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PMID: 14645066 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol.

Biophysical journal ·Vol. 85 ·No. 6 ·2003-12-00 ·Pages 3758-68

Scherfeld D, Kahya N, Schwille P

Abstract

In recent years, the implication of sphingomyelin in lipid raft formation has intensified the long sustained interest in this membrane lipid. Accumulating evidences show that cholesterol preferentially interacts with sphingomyelin, conferring specific physicochemical properties to the bilayer membrane. The molecular packing created by cholesterol and sphingomyelin, which presumably is one of the driving forces for lipid raft formation, is known in general to differ from that of cholesterol and phosphatidylcholine membranes. However, in many studies, saturated phosphatidylcholines are still considered as a model for sphingolipids. Here, we investigate the effect of cholesterol on mixtures of dioleoyl-phosphatidylcholine (DOPC) and dipalmitoyl-phosphatidylcholine (DPPC) or distearoyl-phosphatidylcholine (DSPC) and compare it to that on mixtures of DOPC and sphingomyelin analyzed in previous studies. Giant unilamellar vesicles prepared from ternary mixtures of various lipid compositions were imaged by confocal fluorescence microscopy and, within a certain range of sterol content, domain formation was observed. The assignment of distinct lipid phases and the molecular mobility in the membrane bilayer was investigated by fluorescence correlation spectroscopy. Cholesterol was shown to affect lipid dynamics in a similar way for DPPC and DSPC when the two phospholipids were combined with cholesterol in binary mixtures. However, the corresponding ternary mixtures exhibited different spatial lipid organization and dynamics. Finally, evidences of a weaker interaction of cholesterol with saturated phosphatidylcholines than with sphingomyelin (with matched chain length) are discussed.

