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Article

Piezo1 Channels Contribute to the Regulation of Human Atrial Fibroblast Mechanical Properties and Matrix Stiffness Sensing

1
Institute for Experimental Cardiovascular Medicine, University Heart Center Freiburg Bad Krozingen, and Faculty of Medicine, University of Freiburg, 79110 Freiburg, Germany
2
CIBSS Centre for Integrative Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany
3
Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany
4
Institute of Neuropathology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106 Freiburg, Germany
5
Signalling Research Centres BIOSS and CIBSS, University of Freiburg, 79104 Freiburg, Germany
6
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, 79104 Freiburg, Germany
*
Author to whom correspondence should be addressed.
These authors contributed equally.
Academic Editors: Cord Brakebusch and Kate Møller Herum
Cells 2021, 10(3), 663; https://doi.org/10.3390/cells10030663
Received: 25 January 2021 / Revised: 8 March 2021 / Accepted: 12 March 2021 / Published: 16 March 2021
(This article belongs to the Special Issue Biomechanical Signaling and Fibrosis)
The mechanical environment of cardiac cells changes continuously and undergoes major alterations during diseases. Most cardiac diseases, including atrial fibrillation, are accompanied by fibrosis which can impair both electrical and mechanical function of the heart. A key characteristic of fibrotic tissue is excessive accumulation of extracellular matrix, leading to increased tissue stiffness. Cells are known to respond to changes in their mechanical environment, but the molecular mechanisms underlying this ability are incompletely understood. We used cell culture systems and hydrogels with tunable stiffness, combined with advanced biophysical and imaging techniques, to elucidate the roles of the stretch-activated channel Piezo1 in human atrial fibroblast mechano-sensing. Changing the expression level of Piezo1 revealed that this mechano-sensor contributes to the organization of the cytoskeleton, affecting mechanical properties of human embryonic kidney cells and human atrial fibroblasts. Our results suggest that this response is independent of Piezo1-mediated ion conduction at the plasma membrane, and mediated in part by components of the integrin pathway. Further, we show that Piezo1 is instrumental for fibroblast adaptation to changes in matrix stiffness, and that Piezo1-induced cell stiffening is transmitted in a paracrine manner to other cells by a signaling mechanism requiring interleukin-6. Piezo1 may be a new candidate for targeted interference with cardiac fibroblast function.
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Keywords: heart; cardiac fibrosis; integrin; actin; cytoskeleton; adhesion; Young’s modulus; calpain; ROCK; FAK heart; cardiac fibrosis; integrin; actin; cytoskeleton; adhesion; Young’s modulus; calpain; ROCK; FAK
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MDPI and ACS Style

Emig, R.; Knodt, W.; Krussig, M.J.; Zgierski-Johnston, C.M.; Gorka, O.; Groß, O.; Kohl, P.; Ravens, U.; Peyronnet, R. Piezo1 Channels Contribute to the Regulation of Human Atrial Fibroblast Mechanical Properties and Matrix Stiffness Sensing. Cells 2021, 10, 663. https://doi.org/10.3390/cells10030663

AMA Style

Emig R, Knodt W, Krussig MJ, Zgierski-Johnston CM, Gorka O, Groß O, Kohl P, Ravens U, Peyronnet R. Piezo1 Channels Contribute to the Regulation of Human Atrial Fibroblast Mechanical Properties and Matrix Stiffness Sensing. Cells. 2021; 10(3):663. https://doi.org/10.3390/cells10030663

Chicago/Turabian Style

Emig, Ramona, Wiebke Knodt, Mario J. Krussig, Callum M. Zgierski-Johnston, Oliver Gorka, Olaf Groß, Peter Kohl, Ursula Ravens, and Rémi Peyronnet. 2021. "Piezo1 Channels Contribute to the Regulation of Human Atrial Fibroblast Mechanical Properties and Matrix Stiffness Sensing" Cells 10, no. 3: 663. https://doi.org/10.3390/cells10030663

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