Optical control of PIEZO1 channels

Francisco Andrés Peralta, Mélaine Balcon, Adeline Martz, Deniza Biljali, Federico Cevoli, Benoit Arnould, Antoine Taly, Thierry Chataigneau and Thomas Grutter ()
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Francisco Andrés Peralta: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Mélaine Balcon: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Adeline Martz: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Deniza Biljali: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Federico Cevoli: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Benoit Arnould: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Antoine Taly: Université Paris Cité
Thierry Chataigneau: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie
Thomas Grutter: Université de Strasbourg, Centre National de la Recherche Scientifique, Faculté de Pharmacie

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract PIEZO proteins are unusually large, mechanically-activated trimeric ion channels. The central pore features structural similarities with the pore of other trimeric ion channels, including purinergic P2X receptors, for which optical control of channel gating has been previously achieved with photoswitchable azobenzenes. Extension of these chemical optogenetics methods to mechanically-activated ion channels would provide tools for specific manipulation of pore activity alternative to non-specific mechanical stimulations. Here we report a light-gated mouse PIEZO1 channel, in which an azobenzene-based photoswitch covalently tethered to an engineered cysteine, Y2464C, localized at the extracellular apex of the transmembrane helix 38, rapidly triggers channel gating upon 365-nm-light irradiation. We provide evidence that this light-gated channel recapitulates mechanically-activated PIEZO1 functional properties, and show that light-induced molecular motions are similar to those evoked mechanically. These results push the limits of azobenzene-based methods to unusually large ion channels and provide a simple stimulation means to specifically interrogate PIEZO1 function.

Date: 2023
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DOI: 10.1038/s41467-023-36931-0

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