Short-term bioelectric stimulation of collective cell migration in tissues reprograms long-term supracellular dynamics.
bioelectricity
collective cell migration
electrotaxis
supracellularity
tissue engineering
Journal
PNAS nexus
ISSN: 2752-6542
Titre abrégé: PNAS Nexus
Pays: England
ID NLM: 9918367777906676
Informations de publication
Date de publication:
Mar 2022
Mar 2022
Historique:
received:
03
09
2021
revised:
03
09
2021
accepted:
07
01
2022
entrez:
1
4
2022
pubmed:
2
4
2022
medline:
2
4
2022
Statut:
epublish
Résumé
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.
Identifiants
pubmed: 35360553
doi: 10.1093/pnasnexus/pgac002
pii: pgac002
pmc: PMC8962779
doi:
Types de publication
Journal Article
Langues
eng
Pagination
pgac002Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM133574
Pays : United States
Informations de copyright
© The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences.
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