Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis

  1. Andrew S Kennard
  2. Julie A Theriot  Is a corresponding author
  1. University of Washington, United States

Abstract

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.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. All code used to generate figures is available at https://gitlab.com/theriot_lab/fish-wound-healing-nacl

Article and author information

Author details

  1. Andrew S Kennard

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Julie A Theriot

    Biology, University of Washington, Seattle, WA, United States
    For correspondence
    jtheriot@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2334-2535

Funding

Howard Hughes Medical Institute

  • Julie A Theriot

Washington Research Foundation

  • Julie A Theriot

National Institute of General Medical Sciences (T32GM008294)

  • Andrew S Kennard

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Zebrafish (TAB5 background wildtype strain) were raised and embryos harvested according to standard procedures. Experiments were approved by the University of Washington Institutional Animal Care and Use Committee (protocol 4427-01).

Reviewing Editor

  1. Jody Rosenblatt, King's College London, United Kingdom

Publication history

  1. Received: August 23, 2020
  2. Accepted: November 17, 2020
  3. Accepted Manuscript published: November 23, 2020 (version 1)
  4. Version of Record published: December 7, 2020 (version 2)

Copyright

© 2020, Kennard & Theriot

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Andrew S Kennard
  2. Julie A Theriot
(2020)
Osmolarity-independent electrical cues guide rapid response to injury in zebrafish epidermis
eLife 9:e62386.
https://doi.org/10.7554/eLife.62386

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