Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Jan;74(1):328–337. doi: 10.1016/S0006-3495(98)77790-2

Gramicidin channel kinetics under tension.

M Goulian 1, O N Mesquita 1, D K Fygenson 1, C Nielsen 1, O S Andersen 1, A Libchaber 1
PMCID: PMC1299385  PMID: 9449333

Abstract

We have measured the effect of tension on dimerization kinetics of the channel-forming peptide gramicidin A. By aspirating large unilamellar vesicles into a micropipette electrode, we are able to simultaneously monitor membrane tension and electrical activity. We find that the dimer formation rate increases by a factor of 5 as tension ranges from 0 to 4 dyn/cm. The dimer lifetime also increases with tension. This behavior is well described by a phenomenological model of membrane elasticity in which tension modulates the mismatch in thickness between the gramicidin dimer and membrane.

Full Text

The Full Text of this article is available as a PDF (156.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersen O. S. Ion movement through gramicidin A channels. Single-channel measurements at very high potentials. Biophys J. 1983 Feb;41(2):119–133. doi: 10.1016/S0006-3495(83)84414-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andersen O. S., Saberwal G., Greathouse D. V., Koeppe R. E., 2nd Gramicidin channels--a solvable membrane "protein" folding problem. Indian J Biochem Biophys. 1996 Oct;33(5):331–342. [PubMed] [Google Scholar]
  3. Bamberg E., Läuger P. Channel formation kinetics of gramicidin A in lipid bilayer membranes. J Membr Biol. 1973;11(2):177–194. doi: 10.1007/BF01869820. [DOI] [PubMed] [Google Scholar]
  4. Cifu A. S., Koeppe R. E., 2nd, Andersen O. S. On the supramolecular organization of gramicidin channels. The elementary conducting unit is a dimer. Biophys J. 1992 Jan;61(1):189–203. doi: 10.1016/S0006-3495(92)81826-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Devaux P. F., Seigneuret M. Specificity of lipid-protein interactions as determined by spectroscopic techniques. Biochim Biophys Acta. 1985 Jun 12;822(1):63–125. doi: 10.1016/0304-4157(85)90004-8. [DOI] [PubMed] [Google Scholar]
  6. Durkin J. T., Koeppe R. E., 2nd, Andersen O. S. Energetics of gramicidin hybrid channel formation as a test for structural equivalence. Side-chain substitutions in the native sequence. J Mol Biol. 1990 Jan 5;211(1):221–234. doi: 10.1016/0022-2836(90)90022-E. [DOI] [PubMed] [Google Scholar]
  7. Elbaum M, Kuchnir Fygenson D, Libchaber A. Buckling microtubules in vesicles. Phys Rev Lett. 1996 May 20;76(21):4078–4081. doi: 10.1103/PhysRevLett.76.4078. [DOI] [PubMed] [Google Scholar]
  8. Elliott J. R., Needham D., Dilger J. P., Haydon D. A. The effects of bilayer thickness and tension on gramicidin single-channel lifetime. Biochim Biophys Acta. 1983 Oct 26;735(1):95–103. doi: 10.1016/0005-2736(83)90264-x. [DOI] [PubMed] [Google Scholar]
  9. Evans E, Rawicz W. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett. 1990 Apr 23;64(17):2094–2097. doi: 10.1103/PhysRevLett.64.2094. [DOI] [PubMed] [Google Scholar]
  10. Hanke W., Methfessel C., Wilmsen H. U., Katz E., Jung G., Boheim G. Melittin and a chemically modified trichotoxin form alamethicin-type multi-state pores. Biochim Biophys Acta. 1983 Jan 5;727(1):108–114. doi: 10.1016/0005-2736(83)90374-7. [DOI] [PubMed] [Google Scholar]
