Lipid Rafts: Elusive or Illusive?

Cell

Volumn 115, Issue 4, 2003, Pages 377-388

  Munro, Sean ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD59 ANTIGEN; CHOLESTEROL; DECAY ACCELERATING FACTOR; GLYCEROPHOSPHOLIPID; LIPID; PROTEIN; SPHINGOMYELIN;

BASOLATERAL MEMBRANE; BILAYER MEMBRANE; CELL MEMBRANE; CELL PROTECTION; CELLULAR DISTRIBUTION; CHOLESTEROL SYNTHESIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENERGY TRANSFER; GELATION; HEMOLYSIS; HYDROGEN BOND; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; MEMBRANE PERMEABILITY; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSPORT VESICLE;

EID: 0344585437     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00882-1     Document Type: Review

References (118)

1. Aman A.T., Fraser S., Merritt E.A., Rodigherio C., Kenny M., Ahn M., Hol W.G., Williams N.A., Lencer W.I., Hirst T.R. A mutant cholera toxin B subunit that binds GM1-ganglioside but lacks immunomodulatory or toxic activity. Proc. Natl. Acad. Sci. USA. 98:2001;8536-8541.
2. Anderson R.G., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 296:2002;1821-1825.
3. Balasubramanian K., Schroit A.J. Aminophospholipid asymmetry. a matter of life and death Annu. Rev. Physiol. 65:2003;701-734.
4. Bretscher M.S. Membrane structure. some general principles Science. 181:1973;622-629.
5. Bretscher M.S., Munro S. Cholesterol and the Golgi apparatus. Science. 261:1993;1280-1281.
6. Bromley S.K., Burack W.R., Johnson K.G., Somersalo K., Sims T.N., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse. Annu. Rev. Immunol. 19:2001;375-396.
7. Brown D. The tyrosine kinase connection. how GPI-anchored proteins activate T cells Curr. Opin. Immunol. 5:1993;349-354.
8. Brown R.E. Sphingolipid organization in biomembranes. what physical studies of model membranes reveal J. Cell Sci. 111:1998;1-9.
9. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:1992;533-544.
10. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:1998;111-136.
11. Bunnell S.C., Hong D.I., Kardon J.R., Yamazaki T., McGlade C.J., Barr V.A., Samelson L.E. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:2002;1263-1275.
12. Chan P.Y., Lawrence M.B., Dustin M.L., Ferguson L.M., Golan D.E., Springer T.A. Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2. J. Cell Biol. 115:1991;245-255.
13. Chen C.S., Martin O.C., Pagano R.E. Changes in the spectral properties of a plasma membrane lipid analog during the first seconds of endocytosis in living cells. Biophys. J. 72:1997;37-50.
14. + influx and efflux following depletion of membrane sterol in L-cells. J. Biol. Chem. 253:1978;3180-3185.
15. Chiu V.K., Bivona T., Hach A., Sajous J.B., Silletti J., Wiener H., Johnson R.L. 2nd, Cox A.D., Philips M.R. Ras signalling on the endoplasmic reticulum and the Golgi. Nat. Cell Biol. 4:2002;343-350.
16. Coetzee T., Suzuki K., Popko B. New perspectives on the function of myelin galactolipids. Trends Neurosci. 21:1998;126-130.
17. Demel R.A., Kinsky S.C., Kinsky C.B., van Deenen L.L. Effects of temperature and cholesterol on the glucose permeability of liposomes prepared with natural and synthetic lecithins. Biochim. Biophys. Acta. 150:1968;655-665.
18. Dietrich C., Bagatolli L.A., Volovyk Z.N., Thompson N.L., Levi M., Jacobson K., Gratton E. Lipid rafts reconstituted in model membranes. Biophys. J. 80:2001;1417-1428. a.
19. Dietrich C., Volovyk Z.N., Levi M., Thompson N.L., Jacobson K. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proc. Natl. Acad. Sci. USA. 98:2001;10642-10647. b.
20. Dietrich C., Yang B., Fujiwara T., Kusumi A., Jacobson K. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82:2002;274-284.
21. Edidin M. Patches and fences. probing for plasma membrane domains J. Cell Sci. Suppl. 17:1993;165-169.
22. Edidin M. The state of lipid rafts. from model membranes to cells Annu. Rev. Biophys. Biomol. Struct. 32:2003;257-283.
23. Ehehalt R., Keller P., Haass C., Thiele C., Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160:2003;113-123.
24. Ferguson M.A. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J. Cell Sci. 112:1999;2799-2809.
25. Finkelstein A. Water and nonelectrolyte permeability of lipid bilayer membranes. J. Gen. Physiol. 68:1976;127-135.
26. Finkelstein A., Cass A. Effect of cholesterol on the water permeability of thin lipid membranes. Nature. 216:1967;717-718.
27. Foster L.J., De Hoog C.L., Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA. 100:2003;5813-5818.
28. Fujiwara T., Ritchie K., Murakoshi H., Jacobson K., Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157:2002;1071-1081.
29. Gaber R.F., Copple D.M., Kennedy B.K., Vidal M., Bard M. The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol. Cell. Biol. 9:1989;3447-3456.
30. Gheber L.A., Edidin M. A model for membrane patchiness. lateral diffusion in the presence of barriers and vesicle traffic Biophys. J. 77:1999;3163-3175.
31. Grunze M., Deuticke B. Changes of membrane permeability due to extensive cholesterol depletion in mammalian erythrocytes. Biochim. Biophys. Acta. 356:1974;125-130.
32. Haines T.H. Do sterols reduce proton and sodium leaks through lipid bilayers? Prog. Lipid Res. 40:2001;299-324.
33. Hao M., Mukherjee S., Maxfield F.R. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc. Natl. Acad. Sci. USA. 98:2001;13072-13077.
34. Hao M., Lin S.X., Karylowski O.J., Wustner D., McGraw T.E., Maxfield F.R. Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J. Biol. Chem. 277:2002;609-617.
35. Harder T., Kuhn M. Selective accumulation of raft-associated membrane protein LAT in T cell receptor signaling assemblies. J. Cell Biol. 151:2000;199-208.
36. Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:1998;929-942.
37. Harris T.J., Siu C.H. Reciprocal raft-receptor interactions and the assembly of adhesion complexes. Bioessays. 24:2002;996-1003.
38. Hartgroves L.C., Lin J., Langen H., Zech T., Weiss A., Harder T. Synergistic assembly of linker for activation of T cells signaling protein complexes in T cell plasma membrane domains. J. Biol. Chem. 278:2003;20389- 20394.
39. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83:2002;2693-2701.
40. Holthuis J.C., Pomorski T., Raggers R.J., Sprong H., Van Meer G. The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81:2001;1689-1723.
41. Ipsen J.H., Karlstrom G., Mouritsen O.G., Wennerstrom H., Zuckermann M.J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta. 905:1987;162-172.
42. Jacobson K., Hou Y., Derzko Z., Wojcieszyn J., Organisciak D. Lipid lateral diffusion in the surface membrane of cells and in multibilayers formed from plasma membrane lipids. Biochemistry. 20:1981;5268-5275.
43. Jain M.K., White H.B. 3rd. Long-range order in biomembranes. Adv. Lipid Res. 15:1977;1-60.
44. Janes P.W., Ley S.C., Magee A.I. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:1999;447-461.
45. Kahya N., Scherfeld D., Bacia K., Poolman B., Schwille P. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 278:2003;28109-28115.
46. Karnovsky M.J., Kleinfeld A.M., Hoover R.L., Klausner R.D. The concept of lipid domains in membranes. J. Cell Biol. 94:1982;1-6.
47. Keller P., Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140:1998;1357-1367.
48. Kenworthy A. Peering inside lipid rafts and caveolae. Trends Biochem. Sci. 27:2002;435-437.
49. Kenworthy A.K., Edidin M. Distribution of a glycosylphosphatidylinositol- anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer. J. Cell Biol. 142:1998;69-84.
50. Kenworthy A.K., Petranova N., Edidin M. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol. Biol. Cell. 11:2000;1645-1655.
51. Kovbasnjuk O., Edidin M., Donowitz M. Role of lipid rafts in Shiga toxin 1 interaction with the apical surface of Caco-2 cells. J. Cell Sci. 114:2001;4025-4031.
52. Krylov A.V., Pohl P., Zeidel M.L., Hill W.G. Water permeability of asymmetric planar lipid bilayers. leaflets of different composition offer independent and additive resistances to permeation J. Gen. Physiol. 118:2001;333-340.
53. Kurzchalia T.V., Ward S. Why do worms need cholesterol? Nat. Cell Biol. 5:2003;684-688.
54. Lange Y., Swaisgood M.H., Ramos B.V., Steck T.L. Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J. Biol. Chem. 264:1989;3786-3793.
55. Launikonis B.S., Stephenson D.G. Effects of membrane cholesterol manipulation on excitation-contraction coupling in skeletal muscle of the toad. J. Physiol. 534:2001;71-85.
