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. 2002 Jan;82(1 Pt 1):182–192. doi: 10.1016/S0006-3495(02)75385-X

Thermodynamic view of activation energies of proton transfer in various gramicidin A channels.

Anatoly Chernyshev 1, Samuel Cukierman 1
PMCID: PMC1302460  PMID: 11751307

Abstract

The temperature dependencies (range: 5-45 degrees C) of single-channel proton conductances (g(H)) in native gramicidin A (gA) and in two diastereoisomers (SS and RR) of the dioxolane-linked gA channels were measured in glycerylmonooleate/decane (GMO) and diphytanoylphosphatidylcholine/decane (DiPhPC) bilayers. Linear Arrhenius plots (ln (g(H)) versus K(-1)) were obtained for the native gA and RR channels in both types of bilayers, and for the SS channel in GMO bilayers only. The Arrhenius plot for proton transfer in the SS channel in DiPhPC bilayers had a break in linearity around 20 degrees C. This break seems to occur only when protons are the permeating cations in the SS channel. The activation energies (E(a)) for proton transfer in various gA channels (approximately 15 kJ/mol) are consistent with the rate-limiting step being in the channel and/or at the membrane-channel/solution interface, and not in bulk solution. E(a) values for proton transfer in gA channels are considerably smaller than for the permeation of nonproton currents in gA as well as in various other ion channels. The E(a) values for proton transfer in native gA channels are nearly the same in both GMO and DiPhPC bilayers. In contrast, for the dioxolane linked gA dimers, E(a) values were strongly modulated by the lipid environment. The Gibbs activation free energies (Delta G(#)(o)) for protons in various gA channels are within the range of 27-29 kJ/mol in GMO bilayers and of 20-22 kJ/mol in DiPhPC bilayers. The largest difference between Delta G(#)(o) for proton currents occurs between native gA (or SS channels) and the RR channel. In general, the activation entropy (Delta S) is mostly responsible for the differences between g(H) values in various gA channels, and also in distinct bilayers. However, significant differences between the activation enthalpies (Delta H(#)(o)) for proton transfer in the SS and RR channels occur in distinct membranes.

