In vivo plasma membrane organization: Results of biophysical approaches

Biochimica et Biophysica Acta - Biomembranes

Volumn 1664, Issue 2, 2004, Pages 119-131

  Lommerse, P H M ^a,b   Spaink, H P ^b   Schmidt, T ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Caveolae; Cytoskeleton; Lipid raft; Membrane domain; Single molecule microscopy; Single particle tracking

Indexed keywords

ACTIN; LIPID;

BIOPHYSICS; CAVEOLA; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CYTOPLASM; CYTOSKELETON; EUKARYOTE; EUKARYOTIC CELL; HUMAN; IN VIVO STUDY; LIPID MEMBRANE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TECHNIQUE;

ACTINS; ANIMALS; BIOPHYSICS; CAVEOLAE; CELL MEMBRANE; HUMANS; MEMBRANE MICRODOMAINS;

EUKARYOTA;

EID: 4344582882     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2004.05.005     Document Type: Review

References (111)

1. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science. 175:1972;720-731
2. Jacobson K., Sheets E.D., Simson R. Revisiting the fluid mosaic model of membranes. Science. 268:1995;1441-1442
3. Edidin M. Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7:1997;528-532
4. Jacobson K., Dietrich C. Looking at lipid rafts? Trends Cell Biol. 9:1999;87-91
5. Maxfield F.R. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14:2002;483-487
6. Vereb G., Szollosi J., Matko J., Nagy P., Farkas T., Vigh L., Matyus L., Waldmann T.A., Damjanovich S. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. U. S. A. 100:2003;8053-8058
7. Razani B., Woodman S.E., Lisanti M.P. Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 54:2002;431-467
8. Varma R., Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:1998;798-801
9. Pralle A., Keller P., Florin E.L., Simons K., Hörber J.K. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:2000;997-1008
10. 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
11. Schütz G.J., Kada G., Pastushenko V.P., Schindler H. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J. 19:2000;892-901
12. Kusumi A., Sako Y. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:1996;566-574
13. De Brabander M., Geerts H., Nuydens R., Nuyens R. Detection of gold probes with video-enhanced contrast microscopy: nanovid microscopy. Am. J. Anat. 185:1989;282-295
14. Ghosh R.N., Webb W.W. Automated detection and tracking of individual and clustered cell surface low density lipoprotein receptor molecules. Biophys. J. 66:1994;1301-1318
15. Simson R., Sheets E.D., Jacobson K. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys. J. 69:1995;989-993
16. 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
17. Ashkin A. Acceleration and trapping of particles by radiation pressure. Phys. Rev. Lett. 24:1970;156-159
18. Edidin M., Kuo S.C., Sheetz M.P. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 254:1991;1379-1382
19. Sako Y., Kusumi A. Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129:1995;1559-1574
20. Gross D., Webb W.W. Molecular counting of low-density lipoprotein particles as individuals and small clusters on cell surfaces. Biophys. J. 49:1986;901-911
21. Morrison I.E., Anderson C.M., Georgiou G.N., Stevenson G.V., Cherry R.J. Analysis of receptor clustering on cell surfaces by imaging fluorescent particles. Biophys. J. 67:1994;1280-1290
22. Wilson K.M., Morrison I.E., Smith P.R., Fernandez N., Cherry R.J. Single particle tracking of cell-surface HLA-DR molecules using R-phycoerythrin labeled monoclonal antibodies and fluorescence digital imaging. J. Cell. Sci. 109(Pt 8):1996;2101-2109
23. Cherry R.J., Wilson K.M., Triantafilou K., O'Toole P., Morrison I.E., Smith P.R., Fernandez N. Detection of dimers of dimers of human leukocyte antigen (HLA)-DR on the surface of living cells by single-particle fluorescence imaging. J. Cell Biol. 140:1998;71-79
24. Schmidt T., Schütz G.J., Baumgartner W., Gruber H.J., Schindler H. Imaging of single molecule diffusion. Proc. Natl. Acad. Sci. U. S. A. 93:1996;2926-2929
25. Sako Y., Minoghchi S., Yanagida T. Single-molecule imaging of EGFR signalling on the surface of living cells. Nat. Cell Biol. 2:2000;168-172