56. Le Grimellec C., Friedlander G., el Yandouzi E.H., Zlatkine P., Giocondi M.C. Membrane fluidity and transport properties in epithelia. Kidney Int. 42:1992;825-836.
57. le Maire M., Champeil P., Moller J.V. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim. Biophys. Acta. 1508:2000;86-111.
58. Levine T.P., Wiggins C.A., Munro S. Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Mol. Biol. Cell. 11:2000;2267-2281.
59. Li X.M., Momsen M.M., Smaby J.M., Brockman H.L., Brown R.E. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins. Biochemistry. 40:2001;5954-5963.
60. Luzzatto L., Bessler M., Rotoli B. Somatic mutations in paroxysmal nocturnal hemoglobinuria. a blessing in disguise? Cell. 88:1997;1-4.
61. Mayor S., Maxfield F.R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell. 6:1995;929-944.
62. Mayor S., Rothberg K.G., Maxfield F.R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264:1994;1948-1951.
63. McConnell H.M., Vrljic M. Liquid-liquid immiscibility in membranes. Annu. Rev. Biophys. Biomol. Struct. 32:2003;469-492.
64. McIntosh T.J., Simon S.A., Needham D., Huang C.H. Structure and cohesive properties of sphingomyelin/cholesterol bilayers. Biochemistry. 31:1992;2012-2020.
65. Merritt E.A., Sarfaty S., van den Akker F., L'Hoir C., Martial J.A., Hol W.G. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 3:1994;166-175.
66. Miller R.G. The use and abuse of filipin to localize cholesterol in membranes. Cell Biol. Int. Rep. 8:1984;519-535.
67. Montixi C., Langlet C., Bernard A.M., Thimonier J., Dubois C., Wurbel M.A., Chauvin J.P., Pierres M., He H.T. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:1998;5334-5348.
68. Mukherjee S., Zha X., Tabas I., Maxfield F.R. Cholesterol distribution in living cells. fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog Biophys. J. 75:1998;1915-1925.
69. Mukherjee S., Soe T.T., Maxfield F.R. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol. 144:1999;1271-1284.
70. Muller P., Herrmann A. Rapid transbilayer movement of spin-labeled steroids in human erythrocytes and in liposomes. Biophys. J. 82:2002;1418-1428.
71. Naslavsky N., Stein R., Yanai A., Friedlander G., Taraboulos A. Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272:1997;6324-6331.
72. Nichols B.J. Caveosomes and lipid raft based endocytosis. J. Cell Sci. 116:2003;4707-4714.
73. Nichols B.J., Kenworthy A.K., Polishchuk R.S., Lodge R., Roberts T.H., Hirschberg K., Phair R.D., Lippincott-Schwartz J. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:2001;529-541.
74. Niv H., Gutman O., Kloog Y., Henis Y.I. Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells. J. Cell Biol. 157:2002;865-872.
75. Ohvo-Rekila H., Ramstedt B., Leppimaki P., Slotte J.P. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41:2002;66-97.
76. Owicki J.C., McConnell H.M. Lateral diffusion in inhomogeneous membranes. Model membranes containing cholesterol. Biophys. J. 30:1980;383-397.
77. Paratcha G., Ibanez C.F. Lipid rafts and the control of neurotrophic factor signaling in the nervous system. variations on a theme Curr. Opin. Neurobiol. 12:2002;542-549.
78. Pizzo P., Viola A. Lymphocyte lipid rafts. structure and function Curr. Opin. Immunol. 15:2003;255-260.
79. Pizzo P., Giurisato E., Tassi M., Benedetti A., Pozzan T., Viola A. Lipid rafts and T cell receptor signaling. a critical re-evaluation Eur. J. Immunol. 32:2002;3082-3091.
80. Pralle A., Keller P., Florin E.L., Simons K., Horber J.K. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:2000;997-1008.
81. Prior I.A., Muncke C., Parton R.G., Hancock J.F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160:2003;165-170.
82. Ramstedt B., Slotte J.P. Membrane properties of sphingomyelins. FEBS Lett. 531:2002;33-37.
83. Rietveld A., Simons K. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta. 1376:1998;467-479.
84. Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E., Rolls B., Hancock J.F., Parton R.G. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1:1999;98-105.
85. Sankaram M.B., Thompson T.E. Interaction of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry. 29:1990;10670-10675.
86. Schmidt C.F., Barenholz Y., Huang C., Thompson T.E. Monolayer coupling in sphingomyelin bilayer systems. Nature. 271:1978;775-777.
