Cell membrane tethers generate mechanical force in response to electrical stimulation

Biophysical Journal

Volumn 99, Issue 3, 2010, Pages 845-852

  Brownell, William E ^a,b   Qian, Feng ^b,c   Anvari, Bahman ^b,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

^c University of California Riverside   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CELL LINE; CELL MEMBRANE; ELECTROSTIMULATION; HUMAN; MEMBRANE POTENTIAL; PHYSIOLOGY;

BIOMECHANICAL PHENOMENA; CELL LINE; CELL MEMBRANE; ELECTRIC STIMULATION; HUMANS; MEMBRANE POTENTIALS;

EID: 77955686898     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.05.025     Document Type: Article

References (58)

1. Dowhan, W., M. Bogdanov, and E. Mileykowskaya. 2008. Functional roles of lipids in membranes. In Biochemistry of Lipids, Lipoproteins and Membranes. D. E. Vance and J. E. Vance, editors. Elsevier B.V. Dordrecht, The Netherlands.
2. Sachs, F., W. E. Brownell, and A. G. Petrov. 2009. Membrane electromechanics in biology, with a focus on hearing. MRS Bull. 34:665.
3. Daleke, D. L. 2003. Regulation of transbilayer plasma membrane phospholipid asymmetry. J. Lipid Res. 44:233-242.
4. Cohen, L. B., R. D. Keynes, and B. Hille. 1968. Light scattering and birefringence changes during nerve activity. Nature. 218:438-441.
5. Iwasa, K., and I. Tasaki. 1980. Mechanical changes in squid giant axons associated with production of action potentials. Biochem. Biophys. Res. Commun. 95:1328-1331.
6. Terakawa, S. 1983. Changes in intracellular pressure in squid giant axons associated with production of action potentials. Biochem. Biophys. Res. Commun. 114:1006-1010.
7. Akkin, T., D. Landowne, and A. Sivaprakasam. 2009. Optical coherence tomography phase measurement of transient changes in squid giant axons during activity. J. Membr. Biol. 231:35-46.
8. Brownell, W. E., C. R. Bader, Y. de Ribaupierre. 1985. Evoked mechanical responses of isolated cochlear outer hair cells. Science. 227:194-196.
9. Kietis, P., M. Vengris, and L. Valkunas. 2001. Electrical-to-mechanical coupling in purple membranes: membrane as electrostrictive medium. Biophys. J. 80:1631-1640.
10. Ludwig, J., D. Oliver, B. Fakler. 2001. Reciprocal electromechanical properties of rat prestin: the motor molecule from rat outer hair cells. Proc. Natl. Acad. Sci. USA. 98:4178-4183.
11. Mosbacher, J., M. Langer, F. Sachs. 1998. Voltage-dependent membrane displacements measured by atomic force microscopy. J. Gen. Physiol. 111:65-74.
12. Zhang, P. C., A. M. Keleshian, and F. Sachs. 2001. Voltage-induced membrane movement. Nature. 413:428-432.
13. Zheng, J., W. Shen, P. Dallos. 2000. Prestin is the motor protein of cochlear outer hair cells. Nature. 405:149-155.
14. Oghalai, J. S., H. B. Zhao, W. E. Brownell. 2000. Voltage- and tension-dependent lipid mobility in the outer hair cell plasma membrane. Science. 287:658-661.
15. Todorov, A. T., A. G. Petrov, and J. H. Fendler. 1994. First observation of the converse flexoelectric effect in bilayer-lipid membranes. J. Phys. Chem. 98:3076-3079.
16. Qian, F., S. Ermilov, B. Anvari. 2004. Combining optical tweezers and patch clamp for studies of cell membrane electromechanics. Rev. Sci. Instrum. 75:2937-2942.
17. Zhang, R., F. Qian, B. Anvari. 2007. Prestin modulates mechanics and electromechanical force of the plasma membrane. Biophys. J. 93:L07-L09.
18. Cuvelier, D., N. Chiaruttini, P. Nassoy. 2005. Pulling long tubes from firmly adhered vesicles. Europhys. Lett. 71:1015-1021.
19. Dai, J., and M. P. Sheetz. 1999. Membrane tether formation from blebbing cells. Biophys. J. 77:3363-3370.
20. Ermilov, S. A., D. R. Murdock, B. Anvari. 2005. Effects of salicylate on plasma membrane mechanics. J. Neurophysiol. 94: 2105-2110.
21. Li, Z., B. Anvari, W. E. Brownell. 2002. Membrane tether formation from outer hair cells with optical tweezers. Biophys. J. 82: 1386-1395.
22. Oghalai, J. S., A. A. Patel, W. E. Brownell. 1998. Fluorescenceimaged microdeformation of the outer hair cell lateral wall. J. Neurosci. 18:48-58.
23. Sheetz, M. P. 2001. Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2:392-396.
24. Sit, P. S., A. A. Spector, W. E. Brownell. 1997. Micropipette aspiration on the outer hair cell lateral wall. Biophys. J. 72:2812-2819.
25. Hochmuth, R. M., H. C. Wiles, J. T. McCown. 1982. Extensional flow of erythrocyte membrane from cell body to elastic tether. II. Experiment. Biophys. J. 39:83-89.
26. Marcus, W. D., and R. M. Hochmuth. 2002. Experimental studies of membrane tethers formed from human neutrophils. Ann. Biomed. Eng. 30:1273-1280.
