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Elastic properties and shape of the Piezo dome underlying its mechanosensory function.

ABSTRACT: We show in the companion paper that the free membrane shape of lipid bilayer vesicles containing the mechanosensitive ion channel Piezo can be predicted, with no free parameters, from membrane elasticity theory together with measurements of the protein geometry and vesicle size [C. A. Haselwandter, Y. R. Guo, Z. Fu, R. MacKinnon, Proc. Natl. Acad. Sci. U.S.A., 10.1073/pnas.2208027119 (2022)]. Here we use these results to determine the force that the Piezo dome exerts on the free membrane and hence, that the free membrane exerts on the Piezo dome, for a range of vesicle sizes. From vesicle shape measurements alone, we thus obtain a force-distortion relationship for the Piezo dome, from which we deduce the Piezo dome's intrinsic radius of curvature, [Formula: see text] nm, and bending stiffness, [Formula: see text], in freestanding lipid bilayer membranes mimicking cell membranes. Applying these estimates to a spherical cap model of Piezo embedded in a lipid bilayer, we suggest that Piezo's intrinsic curvature, surrounding membrane footprint, small stiffness, and large area are the key properties of Piezo that give rise to low-threshold, high-sensitivity mechanical gating.

SUBMITTER: Haselwandter CA

PROVIDER: S-EPMC9546593 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Elastic properties and shape of the Piezo dome underlying its mechanosensory function.

Haselwandter Christoph A CA Guo Yusong R YR Fu Ziao Z MacKinnon Roderick R

Proceedings of the National Academy of Sciences of the United States of America 20220927 40

We show in the companion paper that the free membrane shape of lipid bilayer vesicles containing the mechanosensitive ion channel Piezo can be predicted, with no free parameters, from membrane elasticity theory together with measurements of the protein geometry and vesicle size [C. A. Haselwandter, Y. R. Guo, Z. Fu, R. MacKinnon, <i>Proc. Natl. Acad. Sci. U.S.A.</i>, 10.1073/pnas.2208027119 (2022)]. Here we use these results to determine the force that the Piezo dome exerts on the free membrane ...[more]

PMID: 36166476

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Project description:Micro-/nanomechanical resonators are often used in material science to measure the elastic properties of ultrathin films or mass spectrometry to estimate the mass of various chemical and biological molecules. Measurements with these sensors utilize changes in the resonant frequency of the resonator exposed to an investigated quantity. Their sensitivities are, therefore, determined by the resonant frequency. The higher resonant frequency and, correspondingly, higher quality factor (Q-factor) yield higher sensitivity. In solution, the resonant frequency (Q-factor) decreases causing a significant lowering of the achievable sensitivity. Hence, the nanomechanical resonator-based sensors mainly operate in a vacuum. Identification by nanomechanical resonator also requires an additional reference measurement on the identical unloaded resonator making experiments, due to limiting achievable accuracies in current nanofabrication processes, yet challenging. In addition, the mass spectrometry by nanomechanical resonator can be routinely performed for light analytes (i.e., analyte is modelled as a point particle). For heavy analytes such as bacteria clumps neglecting their stiffness result in a significant underestimation of determined mass values. In this work, we demonstrate the extraordinary capability of hybrid shape memory alloy (SMA)-based nanomechanical resonators to i) notably tune the resonant frequencies and improve Q-factor of the resonator immersed in fluid, ii) determine the Young's (shear) modulus of prepared ultrathin film only from frequency response of the resonator with sputtered film, and iii) perform heavy analyte mass spectrometry by monitoring shift in frequency of just a single vibrational mode. The procedures required to estimate the Young's (shear) modulus of ultrathin film and the heavy analyte mass from observed changes in the resonant frequency caused by a phase transformation in SMA are developed and, afterward, validated using numerical simulations. The present results demonstrate the outstanding potential and capability of high frequency operating hybrid SMA-based nanomechanical resonators in sensing applications that can be rarely achieved by current nanomechanical resonator-based sensors.

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Elastic properties and shape of the Piezo dome underlying its mechanosensory function.

Publications

Elastic properties and shape of the Piezo dome underlying its mechanosensory function.

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