Lipid rafts have different sizes depending on membrane composition: A time-resolved fluorescence resonance energy transfer study

Journal of Molecular Biology

Volumn 346, Issue 4, 2005, Pages 1109-1120

  De Almeida, Rodrigo F M ^a,b   Loura, Luís M S ^a,c   Fedorov, Alexander ^a   Prieto, Manuel ^a  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c UNIVERSITY OF ÉVORA   (Portugal)

Author keywords

Cholesterol; FRET; Ganglioside GM1; Lipid rafts; Sphingomyelin

Indexed keywords

CHOLERA TOXIN B SUBUNIT; CHOLESTEROL; GANGLIOSIDE GM1; LIPID; PHOSPHATIDYLCHOLINE;

ARTICLE; CELL MEMBRANE; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID ANALYSIS; LIPID RAFT; MEMBRANE STRUCTURE; METHODOLOGY; MOLECULAR MODEL; PRIORITY JOURNAL;

EID: 13544250813     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.12.026     Document Type: Article

References (53)

1. K. Simons, and I. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
2. R. Schroeder, E. London, and D. Brown Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior Proc. Natl Acad. Sci. USA 91 1994 12130 12134
3. E. London, and D.A. Brown Insolubility of lipids in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts) Biochim. Biophys. Acta 1508 2000 182 195
4. M.-C. Giocondi, V. Vié, E. Lesniewska, J.-P. Goudonnet, and C. Le Grimellec In situ imaging of detergent-resistant membranes by atomic force microscopy J. Struct. Biol. 131 2000 38 43
5. J.L. Thomas, D. Howloka, B. Baird, and W.W. Webb Large-scale co-aggregation of fluorescent lipid probes with cell surface proteins J. Cell Biol. 126 1994 795 802
6. C. Zurzolo, G. van Meer, and S. Mayor The order of rafts. Conference on microdomains, lipid rafts and caveolae EMBO Rep. 4 2003 1117 1121
7. A. Pralle, P. Keller, E.-L. Florin, K. Simons, and J.K.H. Hörber Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells J. Cell Biol. 148 2000 997 1007
8. C. Dietrich, L.A. Bagatolli, Z.N. Volovyk, N.L. Thompson, M. Levi, K. Jacobson, and E. Gratton Lipid rafts reconstituted in model membranes Biophys. J. 80 2001 1417 1428
9. C. Dietrich, Z.N. Volovyk, M. Levi, N.L. Thompson, and K. Jacobson Partitioning of Thy-1, GM1 and crossed-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers Proc. Natl Acad. Sci. USA 98 2001 10642 10647
10. H.O. Ribi, D.S. Ludwig, K.L. Mercer, G.K. Schoolnik, and R.D. Kornberg Three-dimensional structure of cholera toxin penetrating a lipid membrane Science 239 1988 1272 1276
11. R.G.W. Anderson, and K. Jacobson A role for lipid shells in targeting proteins to caveolae, rafts and other lipid domains Science 296 2002 1821 1825
12. K. Simons, and W.L.C. Vaz Model systems, lipid rafts and cell membranes Annu. Rev. Biophys. Biomol. Struct. 33 2004 269 295
13. H. Heerklotz, H. Szadkowska, T. Anderson, and J. Seelig The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton J. Mol. Biol. 329 2003 793 799
14. R.F.M. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416
15. S.L. Veatch, and S.L. Keller Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophys. J. 85 2003 3074 3083
16. S.L. Veatch, and S.L. Keller A closer look at the canonical "raft mixture" in model membrane studies Biophys. J. 84 2003 725 726
17. J. Sot, M.I. Collado, J.L.R. Arrondo, A. Alonso, and F.M. Goñi Triton X-100 resistant bilayers: effect of lipid composition and relevance to the raft phenomenon Langmuir 18 2002 2828 2835
18. L. Stryer Fluorescence energy transfer as a spectroscopic ruler Annu. Rev. Biochem. 47 1978 819 846
19. L.M.S. Loura, R.F.M. de Almeida, and M. Prieto Detection and characterization of membrane microheterogeneity by resonance energy transfer J. Fluorescence 11 2001 197 209
20. G.W. Feigenson, and T. Buboltz Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol Biophys. J. 80 2001 2775 2788
21. J.R. Silvius Fluorescence energy transfer reveals microdomain formation at physiological temperatures in lipid mixtures modeling the outer leaflet of the plasma membrane Biophys. J. 85 2003 1034 1045
22. L.M.S. Loura, A. Fedorov, and M. Prieto Membrane probe distribution heterogeneity: a resonance energy transfer study J. Phys. Chem. B 104 2000 6920 6931
23. L.M.S. Loura, A. Fedorov, and M. Prieto Fluid-fluid membrane microheterogeneity: a fluorescence resonance energy transfer study Biophys. J. 80 2001 776 788
24. R.F.M. de Almeida, L.M.S. Loura, A. Fedorov, and M. Prieto Non-equilibrium phenomena in the phase separation of a two-component lipid bilayer Biophys. J. 82 2002 823 834
