The Journal of Membrane Biology

, Volume 208, Issue 3, pp 193–202 | Cite as

Structure of Fully Hydrated Fluid Phase Lipid Bilayers with Monounsaturated Chains

  • Norbert Kučerka
  • Stephanie Tristram-Nagle
  • John F. Nagle
Article

Abstract

Quantitative structures are obtained at 30°C for the fully hydrated fluid phases of palmitoyloleoylphosphatidylcholine (POPC), with a double bond on the sn-2 hydrocarbon chain, and for dierucoylphosphatidylcholine (di22:1PC), with a double bond on each hydrocarbon chain. The form factors F(qz) for both lipids are obtained using a combination of three methods. (1) Volumetric measurements provide F(0). (2) X-ray scattering from extruded unilamellar vesicles provides ΙF(qz)Ι for low qz. (3) Diffuse X-ray scattering from oriented stacks of bilayers provides ΙF(qz)Ι for high qz. Also, data using method (2) are added to our recent data for dioleoylphosphatidylcholine (DOPC) using methods (1) and (3); the new DOPC data agree very well with the recent data and with (4) our older data obtained using a liquid crystallographic X-ray method. We used hybrid electron density models to obtain structural results from these form factors. The result for area per lipid (A) for DOPC 72.4 ± 0.5 Å2 agrees well with our earlier publications, and we find A = 69.3 ± 0.5 Å2 for di22:1PC and A = 68.3 ± 1.5 Å2 for POPC. We obtain the values for five different average thicknesses: hydrophobic, steric, head-head, phosphate-phosphate and Luzzati. Comparison of the results for these three lipids and for our recent dimyristoylphosphatidylcholine (DMPC) determination provides quantitative measures of the effect of unsaturation on bilayer structure. Our results suggest that lipids with one monounsaturated chain have quantitative bilayer structures closer to lipids with two monounsaturated chains than to lipids with two completely saturated chains.

Keywords

X-ray scattering Phospholipid bilayer Dierucoylphosphatidylcholine Palmitoyloleoyl- phosphatidylcholine Dioleoylphosphatidylcholine Unsaturated lipids Bilayer structure Area per lipid Fully hydrated fluid phase 

