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Voltage-induced membrane movement

Abstract

Thermodynamics predicts that transmembrane voltage modulates membrane tension1 and that this will cause movement. The magnitude and polarity of movement is governed by cell stiffness and surface potentials. Here we confirm these predictions using the atomic force microscope to dynamically follow the movement of voltage-clamped HEK293 cells2 in different ionic-strength solutions. In normal saline, depolarization caused an outward movement, and at low ionic strength an inward movement. The amplitude was proportional to voltage (about 1 nm per 100 mV) and increased with indentation depth. A simple physical model of the membrane and tip provided an estimate of the external and internal surface charge densities (-5 × 10-3 C m-2 and -18 × 10-3 C m-2, respectively). Salicylate (a negative amphiphile3) inhibited electromotility by increasing the external charge density by -15 × 10-3 C m-2. As salicylate blocks electromotility in cochlear outer hair cells at the same concentration4,5, the role of prestin as a motor protein6 may need to be reassessed.

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Figure 1: Voltage-induced membrane movement in HEK293 cells.
Figure 2: Experimental and predicted voltage-induced AFM movement in differing ionic-strength solutions.
Figure 3: Reduction of voltage-induced membrane displacement in the presence of salicylate.

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Acknowledgements

We would like to thank K. Snyder and A. Petrov, A. Boulbitch, R. Raphael, J. Santos-Sacchi, O. Anderson and W. Brownell for encouragement and suggestions, and the US Army Research Office, NIH and the Cell Mechanosensing Project, ICORP, Japan Science and Technology Corporation for support. This work was also funded in part by the Ralph Hochstetter Medical Research Fund.

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Correspondence to Frederick Sachs.

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Zhang, PC., Keleshian, A. & Sachs, F. Voltage-induced membrane movement. Nature 413, 428–432 (2001). https://doi.org/10.1038/35096578

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