Order Parameters and Areas in Fluid-phase Oriented Lipid Membranes Using Wide Angle X-ray Scattering

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2008 Apr 9

PMID 18390624

Citations 74

Authors

Thalia T Mills

Gilman E S Toombes

Stephanie Tristram-Nagle

Detlef-M Smilgies

Gerald W Feigenson

John F Nagle

Affiliations

Soon will be listed here.

Abstract

We used wide angle x-ray scattering (WAXS) from stacks of oriented lipid bilayers to measure chain orientational order parameters and lipid areas in model membranes consisting of mixtures of 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC)/cholesterol and 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC)/cholesterol in fluid phases. The addition of 40% cholesterol to either DOPC or DPPC changes the WAXS pattern due to an increase in acyl chain orientational order, which is one of the main properties distinguishing the cholesterol-rich liquid-ordered (Lo) phase from the liquid-disordered (Ld) phase. In contrast, powder x-ray data from multilamellar vesicles does not yield information about orientational order, and the scattering from the Lo and Ld phases looks similar. An analytical model to describe the relationship between the chain orientational distribution and WAXS data was used to obtain an average orientational order parameter, S(x-ray). When 40% cholesterol is added to either DOPC or DPPC, S(x-ray) more than doubles, consistent with previous NMR order parameter measurements. By combining information about the average chain orientation with the chain-chain correlation spacing, we extended a commonly used method for calculating areas for gel-phase lipids to fluid-phase lipids and obtained agreement to within 5% of literature values.

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References

Greenwood A, Tristram-Nagle S, Nagle J . Partial molecular volumes of lipids and cholesterol. Chem Phys Lipids. 2006; 143(1-2):1-10. PMC: 2695672. DOI: 10.1016/j.chemphyslip.2006.04.002. View

Reinl H, Brumm T, Bayerl T . Changes of the physical properties of the liquid-ordered phase with temperature in binary mixtures of DPPC with cholesterol: A H-NMR, FT-IR, DSC, and neutron scattering study. Biophys J. 2009; 61(4):1025-35. PMC: 1260362. DOI: 10.1016/S0006-3495(92)81910-0. View

Tristram-Nagle S . Preparation of oriented, fully hydrated lipid samples for structure determination using X-ray scattering. Methods Mol Biol. 2007; 400:63-75. PMC: 2697614. DOI: 10.1007/978-1-59745-519-0_5. View

Nagle J . Area/lipid of bilayers from NMR. Biophys J. 1993; 64(5):1476-81. PMC: 1262472. DOI: 10.1016/S0006-3495(93)81514-5. View

Sun , Suter , Knewtson , Worthington , Zhang , Nagle . Order and disorder in fully hydrated unoriented bilayers of gel-phase dipalmitoylphosphatidylcholine. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1994; 49(5):4665-4676. DOI: 10.1103/physreve.49.4665. View

Tristram-Nagle S, Zhang R, Suter R, Worthington C, Sun W, Nagle J . Measurement of chain tilt angle in fully hydrated bilayers of gel phase lecithins. Biophys J. 1993; 64(4):1097-109. PMC: 1262427. DOI: 10.1016/S0006-3495(93)81475-9. View

Scheidt H, Huster D, Gawrisch K . Diffusion of cholesterol and its precursors in lipid membranes studied by 1H pulsed field gradient magic angle spinning NMR. Biophys J. 2005; 89(4):2504-12. PMC: 1366749. DOI: 10.1529/biophysj.105.062018. View

Huang J, Feigenson G . A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J. 1999; 76(4):2142-57. PMC: 1300186. DOI: 10.1016/S0006-3495(99)77369-8. View

Petrache H, Dodd S, Brown M . Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by (2)H NMR spectroscopy. Biophys J. 2000; 79(6):3172-92. PMC: 1301193. DOI: 10.1016/S0006-3495(00)76551-9. View

10.

Jensen M, Mouritsen O . Lipids do influence protein function-the hydrophobic matching hypothesis revisited. Biochim Biophys Acta. 2004; 1666(1-2):205-26. DOI: 10.1016/j.bbamem.2004.06.009. View

11.

Vist M, Davis J . Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 1990; 29(2):451-64. DOI: 10.1021/bi00454a021. View

12.

Stockton G, Smith I . A deuterium nuclear magnetic resonance study of the condensing effect of cholesterol on egg phosphatidylcholine bilayer membranes. I. Perdeuterated fatty acid probes. Chem Phys Lipids. 1976; 17(2-3 SPEC NO):251-63. DOI: 10.1016/0009-3084(76)90070-0. View

13.

Nagle J, Tristram-Nagle S . Structure of lipid bilayers. Biochim Biophys Acta. 2000; 1469(3):159-95. PMC: 2747654. DOI: 10.1016/s0304-4157(00)00016-2. View

14.

Kucerka N, Liu Y, Chu N, Petrache H, Tristram-Nagle S, Nagle J . Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using X-ray scattering from oriented multilamellar arrays and from unilamellar vesicles. Biophys J. 2005; 88(4):2626-37. PMC: 1305359. DOI: 10.1529/biophysj.104.056606. View

15.

Ipsen J, Karlstrom G, Mouritsen O, Wennerstrom H, Zuckermann M . Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta. 1987; 905(1):162-72. DOI: 10.1016/0005-2736(87)90020-4. View

16.

Simons K, Vaz W . Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct. 2004; 33:269-95. DOI: 10.1146/annurev.biophys.32.110601.141803. View

17.

Hung W, Lee M, Chen F, Huang H . The condensing effect of cholesterol in lipid bilayers. Biophys J. 2007; 92(11):3960-7. PMC: 1868968. DOI: 10.1529/biophysj.106.099234. View

18.

Spaar A, Salditt T . Short range order of hydrocarbon chains in fluid phospholipid bilayers studied by x-ray diffraction from highly oriented membranes. Biophys J. 2003; 85(3):1576-84. PMC: 1303333. DOI: 10.1016/S0006-3495(03)74589-5. View

19.

Levine Y, Wilkins M . Structure of oriented lipid bilayers. Nat New Biol. 1971; 230(11):69-72. DOI: 10.1038/newbio230069a0. View

20.

Warschawski D, Devaux P . Order parameters of unsaturated phospholipids in membranes and the effect of cholesterol: a 1H-13C solid-state NMR study at natural abundance. Eur Biophys J. 2005; 34(8):987-96. DOI: 10.1007/s00249-005-0482-z. View