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Myosin-II mediated traction forces evoke localized Piezo1 Ca2+ flickers

Kyle L. Ellefsen, Jesse R. Holt, Alice Chang, Jamison L. Nourse, Janahan Arulmoli, Armen Mekhdjian, Hamid Abuwarda, Francesco Tombola, Lisa A. Flanagan, Alexander R. Dunn, Ian Parker, Medha M. Pathak
doi: https://doi.org/10.1101/294611
Kyle L. Ellefsen
1Department of Neurobiology & Behavior, UC Irvine, Irvine, CA 92697
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Jesse R. Holt
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
4Center for Complex Biological Systems, UC Irvine, Irvine, CA 92697
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Alice Chang
5Department of Chemical Engineering, Stanford University, Stanford, CA 94305
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Jamison L. Nourse
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
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Janahan Arulmoli
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
4Center for Complex Biological Systems, UC Irvine, Irvine, CA 92697
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Armen Mekhdjian
5Department of Chemical Engineering, Stanford University, Stanford, CA 94305
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Hamid Abuwarda
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
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Francesco Tombola
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
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Lisa A. Flanagan
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
6Department of Biomedical Engineering, UC Irvine, Irvine, CA 92697
7Department of Neurology, UC Irvine, Irvine, CA 92697
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Alexander R. Dunn
5Department of Chemical Engineering, Stanford University, Stanford, CA 94305
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Ian Parker
1Department of Neurobiology & Behavior, UC Irvine, Irvine, CA 92697
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
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Medha M. Pathak
2Department of Physiology & Biophysics, UC Irvine, Irvine, CA 92697
3Sue and Bill Gross Stem Cell Research Center, UC Irvine, Irvine, CA 92697
4Center for Complex Biological Systems, UC Irvine, Irvine, CA 92697
6Department of Biomedical Engineering, UC Irvine, Irvine, CA 92697
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  • For correspondence: medhap@uci.edu
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ABSTRACT

Piezo channels transduce mechanical stimuli into electrical and chemical signals, and in doing so, powerfully influence development, tissue homeostasis, and regeneration. While much is known about how Piezo1 responds to external forces, its response to internal, cell-generated forces remains poorly understood. Here, using measurements of endogenous Piezo1 activity and traction forces in native cellular conditions, we show that actomyosin-based cellular traction forces generate spatially-restricted Ca2+ flickers in the absence of externally-applied mechanical forces. Although Piezo1 channels diffuse readily in the plasma membrane and are widely distributed across the cell, their flicker activity is enriched in regions proximal to force-producing adhesions. The mechanical force that activates Piezo1 arises from Myosin II phosphorylation by Myosin Light Chain Kinase. We propose that Piezo1 Ca2+ flickers allow spatial segregation of mechanotransduction events, and that diffusion allows channel molecules to efficiently respond to transient, local mechanical stimuli.

Footnotes

  • New data added to Fig. 3 (Original Fig. 3 is now Fig. S3), Figures 2 and S4 updated, revisions to text and figures for clarity.

Copyright 
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 May 13, 2019.
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Myosin-II mediated traction forces evoke localized Piezo1 Ca2+ flickers
Kyle L. Ellefsen, Jesse R. Holt, Alice Chang, Jamison L. Nourse, Janahan Arulmoli, Armen Mekhdjian, Hamid Abuwarda, Francesco Tombola, Lisa A. Flanagan, Alexander R. Dunn, Ian Parker, Medha M. Pathak
bioRxiv 294611; doi: https://doi.org/10.1101/294611
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Myosin-II mediated traction forces evoke localized Piezo1 Ca2+ flickers
Kyle L. Ellefsen, Jesse R. Holt, Alice Chang, Jamison L. Nourse, Janahan Arulmoli, Armen Mekhdjian, Hamid Abuwarda, Francesco Tombola, Lisa A. Flanagan, Alexander R. Dunn, Ian Parker, Medha M. Pathak
bioRxiv 294611; doi: https://doi.org/10.1101/294611

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