Highly specific and non-invasive imaging of Piezo1-dependent activity across scales using GenEPi

Sine Yaganoglu, Konstantinos Kalyviotis, Christina Vagena-Pantoula, Dörthe Jülich, Benjamin M. Gaub, Maaike Welling, Tatiana Lopes, Dariusz Lachowski, See Swee Tang, Armando Del Rio Hernandez, Victoria Salem, Daniel J. Müller, Scott A. Holley, Julien Vermot, Jian Shi, Nordine Helassa, Katalin Török and Periklis Pantazis ()
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Sine Yaganoglu: Eidgenössische Technische Hochschule (ETH) Zurich
Konstantinos Kalyviotis: Imperial College London
Christina Vagena-Pantoula: Imperial College London
Dörthe Jülich: Yale University
Benjamin M. Gaub: Eidgenössische Technische Hochschule (ETH) Zurich
Maaike Welling: Eidgenössische Technische Hochschule (ETH) Zurich
Tatiana Lopes: Digestion, and Reproduction, Imperial College London
Dariusz Lachowski: Imperial College London
See Swee Tang: Imperial College London
Armando Del Rio Hernandez: Imperial College London
Victoria Salem: Imperial College London
Daniel J. Müller: Eidgenössische Technische Hochschule (ETH) Zurich
Scott A. Holley: Yale University
Julien Vermot: Imperial College London
Jian Shi: University of Leeds
Nordine Helassa: St. George’s, University of London
Katalin Török: St. George’s, University of London
Periklis Pantazis: Eidgenössische Technische Hochschule (ETH) Zurich

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract Mechanosensing is a ubiquitous process to translate external mechanical stimuli into biological responses. Piezo1 ion channels are directly gated by mechanical forces and play an essential role in cellular mechanotransduction. However, readouts of Piezo1 activity are mainly examined by invasive or indirect techniques, such as electrophysiological analyses and cytosolic calcium imaging. Here, we introduce GenEPi, a genetically-encoded fluorescent reporter for non-invasive optical monitoring of Piezo1-dependent activity. We demonstrate that GenEPi has high spatiotemporal resolution for Piezo1-dependent stimuli from the single-cell level to that of the entire organism. GenEPi reveals transient, local mechanical stimuli in the plasma membrane of single cells, resolves repetitive contraction-triggered stimulation of beating cardiomyocytes within microtissues, and allows for robust and reliable monitoring of Piezo1-dependent activity in vivo. GenEPi will enable non-invasive optical monitoring of Piezo1 activity in mechanochemical feedback loops during development, homeostatic regulation, and disease.

Date: 2023
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DOI: 10.1038/s41467-023-40134-y

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