Lipid rafts, fluid/fluid phase separation, and their relevance to plasma membrane structure and function

Seminars in Cell and Developmental Biology

Volumn 18, Issue 5, 2007, Pages 583-590

  Sengupta, Prabuddha ^a   Baird, Barbara ^a   Holowka, David ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Cholesterol; IgE receptors; Lipid probes; Liquid ordered; Mast cells

Indexed keywords

ARTIFICIAL MEMBRANE; CELL ACTIVATION; CELL HETEROGENEITY; CELL MEMBRANE; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID RAFT; MEMBRANE STRUCTURE; MEMBRANE VESICLE; NONHUMAN; PHASE SEPARATION; REVIEW;

EID: 35649010379     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2007.07.010     Document Type: Review

References (72)

1. Jain M.K. Introduction to biological membranes (1988), John Wiley & Sons, New York
2. Singer S.J., and Nicholson G.L. The fluid mosaic model of the structure of cell membrane. Science 175 (1972) 720-731
3. Simons K., and Ikonen E. Functional rafts in cell membrane. Nature 387 (1997) 569-572
4. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1 (2000) 31-39
5. Brown D.A., and London E. Structure and function of sphingolipid and cholesterol-rich membrane rafts. J Biol Chem 275 (2000) 17221-17224
6. Silvius J.R. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim Biophys Acta 1610 (2001) 174-183
7. Edidin M. The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32 (2003) 257-283
8. Simons K., and Vaz W.L. Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33 (2004) 351-378
9. Pierce S.K. Lipid rafts and B-cell activation. Nat Rev Immunol 2 (2002) 96-105
10. Holowka D., Gosse J.A., Hammond A.T., Han X., Sengupta P., Smith N.L., et al. Lipid segregation and IgE receptor signaling: a decade of progress. Biochim Biophys Acta 1746 (2005) 252-259
11. Kabouridis P.S. Lipid rafts in T cell receptor signaling. Mol Membr Biol 23 (2006) 49-57
12. Parton R.G., and Richards A.A. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4 (2003) 724-738
13. Salaun C., James D.J., and Chamberlain L.H. Lipid rafts and the regulation of exocytosis. Traffic 5 (2004) 255-264
14. Manes S., and Viola A. Lipid rafts in lymphocyte activation and migration. Mol Membr Biol 23 (2006) 59-69
15. Manes S., del Real G., and Martinez-A C. Pathogens: raft hijackers. Nat Rev Immunol 3 (2003) 557-568
16. Lafont F., and van der Goot F.G. Bacterial invasion via lipid rafts. Cell Microbiol 7 (2005) 613-620
17. Korlach J., Schwille P., Webb W.W., and Feigenson G.W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc Natl Acad Sci USA 96 (1999) 8461-8466
18. De Almeida R.F., Fedorov A., and Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys J 85 (2003) 2406-2416
19. Veatch S.L., and Keller S.L. Seeing spots: complex phase behavior in simple membranes. Biochim Biophys Acta 1746 (2005) 172-185
20. Dietrich C., Volovyk Z.N., Levi M., Thompson N.L., and 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
21. Dietrich C., Bagatolli L.A., Volovyk Z.N., Thompson N.L., Levi M., Jacobson K., et al. Lipid rafts reconstituted in model membranes. Biophys J 80 (2001) 1417-1428
22. Samsonov A.V., Mihalyov I., and Cohen F.S. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys J 81 (2001) 1486-1500
23. Hammond A.T., Heberle F.A., Baumgart T., Holowka D., Baird B., and Feigenson G.W. Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc Natl Acad Sci USA 102 (2004) 6320-6325
24. Silvius J.R. 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
25. Elliott R., Szleifer I., and Schick M. Phase diagram of a ternary mixture of cholesterol and saturated and unsaturated lipids calculated from a microscopic model. Phys Rev Lett 96 (2006) 98-101
26. Huang J., and Feigenson G.W. A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J 76 (1999) 2142-2157
27. McConnell H.M., and Radhakrishnan A. Condensed complexes of cholesterol and phospholipids. Biochim Biophys Acta 1610 (2003) 159-173
28. McConnell H.M., and Vrljic M. Liquid-liquid immiscibility in membranes. Annu Rev Biophys Biomol Struct 32 (2003) 469-492
29. Pandit S.A., Jacobsson E., and Scott H.L. Simulation of the early stages of nano-domain formation in mixed bilayers of sphingomyelin, cholesterol, and dioleylphosphatidylcholine. Biophys J 87 (2004) 3312-3322
30. De Almeida R.F., Loura L.M., Fedorov A., and Prieto M. Lipid rafts have different sizes depending on membrane composition: a time-resolved fluorescence resonance energy transfer study. J Mol Biol 346 (2005) 1109-1120
31. Brown D.A., and 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
32. Schroeder R., London E., and 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
33. Ahmed S.N., Brown D.A., and London E. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. Biochemistry 36 (1997) 10944-10953
34. Brown D.A., and London E. Structure and origin of ordered lipid domains in biological membranes. J Membr Biol 164 (1998) 103-114
35. Fridriksson E.K., Shipkova P.A., Sheets E.D., Holowka D., Baird B., and McLafferty F.W. Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry 38 (1999) 8056-8063
36. Gidwani A., Holowka D., and Baird B. Fluorescence anisotropy measurements of lipid order in plasma membranes and lipid rafts from RBL-2H3 mast cells. Biochemistry 40 (2001) 12422-12429
