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. 1999 Nov;77(5):2648–2656. doi: 10.1016/S0006-3495(99)77099-2

Supramolecular structures of peptide assemblies in membranes by neutron off-plane scattering: method of analysis

L Yang 1, TM Weiss 1, TA Harroun 1, WT Heller 1, HW Huang 1
PMCID: PMC1300539  PMID: 10545365

Abstract

In a previous paper (Yang et al., Biophys. J. 75:641-645, 1998), we showed a simple, efficient method of recording the diffraction patterns of supramolecular peptide assemblies in membranes where the samples were prepared in the form of oriented multilayers. Here we develop a method of analysis based on the diffraction theory of two-dimensional liquids. Gramicidin was used as a prototype model because its pore structure in membrane in known. At full hydration, the diffraction patterns of alamethicin and magainin are similar to gramicidin except in the scale of q (the momentum transfer of scattering), clearly indicating that both alamethicin and magainin form pores in membranes but of different sizes. When the hydration of the multilayer samples was decreased while the bilayers were still fluid, the in-plane positions of the membrane pores became correlated from one bilayer to the next. We believe that this is a new manifestation of the hydration force. The effect is most prominent in magainin patterns, which are used to demonstrate the method of analysis. When magainin samples were further dehydrated or cooled, the liquid-like diffraction turned into crystal-like patterns. This discovery points to the possibility of investigating the supramolecular structures with high-order diffraction.