87. Schmidt K., Schrader M., Kern H.F., Kleene R. Regulated apical secretion of zymogens in rat pancreas. Involvement of the glycosylphosphatidylinositol- anchored glycoprotein GP-2, the lectin ZG16p, and cholesterol-glycosphingolipid- enriched microdomains. J. Biol. Chem. 276:2001;14315-14323.
88. Schroeder R., London E., Brown D. 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.
89. Schroeder R.J., Ahmed S.N., Zhu Y., London E., Brown D.A. 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. 273:1998;1150-1157.
90. Sharma D.K., Choudhury A., Singh R.D., Wheatley C.L., Marks D.L., Pagano R.E. Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem. 278:2003;7564-7572.
91. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
92. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry. 27:1988;6197-6202.
93. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:2000;31-39.
94. Smith L.M., Rubenstein J.L., Parce J.W., McConnell H.M. Lateral diffusion of M-13 coat protein in mixtures of phosphatidylcholine and cholesterol. Biochemistry. 19:1980;5907-5911.
95. Sotomayor C.P., Aguilar L.F., Cuevas F.J., Helms M.K., Jameson D.M. Modulation of pig kidney Na+/K+-ATPase activity by cholesterol. role of hydration Biochemistry. 39:2000;10928-10935.
96. Sprong H., van der Sluijs P., van Meer G. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2:2001;504-513.
97. Steck T.L., Ye J., Lange Y. Probing red cell membrane cholesterol movement with cyclodextrin. Biophys. J. 83:2002;2118-2125.
98. Stoffel W., Bosio A. Myelin glycolipids and their functions. Curr. Opin. Neurobiol. 7:1997;654-661.
99. Subczynski W.K., Kusumi A. Dynamics of raft molecules in the cell and artificial membranes. approaches by pulse EPR spin labeling and single molecule optical microscopy Biochim. Biophys. Acta. 1610:2003;231-243.
100. Suomalainen M. Lipid rafts and assembly of enveloped viruses. Traffic. 3:2002;705-709.
101. Thewalt J., Bloom M. Phosphatidylcholine. cholesterol phase diagrams Biophys. J. 63:1992;1176-1181.
102. Thompson T.E., Tillack T.W. Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu. Rev. Biophys. Biophys. Chem. 14:1985;361-386.
103. Tsui-Pierchala B.A., Encinas M., Milbrandt J., Johnson E.M. Jr. Lipid rafts in neuronal signaling and function. Trends Neurosci. 25:2002;412-417.
104. Tsuji A., Kawasaki K., Ohnishi S., Merkle H., Kusumi A. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork. Biochemistry. 27:1988;7447-7452.
105. Uesaka Y., Otsuka Y., Lin Z., Yamasaki S., Yamaoka J., Kurazono H., Takeda Y. Simple method of purification of Escherichia coli heat-labile enterotoxin and cholera toxin using immobilized galactose. Microb. Pathog. 16:1994;71-76.
106. Valdez-Taubas J., Pelham H.R. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr. Biol. 13:2003;1636-1640.
107. van Meer G. Lipids of the Golgi membrane. Trends Cell Biol. 8:1998;29-33.
108. van Meer G. Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5:1989;247-275.
109. Varma R., Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:1998;798-801.
110. 2H nuclear magnetic resonance and differential scanning calorimetry Biochemistry. 29:1990;451-464.
111. Vrljic M., Nishimura S.Y., Brasselet S., Moerner W.E., McConnell H.M. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83:2002;2681-2692.
112. Wang T.Y., Silvius J.R. Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane. Biophys. J. 81:2001;2762-2773.
113. Weimbs T., Low S.H., Chapin S.J., Mostov K.E. Apical targeting in polarized epithelial cells. there's more afloat than rafts Trends Cell Biol. 7:1997;393-399.
114. Xiang T.X., Anderson B.D. Phase structures of binary lipid bilayers as revealed by permeability of small molecules. Biochim. Biophys. Acta. 1370:1998;64-76.
115. Yeagle P.L. Cholesterol and the cell membrane. Biochim. Biophys. Acta. 822:1985;267-287.
116. Yu J., Fischman D.A., Steck T.L. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J. Supramol. Struct. 1:1973;233-248.
117. Zacharias D.A., Violin J.D., Newton A.C., Tsien R.Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:2002;913-916.
118. Zhang W., Trible R.P., Samelson L.E. LAT palmitoylation. its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation Immunity. 9:1998;239-246.