Bioelectric stimulation controls tissue shape and size

Abstract Epithelial tissues sheath organs and electro-mechanically regulate ion and water transport to regulate development, homeostasis, and hydrostatic organ pressure. Here, we demonstrate how external electrical stimulation allows us to control these processes in living tissues. Specifically, we...

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Main Authors: Gawoon Shim, Isaac B. Breinyn, Alejandro Martínez-Calvo, Sameeksha Rao, Daniel J. Cohen
Format: Article
Language:English
Published: Nature Portfolio 2024-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-47079-w
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author Gawoon Shim
Isaac B. Breinyn
Alejandro Martínez-Calvo
Sameeksha Rao
Daniel J. Cohen
author_facet Gawoon Shim
Isaac B. Breinyn
Alejandro Martínez-Calvo
Sameeksha Rao
Daniel J. Cohen
author_sort Gawoon Shim
collection DOAJ
description Abstract Epithelial tissues sheath organs and electro-mechanically regulate ion and water transport to regulate development, homeostasis, and hydrostatic organ pressure. Here, we demonstrate how external electrical stimulation allows us to control these processes in living tissues. Specifically, we electrically stimulate hollow, 3D kidneyoids and gut organoids and find that physiological-strength electrical stimulation of ∼ 5 - 10 V/cm powerfully inflates hollow tissues; a process we call electro-inflation. Electro-inflation is mediated by increased ion flux through ion channels/transporters and triggers subsequent osmotic water flow into the lumen, generating hydrostatic pressure that competes against cytoskeletal tension. Our computational studies suggest that electro-inflation is strongly driven by field-induced ion crowding on the outer surface of the tissue. Electrically stimulated tissues also break symmetry in 3D resulting from electrotaxis and affecting tissue shape. The ability of electrical cues to regulate tissue size and shape emphasizes the role and importance of the electrical micro-environment for living tissues.
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spelling doaj.art-097b33eec8de4e00b8e55baf8f7814d62024-04-07T11:24:29ZengNature PortfolioNature Communications2041-17232024-04-0115111710.1038/s41467-024-47079-wBioelectric stimulation controls tissue shape and sizeGawoon Shim0Isaac B. Breinyn1Alejandro Martínez-Calvo2Sameeksha Rao3Daniel J. Cohen4Department of Mechanical and Aerospace Engineering, Princeton UniversityDepartment of Quantitative and Computational Biology, Princeton UniversityPrinceton Center for Theoretical Science, Princeton UniversityDepartment of Mechanical and Aerospace Engineering, Princeton UniversityDepartment of Mechanical and Aerospace Engineering, Princeton UniversityAbstract Epithelial tissues sheath organs and electro-mechanically regulate ion and water transport to regulate development, homeostasis, and hydrostatic organ pressure. Here, we demonstrate how external electrical stimulation allows us to control these processes in living tissues. Specifically, we electrically stimulate hollow, 3D kidneyoids and gut organoids and find that physiological-strength electrical stimulation of ∼ 5 - 10 V/cm powerfully inflates hollow tissues; a process we call electro-inflation. Electro-inflation is mediated by increased ion flux through ion channels/transporters and triggers subsequent osmotic water flow into the lumen, generating hydrostatic pressure that competes against cytoskeletal tension. Our computational studies suggest that electro-inflation is strongly driven by field-induced ion crowding on the outer surface of the tissue. Electrically stimulated tissues also break symmetry in 3D resulting from electrotaxis and affecting tissue shape. The ability of electrical cues to regulate tissue size and shape emphasizes the role and importance of the electrical micro-environment for living tissues.https://doi.org/10.1038/s41467-024-47079-w
spellingShingle Gawoon Shim
Isaac B. Breinyn
Alejandro Martínez-Calvo
Sameeksha Rao
Daniel J. Cohen
Bioelectric stimulation controls tissue shape and size
Nature Communications
title Bioelectric stimulation controls tissue shape and size
title_full Bioelectric stimulation controls tissue shape and size
title_fullStr Bioelectric stimulation controls tissue shape and size
title_full_unstemmed Bioelectric stimulation controls tissue shape and size
title_short Bioelectric stimulation controls tissue shape and size
title_sort bioelectric stimulation controls tissue shape and size
url https://doi.org/10.1038/s41467-024-47079-w
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