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Selected References

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  1. Arseniev A. S., Barsukov I. L., Bystrov V. F., Lomize A. L., Ovchinnikov YuA 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices. FEBS Lett. 1985 Jul 8;186(2):168–174. doi: 10.1016/0014-5793(85)80702-x. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Duclohier H., Molle G., Spach G. Antimicrobial peptide magainin I from Xenopus skin forms anion-permeable channels in planar lipid bilayers. Biophys J. 1989 Nov;56(5):1017–1021. doi: 10.1016/S0006-3495(89)82746-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dufourcq J., Faucon J. F., Fourche G., Dasseux J. L., Le Maire M., Gulik-Krzywicki T. Morphological changes of phosphatidylcholine bilayers induced by melittin: vesicularization, fusion, discoidal particles. Biochim Biophys Acta. 1986 Jul 10;859(1):33–48. doi: 10.1016/0005-2736(86)90315-9. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Harroun T. A., Heller W. T., Weiss T. M., Yang L., Huang H. W. Experimental evidence for hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys J. 1999 Feb;76(2):937–945. doi: 10.1016/S0006-3495(99)77257-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Harroun T. A., Heller W. T., Weiss T. M., Yang L., Huang H. W. Theoretical analysis of hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys J. 1999 Jun;76(6):3176–3185. doi: 10.1016/S0006-3495(99)77469-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. He K., Ludtke S. J., Huang H. W., Worcester D. L. Antimicrobial peptide pores in membranes detected by neutron in-plane scattering. Biochemistry. 1995 Dec 5;34(48):15614–15618. doi: 10.1021/bi00048a002. [DOI] [PubMed] [Google Scholar]
  9. He K., Ludtke S. J., Worcester D. L., Huang H. W. Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys J. 1996 Jun;70(6):2659–2666. doi: 10.1016/S0006-3495(96)79835-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. He K., Ludtke S. J., Wu Y., Huang H. W. X-ray scattering with momentum transfer in the plane of membrane. Application to gramicidin organization. Biophys J. 1993 Jan;64(1):157–162. doi: 10.1016/S0006-3495(93)81350-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Heller W. T., He K., Ludtke S. J., Harroun T. A., Huang H. W. Effect of changing the size of lipid headgroup on peptide insertion into membranes. Biophys J. 1997 Jul;73(1):239–244. doi: 10.1016/S0006-3495(97)78064-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Heller W. T., Waring A. J., Lehrer R. I., Huang H. W. Multiple states of beta-sheet peptide protegrin in lipid bilayers. Biochemistry. 1998 Dec 8;37(49):17331–17338. doi: 10.1021/bi981314q. [DOI] [PubMed] [Google Scholar]
  13. Huang H. W., Olah G. A. Uniformly oriented gramicidin channels embedded in thick monodomain lecithin multilayers. Biophys J. 1987 Jun;51(6):989–992. doi: 10.1016/S0006-3495(87)83427-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Huang H. W., Wu Y. Lipid-alamethicin interactions influence alamethicin orientation. Biophys J. 1991 Nov;60(5):1079–1087. doi: 10.1016/S0006-3495(91)82144-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Juretić D., Hendler R. W., Kamp F., Caughey W. S., Zasloff M., Westerhoff H. V. Magainin oligomers reversibly dissipate delta microH+ in cytochrome oxidase liposomes. Biochemistry. 1994 Apr 19;33(15):4562–4570. doi: 10.1021/bi00181a017. [DOI] [PubMed] [Google Scholar]
  16. Ladokhin A. S., Selsted M. E., White S. H. Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: pore formation by melittin. Biophys J. 1997 Apr;72(4):1762–1766. doi: 10.1016/S0006-3495(97)78822-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Latorre R., Alvarez O. Voltage-dependent channels in planar lipid bilayer membranes. Physiol Rev. 1981 Jan;61(1):77–150. doi: 10.1152/physrev.1981.61.1.77. [DOI] [PubMed] [Google Scholar]
  18. Ludtke S. J., He K., Heller W. T., Harroun T. A., Yang L., Huang H. W. Membrane pores induced by magainin. Biochemistry. 1996 Oct 29;35(43):13723–13728. doi: 10.1021/bi9620621. [DOI] [PubMed] [Google Scholar]
  19. Ludtke S., He K., Huang H. Membrane thinning caused by magainin 2. Biochemistry. 1995 Dec 26;34(51):16764–16769. doi: 10.1021/bi00051a026. [DOI] [PubMed] [Google Scholar]
  20. Matsuzaki K., Murase O., Fujii N., Miyajima K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry. 1996 Sep 3;35(35):11361–11368. doi: 10.1021/bi960016v. [DOI] [PubMed] [Google Scholar]
  21. Matsuzaki K., Yoneyama S., Miyajima K. Pore formation and translocation of melittin. Biophys J. 1997 Aug;73(2):831–838. doi: 10.1016/S0006-3495(97)78115-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McIntosh T. J., Simon S. A. Hydration force and bilayer deformation: a reevaluation. Biochemistry. 1986 Jul 15;25(14):4058–4066. doi: 10.1021/bi00362a011. [DOI] [PubMed] [Google Scholar]
  23. Nicholson L. K., Cross T. A. Gramicidin cation channel: an experimental determination of the right-handed helix sense and verification of beta-type hydrogen bonding. Biochemistry. 1989 Nov 28;28(24):9379–9385. doi: 10.1021/bi00450a019. [DOI] [PubMed] [Google Scholar]
  24. Olah G. A., Huang H. W., Liu W. H., Wu Y. L. Location of ion-binding sites in the gramicidin channel by X-ray diffraction. J Mol Biol. 1991 Apr 20;218(4):847–858. doi: 10.1016/0022-2836(91)90272-8. [DOI] [PubMed] [Google Scholar]
  25. Seddon J. M. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim Biophys Acta. 1990 Feb 28;1031(1):1–69. doi: 10.1016/0304-4157(90)90002-t. [DOI] [PubMed] [Google Scholar]
  26. Tosteson M. T., Tosteson D. C. The sting. Melittin forms channels in lipid bilayers. Biophys J. 1981 Oct;36(1):109–116. doi: 10.1016/S0006-3495(81)84719-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wack DC, Webb WW. Synchrotron x-ray study of the modulated lamellar phase P beta ' in the lecithin-water system. Phys Rev A Gen Phys. 1989 Sep 1;40(5):2712–2730. doi: 10.1103/physreva.40.2712. [DOI] [PubMed] [Google Scholar]
  28. Wu Y., He K., Ludtke S. J., Huang H. W. X-ray diffraction study of lipid bilayer membranes interacting with amphiphilic helical peptides: diphytanoyl phosphatidylcholine with alamethicin at low concentrations. Biophys J. 1995 Jun;68(6):2361–2369. doi: 10.1016/S0006-3495(95)80418-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yang L., Harroun T. A., Heller W. T., Weiss T. M., Huang H. W. Neutron off-plane scattering of aligned membranes. I. Method Of measurement. Biophys J. 1998 Aug;75(2):641–645. doi: 10.1016/S0006-3495(98)77554-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

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