MeSH Terms
1,2-Dipalmitoylphosphatidylcholine/chemistry Biophysical Phenomena Biophysics Cell Membrane/metabolism Cholesterol/chemistry,metabolism Diffusion Lipid Bilayers Lipids/chemistry Microscopy, Confocal Models, Statistical Phosphatidylcholines/chemistry Protein Structure, Tertiary
Chemicals
Lipid Bilayers Lipids Phosphatidylcholines 1,2-Dipalmitoylphosphatidylcholine Cholesterol 1,2-oleoylphosphatidylcholine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Scherfeld Dag
Experimental Biophysics Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany.
Kahya Nicoletta
Schwille Petra
References (46)
46 references, click to expand
  1. Physiology and pathophysiology of sphingolipid metabolism and signaling.
    Biochim Biophys Acta. 2000 May 31;1485(2-3):63-99 PMID: 10832090
  2. Structure and function of sphingolipid- and cholesterol-rich membrane rafts.
    J Biol Chem. 2000 Jun 9;275(23):17221-4 PMID: 10770957
  3. A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: A two-photon fluorescence microscopy study.
    Biophys J. 2000 Jul;79(1):434-47 PMID: 10866969
  4. Sphingomyelin-cholesterol interactions in biological and model membranes.
    Chem Phys Lipids. 1999 Nov;102(1-2):13-27 PMID: 11001557
  5. Lipid rafts reconstituted in model membranes.
    Biophys J. 2001 Mar;80(3):1417-28 PMID: 11222302
  6. Enzymes of sphingolipid metabolism: from modular to integrative signaling.
    Biochemistry. 2001 Apr 24;40(16):4893-903 PMID: 11305904
  7. Lipid rafts and signal transduction.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9 PMID: 11413487
  8. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10642-7 PMID: 11535814
  9. Seeing is believing: visualization of rafts in model membranes.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10517-8 PMID: 11553797
  10. Condensed complexes and the calorimetry of cholesterol-phospholipid bilayers.
    Biophys J. 2001 Nov;81(5):2774-85 PMID: 11606290
  11. Cholesterol interactions with phospholipids in membranes.
    Prog Lipid Res. 2002 Jan;41(1):66-97 PMID: 11694269
  12. Molecular organization of cholesterol in polyunsaturated membranes: microdomain formation.
    Biophys J. 2002 Jan;82(1 Pt 1):285-98 PMID: 11751316
  13. Fluorescence correlation spectroscopy and its potential for intracellular applications.
    Cell Biochem Biophys. 2001;34(3):383-408 PMID: 11898862
  14. Membrane properties of sphingomyelins.
    FEBS Lett. 2002 Oct 30;531(1):33-7 PMID: 12401199
  15. Role of cholesterol in lipid raft formation: lessons from lipid model systems.
    Biochim Biophys Acta. 2003 Mar 10;1610(2):174-83 PMID: 12648772
  16. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy.
    J Biol Chem. 2003 Jul 25;278(30):28109-15 PMID: 12736276
  17. Liquid-liquid immiscibility in membranes.
    Annu Rev Biophys Biomol Struct. 2003;32:469-92 PMID: 12574063
  18. The function of sterols in membranes.
    Biochim Biophys Acta. 1976 Oct 26;457(2):109-32 PMID: 184844
  19. Phospholipid head-group conformations; intermolecular interactions and cholesterol effects.
    Biochemistry. 1977 Oct 4;16(20):4344-9 PMID: 911759
  20. The affinity of cholesterol for phosphatidylcholine and sphingomyelin.
    Biochim Biophys Acta. 1979 Oct 5;556(3):388-98 PMID: 486469
  21. Cholesterol and the cell membrane.
    Biochim Biophys Acta. 1985 Dec 9;822(3-4):267-87 PMID: 3904832
  22. Factors contributing to the distribution of cholesterol among phospholipid vesicles.
    J Biol Chem. 1986 Jun 25;261(18):8175-81 PMID: 3722148
  23. Phase equilibria in the phosphatidylcholine-cholesterol system.
    Biochim Biophys Acta. 1987 Nov 27;905(1):162-72 PMID: 3676307
  24. Lipid sorting in epithelial cells.
    Biochemistry. 1988 Aug 23;27(17):6197-202 PMID: 3064805
  25. Lipid recycling between the plasma membrane and intracellular compartments: transport and metabolism of fluorescent sphingomyelin analogues in cultured fibroblasts.
    J Cell Biol. 1989 Jun;108(6):2169-81 PMID: 2738091
  26. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry.
    Biochemistry. 1990 Jan 16;29(2):451-64 PMID: 2302384
  27. Partitioning behavior of indocarbocyanine probes between coexisting gel and fluid phases in model membranes.
    Biochim Biophys Acta. 1990 Mar 30;1023(1):25-33 PMID: 2317494
  28. Elastic deformation and failure of lipid bilayer membranes containing cholesterol.
    Biophys J. 1990 Oct;58(4):997-1009 PMID: 2249000
  29. Interaction of cholesterol with various glycerophospholipids and sphingomyelin.
    Biochemistry. 1990 Nov 27;29(47):10670-5 PMID: 2176878
  30. Intracellular transport and metabolism of sphingomyelin.
    Biochim Biophys Acta. 1991 Mar 12;1082(2):113-25 PMID: 2007175
  31. Interaction of cholesterol with synthetic sphingomyelin derivatives in mixed monolayers.
    Biochemistry. 1991 Nov 5;30(44):10746-54 PMID: 1931994
  32. Percolation and diffusion in three-component lipid bilayers: effect of cholesterol on an equimolar mixture of two phosphatidylcholines.
    Biophys J. 1993 Feb;64(2):399-412 PMID: 8457666
  33. Sorting single molecules: application to diagnostics and evolutionary biotechnology.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5740-7 PMID: 7517036
  34. New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry.
    Biochim Biophys Acta. 1995 Mar 8;1234(1):90-8 PMID: 7880863
  35. Cholesterol at different bilayer concentrations can promote or antagonize lateral segregation of phospholipids of differing acyl chain length.
    Biochemistry. 1996 Dec 3;35(48):15198-208 PMID: 8952467
  36. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  37. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes.
    Biochemistry. 1997 Sep 9;36(36):10944-53 PMID: 9283086
  38. Liquid-liquid immiscibility in lipid monolayers.
    Biochim Biophys Acta. 1997 Oct 2;1329(1):7-11 PMID: 9370239
  39. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal.
    J Cell Sci. 1998 Jan;111 ( Pt 1):1-9 PMID: 9394007
  40. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains.
    J Biol Chem. 1998 Jan 9;273(2):1150-7 PMID: 9422781
  41. Does cholesterol discriminate between sphingomyelin and phosphatidylcholine in mixed monolayers containing both phospholipids?
    Chem Phys Lipids. 1996 Jun 17;81(1):69-80 PMID: 9450320
  42. Structure and origin of ordered lipid domains in biological membranes.
    J Membr Biol. 1998 Jul 15;164(2):103-14 PMID: 9662555
  43. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  44. Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length.
    Biophys J. 1999 Feb;76(2):908-15 PMID: 9929492
  45. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy.
    Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8461-6 PMID: 10411897
  46. Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles.
    Biophys J. 1999 Oct;77(4):2090-101 PMID: 10512829
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2003-12-00
Pages
3758-68
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1303678
Subset
IM
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