Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Voltage-induced membrane movement


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

Buy this article

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others


  1. Bockris, J. O. & Reddy, A. K. N. Modern Electrochemistry: an Introduction to an Interdisciplinary Area Vol. 2 (Plenum, New York, 1973).

    Book  Google Scholar 

  2. 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).

    Article  CAS  Google Scholar 

  3. McLaughlin, S. Salicylates and phospholipid bilayer membranes. Nature 203, 234–236 (1973).

    Article  ADS  Google Scholar 

  4. 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).

    Article  CAS  Google Scholar 

  5. 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).

    Article  CAS  Google Scholar 

  6. Iwasa, K. H. & Adachi, M. Force generation in the outer hair cell of the cochlea. Biophys. J. 73, 546–555 (1997).

    Article  ADS  CAS  Google Scholar 

  7. 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).

    Article  CAS  Google Scholar 

  8. Iwasa, K., Tasaki, I. & Gibbons, R. C. Swelling of nerve fibers associated with action potentials. Science 210, 338–339 (1980).

    Article  ADS  CAS  Google Scholar 

  9. 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).

    Article  CAS  Google Scholar 

  10. 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).

    CAS  PubMed  Google Scholar 

  11. Chou, T., Jaric, M. V. & Siggia, E. D. Electrostatics of lipid bilayer bending. Biophys. J. 72, 2042–2055 (1997).

    Article  ADS  CAS  Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

  13. Akinlaja, J. & Sachs, F. The breakdown of cell membranes by electrical and mechanical stress. Biophys. J. 75, 247–254 (1998).

    Article  ADS  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Carslaw, H. S. & Jaegger, J. C. Conduction of Heat in Solids 2nd edn (Oxford Univ. Press, London, 1959).

    Google Scholar 

  16. Hille, B. Ionic Channels of Excitable Membranes 2nd edn (Sinauer, Sunderland, 1992).

    Google Scholar 

  17. 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).

    Article  CAS  Google Scholar 

  18. Carnie, S. & McLaughlin, S. Large divalent cations and electrostatic potentials adjacent to membranes: a theoretical calculation. Biophys. J. 44, 325–332 (1983).

    Article  ADS  CAS  Google Scholar 

  19. 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).

    Article  CAS  Google Scholar 

  20. 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).

    Article  ADS  CAS  Google Scholar 

  21. 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).

    Article  ADS  CAS  Google Scholar 

  22. Lue, A. J.-C. & Brownell, W. E. Salicylate induced changes in outer hair cell lateral wall stiffness. Hearing Res. 135, 163–168 (1999).

    Article  CAS  Google Scholar 

  23. Oliver, D. et al. Intracellular anions as the voltage-sensor of prestin, the outer hair cell motor protein. Science 292, 2340–2343 (2001).

    Article  CAS  Google Scholar 

  24. Raphael, R. M., Popel, A. S. & Brownell, W. E. A membrane bending model of outer hair cell electromotility. Biophys. J. 78, 2844–2862 (2000).

    Article  CAS  Google Scholar 

  25. Santos-Sacchi, J. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J. Neurosci. 11, 3096–3110 (1991).

    Article  CAS  Google Scholar 

  26. Zheng, J. et al. Prestin is the motor protein of cochlear outer hair cell. Nature 405, 149–155 (2000).

    Article  ADS  CAS  Google Scholar 

  27. Wu, M. & Santos-Sacchi, J. Effects of lipophilic ions on outer hair cell membrane capacitance and motility. J. Memb. Biol. 166, 111–118 (1998).

    Article  CAS  Google Scholar 

  28. Markin, V. S. & Martinac, B. Mechanosensitive ion channels as reporters of bilayer expansion: a theoretical model. Biophys. J. 60, 1120–1127 (1991).

    Article  ADS  CAS  Google Scholar 

  29. 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).

    Article  CAS  Google Scholar 

  30. 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).

    Article  ADS  CAS  Google Scholar 

Download references


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

Correspondence to Frederick Sachs.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, PC., Keleshian, A. & Sachs, F. Voltage-induced membrane movement. Nature 413, 428–432 (2001).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


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.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing