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. 1988 Jan;53(1):111–117. doi: 10.1016/s0006-3495(88)83072-8

Proposed Mechanism for HII Phase Induction by Gramicidin in Model Membranes and Its Relation to Channel Formation

J Antoinette Killian, Ben de Kruijff
PMCID: PMC1330128  PMID: 19431714

Abstract

A model is proposed for the molecular mechanism of HII phase induction by gramicidin in model membranes. The model describes the sequence of events that occurs upon hydration of a mixed lipid/gramicidin film, relating them to gramicidin channel formation and to relevant literature on gramicidin and lipid structure.

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Selected References

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  1. Bohg A., Ristow H. DNA-supercoiling is affected in vitro by the peptide antibiotics tyrocidine and gramicidin. Eur J Biochem. 1986 Nov 3;160(3):587–591. doi: 10.1111/j.1432-1033.1986.tb10078.x. [DOI] [PubMed] [Google Scholar]
  2. Boni L. T., Connolly A. J., Kleinfeld A. M. Transmembrane distribution of gramicidin by tryptophan energy transfer. Biophys J. 1986 Jan;49(1):122–123. doi: 10.1016/S0006-3495(86)83619-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brasseur R., Killian J. A., De Kruijff B., Ruysschaert J. M. Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HII phase. Biochim Biophys Acta. 1987 Sep 18;903(1):11–17. doi: 10.1016/0005-2736(87)90150-7. [DOI] [PubMed] [Google Scholar]
  4. Büldt G., Gally H. U., Seelig A., Seelig J., Zaccai G. Neutron diffraction studies on selectively deuterated phospholipid bilayers. Nature. 1978 Jan 12;271(5641):182–184. doi: 10.1038/271182a0. [DOI] [PubMed] [Google Scholar]
  5. Chapman D., Cornell B. A., Ellasz A. W., Perry A. Interactions of helical polypepetide segments which span the hydrocarbon region of lipid bilayers. Studies of the gramicidin A lipid-water system. J Mol Biol. 1977 Jul 5;113(3):517–538. doi: 10.1016/0022-2836(77)90236-4. [DOI] [PubMed] [Google Scholar]
  6. Chupin V., Killian J. A., de Kruijff B. 2H-nuclear magnetic resonance investigations on phospholipid acyl chain order and dynamics in the gramicidin-induced hexagonal HII phase. Biophys J. 1987 Mar;51(3):395–405. doi: 10.1016/S0006-3495(87)83361-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Classen J., Haest C. W., Tournois H., Deuticke B. Gramicidin-induced enhancement of transbilayer reorientation of lipids in the erythrocyte membrane. Biochemistry. 1987 Oct 20;26(21):6604–6612. doi: 10.1021/bi00395a007. [DOI] [PubMed] [Google Scholar]
  8. Cullis P. R., de Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta. 1979 Dec 20;559(4):399–420. doi: 10.1016/0304-4157(79)90012-1. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Fisher R., Blumenthal T. An interaction between gramicidin and the sigma subunit of RNA polymerase. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1045–1048. doi: 10.1073/pnas.79.4.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Haigh E. A., Thulborn K. R., Sawyer W. H. Comparison of fluorescence energy transfer and quenching methods to establish the position and orientation of components within the transverse plane of the lipid bilayer. Application to the gramicidin A--bilayer interaction. Biochemistry. 1979 Aug 7;18(16):3525–3532. doi: 10.1021/bi00583a014. [DOI] [PubMed] [Google Scholar]
  12. Hladky S. B., Haydon D. A. Discreteness of conductance change in bimolecular lipid membranes in the presence of certain antibiotics. Nature. 1970 Jan 31;225(5231):451–453. doi: 10.1038/225451a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Katz E., Demain A. L. The peptide antibiotics of Bacillus: chemistry, biogenesis, and possible functions. Bacteriol Rev. 1977 Jun;41(2):449–474. doi: 10.1128/br.41.2.449-474.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Killian J. A., Burger K. N., de Kruijff B. Phase separation and hexagonal HII phase formation by gramicidins A, B and C in dioleoylphosphatidylcholine model membranes. A study on the role of the tryptophan residues. Biochim Biophys Acta. 1987 Feb 26;897(2):269–284. doi: 10.1016/0005-2736(87)90423-8. [DOI] [PubMed] [Google Scholar]
  16. Killian J. A., Timmermans J. W., Keur S., de Kruijff B. The tryptophans of gramicidin are essential for the lipid structure modulating effect of the peptide. Biochim Biophys Acta. 1985 Oct 24;820(1):154–156. doi: 10.1016/0005-2736(85)90227-5. [DOI] [PubMed] [Google Scholar]
  17. Killian J. A., de Kruijff B. Importance of hydration for gramicidin-induced hexagonal HII phase formation in dioleoylphosphatidylcholine model membranes. Biochemistry. 1985 Dec 31;24(27):7890–7898. doi: 10.1021/bi00348a007. [DOI] [PubMed] [Google Scholar]
  18. Killian J. A., de Kruijff B. The influence of proteins and peptides on the phase properties of lipids. Chem Phys Lipids. 1986 Jun-Jul;40(2-4):259–284. doi: 10.1016/0009-3084(86)90073-3. [DOI] [PubMed] [Google Scholar]
  19. Killian J. A., de Kruijff B. Thermodynamic, motional, and structural aspects of gramicidin-induced hexagonal HII phase formation in phosphatidylethanolamine. Biochemistry. 1985 Dec 31;24(27):7881–7890. doi: 10.1021/bi00348a006. [DOI] [PubMed] [Google Scholar]
  20. Killian J. A., de Kruijff B., van Echteld C. J., Verkleij A. J., Leunissen-Bijvelt J., de Gier J. Mixtures of gramicidin and lysophosphatidylcholine form lamellar structures. Biochim Biophys Acta. 1983 Feb 9;728(1):141–144. doi: 10.1016/0005-2736(83)90446-7. [DOI] [PubMed] [Google Scholar]
  21. Killian J. A., van den Berg C. W., Tournois H., Keur S., Slotboom A. J., van Scharrenburg G. J., de Kruijff B. Gramicidin-induced hexagonal HII phase formation in negatively charged phospholipids and the effect of N- and C-terminal modification of gramicidin on its interaction with zwitterionic phospholipids. Biochim Biophys Acta. 1986 May 9;857(1):13–27. doi: 10.1016/0005-2736(86)90094-5. [DOI] [PubMed] [Google Scholar]
  22. Kolb H. A., Bamberg E. Influence of membrane thickness and ion concentration on the properties of the gramicidin a channel. Autocorrelation, spectral power density, relaxation and single-channel studies. Biochim Biophys Acta. 1977 Jan 4;464(1):127–141. doi: 10.1016/0005-2736(77)90376-5. [DOI] [PubMed] [Google Scholar]
  23. Madden T. D., Cullis P. R. Stabilization of bilayer structure for unsaturated phosphatidylethanolamines by detergents. Biochim Biophys Acta. 1982 Jan 4;684(1):149–153. doi: 10.1016/0005-2736(82)90061-x. [DOI] [PubMed] [Google Scholar]
  24. Mazet J. L., Andersen O. S., Koeppe R. E., 2nd Single-channel studies on linear gramicidins with altered amino acid sequences. A comparison of phenylalanine, tryptophane, and tyrosine substitutions at positions 1 and 11. Biophys J. 1984 Jan;45(1):263–276. doi: 10.1016/S0006-3495(84)84153-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Naik V. M., Krimm S. The structure of crystalline and membrane-bound gramicidin A by vibrational analysis. Biochem Biophys Res Commun. 1984 Dec 28;125(3):919–925. doi: 10.1016/0006-291x(84)91371-8. [DOI] [PubMed] [Google Scholar]
  26. Naik V. M., Krimm S. Vibrational analysis of the structure of gramicidin A. II. Vibrational spectra. Biophys J. 1986 Jun;49(6):1147–1154. doi: 10.1016/S0006-3495(86)83743-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pasquali-Ronchetti I., Spisni A., Casali E., Masotti L., Urry D. W. Gramicidin A induces lysolecithin to form bilayers. Biosci Rep. 1983 Feb;3(2):127–133. doi: 10.1007/BF01121943. [DOI] [PubMed] [Google Scholar]
  28. Paulus H., Sarkar N., Mukherjee P. K., Langley D., Ivanov V. T., Shepel E. N., Veatch W. Comparison of the effect of linear gramicidin analogues on bacterial sporulation, membrane permeability, and ribonucleic acid polymerase. Biochemistry. 1979 Oct 16;18(21):4532–4536. doi: 10.1021/bi00588a012. [DOI] [PubMed] [Google Scholar]
  29. Prasad K. U., Trapane T. L., Busath D., Szabo G., Urry D. W. Synthesis and characterization of (1-13C) Phe9 gramicidin A. Effects of side chain variations. Int J Pept Protein Res. 1983 Sep;22(3):341–347. doi: 10.1111/j.1399-3011.1983.tb02100.x. [DOI] [PubMed] [Google Scholar]
  30. Rothschild K. J., Stanley H. E. Raman spectroscopic investigation of gramicidin A' conformations. Science. 1974 Aug 16;185(4151):616–618. doi: 10.1126/science.185.4151.616. [DOI] [PubMed] [Google Scholar]
  31. Sarkar N., Langley D., Paulus H. Studies on the mechanism and specificity of inhibition of ribonucleic acid polymerase by linear gramicidin. Biochemistry. 1979 Oct 16;18(21):4536–4541. doi: 10.1021/bi00588a013. [DOI] [PubMed] [Google Scholar]
  32. Sarkar N., Paulus H. Function of peptide antibiotics in sporulation. Nat New Biol. 1972 Oct 25;239(95):228–230. doi: 10.1038/newbio239228a0. [DOI] [PubMed] [Google Scholar]
  33. Seddon J. M., Cevc G., Kaye R. D., Marsh D. X-ray diffraction study of the polymorphism of hydrated diacyl- and dialkylphosphatidylethanolamines. Biochemistry. 1984 Jun 5;23(12):2634–2644. doi: 10.1021/bi00307a015. [DOI] [PubMed] [Google Scholar]
  34. Tate M. W., Gruner S. M. Lipid polymorphism of mixtures of dioleoylphosphatidylethanolamine and saturated and monounsaturated phosphatidylcholines of various chain lengths. Biochemistry. 1987 Jan 13;26(1):231–236. doi: 10.1021/bi00375a031. [DOI] [PubMed] [Google Scholar]
  35. Tilcock C. P. Lipid polymorphism. Chem Phys Lipids. 1986 Jun-Jul;40(2-4):109–125. doi: 10.1016/0009-3084(86)90066-6. [DOI] [PubMed] [Google Scholar]
  36. Tournois H., Killian J. A., Urry D. W., Bokking O. R., de Gier J., de Kruijff B. Solvent determined conformation of gramicidin affects the ability of the peptide to induce hexagonal HII phase formation in dioleoylphosphatidylcholine model membranes. Biochim Biophys Acta. 1987 Nov 27;905(1):222–226. doi: 10.1016/0005-2736(87)90026-5. [DOI] [PubMed] [Google Scholar]
  37. Tournois H., Leunissen-Bijvelt J., Haest C. W., de Gier J., de Kruijff B. Gramicidin-induced hexagonal HII phase formation in erythrocyte membranes. Biochemistry. 1987 Oct 20;26(21):6613–6621. doi: 10.1021/bi00395a008. [DOI] [PubMed] [Google Scholar]
  38. Urry D. W. A molecular theory of ion-conductng channels: a field-dependent transition between conducting and nonconducting conformations. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1610–1614. doi: 10.1073/pnas.69.6.1610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Urry D. W., Goodall M. C., Glickson J. D., Mayers D. F. The gramicidin A transmembrane channel: characteristics of head-to-head dimerized (L,D) helices. Proc Natl Acad Sci U S A. 1971 Aug;68(8):1907–1911. doi: 10.1073/pnas.68.8.1907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Urry D. W., Long M. M., Jacobs M., Harris R. D. Conformation and molecular mechanisms of carriers and channels. Ann N Y Acad Sci. 1975 Dec 30;264:203–220. doi: 10.1111/j.1749-6632.1975.tb31484.x. [DOI] [PubMed] [Google Scholar]
  41. Urry D. W., Trapane T. L., Prasad K. U. Is the gramicidin a transmembrane channel single-stranded or double-stranded helix? A simple unequivocal determination. Science. 1983 Sep 9;221(4615):1064–1067. doi: 10.1126/science.221.4615.1064. [DOI] [PubMed] [Google Scholar]
  42. Veatch W. R., Fossel E. T., Blout E. R. The conformation of gramicidin A. Biochemistry. 1974 Dec 17;13(26):5249–5256. doi: 10.1021/bi00723a001. [DOI] [PubMed] [Google Scholar]
  43. Wallace B. A. Ion-bond forms of the gramicidin a transmembrane channel. Biophys J. 1984 Jan;45(1):114–116. doi: 10.1016/S0006-3495(84)84131-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wallace B. A. Structure of gramicidin A. Biophys J. 1986 Jan;49(1):295–306. doi: 10.1016/S0006-3495(86)83642-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wallace B. A., Veatch W. R., Blout E. R. Conformation of gramicidin A in phospholipid vesicles: circular dichroism studies of effects of ion binding, chemical modification, and lipid structure. Biochemistry. 1981 Sep 29;20(20):5754–5760. doi: 10.1021/bi00523a018. [DOI] [PubMed] [Google Scholar]
  46. Weinstein S., Durkin J. T., Veatch W. R., Blout E. R. Conformation of the gramicidin A channel in phospholipid vesicles: a fluorine-19 nuclear magnetic resonance study. Biochemistry. 1985 Jul 30;24(16):4374–4382. doi: 10.1021/bi00337a019. [DOI] [PubMed] [Google Scholar]
  47. Weinstein S., Wallace B. A., Blout E. R., Morrow J. S., Veatch W. Conformation of gramicidin A channel in phospholipid vesicles: a 13C and 19F nuclear magnetic resonance study. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4230–4234. doi: 10.1073/pnas.76.9.4230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Young M., Mandelstam J. Early events during bacterial endospore formation. Adv Microb Physiol. 1979;20:103-62, 321-3. doi: 10.1016/s0065-2911(08)60207-6. [DOI] [PubMed] [Google Scholar]

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