimulus is permanent, what are the long-term effects of transient commands on collective cell dynamics? We investigate these questions by bioelectrically programming large epithelial tissues to globally migrate ‘rightward’ via electrotaxis. Tissues clearly developed distinct rear, middle, side, and front responses to a single global migration stimulus. Furthermore, at no point poststimulation did tissues return to their prestimulation behavior, instead equilibrating to a 3rd, new migratory state. These unique dynamics suggested that programmed migration resets tissue mechanical state, which was confirmed by transient chemical disruption of cell–cell junctions, analysis of strain wave propagation patterns, and quantification of cellular crowd dynamics. Overall, this work demonstrates how externally driving the collective migration of a tissue can reprogram baseline cell–cell interactions and collective dynamics, even well beyond the end of the global migratory cue, and emphasizes the importance of considering the supracellular context of tissues and other collectives when attempting to program crowd behaviors. Oxford University Press 2022-03-02 /pmc/articles/PMC8962779/ /pubmed/35360553 http://dx.doi.org/10.1093/pnasnexus/pgac002 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Physical Sciences and Engineering Wolf, Abraham E Heinrich, Matthew A Breinyn, Isaac B Zajdel, Tom J Cohen, Daniel J Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title | Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title_full | Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title_fullStr | Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title_full_unstemmed | Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title_short | Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
title_sort | short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics |
topic | Physical Sciences and Engineering |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8962779/ https://www.ncbi.nlm.nih.gov/pubmed/35360553 http://dx.doi.org/10.1093/pnasnexus/pgac002 |
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