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. 1994 Jan;66(1):71–74. doi: 10.1016/S0006-3495(94)80751-9

Transduction of membrane tension by the ion channel alamethicin.

L R Opsahl 1, W W Webb 1
PMCID: PMC1275664  PMID: 7510531

Abstract

Mechanoelectrical transduction in biological cells is generally attributed to tension-sensitive ion channels, but their mechanisms and physiology remain controversial due to the elusiveness of the channel proteins and potential cytoskeletal interactions. Our discovery of membrane tension sensitivity in ion channels formed by the protein alamethicin reconstituted into pure lipid membranes has demonstrated two simple physical mechanisms of cytoskeleton-independent transduction. Single channel analysis has shown that membrane tension energizes mechanical work for changes of conductance state equal to tension times the associated increase in membrane area. Results show a approximately 40 A2 increase in pore area and transfer of an 80-A2 polypeptide into the membrane. Both mechanisms may be implicated in mechanical signal transduction by cells.

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Selected References

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  1. Archer S. J., Ellena J. F., Cafiso D. S. Dynamics and aggregation of the peptide ion channel alamethicin. Measurements using spin-labeled peptides. Biophys J. 1991 Aug;60(2):389–398. doi: 10.1016/S0006-3495(91)82064-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Assad J. A., Hacohen N., Corey D. P. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2918–2922. doi: 10.1073/pnas.86.8.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baumann G., Mueller P. A molecular model of membrane excitability. J Supramol Struct. 1974;2(5-6):538–557. doi: 10.1002/jss.400020504. [DOI] [PubMed] [Google Scholar]
  4. Christensen O. Mediation of cell volume regulation by Ca2+ influx through stretch-activated channels. Nature. 1987 Nov 5;330(6143):66–68. doi: 10.1038/330066a0. [DOI] [PubMed] [Google Scholar]
  5. Corey D. P., Hudspeth A. J. Ionic basis of the receptor potential in a vertebrate hair cell. Nature. 1979 Oct 25;281(5733):675–677. doi: 10.1038/281675a0. [DOI] [PubMed] [Google Scholar]
  6. Coronado R., Latorre R. Phospholipid bilayers made from monolayers on patch-clamp pipettes. Biophys J. 1983 Aug;43(2):231–236. doi: 10.1016/S0006-3495(83)84343-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Denk W., Keolian R. M., Webb W. W. Mechanical response of frog saccular hair bundles to the aminoglycoside block of mechanoelectrical transduction. J Neurophysiol. 1992 Sep;68(3):927–932. doi: 10.1152/jn.1992.68.3.927. [DOI] [PubMed] [Google Scholar]
  8. Denk W., Webb W. W. Forward and reverse transduction at the limit of sensitivity studied by correlating electrical and mechanical fluctuations in frog saccular hair cells. Hear Res. 1992 Jun;60(1):89–102. doi: 10.1016/0378-5955(92)90062-r. [DOI] [PubMed] [Google Scholar]
  9. Fox R. O., Jr, Richards F. M. A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1.5-A resolution. Nature. 1982 Nov 25;300(5890):325–330. doi: 10.1038/300325a0. [DOI] [PubMed] [Google Scholar]
  10. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol. 1984 Jul;352:685–701. doi: 10.1113/jphysiol.1984.sp015317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gustin M. C. Single-channel mechanosensitive currents. Science. 1991 Aug 16;253(5021):800–800. doi: 10.1126/science.253.5021.800. [DOI] [PubMed] [Google Scholar]
  12. Gustin M. C., Zhou X. L., Martinac B., Kung C. A mechanosensitive ion channel in the yeast plasma membrane. Science. 1988 Nov 4;242(4879):762–765. doi: 10.1126/science.2460920. [DOI] [PubMed] [Google Scholar]
