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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bockris, J. O. & Reddy, A. K. N. Modern Electrochemistry: an Introduction to an Interdisciplinary Area Vol. 2 (Plenum, New York, 1973).
Mosbacher, J., Langer, M., Horber, J. K. & Sachs, F. Voltage-dependent membrane displacements measured by atomic force microscopy. J. Gen. Physiol. 111, 65–74 (1998).
McLaughlin, S. Salicylates and phospholipid bilayer membranes. Nature 203, 234–236 (1973).
Shehata, W. E., Brownell, W. E. & Dieler, R. Effects of salicylate on shape, electromotility and membrane characteristics of isolated outer hair cells from guinea pig cochlea. Acta Otolaryngol 111, 707–718 (1991).
Kakehata, S. & Santos-Sacchi, J. Effects of salicylate and lanthanides on outer hair cell motility and associated gating charge. J. Neurosci. 16, 4881–4889 (1996).
Iwasa, K. H. & Adachi, M. Force generation in the outer hair cell of the cochlea. Biophys. J. 73, 546–555 (1997).
Yamaguchi, T., Nishizaki K. & Itai, S. Molecular interactions between phospholipids and electrolytes in a monolayer of parenteral lipid emulsion. Colloid Surf. B 9, 275–282 (1997).
Iwasa, K., Tasaki, I. & Gibbons, R. C. Swelling of nerve fibers associated with action potentials. Science 210, 338–339 (1980).
Todorov, A. T., Petrov, A. G. & Fendler, J. H. Flexoelectricity of charged and dipolar bilayer-lipid membranes studied by stroboscopic interferometry. Langmuir 10, 2344–2350 (1994).
Petrov, A. G., Miller, B. A., Hristova, K. & Usherwood, P. N. Flexoelectric effects in model and native membranes containing ion channels. Eur. Biophys. J. 22, 289–300 (1993).
Chou, T., Jaric, M. V. & Siggia, E. D. Electrostatics of lipid bilayer bending. Biophys. J. 72, 2042–2055 (1997).
Winiski, A. P., McLaughlin, A. C., McDaniel, R. V., Eisenberg, M. & McLaughlin, S. An experimental test of the discreteness-of-charge effect in positive and negative lipid bilayers. Biochemistry 25, 8206–8214 (1986).
Akinlaja, J. & Sachs, F. The breakdown of cell membranes by electrical and mechanical stress. Biophys. J. 75, 247–254 (1998).
Wu, H. W. & Moy, V. T. Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking. Scanning 20, 389–397 (1998).
Carslaw, H. S. & Jaegger, J. C. Conduction of Heat in Solids 2nd edn (Oxford Univ. Press, London, 1959).
Hille, B. Ionic Channels of Excitable Membranes 2nd edn (Sinauer, Sunderland, 1992).
Singh, A. K., Kasinath, B. S. & Lewis, E. J. Interaction of polycations with cell surface negative charges of epithelial cells. Biochim. Biophys. Acta 1120, 337–342 (1992).
Carnie, S. & McLaughlin, S. Large divalent cations and electrostatic potentials adjacent to membranes: a theoretical calculation. Biophys. J. 44, 325–332 (1983).
Kraayenhof, R., Sterk, G. J. & Wong Fong Sang, H. W. Probing biomembrane interfacial potential and pH profiles with a new type of float-like fluorophores positioned at varying distance from the membrane surface. Biochemistry 32, 10057–10066 (1993).
Hwang, W. C. & Waugh, R. E. Energy of dissociation of lipid bilayer from the membrane skeleton of red blood cells. Biophys. J. 72, 2669–2678 (1997).
Gutknecht, J. & Tosteson, D. C. Diffusion of weak acids across lipid bilayer membranes: effects of chemical reactions in the unstirred layers. Science 182, 1258–1261 (1973).
Lue, A. J.-C. & Brownell, W. E. Salicylate induced changes in outer hair cell lateral wall stiffness. Hearing Res. 135, 163–168 (1999).
Oliver, D. et al. Intracellular anions as the voltage-sensor of prestin, the outer hair cell motor protein. Science 292, 2340–2343 (2001).
Raphael, R. M., Popel, A. S. & Brownell, W. E. A membrane bending model of outer hair cell electromotility. Biophys. J. 78, 2844–2862 (2000).
Santos-Sacchi, J. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J. Neurosci. 11, 3096–3110 (1991).
Zheng, J. et al. Prestin is the motor protein of cochlear outer hair cell. Nature 405, 149–155 (2000).
Wu, M. & Santos-Sacchi, J. Effects of lipophilic ions on outer hair cell membrane capacitance and motility. J. Memb. Biol. 166, 111–118 (1998).
Markin, V. S. & Martinac, B. Mechanosensitive ion channels as reporters of bilayer expansion: a theoretical model. Biophys. J. 60, 1120–1127 (1991).
Maingret, F., Fosset, M., Lesage, F., Lazdunski, M. & Honore, E. TRAAK is a mammalian neuronal mechano-gated K+ channel. J. Biol. Chem. 274, 1381–1387 (1999).
Shih, C. W., Schlein, W. S. & Li, J. C. M. Photoelastic and finite element analysis of different size spheres in contact. J. Mater. Res. 7, 1011–1017 (1992).
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, PC., Keleshian, A. & Sachs, F. Voltage-induced membrane movement. Nature 413, 428–432 (2001). https://doi.org/10.1038/35096578
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/35096578
This article is cited by
-
Photolipid excitation triggers depolarizing optocapacitive currents and action potentials
Nature Communications (2024)
-
Measuring sub-nanometer undulations at microsecond temporal resolution with metal- and graphene-induced energy transfer spectroscopy
Nature Communications (2024)
-
Impedance spectroscopy of the cell/nanovolcano interface enables optimization for electrophysiology
Microsystems & Nanoengineering (2023)
-
Salicylate- and Noise-induced Tinnitus. Different Mechanisms Producing the same Result? An Experimental Model
Indian Journal of Otolaryngology and Head & Neck Surgery (2023)
-
Detection of cellular micromotion by advanced signal processing
Scientific Reports (2020)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.