An Innovative Procedure Using a Sublimable Solid to Align Lipid Bilayers for Solid-state NMR Studies

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2002 Apr 20

PMID 11964237

Citations 41

Authors

Kevin J Hallock

Katherine Henzler Wildman

Dong-Kuk Lee

Ayyalusamy Ramamoorthy

Affiliations

Soon will be listed here.

Abstract

Uniaxially aligned phospholipid bilayers are often used as model membranes to obtain structural details of membrane-associated molecules, such as peptides, proteins, drugs, and cholesterol. Well-aligned bilayer samples can be difficult to prepare and no universal procedure has been reported that orients all combinations of membrane-embedded components. In this study, a new method for producing mechanically aligned phospholipid bilayer samples using naphthalene, a sublimable solid, was developed. Using (31)P-NMR spectroscopy, comparison of a conventional method of preparing mechanically aligned samples with the new naphthalene procedure found that the use of naphthalene significantly enhanced the alignment of 3:1 1-palmitoyl-2-oleoyl-phosphatidylethanolamine to 1-palmitoyl-2-oleoyl-phosphatidylglycerol. The utility of the naphthalene procedure is also demonstrated on bilayers of many different compositions, including bilayers containing peptides such as pardaxin and gramicidin. These results show that the naphthalene procedure is a generally applicable method for producing mechanically aligned samples for use in NMR spectroscopy. The increase in bilayer alignment implies that this procedure will improve the sensitivity of solid-state NMR experiments, in particular those techniques that detect low-sensitivity nuclei, such as 15N and 13C.

Citing Articles

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References

Cotten M, Fu R, Cross T . Solid-state NMR and hydrogen-deuterium exchange in a bilayer-solubilized peptide: structural and mechanistic implications. Biophys J. 1999; 76(3):1179-89. PMC: 1300099. DOI: 10.1016/S0006-3495(99)77282-6. View

Zhou Z, Sayer B, Hughes D, Stark R, Epand R . Studies of phospholipid hydration by high-resolution magic-angle spinning nuclear magnetic resonance. Biophys J. 1999; 76(1 Pt 1):387-99. PMC: 1302527. DOI: 10.1016/S0006-3495(99)77205-X. View

Kovacs F, Denny J, Song Z, Quine J, Cross T . Helix tilt of the M2 transmembrane peptide from influenza A virus: an intrinsic property. J Mol Biol. 2000; 295(1):117-25. DOI: 10.1006/jmbi.1999.3322. View

Morein S, Koeppe II R, LINDBLOM G, de Kruijff B, Killian J . The effect of peptide/lipid hydrophobic mismatch on the phase behavior of model membranes mimicking the lipid composition in Escherichia coli membranes. Biophys J. 2000; 78(5):2475-85. PMC: 1300837. DOI: 10.1016/s0006-3495(00)76792-0. View

Liu F, LEWIS R, Hodges R, McElhaney R . A differential scanning calorimetric and 31P NMR spectroscopic study of the effect of transmembrane alpha-helical peptides on the lamellar-reversed hexagonal phase transition of phosphatidylethanolamine model membranes. Biochemistry. 2001; 40(3):760-8. DOI: 10.1021/bi001942j. View

Murphy 3rd O, Kovacs F, Sicard E, Thompson L . Site-directed solid-state NMR measurement of a ligand-induced conformational change in the serine bacterial chemoreceptor. Biochemistry. 2001; 40(5):1358-66. DOI: 10.1021/bi0015109. View

Yang J, Gabrys C, Weliky D . Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry. 2001; 40(27):8126-37. DOI: 10.1021/bi0100283. View

Killian J, de Kruijff B . Importance of hydration for gramicidin-induced hexagonal HII phase formation in dioleoylphosphatidylcholine model membranes. Biochemistry. 1985; 24(27):7890-8. DOI: 10.1021/bi00348a007. View

Nicholson L, Moll F, Mixon T, LoGrasso P, Lay J, Cross T . Solid-state 15N NMR of oriented lipid bilayer bound gramicidin A'. Biochemistry. 1987; 26(21):6621-6. DOI: 10.1021/bi00395a009. View

10.

Gasset M, Killian J, Tournois H, de Kruijff B . Influence of cholesterol on gramicidin-induced HII phase formation in phosphatidylcholine model membranes. Biochim Biophys Acta. 1988; 939(1):79-88. DOI: 10.1016/0005-2736(88)90049-1. View

11.

Shai Y, Fox J, Caratsch C, Shih Y, Edwards C, Lazarovici P . Sequencing and synthesis of pardaxin, a polypeptide from the Red Sea Moses sole with ionophore activity. FEBS Lett. 1988; 242(1):161-6. DOI: 10.1016/0014-5793(88)81007-x. View

12.

Moll 3rd F, Cross T . Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D. Biophys J. 1990; 57(2):351-62. PMC: 1280675. DOI: 10.1016/S0006-3495(90)82536-4. View

13.

Fenske D, Jarrell H . Phosphorus-31 two-dimensional solid-state exchange NMR. Application to model membrane and biological systems. Biophys J. 1991; 59(1):55-69. PMC: 1281118. DOI: 10.1016/S0006-3495(91)82198-1. View

14.

Fenske D, Cullis P . Chemical exchange between lamellar and non-lamellar lipid phases. A one- and two-dimensional 31P-NMR study. Biochim Biophys Acta. 1992; 1108(2):201-9. DOI: 10.1016/0005-2736(92)90026-i. View

15.

Webb M, Hui S, Steponkus P . Dehydration-induced lamellar-to-hexagonal-II phase transitions in DOPE/DOPC mixtures. Biochim Biophys Acta. 1993; 1145(1):93-104. DOI: 10.1016/0005-2736(93)90385-d. View

16.

Ketchem R, Hu W, Cross T . High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science. 1993; 261(5127):1457-60. DOI: 10.1126/science.7690158. View

17.

Roux M, Nezil F, Monck M, Bloom M . Fragmentation of phospholipid bilayers by myelin basic protein. Biochemistry. 1994; 33(1):307-11. DOI: 10.1021/bi00167a040. View

18.

Bechinger B, Zasloff M, Opella S . Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Protein Sci. 1993; 2(12):2077-84. PMC: 2142334. DOI: 10.1002/pro.5560021208. View

19.

Shai Y . Pardaxin: channel formation by a shark repellant peptide from fish. Toxicology. 1994; 87(1-3):109-29. DOI: 10.1016/0300-483x(94)90157-0. View

20.

Smith S, Jonas R, Braiman M, Bormann B . Structure and orientation of the transmembrane domain of glycophorin A in lipid bilayers. Biochemistry. 1994; 33(20):6334-41. DOI: 10.1021/bi00186a037. View