Surface analysis of membrane dynamics

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 4, 2010, Pages 766-776

  García Sáez, Ana J ^a   Schwille, Petra ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

AFM; FCS; FRAP; Giant unilamellar vesicle; Image correlation spectroscopy; Membrane domain; Membrane dynamic; Membrane organization; Single particle tracking; Supported lipid bilayer; TIRF microscopy

Indexed keywords

CHOLESTEROL; LIPID; MEMBRANE PROTEIN;

ANALYTIC METHOD; ARTICLE; BLEACHING; CELL MEMBRANE; CELL STRUCTURE; CELL VACUOLE; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE ANALYSIS; HUMAN; ILLUMINATION; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; LIPID RAFT; LIPOPHILICITY; MEMBRANE BIOLOGY; MEMBRANE MODEL; MEMBRANE STRUCTURE; MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SURFACE PROPERTY;

CELL MEMBRANE; KINETICS; LIPID BILAYERS; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; SURFACE PROPERTIES;

EID: 77449154877     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.09.016     Document Type: Article

References (165)

1. Wallin E., and von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7 (1998) 1029
2. van Meer G. Cellular lipidomics. EMBO J. 24 (2005) 3159
3. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569
4. Minsky M. Memoir on inventing the confocal scanning microscope. Scanning 10 (1988) 128
5. Mavrakis M., Rikhy R., Lilly M., and Lippincott-Schwartz J. Fluorescence imaging techniques for studying Drosophila embryo development. Curr. Protoc. Cell Biol. Chapter 4 (2008) Unit
6. Snapp E.L., Altan N., and Lippincott-Schwartz J. Measuring protein mobility by photobleaching GFP chimeras in living cells. Curr. Protoc. Cell Biol. Chapter 21 (2003) Unit
7. Groves J.T., Parthasarathy R., and Forstner M.B. Fluorescence imaging of membrane dynamics. Annu. Rev. Biomed. Eng. 10 (2008) 311
8. Beaumont V. Visualizing membrane trafficking using total internal reflection fluorescence microscopy. Biochem. Soc. Trans. 31 (2003) 819
9. Garcia-Saez A.J., and Schwille P. Single molecule techniques for the study of membrane proteins. Applied Microbiology and Biotechnology 76 (2007) 257
10. Kusumi A., Nakada C., Ritchie K., Murase K., Suzuki K., Murakoshi H., Kasai R.S., Kondo J., and Fujiwara T. 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
11. Lenne P.F., Wawrezinieck L., Conchonaud F., Wurtz O., Boned A., Guo X.J., Rigneault H., He H.T., and Marguet D. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25 (2006) 3245
12. Bouzigues C., and Dahan M. Transient directed motions of GABA(A) receptors in growth cones detected by a speed correlation index. Biophys. J. 92 (2007) 654
13. Trabesinger W., Hecht B., Wild U.P., Schutz G.J., Schindler H., and Schmidt T. Statistical analysis of single-molecule colocalization assays. Anal. Chem 73 (2001) 1100
14. Alcor D., Gouzer G., and Triller A. Single-particle tracking methods for the study of membrane receptors dynamics. Eur. J. Neurosci. 30 6 (2009) 978-997
15. Ying W., Huerta G., Steinberg S., and Zuniga M. Time series analysis of particle tracking data for molecular motion on the cell membrane. Bull. Math. Biol. 71 8 (2009) 1967-2024
16. Haustein E., and Schwille P. Single-molecule spectroscopic methods. Curr. Opin. Struct. Biol 14 (2004) 531
17. Dertinger T., Pacheco V., von d.H., Hartmann I.R., Gregor I., and Enderlein J. Two-focus fluorescence correlation spectroscopy: a new tool for accurate and absolute diffusion measurements. Chemphyschem. 8 (2007) 433
