Skip to main content
SpringerLink
Log in

Structure of Fully Hydrated Fluid Phase Lipid Bilayers with Monounsaturated Chains

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

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(q z ) 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(q z )Ι for low q z . (3) Diffuse X-ray scattering from oriented stacks of bilayers provides ΙF(q z )Ι for high q z . 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  • Armen R.S., Uitto O.D., Feller S.E. 1998. Phospholipid component volumes: Determination and application to bilayer structure calculations. Biophys. J. 75:734–744

    CAS  PubMed  Google Scholar 

  • 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 1512:40–52

    PubMed  Google Scholar 

  • Barna S.L., Tate M.W., Gruner S.M., Eikenberry E.F. 1999. Calibration procedures for charge-coupled X-ray detectors. Rev. Sci. Instrum. 70:2927

    Article  CAS  Google Scholar 

  • 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)

    Article  CAS  Google Scholar 

  • 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. 125:6409–6421

    Article  CAS  PubMed  Google Scholar 

  • 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 260:49–58

    CAS  PubMed  Google Scholar 

  • Gennis R.B. 1989. Biomembranes. Molecular Structure and Function. Springer-Verlag, New York

    Google Scholar 

  • Hanahan D.J. 1997. A Guide to Phospholipid Chemistry, Oxford University Press, New York pp. 65–66

    Google Scholar 

  • 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 139:189–197

    Article  CAS  Google Scholar 

  • 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)

  • Koenig B.W., Gawrisch K. 2005. Specific volumes of unsaturated phosphatidylcholines in the liquid crystalline lamellar phase. Biochem. Biophys. Acta 1715:65–70

    CAS  PubMed  Google Scholar 

  • 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. 73:1954–1966

    CAS  PubMed  Google Scholar 

  • 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. 33:328–334

    Google Scholar 

  • 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. 88:2626–2637

    Article  PubMed  CAS  Google Scholar 

  • 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.69:051903

    Google Scholar 

  • 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–e642

    Article  CAS  Google Scholar 

  • Lewis B.A., Engelman D.M. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211–217

    CAS  PubMed  Google Scholar 

  • 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 27:880–887

    Article  CAS  PubMed  Google Scholar 

  • Liu Y., Nagle J.F. 2004. Diffuse scattering provides material parameters and electron density profiles of biomembranes. Phys. Rev. E 69:040901

    Article  CAS  Google Scholar 

  • 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 63:011907

    Article  CAS  Google Scholar 

  • Nagle J.F., Tristram-Nagle S. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta 1469:159–195

    CAS  PubMed  Google Scholar 

  • Nagle J.F., Wiener M.C. 1988. Structure of fully hydrated bilayer dispersions. Biochim. Biophys. Acta 942:1–10

    CAS  PubMed  Google Scholar 

  • 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. 70:1419–1431

    CAS  PubMed  Google Scholar 

  • 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 27:8261–8269

    Article  CAS  PubMed  Google Scholar 

  • 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 62:4000–4009

    CAS  Google Scholar 

  • 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 24:1055–1063

    Article  CAS  PubMed  Google Scholar 

  • Petrache H.I., Feller S.E., Nagle J.F. 1997. Determination of component volumes of lipid bilayers from simulations. Biophys. J. 72:2237–2242

    CAS  PubMed  Google Scholar 

  • Petrache H.I., Tristram-Nagle S., Nagle J.F. 1998. Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids 95:83–94

    Article  CAS  PubMed  Google Scholar 

  • Rand R.P., Parsegian V.A. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta 988:351–376

    CAS  Google Scholar 

  • 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. 79:328–339

    CAS  PubMed  Google Scholar 

  • Seelig A., Seelig J. 1977. Effect of a single cis double bond on the structure of a phospholipid bilayer. Biochemistry 16:45–49

    Article  CAS  PubMed  Google Scholar 

  • Tattrie N.H., Bennett J.R., Cyr R. 1968. Maximum and minimum values for lecithin classes from various biological sources. Biochemistry 46:819–829

    CAS  Google Scholar 

  • Torbet J., Wilkins M.H.F. 1976. X-ray diffraction studies of lecithin bilayers. J. Theor. Biol. 62:447–458

    Article  CAS  PubMed  Google Scholar 

  • Tristram-Nagle S., Liu Y. Legleiter J., Nagle J.F. 2002. Structure of gel phase DMPC determined by X-ray diffraction. Biophys. J. 83:3324–3335

    CAS  PubMed  Google Scholar 

  • Tristram-Nagle S., Petrache H.I., Nagle J.F. 1998. Structure and interactions of fully hydrated dioleoylphosphatidylcholine bilayers. Biophys. J. 75:917–925

    CAS  PubMed  Google Scholar 

  • 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. 64:1097–1109

    CAS  PubMed  Google Scholar 

  • Wiener M.C., Suter R.M., Nagle J.F.h. 1989. Structure of the fully hydrated gel phase of DPPC. Biophys. J. 55:315

    CAS  PubMed  Google Scholar 

  • 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. 61:428–433

    CAS  PubMed  Google Scholar 

  • 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. 70:349–357

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Synchrotron X-ray beamtime was provided by CHESS (National Science Foundation grant DMR-0225180). We thank Hee Kyoung Ko for her help with the data collection at CHESS and Alex Greenwood, a student in the Howard Hughes Summer Undergraduate Research Program, for his help in determining lipid volumes using density centrifugation. This research was supported by National Institutes of Health grant GM44976 (to J. F. N.).

Author information

Authors and Affiliations

  1. Physics Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, 15213, USA

    Norbert Kučerka, Stephanie Tristram-Nagle & John F. Nagle

  2. Biological Sciences Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, 15213, USA

    John F. Nagle

Authors
  1. Norbert Kučerka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie Tristram-Nagle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John F. Nagle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John F. Nagle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kučerka, N., Tristram-Nagle, S. & Nagle, J.F. Structure of Fully Hydrated Fluid Phase Lipid Bilayers with Monounsaturated Chains. J Membrane Biol 208, 193–202 (2006). https://doi.org/10.1007/s00232-005-7006-8

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-005-7006-8

Keywords

Search

Navigation