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Spatiotemporal dynamics of PIEZO1 localization controls keratinocyte migration during wound healing

Jesse R. Holt, Wei-Zheng Zeng, Elizabeth L. Evans, Seung-Hyun Woo, Shang Ma, Hamid Abuwarda, Meaghan Loud, View ORCID ProfileArdem Patapoutian, View ORCID ProfileMedha M. Pathak
doi: https://doi.org/10.1101/2020.10.18.344598
Jesse R. Holt
1Department of Physiology & Biophysics, UC Irvine, Irvine, CA, 92697, USA
2Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA, 92697, USA
3Center for Complex Biological Systems, UC Irvine, Irvine, CA, 92697, USA
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Wei-Zheng Zeng
4Howard Hughes Medical Institute, Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA
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Elizabeth L. Evans
1Department of Physiology & Biophysics, UC Irvine, Irvine, CA, 92697, USA
2Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA, 92697, USA
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Seung-Hyun Woo
4Howard Hughes Medical Institute, Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA
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Shang Ma
4Howard Hughes Medical Institute, Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA
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Hamid Abuwarda
1Department of Physiology & Biophysics, UC Irvine, Irvine, CA, 92697, USA
2Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA, 92697, USA
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Meaghan Loud
4Howard Hughes Medical Institute, Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA
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Ardem Patapoutian
4Howard Hughes Medical Institute, Department of Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA
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  • ORCID record for Ardem Patapoutian
  • For correspondence: medhap@uci.edu ardem@scripps.edu
Medha M. Pathak
1Department of Physiology & Biophysics, UC Irvine, Irvine, CA, 92697, USA
2Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA, 92697, USA
3Center for Complex Biological Systems, UC Irvine, Irvine, CA, 92697, USA
5Department of Biomedical Engineering, UC Irvine, Irvine, CA, 92697, USA
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  • ORCID record for Medha M. Pathak
  • For correspondence: medhap@uci.edu ardem@scripps.edu
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Abstract

Keratinocytes, the predominant cell type of the epidermis, migrate to reinstate the epithelial barrier during wound healing. Mechanical cues are known to regulate keratinocyte re-epithelization and wound healing however, the underlying molecular transducers and biophysical mechanisms remain elusive. Here, we show through molecular, cellular and organismal studies that the mechanically-activated ion channel PIEZO1 regulates keratinocyte migration and wound healing. Epidermal-specific Piezo1 knockout mice exhibited faster wound closure while gain-of-function mice displayed slower wound closure compared to littermate controls. By imaging the spatiotemporal localization dynamics of endogenous PIEZO1 channels we find that channel enrichment in sub-cellular regions induces a localized cellular retraction that slows keratinocyte migration. Our findings suggest a potential pharmacological target for wound treatment. More broadly, we show that nanoscale spatiotemporal dynamics of Piezo1 channels can control tissue-scale events, a finding with implications beyond wound healing to processes as diverse as development, homeostasis, disease and repair.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Text and figures revised for greater clarity

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 03, 2020.
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Spatiotemporal dynamics of PIEZO1 localization controls keratinocyte migration during wound healing
Jesse R. Holt, Wei-Zheng Zeng, Elizabeth L. Evans, Seung-Hyun Woo, Shang Ma, Hamid Abuwarda, Meaghan Loud, Ardem Patapoutian, Medha M. Pathak
bioRxiv 2020.10.18.344598; doi: https://doi.org/10.1101/2020.10.18.344598
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Spatiotemporal dynamics of PIEZO1 localization controls keratinocyte migration during wound healing
Jesse R. Holt, Wei-Zheng Zeng, Elizabeth L. Evans, Seung-Hyun Woo, Shang Ma, Hamid Abuwarda, Meaghan Loud, Ardem Patapoutian, Medha M. Pathak
bioRxiv 2020.10.18.344598; doi: https://doi.org/10.1101/2020.10.18.344598

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