18. Humpolickova J., Gielen E., Benda A., Fagulova V., Vercammen J., Vandeven M., Hof M., Ameloot M., and Engelborghs Y. Probing diffusion laws within cellular membranes by Z-scan fluorescence correlation spectroscopy. Biophys. J. 91 (2006) L23-L25
19. Ries J., and Schwille P. Studying slow membrane dynamics with continuous wave scanning fluorescence correlation spectroscopy. Biophys. J. 91 (2006) 1915
20. Ries J., Chiantia S., and Schwille P. Accurate determination of membrane dynamics with line-scan FCS. Biophys. J. 96 (2009) 1999
21. Schwille P., Meyer-Almes F.J., and Rigler R. Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophys. J. 72 (1997) 1878
22. Garcia-Saez A.J., and Schwille P. Fluorescence correlation spectroscopy for the study of membrane dynamics and protein/lipid interactions. Methods 46 (2008) 116
23. Ries J., and Schwille P. New concepts for fluorescence correlation spectroscopy on membranes. Phys. Chem. Chem. Phys. 10 (2008) 3487
24. Kolin D.L., and Wiseman P.W. Advances in image correlation spectroscopy: measuring number densities, aggregation states, and dynamics of fluorescently labeled macromolecules in cells. Cell Biochem. Biophys. 49 (2007) 141
25. Petersen N.O., Hoddelius P.L., Wiseman P.W., Seger O., and Magnusson K.E. Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application. Biophys. J. 65 (1993) 1135
26. Costantino S., Comeau J.W., Kolin D.L., and Wiseman P.W. Accuracy and dynamic range of spatial image correlation and cross-correlation spectroscopy. Biophys. J. 89 (2005) 1251
27. Srivastava M., and Petersen N.O. Diffusion of transferrin receptor clusters. Biophys. Chem. 75 (1998) 201
28. Hebert B., Costantino S., and Wiseman P.W. Spatiotemporal image correlation spectroscopy (STICS) theory, verification, and application to protein velocity mapping in living CHO cells. Biophys. J. 88 (2005) 3601
29. Kolin D.L., Ronis D., and Wiseman P.W. k-Space image correlation spectroscopy: a method for accurate transport measurements independent of fluorophore photophysics. Biophys. J. 91 (2006) 3061
30. Digman M.A., Brown C.M., Sengupta P., Wiseman P.W., Horwitz A.R., and Gratton E. Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophys. J. 89 (2005) 1317
31. Digman M.A., Sengupta P., Wiseman P.W., Brown C.M., Horwitz A.R., and Gratton E. Fluctuation correlation spectroscopy with a laser-scanning microscope: exploiting the hidden time structure. Biophys. J. 88 (2005) L33-L36
32. Semrau S., and Schmidt T. Particle image correlation spectroscopy (PICS): retrieving nanometer-scale correlations from high-density single-molecule position data. Biophys. J. 92 (2007) 613
33. Levitt J.A., Matthews D.R., Ameer-Beg S.M., and Suhling K. Fluorescence lifetime and polarization-resolved imaging in cell biology. Curr. Opin. Biotechnol. 20 (2009) 28
34. Loura L.M., de Almeida R.F., Silva L.C., and Prieto M. FRET analysis of domain formation and properties in complex membrane systems. Biochim. Biophys. Acta 1788 (2009) 209
35. Wallrabe H., and Periasamy A. Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16 (2005) 19
36. Morris V.J., Kirby A.R., and Gunning A.P. Atomic force microscopy for biologists (1999), Imperial College Press
37. Frederix P.L., Bosshart P.D., and Engel A. Atomic force microscopy of biological membranes. Biophys. J. 96 (2009) 329
38. Goksu E.I., Vanegas J.M., Blanchette C.D., Lin W.C., and Longo M.L. AFM for structure and dynamics of biomembranes. Biochim. Biophys. Acta 1788 (2009) 254
39. Muller D.J. AFM: a nanotool in membrane biology. Biochemistry 47 (2008) 7986