  13. Hall J. E., Vodyanoy I., Balasubramanian T. M., Marshall G. R. Alamethicin. A rich model for channel behavior. Biophys J. 1984 Jan;45(1):233–247. doi: 10.1016/S0006-3495(84)84151-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hamill O. P., McBride D. W., Jr Rapid adaptation of single mechanosensitive channels in Xenopus oocytes. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7462–7466. doi: 10.1073/pnas.89.16.7462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hanke W., Boheim G. The lowest conductance state of the alamethicin pore. Biochim Biophys Acta. 1980 Mar 13;596(3):456–462. doi: 10.1016/0005-2736(80)90134-0. [DOI] [PubMed] [Google Scholar]
  16. Howard J., Roberts W. M., Hudspeth A. J. Mechanoelectrical transduction by hair cells. Annu Rev Biophys Biophys Chem. 1988;17:99–124. doi: 10.1146/annurev.bb.17.060188.000531. [DOI] [PubMed] [Google Scholar]
  17. Huang H. W. Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime. Biophys J. 1986 Dec;50(6):1061–1070. doi: 10.1016/S0006-3495(86)83550-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lansman J. B., Hallam T. J., Rink T. J. Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers? 1987 Feb 26-Mar 4Nature. 325(6107):811–813. doi: 10.1038/325811a0. [DOI] [PubMed] [Google Scholar]
  19. Morris C. E., Horn R. Failure to elicit neuronal macroscopic mechanosensitive currents anticipated by single-channel studies. Science. 1991 Mar 8;251(4998):1246–1249. doi: 10.1126/science.1706535. [DOI] [PubMed] [Google Scholar]
  20. Morris C. E., Horn R. Response. Science. 1991 Aug 16;253(5021):801–801. doi: 10.1126/science.253.5021.801. [DOI] [PubMed] [Google Scholar]
  21. Olesen S. P., Clapham D. E., Davies P. F. Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature. 1988 Jan 14;331(6152):168–170. doi: 10.1038/331168a0. [DOI] [PubMed] [Google Scholar]
  22. Opsahl L. R., Webb W. W. Lipid-glass adhesion in giga-sealed patch-clamped membranes. Biophys J. 1994 Jan;66(1):75–79. doi: 10.1016/S0006-3495(94)80752-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rizzo V., Schwarz G., Voges K. P., Jung G. Molecular shape and dipole moment of alamethicin-like synthetic peptides. Eur Biophys J. 1985;12(2):67–73. doi: 10.1007/BF00260429. [DOI] [PubMed] [Google Scholar]
  24. Ruknudin A., Song M. J., Sachs F. The ultrastructure of patch-clamped membranes: a study using high voltage electron microscopy. J Cell Biol. 1991 Jan;112(1):125–134. doi: 10.1083/jcb.112.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sachs F., Lecar H. Stochastic models for mechanical transduction. Biophys J. 1991 May;59(5):1143–1145. doi: 10.1016/S0006-3495(91)82329-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sachs F., Sigurdson W., Ruknudin A., Bowman C. Single-channel mechanosensitive currents. Science. 1991 Aug 16;253(5021):800–801. doi: 10.1126/science.253.5021.800-a. [DOI] [PubMed] [Google Scholar]
  27. Sansom M. S. The biophysics of peptide models of ion channels. Prog Biophys Mol Biol. 1991;55(3):139–235. doi: 10.1016/0079-6107(91)90004-c. [DOI] [PubMed] [Google Scholar]
  28. Schwarz G., Gerke H., Rizzo V., Stankowski S. Incorporation kinetics in a membrane, studied with the pore-forming peptide alamethicin. Biophys J. 1987 Nov;52(5):685–692. doi: 10.1016/S0006-3495(87)83263-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Souvignet C., Pelosin J. M., Daniel S., Chambaz E. M., Ransac S., Verger R. Activation of protein kinase C in lipid monolayers. J Biol Chem. 1991 Jan 5;266(1):40–44. [PubMed] [Google Scholar]
  30. Zhou X. L., Stumpf M. A., Hoch H. C., Kung C. A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces. Science. 1991 Sep 20;253(5026):1415–1417. doi: 10.1126/science.1716786. [DOI] [PubMed] [Google Scholar]

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