References

  1. Armen R.S., Uitto O.D., Feller S.E. 1998. Phospholipid component volumes: Determination and application to bilayer structure calculations. Biophys. J. 75:734–744PubMedGoogle Scholar
  2. Balgavý P., Dubničková M., Kučerka N., Kiselev M.A., Yaradaikin S.P., Uhríková D. 2001. Bilayer thickness and lipid interface area in unilamellar extruded 1,2-diacylphosphatidylcholine liposomes: A small-angle neutron scattering study. Biochim. Biophys. Acta 1512:40–52PubMedGoogle Scholar
  3. Barna S.L., Tate M.W., Gruner S.M., Eikenberry E.F. 1999. Calibration procedures for charge-coupled X-ray detectors. Rev. Sci. Instrum. 70:2927CrossRefGoogle Scholar
  4. Chu N., Kučerka, N., Liu, Y., Tristram-Nagle, S., Nagle, J.F. 2005. Anomalous swelling of lipid bilayer stacks is caused by softening of the bilayer modulus. Phys. Rev. E. 71:041904 (1–8)CrossRefGoogle Scholar
  5. Eldho N.V., Feller S.E., Tristram-Nagle S., Polozov I.V., Gawrisch K. 2003. Polyunsaturated docosahexaenoic vs docosapentaenoic acid - differences in lipid matrix properties from the loss of one double bond. J. Am. Chem. Soc. 125:6409–6421CrossRefPubMedGoogle Scholar
  6. Finer E.G., Flook A.G., Hauser H. 1972. Mechanism of sonication of aqueous egg yolk lecithin dispersions and nature of the resultant particles. Biochim. Biophys. Acta 260:49–58PubMedGoogle Scholar
  7. Gennis R.B. 1989. Biomembranes. Molecular Structure and Function. Springer-Verlag, New YorkGoogle Scholar
  8. Hanahan D.J. 1997. A Guide to Phospholipid Chemistry, Oxford University Press, New York pp. 65–66Google Scholar
  9. Hianik T., Haburcáak M., Lohner K., Prenner E., Paltauf F., Hermetter A. 1998. Compressibility and density of lipid bilayers composed of polyunsaturated phospholipids and cholesterol. Colloids Surf A Physicochem Eng Aspects 139:189–197CrossRefGoogle Scholar
  10. Klauda J.B., Brooks B.R., Pastor R.W., Kučerka N., Nagle J.F. 2005. A simulation-based model for interpreting X-ray data from lipid bilayers. Biophys. J. (in press) Google Scholar
  11. Koenig B.W., Gawrisch K. 2005. Specific volumes of unsaturated phosphatidylcholines in the liquid crystalline lamellar phase. Biochem. Biophys. Acta 1715:65–70PubMedGoogle Scholar
  12. Koenig B.W., Strey H.H., Gawrisch K. 1997. Membrane lateral compressibility determined by NMR and X-ray diffraction: Effect of acyl chain polyunsaturation. Biophys. J. 73:1954–1966PubMedGoogle Scholar
  13. Kučerka N., Kiselev A.M., Balgavý P. 2004a. Determination of the bilayer thickness and lipid surface area in unilamellar dimyristoylphosphatidylcholine vesicles from small-angle neutron scattering curves: A comparison of evaluation methods. Eur. Biophys. J. 33:328–334Google Scholar
  14. Kučerka N., Liu Y., Chu N., Petrache H.I., Tristram-Nagle S., Nagle J.F. 2005. 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. 88:2626–2637CrossRefPubMedGoogle Scholar
  15. Kučerka N., Nagle J.F., Feller S.E., Balgavý P. 2004b. Models to analyze small-angle neutron scattering from unilamellar lipid vesicles. Phys. Rev. E.69:051903Google Scholar
  16. Kučerka N., Uhríkova D., Teixeira J., Balgavý P. 2004c. Bilayer thickness in unilamellar phosphatidylcholine vesicles: Small-angle neutron scattering using constrast variation. Physica B 350:e639–e642CrossRefGoogle Scholar
  17. Lewis B.A., Engelman D.M. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211–217PubMedGoogle Scholar
  18. Lewis R.N.A.H., Sykes B.D., McElhaney R. 1988. Thermotropic phase-behavior of model membranes composed of phosphatidylcholines containing cis-monounsaturated chain homologs of oleic acid-differential scanning calorimetry and 31P NMR spectroscopic studies. Biochemistry 27:880–887CrossRefPubMedGoogle Scholar
  19. Liu Y., Nagle J.F. 2004. Diffuse scattering provides material parameters and electron density profiles of biomembranes. Phys. Rev. E 69:040901CrossRefGoogle Scholar
  20. Lyatskaya J., Liu Y., Tristram-Nagle S., Katsaras J., Nagle J.F. 2001. Method for obtaining structure andstructure interactions from oriented lipid bilayers. Phys. Rev. E 63:011907CrossRefGoogle Scholar
  21. Nagle J.F., Tristram-Nagle S. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta 1469:159–195PubMedGoogle Scholar
  22. Nagle J.F., Wiener M.C. 1988. Structure of fully hydrated bilayer dispersions. Biochim. Biophys. Acta 942:1–10PubMedGoogle Scholar
  23. Nagle J.F., Zhang R., Tristram-Nagle S., Sun W.-J., Petrache H.I., Suter R.M. 1996. X-ray structure determination of fully hydrated L-alpha phase dipalmitoylphosphatidylcholine bilayers. Biophys. J. 70:1419–1431PubMedGoogle Scholar
  24. Needham D., Evans E. 1988. Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20°C below to 10°C above the liquid crystal-crystalline phase transition at 24°C. Biochemistry 27:8261–8269CrossRefPubMedGoogle Scholar
  25. Pabst G., Rappolt M., Amenitsch A., Laggner P. 2000. Structural information from multilamellar liposomes at full hydration: Full q-range fitting with high quality X-ray data. Phys. Rev. E Stat Nonlin Soft Matter Phys 62:4000–4009Google Scholar
  26. Perly B., Smith I.P., Jarrell H.C. 1985. Effects of the replacement of a double bond by a cyclopropane ring in phosphatidylethanolamines: A 2H NMR study of phase transitions and molecular organization. Biochemistry 24:1055–1063CrossRefPubMedGoogle Scholar
  27. Petrache H.I., Feller S.E., Nagle J.F. 1997. Determination of component volumes of lipid bilayers from simulations. Biophys. J. 72:2237–2242PubMedGoogle Scholar
  28. Petrache H.I., Tristram-Nagle S., Nagle J.F. 1998. Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids 95:83–94CrossRefPubMedGoogle Scholar
  29. Rand R.P., Parsegian V.A. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta 988:351–376Google Scholar
  30. Rawicz W., Olbrich K.C., McIntosh T., Needham D., Evans E. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328–339PubMedGoogle Scholar
  31. Seelig A., Seelig J. 1977. Effect of a single cis double bond on the structure of a phospholipid bilayer. Biochemistry 16:45–49CrossRefPubMedGoogle Scholar
  32. Tattrie N.H., Bennett J.R., Cyr R. 1968. Maximum and minimum values for lecithin classes from various biological sources. Biochemistry 46:819–829Google Scholar
  33. Torbet J., Wilkins M.H.F. 1976. X-ray diffraction studies of lecithin bilayers. J. Theor. Biol. 62:447–458CrossRefPubMedGoogle Scholar
  34. Tristram-Nagle S., Liu Y. Legleiter J., Nagle J.F. 2002. Structure of gel phase DMPC determined by X-ray diffraction. Biophys. J. 83:3324–3335PubMedGoogle Scholar
  35. Tristram-Nagle S., Petrache H.I., Nagle J.F. 1998. Structure and interactions of fully hydrated dioleoylphosphatidylcholine bilayers. Biophys. J. 75:917–925PubMedGoogle Scholar
  36. Tristram-Nagle S., Zhang R., Suter R.M., Worthington C.R., Sun W.-J., Nagle J.F. 1993. Measurement of chain tilt angle in fully hydrated bilayers of gel phase lecithins. Biophys. J. 64:1097–1109PubMedGoogle Scholar
  37. Wiener M.C., Suter R.M., Nagle J.F.h. 1989. Structure of the fully hydrated gel phase of DPPC. Biophys. J. 55:315PubMedGoogle Scholar
  38. Wiener M.C., White S.H. 1992. Structure of fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. II. Distribution and packing of terminal methyl groups. Biophys. J. 61:428–433PubMedGoogle Scholar
  39. Zhang R.S., Tristram-Nagle S., Sun W-J., Headrick R.L., Irving T.C., Suter R.M., Nagle J.F. 1996. Small-angle X-ray scattering from lipid bilayers is well described by modified Caillé theory but not by paracrystalline theory. Biophys. J. 70:349–357PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Norbert Kučerka
    • 1
  • Stephanie Tristram-Nagle
    • 1
  • John F. Nagle
    • 1
    • 2
  1. 1.Physics DepartmentCarnegie Mellon UniversityPittsburghUSA
  2. 2.Biological Sciences DepartmentCarnegie Mellon UniversityPittsburghUSA

Personalised recommendations