40. Kraft M.L., Weber P.K., Longo M.L., Hutcheon I.D., and Boxer S.G. Phase separation of lipid membranes analyzed with high-resolution secondary ion mass spectrometry. Science 313 (2006) 1948
41. Nagerl U.V., Willig K.I., Hein B., Hell S.W., and Bonhoeffer T. Live-cell imaging of dendritic spines by STED microscopy. Proc. Natl. Acad. Sci. U. S. A 105 (2008) 18982
42. Shroff H., Galbraith C.G., Galbraith J.A., and Betzig E. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat. Methods 5 (2008) 417
43. Ianoul A., and Johnston L.J. Near-field scanning optical microscopy to identify membrane microdomains. Methods Mol. Biol. 400 (2007) 469
44. Lewis A., Radko A., Ben Ami N., Palanker D., and Lieberman K. Near-field scanning optical microscopy in cell biology. Trends Cell Biol. 9 (1999) 70
45. Richter R.P., Berat R., and Brisson A.R. Formation of solid-supported lipid bilayers: an integrated view. Langmuir 22 (2006) 3497
46. Wagner M.L., and Tamm L.K. Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker. Biophys. J. 79 (2000) 1400
47. Diaz A.J., Albertorio F., Daniel S., and Cremer P.S. Double cushions preserve transmembrane protein mobility in supported bilayer systems. Langmuir 24 (2008) 6820
48. Merzlyakov M., Li E., Gitsov I., and Hristova K. Surface-supported bilayers with transmembrane proteins: role of the polymer cushion revisited. Langmuir 22 (2006) 10145
49. Angelova M.I., and Dimitrov D.S. Liposome electroformation. Faraday Discussions (1986) 303
50. Montes L.R., Alonso A., Goni F.M., and Bagatolli L.A. Giant unilamellar vesicles electroformed from native membranes and organic lipid mixtures under physiological conditions. Biophys. J. 93 (2007) 3548
51. Baumgart T., Hammond A.T., Sengupta P., Hess S.T., Holowka D.A., Baird B.A., and Webb W.W. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 3165
52. Lingwood D., Ries J., Schwille P., and Simons K. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. U. S. A 105 (2008) 10005
53. Perez J.B., Martinez K.L., Segura J.M., and Vogel H. Supported cell-membrane sheets for functional fluorescence imaging of membrane proteins. Adv. Funct. Mater. 16 (2006) 306
54. Danelon C., Perez J.B., Santschi C., Brugger J., and Vogel H. Cell membranes suspended across nanoaperture arrays. Langmuir 22 (2006) 22
55. Simons K., and Vaz W.L.C. Model systems, lipid rafts, and cell membranes. Annual Review of Biophysics and Biomolecular Structure 33 (2004) 269
56. Chiantia S., Ries J., and Schwille P. Fluorescence correlation spectroscopy in membrane structure elucidation. Biochim. Biophys. Acta 1788 (2009) 225
57. 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. U. S. A 96 (1999) 8461
58. Scherfeld D., Kahya N., and Schwille P. Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol. Biophys. J. 85 (2003) 3758
59. Kahya N., Scherfeld D., Bacia K., Poolman B., and Schwille P. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 278 (2003) 28109
60. Bacia K., Schwille P., and Kurzchalia T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl. Acad. Sci. U. S. A 102 (2005) 3272
61. Kahya N., Scherfeld D., and Schwille P. Differential lipid packing abilities and dynamics in giant unilamellar vesicles composed of short-chain saturated glycerol-phospholipids, sphingomyelin and cholesterol. Chem. Phys. Lipids 135 (2005) 169
62. Kahya N., and Schwille P. How phospholipid-cholesterol interactions modulate lipid lateral diffusion, as revealed by fluorescence correlation spectroscopy. J. Fluoresc. 16 (2006) 671
63. Forstner M.B., Yee C.K., Parikh A.N., and Groves J.T. Lipid lateral mobility and membrane phase structure modulation by protein binding. J. Am. Chem. Soc. 128 (2006) 15221
64. Chiantia S., Ries J., Kahya N., and Schwille P. Combined AFM and two-focus SFCS study of raft-exhibiting model membranes. Chemphyschem 7 (2006) 2409
65. Chiantia S., Kahya N., Ries J., and Schwille P. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys. J. 90 (2006) 4500
66. Chiantia S., Kahya N., and Schwille P. Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 23 (2007) 7659
67. Ries J., Chiantia S., and Schwille P. Accurate determination of membrane dynamics with line-scan FCS. Biophys. J. 96 (2009) 1999
68. Scomparin C., Lecuyer S., Ferreira M., Charitat T., and Tinland B. Diffusion in supported lipid bilayers: influence of substrate and preparation technique on the internal dynamics. Eur. Phys J. E Soft. Matter 28 (2008) 211-220
69. Zhang L., and Granick S. Lipid diffusion compared in outer and inner leaflets of planar supported bilayers. J. Chem. Phys. 123 (2005) 211104
70. Kiessling V., Crane J.M., and Tamm L.K. Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91 (2006) 3313
71. Werner J.H., Montano G.A., Garcia A.L., Zurek N.A., Akhadov E.A., Lopez G.P., and Shreve A.P. Formation and dynamics of supported phospholipid membranes on a periodic nanotextured substrate. Langmuir 25 (2009) 2986
72. Kenworthy A.K., Nichols B.J., Remmert C.L., Hendrix G.M., Kumar M., Zimmerberg J., and Lippincott-Schwartz J. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165 (2004) 735
73. Meder D., Moreno M.J., Verkade P., Vaz W.L., and Simons K. Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc. Natl. Acad. Sci. U. S. A 103 (2006) 329
74. Wawrezinieck L., Rigneault H., Marguet D., and Lenne P.F. Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys. J. 89 (2005) 4029
75. Wenger J., Conchonaud F., Dintinger J., Wawrezinieck L., Ebbesen T.W., Rigneault H., Marguet D., and Lenne P.F. Diffusion analysis within single nanometric apertures reveals the ultrafine cell membrane organization. Biophys. J. 92 (2007) 913
76. Cavey M., Rauzi M., Lenne P.F., and Lecuit T. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453 (2008) 751
77. Lasserre R., Guo X.J., Conchonaud F., Hamon Y., Hawchar O., Bernard A.M., Soudja S.M., Lenne P.F., Rigneault H., Olive D., Bismuth G., Nunes J.A., Payrastre B., Marguet D., and He H.T. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat. Chem. Biol. 4 (2008) 538
78. Eggeling C., Ringemann C., Medda R., Schwarzmann G., Sandhoff K., Polyakova S., Belov V.N., Hein B., von Middendorff C., Schonle A., and Hell S.W. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457 (2009) 1159
79. Umemura Y.M., Vrljic M., Nishimura S.Y., Fujiwara T.K., Suzuki K.G., and Kusumi A. Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking. Biophys. J. 95 (2008) 435
80. Murase K., Fujiwara T., Umemura Y., Suzuki K., Iino R., Yamashita H., Saito M., Murakoshi H., Ritchie K., and Kusumi A. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys. J. 86 (2004) 4075
81. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., Kasai R.S., Yamaguchi K., Fujiwara T., and Kusumi A. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5 (2003) 626
82. Fujiwara T., Ritchie K., Murakoshi H., Jacobson K., and Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157 (2002) 1071
83. 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
84. Ritchie K., Iino 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 (Review). Mol. Membr. Biol 20 (2003) 13
85. Andrews N.L., Lidke K.A., Pfeiffer J.R., Burns A.R., Wilson B.S., Oliver J.M., and Lidke D.S. Actin restricts FcepsilonRI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell Biol. 10 (2008) 955
86. Lommerse P.H., Vastenhoud K., Pirinen N.J., Magee A.I., Spaink H.P., and Schmidt T. Single-molecule diffusion reveals similar mobility for the Lck, H-ras, and K-ras membrane anchors. Biophys. J. 91 (2006) 1090
87. Lommerse P.H., Blab G.A., Cognet L., Harms G.S., Snaar-Jagalska B.E., Spaink H.P., and 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
88. Jacquier V., Prummer M., Segura J.M., Pick H., and Vogel H. Visualizing odorant receptor trafficking in living cells down to the single-molecule level. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 14325
89. 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
90. Rhode S., Grurl R., Brameshuber M., Hermetter A., and Schutz G.J. Plasma membrane fluidity affects transient immobilization of oxidized phospholipids in endocytotic sites for subsequent uptake. J. Biol. Chem. 284 (2009) 2258
91. Cicuta P., Keller S.L., and Veatch S.L. Diffusion of liquid domains in lipid bilayer membranes. J. Phys. Chem. B 111 (2007) 3328
92. Petrov E.P., and Schwille P. Translational diffusion in lipid membranes beyond the Saffman-Delbruck approximation. Biophys. J. 94 (2008) L41-L43
93. Kiessling V., Wan C., and Tamm L.K. Domain coupling in asymmetric lipid bilayers. Biochim. Biophys. Acta 1788 (2009) 64
94. Kiessling V., Crane J.M., and Tamm L.K. Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91 (2006) 3313
95. Collins M.D., and Keller S.L. Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 124
96. Lin W.C., Blanchette C.D., Ratto T.V., and Longo M.L. Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study. Biophys. J. 90 (2006) 228
97. Feng Z.V., Spurlin T.A., and Gewirth A.A. Direct visualization of asymmetric behavior in supported lipid bilayers at the gel-fluid phase transition. Biophys. J. 88 (2005) 2154
98. Kaasgaard T., Leidy C., Crowe J.H., Mouritsen O.G., and Jorgensen K. Temperature-controlled structure and kinetics of ripple phases in one- and two-component supported lipid bilayers. Biophys. J. 85 (2003) 350
99. Blanchette C.D., Lin W.C., Ratto T.V., and Longo M.L. Galactosylceramide domain microstructure: impact of cholesterol and nucleation/growth conditions. Biophys. J. 90 (2006) 4466
100. Blanchette C.D., Lin W.C., Orme C.A., Ratto T.V., and Longo M.L. Using nucleation rates to determine the interfacial line tension of symmetric and asymmetric lipid bilayer domains. Langmuir 23 (2007) 5875
101. Blanchette C.D., Lin W.C., Orme C.A., Ratto T.V., and Longo M.L. Domain nucleation rates and interfacial line tensions in supported bilayers of ternary mixtures containing galactosylceramide. Biophys. J. 94 (2008) 2691
102. Garcia-Saez A.J., Chiantia S., and Schwille P. Effect of line tension on the lateral organization of lipid membranes. J. Biol. Chem. 282 (2007) 33537
103. Baumgart T., Hess S.T., and Webb W.W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425 (2003) 821
104. Trajkovic K., Hsu C., Chiantia S., Rajendran L., Wenzel D., Wieland F., Schwille P., Brugger B., and Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319 (2008) 1244
105. Vind-Kezunovic D., Nielsen C.H., Wojewodzka U., and Gniadecki R. Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells. Biochim. Biophys. Acta 1778 (2008) 2480
106. Veatch S.L., Soubias O., Keller S.L., and Gawrisch K. Critical fluctuations in domain-forming lipid mixtures. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 17650
107. Honerkamp-Smith A.R., Cicuta P., Collins M.D., Veatch S.L., den Nijs M., Schick M., and Keller S.L. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophys. J. 95 (2008) 236
108. Veatch S.L., Cicuta P., Sengupta P., Honerkamp-Smith A., Holowka D., and Baird B. Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 3 (2008) 287
109. Garcia-Saez A.J., Chiantia S., Salgado J., and Schwille P. Pore formation by a Bax-derived peptide: effect on the line tension of the membrane probed by AFM. Biophys. J. 93 (2007) 103
110. 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. U. S. A. 102 (2005) 6320
111. Windschiegl B., Orth A., Romer W., Berland L., Stechmann B., Bassereau P., Johannes L., and Steinem C. Lipid reorganization induced by Shiga toxin clustering on planar membranes. PLoS. One. 4 (2009) e6238
112. Lam K.L., Ishitsuka Y., Cheng Y., Chien K., Waring A.J., Lehrer R.I., and Lee K.Y. Mechanism of supported membrane disruption by antimicrobial peptide protegrin-1. J. Phys. Chem. B 110 (2006) 21282
113. Ira S.Z., Ramirez D.M., Vanderlip S., Ogilvie W., Jakubek Z.J., and Johnston L.J. Enzymatic generation of ceramide induces membrane restructuring: correlated AFM and fluorescence imaging of supported bilayers. J. Struct. Biol. 168 1 (2009) 78-79
114. Chiantia S., Ries J., Chwastek G., Carrer D., Li Z., Bittman R., and Schwille P. Role of ceramide in membrane protein organization investigated by combined AFM and FCS. Biochim. Biophys. Acta 1778 (2008) 1356
115. Manley S., Horton M.R., Lecszynski S., and Gast A.P. Sorting of streptavidin protein coats on phase-separating model membranes. Biophys. J. 95 (2008) 2301
116. Manneville J.B., Casella J.F., Ambroggio E., Gounon P., Bertherat J., Bassereau P., Cartaud J., Antonny B., and Goud B. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. Proc. Natl. Acad. Sci. U. S. A 105 (2008) 16946
117. Loose M., Fischer-Friedrich E., Ries J., Kruse K., and Schwille P. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320 (2008) 789
118. XL. Nat. Struct. Mol. Biol. 16 (2009) 1178-1185
119. Roux A., Cuvelier D., Nassoy P., Prost J., Bassereau P., and Goud B. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J. 24 (2005) 1537
120. Sorre B., Callan-Jones A., Manneville J.B., Nassoy P., Joanny J.F., Prost J., Goud B., and Bassereau P. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc. Natl. Acad. Sci. U. S. A 106 (2009) 5622
121. Tian A., and Baumgart T. Sorting of lipids and proteins in membrane curvature gradients. Biophys. J. 96 (2009) 2676
122. Parthasarathy R., Yu C.H., and Groves J.T. Curvature-modulated phase separation in lipid bilayer membranes. Langmuir 22 (2006) 5095
123. Mossman K.D., Campi G., Groves J.T., and Dustin M.L. Altered TCR signaling from geometrically repatterned immunological synapses. Science 310 (2005) 1191
124. DeMond A.L., Mossman K.D., Starr T., Dustin M.L., and Groves J.T. T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation. Biophys. J. 94 (2008) 3286
125. Hartman N.C., Nye J.A., and Groves J.T. Cluster size regulates protein sorting in the immunological synapse. Proc. Natl. Acad. Sci. U. S. A 106 31 (2009) 12729-12734
126. Ueda M., Sako Y., Tanaka T., Devreotes P., and Yanagida T. Single-molecule analysis of chemotactic signaling in Dictyostelium cells. Science 294 (2001) 864
127. Weiger M.C., Wang C.C., Krajcovic M., Melvin A.T., Rhoden J.J., and Haugh J.M. Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts. J. Cell Sci. 122 (2009) 313
128. Sako Y., Minoghchi S., and Yanagida T. Single-molecule imaging of EGFR signalling on the surface of living cells. Nat. Cell Biol. 2 (2000) 168
129. Teramura Y., Ichinose J., Takagi H., Nishida K., Yanagida T., and Sako Y. Single-molecule analysis of epidermal growth factor binding on the surface of living cells. EMBO J. 25 (2006) 4215
130. Yu C., Hale J., Ritchie K., Prasad N.K., and Irudayaraj J. Receptor overexpression or inhibition alters cell surface dynamics of EGF-EGFR interaction: new insights from real-time single molecule analysis. Biochem. Biophys. Res. Commun. 378 (2009) 376
131. Adjobo-Hermans M.J., Goedhart J., and Gadella Jr. T.W. Regulation of PLCbeta1a membrane anchoring by its substrate phosphatidylinositol (4,5)-bisphosphate. J. Cell Sci. 121 (2008) 3770
132. Patel H., Konig I., Tsujioka M., Frame M.C., Anderson K.I., and Brunton V.G. The multi-FERM-domain-containing protein FrmA is required for turnover of paxillin-adhesion sites during cell migration of Dictyostelium. J. Cell Sci. 121 (2008) 1159
133. Leonard D., Hayakawa A., Lawe D., Lambright D., Bellve K.D., Standley C., Lifshitz L.M., Fogarty K.E., and Corvera S. Sorting of EGF and transferrin at the plasma membrane and by cargo-specific signaling to EEA1-enriched endosomes. J. Cell Sci. 121 (2008) 3445
134. Kyoung M., and Sheets E.D. Vesicle diffusion close to a membrane: intermembrane interactions measured with fluorescence correlation spectroscopy. Biophys. J. 95 (2008) 5789
135. Wessels L., Elting M.W., Scimeca D., and Weninger K. Rapid membrane fusion of individual virus particles with supported lipid bilayers. Biophys. J. 93 (2007) 526
136. Zenisek D., Steyer J.A., and Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406 (2000) 849
137. Bezzi P., Gundersen V., Galbete J.L., Seifert G., Steinhauser C., Pilati E., and Volterra A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci 7 (2004) 613
138. Bowser D.N., and Khakh B.S. Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 4212
139. Cali C., Marchaland J., Regazzi R., and Bezzi P. SDF 1-alpha (CXCL12) triggers glutamate exocytosis from astrocytes on a millisecond time scale: imaging analysis at the single-vesicle level with TIRF microscopy. J. Neuroimmunol. 198 (2008) 82
140. Pangrsic T., Potokar M., Stenovec M., Kreft M., Fabbretti E., Nistri A., Pryazhnikov E., Khiroug L., Giniatullin R., and Zorec R. Exocytotic release of ATP from cultured astrocytes. J. Biol. Chem. 282 (2007) 28749
141. Huang S., Lifshitz L.M., Jones C., Bellve K.D., Standley C., Fonseca S., Corvera S., Fogarty K.E., and Czech M.P. Insulin stimulates membrane fusion and GLUT4 accumulation in clathrin coats on adipocyte plasma membranes. Mol. Cell Biol 27 (2007) 3456
142. Degtyar V.E., Allersma M.W., Axelrod D., and Holz R.W. Increased motion and travel, rather than stable docking, characterize the last moments before secretory granule fusion. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 15929
143. Johns L.M., Levitan E.S., Shelden E.A., Holz R.W., and Axelrod D. Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J. Cell Biol 153 (2001) 177
144. Steyer J.A., Horstmann H., and Almers W. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 388 (1997) 474
145. Ohara-Imaizumi M., Nishiwaki C., Nakamichi Y., Kikuta T., Nagai S., and Nagamatsu S. Correlation of syntaxin-1 and SNAP-25 clusters with docking and fusion of insulin granules analysed by total internal reflection fluorescence microscopy. Diabetologia 47 (2004) 2200
146. Pigeau G.M., Kolic J., Ball B.J., Hoppa M.B., Wang Y.W., Ruckle T., Woo M., Manning Fox J.E., and Macdonald P.E. Insulin granule recruitment and exocytosis is dependent on p110{gamma} in insulinoma and human {beta}-cells. Diabetes 58 9 (2009) 2084-2095