26. Harms G.S., Cognet L., Lommerse P.H.M., Blab G.A., Kahr H., Gamsjager R., Spaink H.P., Soldatov N.M., Romanin C., Schmidt T. Single-molecule imaging of l-type Ca(2+) channels in live cells. Biophys. J. 81:2001;2639-2646
27. Funatsu T., Harada Y., Tokunaga M., Saito K., Yanagida T. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature. 374:1995;555-559
28. Giebel K., Bechinger C., Herminghaus S., Riedel M., Leiderer P., Weiland U., Bastmeyer M. Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy. Biophys. J. 76:1999;509-516
29. Harms G.S., Cognet L., Lommerse P.H.M., Blab G.A., Schmidt T. Autofluorescent proteins in single-molecule research: applications to live cell imaging microscopy. Biophys. J. 80:2001;2396-2408
30. Lommerse P.H.M., Blab G.A., Cognet L., Harms G.S., Snaar-Jagalska B.E., Spaink H.P., Schmidt T. Single-molecule imaging of the H-Ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. Biophys. J. 86:2004;609-616
31. Iino R., Koyama I., Kusumi A. Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys. J. 80:2001;2667-2677
32. Axelrod D., Koppel D.E., Schlessinger J., Elson E., Webb W.W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1976;1055-1069
33. Feder T.J., Brust-Mascher I., Slattery J.P., Baird B., Webb W.W. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70:1996;2767-2773
34. Smith P.R., Morrison I.E., Wilson K.M., Fernandez N., Cherry R.J. Anomalous diffusion of major histocompatibility complex class I molecules on HeLa cells determined by single particle tracking. Biophys. J. 76:1999;3331-3344
35. Yechiel E., Edidin M. Micrometer-scale domains in fibroblast plasma membranes. J. Cell Biol. 105:1987;755-760
36. Förster T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. 2:1948;55-75
37. Jovin T.M., Arndt-Jovin D.J. Luminescence digital imaging microscopy. Annu. Rev. Biophys. Biophys. Chem. 18:1989;271-308
38. Kenworthy A.K., Edidin M. Distribution of a glycosylphosphatidylinositol- anchored protein at the apical surface of MDCK cells examined at a resolution of <100 Å using imaging fluorescence resonance energy transfer. J. Cell Biol. 142:1998;69-84
39. London E., Brown D.A. Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta. 1508:2000;182-195
40. London E. Insights into lipid raft structure and formation from experiments in model membranes. Curr. Opin. Struct. Biol. 12:2002;480-486
41. Silvius J.R. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta. 1610:2003;174-183
42. Golan D.E., Veatch W. Lateral mobility of band 3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: evidence for control by cytoskeletal interactions. Proc. Natl. Acad. Sci. U. S. A. 77:1980;2537-2541
43. Tsuji A., Ohnishi S. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state. Biochemistry. 25:1986;6133-6139
44. Tomishige M., Sako Y., Kusumi A. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell Biol. 142:1998;989-1000
45. Edidin M., Stroynowski I. Differences between the lateral organization of conventional and inositol phospholipid-anchored membrane proteins. A further definition of micrometer scale membrane domains. J. Cell Biol. 112:1991;1143-1150
46. Kusumi A., Sako Y., Yamamoto M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65:1993;2021-2040
47. Sako Y., Kusumi A. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125:1994;1251-1264
48. Edidin M., Zuniga M.C., Sheetz M.P. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc. Natl. Acad. Sci. U. S. A. 91:1994;3378-3382
49. Sako Y., Nagafuchi A., Tsukita S., Takeichi M., Kusumi A. Cytoplasmic regulation of the movement of E-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: corralling and tethering by the membrane skeleton. J. Cell Biol. 140:1998;1227-1240
50. Tang Q., Edidin M. Lowering the barriers to random walks on the cell surface. Biophys. J. 84:2003;400-407
51. Sperotto M.M., Mouritsen O.G. Monte Carlo simulation studies of lipid order parameter profiles near integral membrane proteins. Biophys. J. 59:1991;261-270