  11. Helfrich P., Jakobsson E. Calculation of deformation energies and conformations in lipid membranes containing gramicidin channels. Biophys J. 1990 May;57(5):1075–1084. doi: 10.1016/S0006-3495(90)82625-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Koeppe R. E., 2nd, Anderson O. S. Engineering the gramicidin channel. Annu Rev Biophys Biomol Struct. 1996;25:231–258. doi: 10.1146/annurev.bb.25.060196.001311. [DOI] [PubMed] [Google Scholar]
  14. Kwok R., Evans E. Thermoelasticity of large lecithin bilayer vesicles. Biophys J. 1981 Sep;35(3):637–652. doi: 10.1016/S0006-3495(81)84817-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lewis B. A., Engelman D. M. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J Mol Biol. 1983 May 15;166(2):211–217. doi: 10.1016/s0022-2836(83)80007-2. [DOI] [PubMed] [Google Scholar]
  16. Lundbaek J. A., Andersen O. S. Lysophospholipids modulate channel function by altering the mechanical properties of lipid bilayers. J Gen Physiol. 1994 Oct;104(4):645–673. doi: 10.1085/jgp.104.4.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lundbaek J. A., Maer A. M., Andersen O. S. Lipid bilayer electrostatic energy, curvature stress, and assembly of gramicidin channels. Biochemistry. 1997 May 13;36(19):5695–5701. doi: 10.1021/bi9619841. [DOI] [PubMed] [Google Scholar]
  18. Mattice G. L., Koeppe R. E., 2nd, Providence L. L., Andersen O. S. Stabilizing effect of D-alanine2 in gramicidin channels. Biochemistry. 1995 May 23;34(20):6827–6837. doi: 10.1021/bi00020a029. [DOI] [PubMed] [Google Scholar]
  19. Mouritsen O. G., Bloom M. Models of lipid-protein interactions in membranes. Annu Rev Biophys Biomol Struct. 1993;22:145–171. doi: 10.1146/annurev.bb.22.060193.001045. [DOI] [PubMed] [Google Scholar]
  20. Needham D., Evans E. Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20 degrees C below to 10 degrees C above the liquid crystal-crystalline phase transition at 24 degrees C. Biochemistry. 1988 Oct 18;27(21):8261–8269. doi: 10.1021/bi00421a041. [DOI] [PubMed] [Google Scholar]
  21. O'Connell A. M., Koeppe R. E., 2nd, Andersen O. S. Kinetics of gramicidin channel formation in lipid bilayers: transmembrane monomer association. Science. 1990 Nov 30;250(4985):1256–1259. doi: 10.1126/science.1700867. [DOI] [PubMed] [Google Scholar]
  22. Opsahl L. R., Webb W. W. Transduction of membrane tension by the ion channel alamethicin. Biophys J. 1994 Jan;66(1):71–74. doi: 10.1016/S0006-3495(94)80751-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reeves J. P., Dowben R. M. Formation and properties of thin-walled phospholipid vesicles. J Cell Physiol. 1969 Feb;73(1):49–60. doi: 10.1002/jcp.1040730108. [DOI] [PubMed] [Google Scholar]
  24. Ring A. Gramicidin channel-induced lipid membrane deformation energy: influence of chain length and boundary conditions. Biochim Biophys Acta. 1996 Jan 31;1278(2):147–159. doi: 10.1016/0005-2736(95)00220-0. [DOI] [PubMed] [Google Scholar]
  25. Sawyer D. B., Koeppe R. E., 2nd, Andersen O. S. Induction of conductance heterogeneity in gramicidin channels. Biochemistry. 1989 Aug 8;28(16):6571–6583. doi: 10.1021/bi00442a007. [DOI] [PubMed] [Google Scholar]
  26. Urry D. W. Protein conformation in biomembranes: optical rotation and absorption of membrane suspensions. Biochim Biophys Acta. 1972 Feb 14;265(1):115–168. doi: 10.1016/0304-4157(72)90021-4. [DOI] [PubMed] [Google Scholar]
  27. Veatch W. R., Mathies R., Eisenberg M., Stryer L. Simultaneous fluorescence and conductance studies of planar bilayer membranes containing a highly active and fluorescent analog of gramicidin A. J Mol Biol. 1975 Nov 25;99(1):75–92. doi: 10.1016/s0022-2836(75)80160-4. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES