Lipid rafts as functional heterogeneity in cell membranes

Biochemical Society Transactions

Volumn 37, Issue 5, 2009, Pages 955-960

  Lingwood, Daniel ^a   Kaiser, Hermann Josef ^a   Levental, Ilya ^a   Simons, Kai ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Chemical interaction; Cholesterol; Lateral self organization; Membrane order; Sphingolipid

Indexed keywords

CELL HETEROGENEITY; CELL MEMBRANE; CHEMICAL INTERACTION; CHEMICAL REACTION; CONFERENCE PAPER; HYDROGEN BOND; LIPID ANALYSIS; LIPID COMPOSITION; LIPID RAFT; MOLECULAR DYNAMICS; NANOANALYSIS; PRIORITY JOURNAL;

CELL MEMBRANE; CHOLESTEROL; DETERGENTS; LIPID BILAYERS; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; SPHINGOLIPIDS;

EID: 70350172934     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0370955     Document Type: Conference Paper

References (90)

1. Pike, L.J. (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 46, 1597-1598
2. Hancock, J.F. (2006) Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7, 456-462
3. Lucero, H.A. and Robbins, P.W. (2004) Lipid rafts-protein association and the regulation of protein activity. Arch. Biochem. Biophys. 426, 208-224
4. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
5. Rajendran, L. and Simons, K. (2005) Lipid rafts and membrane dynamics. J. Cell Sci. 116, 1099-1102
6. Simons, K. and van Meer, G. (1988) Lipid sorting in epithelial cells. Biochemistry 27, 6197-6202
7. van Meer, G. and Sprong, H. (2004) Membrane lipids and vesicular traffic. Curr. Opin. Cell Biol. 16, 373-378
8. van Meer, G., Gumbiner, B. and Simons, K. (1986) The tight junction does not allow lipid molecules to diffuse from one epithelial cell to the next. Nature 322, 639-641
9. Klemm, R.W., Ejsing, C.S., Surma, M.A., Kaiser, H.J., Gerl, M.J., Sampaio, J.L., de Robillar, Q., Ferguson, C., Proszynski, T.J., Shevchenko, A. and Simons, K. (2009) Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol., 185, 601-612
10. Karlsson, K.-A. (1977) Aspects on structure and function of sphingolipids in cell surface membranes. In Structure of Biological Membranes (Abrahamsson, S. and Pascher, I., eds), pp. 245-274, Plenum Press, New York
11. Abrahamsson, S., Dahlen, B., Löfgren, H., Pascher, I. and Sundell, S. (1977) Molecular arrangement and conformation of lipids of relavence to membrane structure. in Structure of biological membranes (Abrahamsson, S. and Pascher, I., eds), pp. 1-21, Plenum Press, New York
12. Thompson, T.E. and Tillack, T.W. (1985) Organization of glycosphingolipids in bilayers and plasma membrane of mammalian cells. Annu. Rev. Biophys. Biophys. Chem. 14, 361-386
13. Ipsen, J.H., Karlstrom, G., Mouritsen, O.G., Wennerstrom, H. and Zuckermann, M.J. (1987) Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta 905, 162-172
14. Ipsen, J,H,, Mouritsen, O.G. and Zukermann, M.J. (1989) Theory of thermal anomalies in the specific heat of lipid bilayers containing cholesterol. Biophys. J. 56, 661-667
15. 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 29, 451-464
16. Brown, D.A. and London, E. (1998) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111-136
17. Brown, D.A. and London, E. (1998) Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 15, 103-114
18. Simons, K. and Vaz, W.L. (2004) Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33, 269-295
19. Karnovsky, M.J., Kleinfield, A.M., Hoover, R.L. and Klausner, R.D. (1982) The concept of lipid domains in membranes. J. Cell Biol. 94, 1-6
20. Thompson, T.E., Barenholz, Y., Brown, R.E., Correa-Freire, M., Young, W.W. and Tillack, T.W. (1986) Molecular organization of glycosphingolipids in phosphatidylcholine bilayers and biological membranes. in Enzymes of Lipid Metabolism II (Freysz, L., Dreyfus, H., Massarelli, H. and Gatt, S., eds), pp. 387-396, Plenum Press, New York
21. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39
22. Brown, D.A. and Rose, K.J. (1992) Sorting of GPI-anchored proteins to glycolipid enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
23. Schroeder, R., London, E. and Brown, D. (1994) 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. U.S.A. 91, 12130-12134
24. Brown, D.A. (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21, 430-439
25. Lingwood, D. and Simons, K. (2007) Detergent resistance as a tool in membrane research. Nat. Protoc. 2, 2159-2165
26. lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. U.S.A. 92, 9201-9205
27. Montixi, C., Langlet, C., Bernard, A.M., Thimonier, J., Dubois, C., Wurbel, M.A., Chauvin, J.P., Pierres, M. and He, H.T. (1998) Engagement of T-cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17, 5334-5348
28. Simons, K. and and Ehehalt, R. (2002) Cholesterol, lipid rafts and disease. J. Clin. Invest. 110, 597-603