52. Almeida P.F., Vaz W.L., Thompson T.E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry. 31:1992;6739-6747
53. Bussell S.J., Koch D.L., Hammer D.A. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membranes. Biophys. J. 68:1995;1836-1849
54. Dodd T.L., Hammer D.A., Sangani A.S., Koch D.L. Numerical simulations of the effect of hydrodynamic interactions on diffusivities of integral membrane proteins. J. Fluid Mech. 293:1995;147-180
55. Brown F.L. Regulation of protein mobility via thermal membrane undulations. Biophys. J. 84:2003;842-853
56. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., Kasai R.S., Yamaguchi K., Fujiwara T., Kusumi A. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5:2003;626-632
57. Suzuki K., Sheetz M.P. Binding of cross-linked glycosylphosphatidyl- inositol-anchored proteins to discrete actin-associated sites and cholesterol-dependent domains. Biophys. J. 81:2001;2181-2189
58. Ike H., Kosugi A., Kato A., Iino R., Hirano H., Fujiwara T., Ritchie K., Kusumi A. Mechanism of Lck recruitment to the T-cell receptor cluster as studied by single-molecule-fluorescence video imaging. ChemPhysChem. 4:2003;620-626
59. van Deurs B., Roepstorff K., Hommelgaard A.M., Sandvig K. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 13:2003;92-100
60. Rothberg K.G., Heuser J.E., Donzell W.C., Ying Y.S., Glenney J.R., Anderson R.G. Caveolin, a protein component of caveolae membrane coats. Cell. 68:1992;673-682
61. Dreja K., Voldstedlund M., Vinten J., Tranum-Jensen J., Hellstrand P., Sward K. Cholesterol depletion disrupts caveolae and differentially impairs agonist-induced arterial contraction. Arterioscler. Thromb. Vasc. Biol. 22:2002;1267-1272
62. Schubert W., Frank P.G., Woodman S.E., Hyogo H., Cohen D.E., Chow C.W., Lisanti M.P. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-name, restores normal microvascular permeability in Cav-1 null mice. J. Biol. Chem. 277:2002;40091-40098
63. Woodman S.E., Park D.S., Cohen A.W., Cheung M.W., Chandra M., Shirani J., Tang B., Jelicks L.A., Kitsis R.N., Christ G.J., Factor S.M., Tanowitz H.B., Lisanti M.P. Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade. J. Biol. Chem. 277:2002;38988-38997
64. 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
65. Prior I.A., Harding A., Yan J., Sluimer J., Parton R.G., Hancock J.F. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:2001;368-375
66. Le P.U., Nabi I.R. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J. Cell. Sci. 116:2003;1059-1071
67. van Meer G., Simons K. Lipid polarity and sorting in epithelial cells. J. Cell. Biochem. 36:1988;51-58
68. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572
69. 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
70. Mesquita R.M., Melo E., Thompson T.E., Vaz W.L. Partitioning of amphiphiles between coexisting ordered and disordered phases in two-phase lipid bilayer membranes. Biophys. J. 78:2000;3019-3025
71. Wang T.Y., Silvius J.R. Different sphingolipids show differential partitioning into sphingolipid/cholesterol-rich domains in lipid bilayers. Biophys. J. 79:2000;1478-1489
72. Radhakrishnan A., Anderson T.G., McConnell H.M. Condensed complexes, rafts, and the chemical activity of cholesterol in membranes. Proc. Natl. Acad. Sci. U. S. A. 97:2000;12422-12427
73. 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
74. 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. U. S. A. 98:2001;10642-10647
75. 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 behaviour. Proc. Natl. Acad. Sci. U. S. A. 91:1994;12130-12134
76. Ahmed S.N., Brown D.A., London E. 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
77. Fridriksson E.K., Shipkova P.A., Sheets E.D., Holowka D., Baird B., 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
78. Melkonian K.A., Chu T., Tortorella L.B., Brown D.A. Characterization of proteins in detergent-resistant membrane complexes from Madin-Darby canine kidney epithelial cells. Biochemistry. 34:1995;16161-16170
79. Friedrichson T., Kurzchalia T.V. Microdomains of GPI-anchored proteins in living cells revealed by cross-linking. Nature. 394:1998;802-805
80. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev., Mol. Cell Biol. 1:2000;31-39
81. Heerklotz H., Szadkowska H., Anderson T., Seelig J. The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton. J. Mol. Biol. 329:2003;793-799
82. Schuck S., Honsho M., Ekroos K., Shevchenko A., Simons K. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. U. S. A. 100:2003;5795-5800
83. Hao M., Mukherjee S., Maxfield F.R. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc. Natl. Acad. Sci. U. S. A. 98:2001;13072-13077
84. Sheets E.D., Lee G.M., Simson R., Jacobson K. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry. 36:1997;12449-12458
85. Wu E.S., Jacobson K., Papahadjopoulos D. Lateral diffusion in phospholipid multibilayers measured by fluorescence recovery after photobleaching. Biochemistry. 16:1977;3836-3841
86. 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
87. 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
88. Sharma P., Varma R., Sarasij R.C., Ira K.G., Krishnamoorthy G., Rao M., Mayor S. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell. 116:2004;577-589
89. Glebov O.O., Nichols B.J. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat. Cell Biol. 6:2004;238-243
90. 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
91. Rodgers W., Crise B., Rose J.K. Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction. Mol. Cell. Biol. 14:1994;5384-5391
92. Shenoy-Scaria A.M., Dietzen D.J., Kwong J., Link D.C., Lublin D.M. Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. J. Cell Biol. 126:1994;353-363
93. Melkonian K.A., Ostermeyer A.G., Chen J.Z., Roth M.G., Brown D.A. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274:1999;3910-3917
94. Parmryd I., Adler J., Patel R., Magee A.I. Imaging metabolism of phosphatidylinositol 4,5-bisphosphate in T-cell GM1-enriched domains containing Ras proteins. Exp. Cell Res. 285:2003;27-38
95. 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
96. Hancock J.F., Paterson H., Marshall C.J. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell. 63:1990;133-139
97. Paige L.A., Nadler M.J., Harrison M.L., Cassady J.M., Geahlen R.L. Reversible palmitoylation of the protein-tyrosine kinase p56lck. J. Biol. Chem. 268:1993;8669-8674
98. 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
99. Field K.A., Holowka D., Baird B. Fc epsilon RI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signalling. Proc. Natl. Acad. Sci. U. S. A. 92:1995;9201-9205
100. Sheets E.D., Holowka D., Baird B. Membrane organization in immunoglobulin E receptor signalling. Curr. Opin. Chem. Biol. 3:1999;95-99
101. Pyenta P.S., Holowka D., Baird B. Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and outer leaflet lipid raft components. Biophys. J. 80:2001;2120-2132
102. 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
103. Abney J.R., Scalettar B.A. Fluctuations and membrane heterogeneity. Biophys. Chem. 57:1995;27-36
104. 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
105. Steinman R.M., Mellman I.S., Muller W.A., Cohn Z.A. Endocytosis and the recycling of plasma membrane. J. Cell Biol. 96:1983;1-27
106. 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
107. Tang Q., Edidin M. Vesicle trafficking and cell surface membrane patchiness. Biophys. J. 81:2001;196-203
108. Morrison I.E., Karakikes I., Barber R.E., Fernandez N., Cherry R.J. Detecting and quantifying colocalization of cell surface molecules by single particle fluorescence imaging. Biophys. J. 85:2003;4110-4121
109. Cognet L., Harms G.S., Blab G.A., Lommerse P.H.M., Schmidt T. Simultaneous dual-color and dual-polarization imaging of single molecules. Appl. Phys. Lett. 77:2000;4052-4054
110. Dahan M., Levi S., Luccardini C., Rostaing P., Riveau B., Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science. 302:2003;442-445
111. Cognet L., Tardin C., Boyer D., Choquet D., Tamarat P., Lounis B. Single metallic nanoparticle imaging for protein detection in cells. Proc. Natl. Acad. Sci. U. S. A. 100:2003;11350-11355