37. Ge M., Gidwani A., Brown H.A., Holowka D., Baird B., and Freed J.H. Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells: an ESR study. Biophys J 85 (2003) 1278-1288
38. Keller P., and Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J Cell Biol 140 (1998) 1357-1367
39. Sheets E.D., Holowka D., and Baird B. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcεRI and their association with detergent-resistant membranes. J Cell Biol 145 (1999) 877-887
40. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys J 83 (2002) 2693-2701
41. Heerklotz H., Szadkowska H., Anderson T., and Seelig J. The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton. J Mol Biol 329 (2003) 793-799
42. Kwik J., Boyle S., Fooksman D., Margolis L., Sheetz M.P., and Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100 (2003) 13964-13969
43. Pichler H., and Riezman H. Where sterols are required for endocytosis. Biochim Biophys Acta 1666 (2004) 51-61
44. Baumgart T., Hammond A., Sengupta P., Hess S., Holowka D., Baird B., et al. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci USA 104 (2007) 3165-3170
45. Turner M.S., Sens P., and Socci N.D. Nonequilibrium raftlike membrane domains under continuous recycling. Phys Rev Lett 95 (2005) 1683-1701
46. Sharma P., Verma R., Sarasji R.C., Ira K., Gousset G., Krishnamoorthy M., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116 (2004) 577-589
47. Prior I.A., Muncke C., Parton R.G., and Hancock J.F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 160 (2003) 165-170
48. Plowman S.J., Muncke C., Parton R.G., and Hancock J.F. H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci USA 102 (2005) 15500-15505
49. Swamy M.J., Ciani L., Ge M., Holowka D., Baird B., and Freed J.H. Coexisting domains in the plasma membranes of live cells characterized by spin-label ESR spectroscopy. Biophys J 90 (2006) 4452-4465
50. Mayor S., and Maxfield F.R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol Biol Cell 6 (1995) 929-944
51. Hao M., Mukherjee S., and Maxfield F.R. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc Natl Acad Sci USA 98 (2001) 13072-13077
52. Sengupta P., Holowka D., and Baird B. Fluorescence Resonance Energy Transfer between Lipid Probes Detects Nanoscopic Heterogeneity in the Plasma Membrane of Live Cells. Biophys J 92 (2007) 3564-3574
53. Subczynski W.K., and 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
54. Pralle A., Keller P., Florin E.L., Simons K., and Horber J.K. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148 (2000) 997-1008
55. Sheets E.D., Lee G.M., Simson R., and Jacobson K. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry 36 (1997) 12449-12458
56. Dietrich C., Yang B., Fujiwara T., Kusumi A., and Jacobson K. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys J 82 (2002) 274-282
57. Ritchie K., Ino R., Fujiwara T., Murase K., and Kusumi A. The fence and picket structure of the plasma membrane of live cells as revealed by single molecule techniques. Mol Membr Biol 5 (2003) 626-632
58. Kusumi A., Nakada C., Ritchie K., Murase K., Suzuki K., Murakoshi H., et al. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34 (2005) 351-378
59. Saffman P.G., and Delbrück M. Brownian motion in biological membranes. Proc Natl Acad Sci USA 72 (1975) 3111-3113
60. Vrljic M., Nishimura S.Y., Brasselet B., Moerner W.E., and McConnell H.M. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys J 83 (2002) 2681-2692
61. Vrljic M., Nishimura S.Y., Moerner W.E., and McConnell H.M. Cholesterol depletion suppresses the translational movement of class II major histocompatibility complex proteins in the plasma membrane. Biophys J 88 (2005) 334-347
62. Kenworthy A.K., Nichols B.J., Remmert C.L., Hendrix G.M., Kumar M., Zimmerberg J., et al. Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165 (2004) 735-746
63. Kusumi A., and Suzuki K. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim Biophys Acta 1746 (2005) 234-251
64. Field K.A., Holowka D., and Baird B. FcεRI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc Natl Acad Sci USA 92 (1995) 9201-9205
65. Field K.A., Holowka D., and Baird B. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem 272 (1997) 4276-4280
66. Young R.M., Zheng X., Holowka D., and Baird B. Reconstitution of regulated phosphorylation of FcepsilonRI by a lipid raft-excluded protein-tyrosine phosphatase. J Biol Chem 280 (2005) 1230-1235
67. Larson D.R., Gosse J.A., Holowka D.A., Baird B.A., and Webb W.W. Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. J Cell Biol 171 (2005) 527-536
68. Wu M., Holowka D., Craighead H.G., and Baird B. Visualization of plasma membrane compartmentalization with patterned lipid bilayers. Proc Natl Acad Sci 101 (2004) 13798-13803
69. Douglass A.D., and Vale R.D. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121 (2005) 937-950
70. Nicolau Jr. D.V., Burrage K., Parton R.G., and Hancock J.F. Identifying optimal lipid raft characteristics required to promote nanoscale protein-protein interactions on the plasma membrane. Mol Cell Biol 26 (2006) 313-323
71. Zacharias D.A., Violin J.D., Newton A.C., and Tsien R.Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296 (2002) 913-916
72. Saito T., and Yokosuka T. Immunological synapse and microclusters: the site for recognition and activation of T cells. Curr Opin Immunol 18 (2006) 305-313