25. B. Medhage, E. Mukhtar, B. Kalman, L.B.-Å. Johansson, and J.G. Molotkovsky Electronic energy transfer in anisotropic systems. Part 5 - Rhodamine-lipid derivatives in model membranes J. Chem. Soc. Faraday Trans. 88 1992 2845 2851
26. B. Snyder, and E. Freire Fluorescence energy transfer in two dimensions: a numeric solution for random distributions Biophys. J. 40 1982 137 148
27. B. Van der Meer, G. Coker III, and S.-Y.S. Chen Resonance Energy Transfer: Theory and Data 1994 VCH Publishers New York
28. T.P.W. McMullen, R.N.A.H. Lewis, and R.N. McElhaney Cholesterol- phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes Curr. Opin. Colloid Interface Sci. 8 2004 459 468
29. J.R. Silvius, D. del Giudice, and M. Lafleur Cholesterol at different bilayer concentrations can promote or antagonize lateral segregation of phospholipids of differing acyl chain length Biochemistry 35 1996 15198 15208
30. M.S.C. Abreu, M.J. Moreno, and W.L.C. Vaz Kinetics and thermodynamics of association of a phospholipid derivative with lipid bilayers in liquid-disordered and liquid-ordered phases Biophys. J. 87 2004 353 365
31. W.L.C. Vaz, and E. Melo Fluorescence spectroscopic studies on phase heterogeneity in lipid bilayer membranes J. Fluorescence 11 2001 255 271
32. C. Yuan, J. Furlong, P. Burgos, and L.J. Johnston The size of lipid rafts: an atomic force microscopy study of ganglioside GM1 domains in sphingomyelin/DOPC/cholesterol membranes Biophys. J. 82 2002 2526 2535
33. C. Yuan, and L.J. Johnston Atomic force microscopy studies of ganglioside GM1 domains in phosphatidylcholine and phosphatidylcholine/cholesterol bilayers Biophys. J. 81 2001 1059 1069
34. T. Friedrichson, and T.V. Kurzchalia Microdomains of GPI-anchored proteins in living cells revealed by crosslinking Nature 394 1998 802 805
35. R. Varma, and S. Mayor GPI-anchored proteins are organized in submicron domains at the cell surface Nature 394 1998 798 801
36. I.A. Prior, C. Muncke, R.G. Parton, and J.F. Hancock Direct visualization of Ras proteins in spatially distinct cell surface microdomains J. Cell Biol. 160 2003 165 170
37. H. Heerklotz Triton promotes domain formation in lipid raft mixtures Biophys. J. 83 2002 2693 2701
38. E. London Insights into lipid raft structure and formation from experiments in model membranes Curr. Opin. Struct. Biol. 12 2001 480 486
39. T. Fujiwara, K. Ritchie, H. Murakoshi, K. Jacobson, and A. Kusumi ??? J. Cell Biol. 157 2002 1071 1081
40. G. van Meer Lipids of the Golgi membrane Trends Cell Biol. 8 1998 29 33
41. L.M. Contreras, R.F.M. de Almeida, A. Fedorov, J. Villalaín, and M. Prieto Interaction of α-melanocyte stimulating hormone with binary phospholipid membranes: structural changes and relevance of phase behavior Biophys. J. 80 2001 2273 2283
42. L.A. Sklar, B.S. Hudson, and R.D. Simoni Conjugated polyene fatty acids as fluorescent probes: synthetic phospholipid membrane studies Biochemistry 16 1977 819 828
43. L.M.S. Loura, R.F.M. de Almeida, A. Coutinho, and M. Prieto Interaction of peptides with binary phospholipid membranes: application of fluorescence methodologies Chem. Phys. Lipids 122 2003 77 96
44. T.-Y. Wang, and J.R. Silvius Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane Biophys. J. 84 2001 367 378
45. S.N. Ahmed, D.A. Brown, and E. London 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 36 1997 10944 10953
46. C.W.F. McClare An accurate and convenient organic phosphorus assay Anal. Biochem. 39 1971 527 530
47. L.A. Sklar, B.S. Hudson, M. Petersen, and J. Diamond Conjugated polyene fatty acids on fluorescent probes: spectroscopic characterization Biochemistry 16 1977 813 818
48. B.R. Lentz Membrane "fluidity" from fluorescence anisotropy measurements L.M. Loew Spectroscopic Membrane Probes vol. 1 1988 CRC Boca Raton, FL 13 41
49. R.P. Haugland Handbook of Fluorescent Probes, Research Chemicals 6th edit. 1996 Molecular Probes, Inc. Eugene, OR
50. M. Gandhavadi, D. Allende, A. Vidal, S.A. Simon, and T.J. McIntosh Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts Biophys. J. 82 2002 1469 1482
51. S.-W. Chiu, E. Jakobson, S. Subramaniam, and H.L. Scott Combined Monte Carlo and molecular dynamics simulation of fully hydrated dioleoyl and palmitoyl-oleoyl phosphatidylcholine lipid bilayers Biophys. J. 77 1999 2462 2469
52. X.-M. Li, J.M. Smaby, M.M. Momsen, H.L. Brockman, and R.E. Brown Sphingomyelin interfacial behavior: the impact of changing acyl chain composition Biophys. J. 78 2000 1921 1931
53. J.M. Smaby, M.M. Momsen, H.L. Brockman, and R.E. Brown Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol Biophys. J. 73 1997 1492 1505