29. Harder, T., Scheiffele, P., Verkade, P. and Simons, K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942
30. Janes, P.W., Ley, S.C. and Magee, A.I. (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461
31. Harder, T. and Simons, K. (1999) Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur. J. Immunol. 29, 556-562
32. Rajendran, L., Masilamani, M., Solomon, S., Tikkanen, R., Stuermer, C.A., Plattner, H. and Illges, H. (2003) Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells. Proc. Natl. Acad. Sci. U.S.A. 100, 8241-8246
33. Prior, I.A., Muncke, C., Parton, R.G. and Hancock, J.F. (2003) Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160, 165-170
34. Gri, G., Molon, B., Manes, S., Pozzan, T. and Viola, A. (2004) The inner side of T cell lipid rafts. Immunol. Lett. 94, 247-252
35. Eisenberg, S., Shvartsman, D.E., Ehrlich, M. and Henis, Y.I. (2006) Clustering of raft-associated proteins in the external membrane leaflet modulates internal leaflet H-Ras diffusion and signaling. Mol. Cell. Biol. 26, 7190-7200
36. Mayor, S. and Pagano, R.E. (2007) Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612
37. Harder, T. and Engelhardt, K.R. (2004) Membrane domains in lymphocytes: from lipid rafts to protein scaffolds. Traffic 5, 265-275
38. Zech, T., Ejsing, C.S., Gaus, K., de Wet, B., Shevchenko, A., Simons, K. and Harder, T. (2009) Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signaling. EMBO J. 28, 466-476
39. Lai, E. (2003) Lipid rafts make for slippery platforms. J. Cell Biol. 162, 365-370
40. Kusumi, A. and Suzuki, K. (2005) Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim. Biophys. Acta 1746, 234-251
41. α for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol. 177, 717-730
42. 2+ signaling: single molecule tracking study 2. J. Cell Biol. 177, 731-742
43. Drbal, K., Moertelmaier, M., Holzhauser, C., Muhammad, A., Fuertbauer, E., Howorka, S., Hinterberger, M., Stockinger, H. and Schutz, G.J. (2007) Single-molecule microscopy reveals heterogeneous dynamics of lipid raft components upon TCR engagement. Int. Immunol. 19, 675-684
44. Lenne, P.F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.J., Rigneault, H., He, H.T. and Marguet, D. (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25, 3245-3256
45. Wenger, J., Conchonaud, F., Dintinger, J., Wawrezinieck, L., Ebbesen, T.W., Rigneault, H., Marguet, D. and Lenne, P.F. (2007) Diffusion analysis within single nanometric apertures reveals the ultrafine cell membrane organization. Biophys. J. 92, 913-919
46. Lasserre, R., Guo, X.J., Conchonaud, F., Hamon, Y., Hawchar, O., Bernard, A.M., Soudja, S.M., Lenne, P.F., Rigneault, H., Olive, D. et al. (2008) Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat. Chem. Biol. 4, 538-547
47. Varma, R. and Mayor, S. (2004) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801
48. Sharma, P., Varma, R., Sarasij, R.C., Ira, Gousset, K., Krishnamoorthy, G., Rao, M. and Mayor, S. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577-589
49. Rao, M. and Mayor, S. (2005) Use of Forster's resonance energy transfer microscopy to study lipid rafts. Biochim. Biophys. Acta 1746, 221-233
50. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., Belov, V.N., Hein, B., von Middendorff, C., Schönle, A. and Hell, S.W. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457, 1159-1162
51. Goswami, D, Gowrishankar, K., Bilgrami, S., Ghosh, S., Raghupathy, R., Chadda, R., Vishwakarma, R., Rao, M. and Mayor, S. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135, 1085-1097
52. Ahmed, S.N., Brown, D.A. and London, E. (1997) 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 39, 10944-10953
53. Brown, R.E. (1998) Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 111, 1-9
54. Patra, S.K., Alonso, A., Arrondo, J. and Goñi i, F. (1999) Liposomes containing sphingomyelin and cholesterol: detergent solubilization and infrared spectroscopic studies. J. Liposome Res. 9, 247-260
55. London, E. and Brown, D.A. (2000) Insolubility of lipids in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta 1508, 182-195
56. Veiga, M.P., Arrondo, J.L., Goni, F.M., Alonso, A. and Marsh, D. (2001) Interaction of cholesterol with sphingomyelin in mixed membranes containing phosphatidylcholine, studied by spin-label ESR and IR spectroscopies: a possible stablization of gel-phase sphingolipid domains by cholesterol. Biochemistry 29, 451-464
57. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C. and London, E. (2001) Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts): comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 276, 33540-33546
58. Edidin, M. (2003) The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32, 257-283
59. Baumgart, T., Hess, S.T. and Webb, W.W. (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821-824