147. Tsuboi T., Zhao C., Terakawa S., and Rutter G.A. Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr. Biol. 10 (2000) 1307
148. Letinic K., Sebastian R., Toomre D., and Rakic P. Exocyst is involved in polarized cell migration and cerebral cortical development. Proc. Natl. Acad. Sci. U. S. A 106 (2009) 11342
149. Burtey A., Rappoport J.Z., Bouchet J., Basmaciogullari S., Guatelli J., Simon S.M., Benichou S., and Benmerah A. Dynamic interaction of HIV-1 Nef with the clathrin-mediated endocytic pathway at the plasma membrane. Traffic 8 (2007) 61
150. Licht S.S., Sonnleitner A., Weiss S., and Schultz P.G. A rugged energy landscape mechanism for trapping of transmembrane receptors during endocytosis. Biochemistry 42 (2003) 2916
151. Rappoport J.Z., Benmerah A., and Simon S.M. Analysis of the AP-2 adaptor complex and cargo during clathrin-mediated endocytosis. Traffic 6 (2005) 539
152. Perera R.M., Zoncu R., Lucast L., De Camilli P., and Toomre D. Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. Proc. Natl. Acad. Sci. U. S. A 103 (2006) 19332
153. Zoncu R., Perera R.M., Sebastian R., Nakatsu F., Chen H., Balla T., Ayala G., Toomre D., and De Camilli P.V. Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 3793
154. Zoncu R., Perera R.M., Balkin D.M., Pirruccello M., Toomre D., and De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136 (2009) 1110
155. Grant D.M., McGinty J., McGhee E.J., Bunney T.D., Owen D.M., Talbot C.B., Zhang W., Kumar S., Munro I., Lanigan P.M., Kennedy G.T., Dunsby C., Magee A.I., Courtney P., Katan M., Neil M.A., and French P.M. High speed optically sectioned fluorescence lifetime imaging permits study of live cell signaling events. Opt. Express 15 (2007) 15656
156. Hofman E.G., Ruonala M.O., Bader A.N., van den H.D., Voortman J., Roovers R.C., Verkleij A.J., Gerritsen H.C., and van Bergen En Henegouwen P.M. EGF induces coalescence of different lipid rafts. J. Cell Sci. 121 (2008) 2519
157. Larijani B., Allen-Baume V., Morgan C.P., Li M., and Cockcroft S. EGF regulation of PITP dynamics is blocked by inhibitors of phospholipase C and of the Ras-MAP kinase pathway. Curr. Biol. 13 (2003) 78
158. Calloway N., Vig M., Kinet J.P., Holowka D., and Baird B. Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions. Mol. Biol. Cell 20 (2009) 389
159. Meyer B.H., Segura J.M., Martinez K.L., Hovius R., George N., Johnsson K., and Vogel H. FRET imaging reveals that functional neurokinin-1 receptors are monomeric and reside in membrane microdomains of live cells. Proc. Natl. Acad. Sci. U. S. A 103 (2006) 2138
160. Abankwa D., and Vogel H. A FRET map of membrane anchors suggests distinct microdomains of heterotrimeric G proteins. J. Cell Sci. 120 (2007) 2953
161. Yin J., Lin A.J., Buckett P.D., Wessling-Resnick M., Golan D.E., and Walsh C.T. Single-cell FRET imaging of transferrin receptor trafficking dynamics by Sfp-catalyzed, site-specific protein labeling. Chem. Biol. 12 (2005) 999
162. Gavutis M., Lata S., and Piehler J. Probing 2-dimensional protein-protein interactions on model membranes. Nat. Protoc. 1 (2006) 2091
163. Varma R., and Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394 (1998) 798
164. Sharma P., Varma R., Sarasij R.C., Ira, Gousset K., Krishnamoorthy G., Rao M., and Mayor S. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116 (2004) 577
165. Goswami D., Gowrishankar K., Bilgrami S., Ghosh S., Raghupathy R., Chadda R., Vishwakarma R., Rao M., and Mayor S. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135 (2008) 1085