27. Berk, D. A., and R. M. Hochmuth. 1992. Lateral mobility of integral proteins in red blood cell tethers. Biophys. J. 61:9-18.
28. Zhelev, D. V., and R. M. Hochmuth. 1995. Mechanically stimulated cytoskeleton rearrangement and cortical contraction in human neutrophils. Biophys. J. 68:2004-2014.
29. 4+ T-lymphocytes. Biophys. J. 88:661-669.
30. Chertoff, M. E., and W. E. Brownell. 1994. Characterization of cochlear outer hair cell turgor. Am. J. Physiol. 266:C467-C479.
31. Morimoto, N., R. M. Raphael, W. E. Brownell. 2002. Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall. Am. J. Physiol. Cell Physiol. 282: C1076-C1086.
32. Breneman, K. D., S. M. Highstein, R. D. Rabbitt. 2009. The passive cable properties of hair cell stereocilia and their contribution to somatic capacitance measurements. Biophys. J. 96:1-8.
33. Petrov, A. G., and P. N. Usherwood. 1994. Mechanosensitivity of cell membranes. Ion channels, lipid matrix and cytoskeleton. Eur. Biophys. J. 23:1-19.
34. Rey, A. D. 2006. Liquid crystal model of membrane flexoelectricity. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 74:011710.
35. Petrov, A. G. 2002. Flexoelectricity of model and living membranes. Biochim. Biophys. Acta. 1561:1-25.
36. Lippmann, M. G. 1875. Relation between electrical phenomena and capillaries [Relation entre les phenomenes electriques et capillaires]. Ann. Chim. Phys. 5:494-549.
37. Lee, J., and C. Kim. 2000. Surface-tension-driven microactuation based on continuous electrowetting. J. Microelectromech. Syst. 9:171-180.
38. Glassinger, E., A. C. Lee, and R. M. Raphael. 2005. Electromechanical effects on tether formation from lipid membranes: a theoretical analysis. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:041926.
39. Zimmerberg, J., and M. M. Kozlov. 2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9-19.
40. Rustom, A., R. Saffrich, H. H. Gerdes. 2004. Nanotubular highways for intercellular organelle transport. Science. 303:1007-1010.
41. 2+ changes the force sensitivity of the hair-cell transduction channel. Biophys. J. 90:124-139.
42. Breneman, K. D., W. E. Brownell, and R. D. Rabbitt. 2009. Hair cell bundles: flexoelectric motors of the inner ear. PLoS ONE. 4:e5201.
43. McMahon, H. T., and J. L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature. 438:590-596.
44. Raphael, R. M., A. S. Popel, and W. E. Brownell. 2000. A membrane bending model of outer hair cell electromotility. Biophys. J. 78: 2844-2862.
45. Lee, K. J. 2005. Effects of hydrophobic mismatch and spontaneous curvature on ion channel gating with a hinge. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:031917.
46. Lee, K. J. 2006. Energetics of rotational gating mechanisms of an ion channel induced by membrane deformation. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73:021909.
47. Turner, M. S., and P. Sens. 2004. Gating-by-tilt of mechanically sensitive membrane channels. Phys. Rev. Lett. 93:118103.
48. Wiggins, P., and R. Phillips. 2004. Analytic models for mechanotransduction: gating a mechanosensitive channel. Proc. Natl. Acad. Sci. USA. 101:4071-4076.
49. Wiggins, P., and R. Phillips. 2005. Membrane-protein interactions in mechanosensitive channels. Biophys. J. 88:880-902.
50. Calabrese, B., I. V. Tabarean, C. E. Morris. 2002. Mechanosensitivity of N-type calcium channel currents. Biophys. J. 83:2560-2574.
51. Gu, C. X., P. F. Juranka, and C. E. Morris. 2001. Stretch-activation and stretch-inactivation of Shaker-IR, a voltage-gated K+ channel. Biophys. J. 80:2678-2693.
52. Schmidt, D., Q. X. Jiang, and R. MacKinnon. 2006. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature. 444:775-779.
53. Bond, P. J., and M. S. Sansom. 2007. Bilayer deformation by the Kv channel voltage sensor domain revealed by self-assembly simulations. Proc. Natl. Acad. Sci. USA. 104:2631-2636.
54. Brownell, W. E. 2006. The piezoelectric outer hair cell: bidirectional energy conversion in membranes. In Auditory Mechanisms: Processes and Models. A. L. Nuttall, P. Gillespie, T. Ren, K. Grosh, and E. de Boer, editors. World Scientific, Singapore.
55. Farrell, B., C. Do Shope, and W. E. Brownell. 2006. Voltage-dependent capacitance of human embryonic kidney cells. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73:041930.
56. Sun, S. X., B. Farrell, A. A. Spector. 2009. Voltage and frequency dependence of prestin-associated charge transfer. J. Theor. Biol. 260:137-144.
57. Eisenberg, M., and S. McLaughlin. 1976. Lipid bilayers as models of biological membranes. BioScience. 26:436-443.
58. Finkelstein, A. 1987. Water Movement through Lipid Bilayers, Pores, and Plasma Membranes: Theory and Reality. Wiley Interscience, New York.