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Selected References

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  1. Akeson M., Deamer D. W. Proton conductance by the gramicidin water wire. Model for proton conductance in the F1F0 ATPases? Biophys J. 1991 Jul;60(1):101–109. doi: 10.1016/S0006-3495(91)82034-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong K. M., Quigley E. P., Quigley P., Crumrine D. S., Cukierman S. Covalently linked gramicidin channels: effects of linker hydrophobicity and alkaline metals on different stereoisomers. Biophys J. 2001 Apr;80(4):1810–1818. doi: 10.1016/S0006-3495(01)76151-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bamberg E., Janko K. The action of a carbonsuboxide dimerized gramicidin A on lipid bilayer membranes. Biochim Biophys Acta. 1977 Mar 17;465(3):486–499. doi: 10.1016/0005-2736(77)90267-x. [DOI] [PubMed] [Google Scholar]
  4. Bamberg E., Läuger P. Temperature-dependent properties of gramicidin A channels. Biochim Biophys Acta. 1974 Oct 29;367(2):127–133. doi: 10.1016/0005-2736(74)90037-6. [DOI] [PubMed] [Google Scholar]
  5. Cukierman S. Proton mobilities in water and in different stereoisomers of covalently linked gramicidin A channels. Biophys J. 2000 Apr;78(4):1825–1834. doi: 10.1016/S0006-3495(00)76732-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cukierman S., Quigley E. P., Crumrine D. S. Proton conduction in gramicidin A and in its dioxolane-linked dimer in different lipid bilayers. Biophys J. 1997 Nov;73(5):2489–2502. doi: 10.1016/S0006-3495(97)78277-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeCoursey T. E., Cherny V. V. Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J Gen Physiol. 1998 Oct;112(4):503–522. doi: 10.1085/jgp.112.4.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grygorczyk R. Temperature dependence of Ca2+-activated K+ currents in the membrane of human erythrocytes. Biochim Biophys Acta. 1987 Aug 20;902(2):159–168. doi: 10.1016/0005-2736(87)90291-4. [DOI] [PubMed] [Google Scholar]
  9. Hinton J. F., Easton P. L., Newkirk D. K., Shungu D. C. 23Na-NMR study of ion transport across vesicle membranes facilitated by phenylalanine analogs of gramicidin. Biochim Biophys Acta. 1993 Mar 14;1146(2):191–196. doi: 10.1016/0005-2736(93)90355-4. [DOI] [PubMed] [Google Scholar]
  10. Hladky S. B., Haydon D. A. Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel. Biochim Biophys Acta. 1972 Aug 9;274(2):294–312. doi: 10.1016/0005-2736(72)90178-2. [DOI] [PubMed] [Google Scholar]
  11. Jordan P. C. Ion permeation and chemical kinetics. J Gen Physiol. 1999 Oct;114(4):601–603. doi: 10.1085/jgp.114.4.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Milburn T., Saint D. A., Chung S. H. The temperature dependence of conductance of the sodium channel: implications for mechanisms of ion permeation. Receptors Channels. 1995;3(3):201–211. [PubMed] [Google Scholar]
  14. Miller C., Stahl N., Barrol M. A thermodynamic analysis of monovalent cation permeation through a K(+)-selective ion channel. Neuron. 1988 Apr;1(2):159–164. doi: 10.1016/0896-6273(88)90200-0. [DOI] [PubMed] [Google Scholar]
  15. Nagle J. F., Tristram-Nagle S. Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J Membr Biol. 1983;74(1):1–14. doi: 10.1007/BF01870590. [DOI] [PubMed] [Google Scholar]
  16. Phillips L. R., Cole C. D., Hendershot R. J., Cotten M., Cross T. A., Busath D. D. Noncontact dipole effects on channel permeation. III. Anomalous proton conductance effects in gramicidin. Biophys J. 2008 Nov 21;77(5):2492–2501. doi: 10.1016/S0006-3495(99)77085-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pomès R., Roux B. Free energy profiles for H+ conduction along hydrogen-bonded chains of water molecules. Biophys J. 1998 Jul;75(1):33–40. doi: 10.1016/S0006-3495(98)77492-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pomès R., Roux B. Structure and dynamics of a proton wire: a theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel. Biophys J. 1996 Jul;71(1):19–39. doi: 10.1016/S0006-3495(96)79211-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Quigley E. P., Crumrine D. S., Cukierman S. Gating and permeation in ion channels formed by gramicidin A and its dioxolane-linked dimer in Na(+) and Cs(+) solutions. J Membr Biol. 2000 Apr 1;174(3):207–212. doi: 10.1007/s002320001045. [DOI] [PubMed] [Google Scholar]
  20. Quigley E. P., Quigley P., Crumrine D. S., Cukierman S. The conduction of protons in different stereoisomers of dioxolane-linked gramicidin A channels. Biophys J. 1999 Nov;77(5):2479–2491. doi: 10.1016/S0006-3495(99)77084-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rudnev V. S., Ermishkin L. N., Fonina L. A., Rovin YuG The dependence of the conductance and lifetime of gramicidin channels on the thickness and tension of lipid bilayers. Biochim Biophys Acta. 1981 Mar 20;642(1):196–202. doi: 10.1016/0005-2736(81)90149-8. [DOI] [PubMed] [Google Scholar]
  22. Schumaker M. F., Pomès R., Roux B. A combined molecular dynamics and diffusion model of single proton conduction through gramicidin. Biophys J. 2000 Dec;79(6):2840–2857. doi: 10.1016/S0006-3495(00)76522-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sitsapesan R., Montgomery R. A., MacLeod K. T., Williams A. J. Sheep cardiac sarcoplasmic reticulum calcium-release channels: modification of conductance and gating by temperature. J Physiol. 1991 Mar;434:469–488. doi: 10.1113/jphysiol.1991.sp018481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stankovic C. J., Heinemann S. H., Delfino J. M., Sigworth F. J., Schreiber S. L. Transmembrane channels based on tartaric acid-gramicidin A hybrids. Science. 1989 May 19;244(4906):813–817. doi: 10.1126/science.2471263. [DOI] [PubMed] [Google Scholar]
  25. Urry D. W., Alonso-Romanowski S., Venkatachalam C. M., Bradley R. J., Harris R. D. Temperature dependence of single channel currents and the peptide libration mechanism for ion transport through the gramicidin A transmembrane channel. J Membr Biol. 1984;81(3):205–217. doi: 10.1007/BF01868714. [DOI] [PubMed] [Google Scholar]
  26. Urry D. W. The gramicidin A transmembrane channel: a proposed pi(L,D) helix. Proc Natl Acad Sci U S A. 1971 Mar;68(3):672–676. doi: 10.1073/pnas.68.3.672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. de Godoy C. M., Cukierman S. Modulation of proton transfer in the water wire of dioxolane-linked gramicidin channels by lipid membranes. Biophys J. 2001 Sep;81(3):1430–1438. doi: 10.1016/s0006-3495(01)75798-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

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