Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis
The ability of epithelial tissues to heal after injury is essential for animal life, yet the mechanisms by which epithelial cells sense tissue damage are incompletely understood. In aquatic organisms such as zebrafish, osmotic shock following injury is believed to be an early and potent activator of...
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/62386 |
| _version_ | 1811181462663200768 |
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| author | Andrew S Kennard Julie A Theriot |
| author_facet | Andrew S Kennard Julie A Theriot |
| author_sort | Andrew S Kennard |
| collection | DOAJ |
| description | The ability of epithelial tissues to heal after injury is essential for animal life, yet the mechanisms by which epithelial cells sense tissue damage are incompletely understood. In aquatic organisms such as zebrafish, osmotic shock following injury is believed to be an early and potent activator of a wound response. We find that, in addition to sensing osmolarity, basal skin cells in zebrafish larvae are also sensitive to changes in the particular ionic composition of their surroundings after wounding, specifically the concentration of sodium chloride in the immediate vicinity of the wound. This sodium chloride-specific wound detection mechanism is independent of cell swelling, and instead is suggestive of a mechanism by which cells sense changes in the transepithelial electrical potential generated by the transport of sodium and chloride ions across the skin. Consistent with this hypothesis, we show that electric fields directly applied within the skin are sufficient to initiate actin polarization and migration of basal cells in their native epithelial context in vivo, even overriding endogenous wound signaling. This suggests that, in order to mount a robust wound response, skin cells respond to both osmotic and electrical perturbations arising from tissue injury. |
| first_indexed | 2024-04-11T09:18:09Z |
| format | Article |
| id | doaj.art-7ac78b8de76a45b2943a8de6529f40ec |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:18:09Z |
| publishDate | 2020-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-7ac78b8de76a45b2943a8de6529f40ec2022-12-22T04:32:16ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.62386Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermisAndrew S Kennard0https://orcid.org/0000-0002-0472-9144Julie A Theriot1https://orcid.org/0000-0002-2334-2535Biophysics Program, Stanford University, Stanford, United States; Department of Biology and Howard Hughes Medical Institute, University of Washington, Seattle, United StatesDepartment of Biology and Howard Hughes Medical Institute, University of Washington, Seattle, United StatesThe ability of epithelial tissues to heal after injury is essential for animal life, yet the mechanisms by which epithelial cells sense tissue damage are incompletely understood. In aquatic organisms such as zebrafish, osmotic shock following injury is believed to be an early and potent activator of a wound response. We find that, in addition to sensing osmolarity, basal skin cells in zebrafish larvae are also sensitive to changes in the particular ionic composition of their surroundings after wounding, specifically the concentration of sodium chloride in the immediate vicinity of the wound. This sodium chloride-specific wound detection mechanism is independent of cell swelling, and instead is suggestive of a mechanism by which cells sense changes in the transepithelial electrical potential generated by the transport of sodium and chloride ions across the skin. Consistent with this hypothesis, we show that electric fields directly applied within the skin are sufficient to initiate actin polarization and migration of basal cells in their native epithelial context in vivo, even overriding endogenous wound signaling. This suggests that, in order to mount a robust wound response, skin cells respond to both osmotic and electrical perturbations arising from tissue injury.https://elifesciences.org/articles/62386wound healingelectric fieldcell migrationepidermistransepithelial potentialcell polarization |
| spellingShingle | Andrew S Kennard Julie A Theriot Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis eLife wound healing electric field cell migration epidermis transepithelial potential cell polarization |
| title | Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis |
| title_full | Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis |
| title_fullStr | Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis |
| title_full_unstemmed | Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis |
| title_short | Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis |
| title_sort | osmolarity independent electrical cues guide rapid response to injury in zebrafish epidermis |
| topic | wound healing electric field cell migration epidermis transepithelial potential cell polarization |
| url | https://elifesciences.org/articles/62386 |
| work_keys_str_mv | AT andrewskennard osmolarityindependentelectricalcuesguiderapidresponsetoinjuryinzebrafishepidermis AT julieatheriot osmolarityindependentelectricalcuesguiderapidresponsetoinjuryinzebrafishepidermis |