60. Veatch, S.L. and Keller, S.L. (2003) Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85, 3074-3083
61. Niemelä, P.S., Hyvönen, M.T. and Vattulainen, I. (2009) Atom-scale molecular interactions in lipid raft mixtures. Biochim. Biophys. Acta 1788, 122-135
62. Feigenson, G.W. (2009) Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures. Biochim. Biophys. Acta 1788, 47-52
63. Veatch, S.L., Soubias, O., Keller, S.L. and Gawrisch, K. (2007) Critical fluctuations in domain-forming lipid mixtures. Proc. Natl. Acad. Sci. U.S.A. 104, 17650-17655
64. Honerkamp-Smith, A.R., Veatch, S.L. and Keller, S.L. (2009) An introduction to critical points for biophysicists; observations of compositional heterogeneity in lipid membranes. Biochim. Biophys. Acta 1788, 53-63
65. Almeida, P.F., Pokorny, A. and Hinderliter, A. (2005) Thermodynamics of membrane domains. Biochim. Biophys. Acta 1720, 1-13
66. Risselada, H.J. and Marrink, S.J. (2008) The molecular face of lipid rafts in model membranes. Proc. Natl. Acad. Sci. U.S.A. 105, 17367-17372
67. Baumgart, T., Hammond, A.T., Sengupta, P., Hess, S.T., Holowka, D.A., Baird, B.A. and Webb, W.W. (2007) Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc. Natl. Acad. Sci. U.S.A. 104, 3165-3170
68. Veatch, S.L., Cicuta, P., Sengupta, P., Honerkamp-Smith, A., Holowka, D. and Baird, B. (2008) Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 3, 287-293
69. Meder, D. and Simons, K. (2006) Lipid rafts, caveolae and membrane traffic. in Lipid Rafts and Caveolae: from Membrane Biophysics to Cell Biology (Fielding, C.J., ed.), pp. 1-23, Wiley-Vgh, Wienheim
70. Schuck, S. and Simons, K. (2004) Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117, 5955-5964
71. Hammond, A.T., Heberle, F.A., Baumgart, T., Holowka, D., Baird, B. and Feigenson, G.W. (2005) Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc. Natl. Acad. Sci. U.S.A. 102, 6320-6325
72. de Planque, M.R. and Killian, J.A. (2003) Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 20, 271-284
73. Shogomori, H., Hammond, A.T., Ostermeyer-Fay, A.G., Barr, D.J., Feigenson, G.W., London, E. and Brown, D.A. (2005) Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells. J. Biol. Chem. 280, 18931-18942
74. Kalvodova, L., Kahya, N., Schwille, P., Ehehalt, R., Verkade, P., Drechsel, D. and Simons, K. (2005) Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids and anionic phospholipids in vitro. J. Biol. Chem. 280, 36815-36823
75. Sengupta, P., Hammond, A.T., Holowka, D. and Baird, B. (2008) Structural determinants for partitioning of lipids and proteins between coexisting fluid phases in giant plasma membrane vesicles. Biochim. Biophys. Acta 1778, 20-32
76. Lingwood, D., Ries, J., Schwille, P. and Simons, K. (2008) Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. U.S.A. 105, 10005-10010
77. Kaiser, H.-J., Lingwood, D., Levental, I., Sampaio, J., Kalvodova, L., Rajendran, L. and Simons, K. (2009) Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. U.S.A., in the press
78. Dupuy, A.D. and Engelman, D.M. (2008) Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 105, 2848-2852
79. Engelman, D.M. (2005) Membranes are more mosaic than fluid. Nature 438, 578-580
80. Mouritsen, O.G. and Bloom, M. (1993) Models of lipid-protein interactions in membranes. Annu. Rev. Biophys. Biomol. Struct. 22, 145-171
81. Mitra, K., Ubarretxena-Belandia, I., Taguchi, T., Warren, G. and Engelman, D.M. (2004) Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl. Acad. Sci. U.S.A. 101, 4083-4088
82. Ryan, T.A., Meyers, J., Holowka, D., Baird, B. and Webb, W.W. (1988) Molecular crowding on the cell surface. Science 239, 61-64
83. Marsh, D. and Horváth, L.I. (1998) Structure, dynamics and composition of the lipid-protein interface: perspectives from spin-labelling. Biochim. Biophys. Acta 1376, 267-296
84. Belrhali, H., Nollert, P., Royant, A., Menzel, C., Rosenbusch, J.P., Landau, E.M. and Pebay-Peyroula, E. (1999) Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution. Structure 7, 909-917
85. Lee, A.G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta 1612, 1-40
86. Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sugimura, T., Kurono, S., Tsujimoto, K. et al. (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26, 1713-1725
87. 2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
88. 2-adrenergic receptor. Structure 16, 897-905
89. Wenz, T., Hielscher, R., Hellwig, P., Schägger, H., Richers, S. and Hunte, C. (2009) Role of phospholipids in respiratory cytochrome bc1 complex catalysis and supercomplex formation. Biochim. Biophys. Acta 1787, 609-616
90. Anderson, R.G. and and Jacobson, K. (2002) A role for lipid shells in targeting proteins to caveolae, rafts and other lipid domains. Science 296, 1821-1825