Membrane mechanisms for signal transduction: The coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes

Seminars in Cell and Developmental Biology

Volumn 23, Issue 2, 2012, Pages 126-144

  Kusumi, Akihiro ^a,b   Fujiwara, Takahiro K ^a   Morone, Nobuhiro ^a   Yoshida, Kenta J ^a   Chadda, Rahul ^a   Xie, Min ^a   Kasai, Rinshi S ^b   Suzuki, Kenichi G N ^a,c,d  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Actin based membrane skeleton; Dynamic protein complex; GPI anchored receptor; Picket fence model; Raft domains; Single molecule imaging

Indexed keywords

ACTIN; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; DETERGENT; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTIFICIAL MEMBRANE; CELL MEMBRANE; CELL TRACKING; CYTOPLASM; DIFFUSION COEFFICIENT; HUMAN; IMMUNOFLUORESCENCE; IMMUNOLOCALIZATION; NONHUMAN; OLIGOMERIZATION; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; STIMULATION;

EID: 84862800913     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.01.018     Document Type: Review

References (194)

1. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
2. 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 2005, 34:351-378.
3. Lingwood D., Simons K. Lipid rafts as a membrane-organizing principle. Science 2010, 327:46-50.
4. Simons K., Gerl M.J. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 2010, 11:688-699.
5. 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 2003, 160:165-170.
6. Parton R.G., Hancock J.F. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol 2004, 14:141-147.
7. Nicolau D.V., Burrage K., Parton R.G., Hancock J.F. Identifying optimal lipid raft characteristics required to promote nanoscale protein-protein interactions on the plasma membrane. Mol Cell Biol 2006, 26:313-323.
8. Tian T.H., Harding A., Inder K., Plowman S., Parton R.G., Hancock J.F. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol 2007, 9:905-914.
9. Sharma P., Varma R., Sarasij R.C., Ira Gousset K., Krishnamoorthy G., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 2004, 116:577-589.
10. Goswami D., Gowrishankar K., Bilgrami S., Ghosh S., Raghupathy R., Chadda R., et al. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008, 135:1085-1097.
11. Eggeling C., Ringemann C., Medda R., Schwarzmann G., Sandhoff K., Polyakova S., et al. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 2009, 457:1159-1162.
12. Sahl S.J., Leutenegger M., Hilbert M., Hell S.W., Eggeling C. Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids. Proc Natl Acad Sci USA 2010, 107:6829-6834.
13. Fujita A., Cheng J.L., Hirakawa M., Furukawa K., Kusunoki S., Fujimoto T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol Biol Cell 2007, 18:2112-2122.
14. Fujita A., Cheng J., Fujimoto T. Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim Biophys Acta Mol Cell Biol Lipids 2009, 1791:388-396.
15. Fujita A., Cheng J.L., Tauchi-Sato K., Takenawa T., Fujimoto T. A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc Natl Acad Sci USA 2009, 106:11818.
16. Lenne P.F., Wawrezinieck L., Conchonaud F., Wurtz O., Boned A., Guo X.J., et al. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J 2006, 25:3245-3256.
17. van Zanten T.S., Gomez J., Manzo C., Cambi A., Buceta J., Reigada R., et al. Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc Natl Acad Sci USA 2010, 107:15437-15442.
18. Lommerse P.H.M., Vastenhoud K., Pirinen N.J., Magee A.I., Spaink H.P., Schmidt T. Single-molecule diffusion reveals similar mobility for the Lck, H-Ras, and K-Ras membrane anchors. Biophys J 2006, 91:1090-1097.
19. Plowman S.J., Muncke C., Parton R.G., 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 2005, 102:15500-15505.
20. Parton R.G., Hanzal-Bayer M., Hancock J.F. Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J Cell Sci 2006, 119:787-796.
21. Parton R.G., Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007, 8:185-194.
22. Hill M.M., Bastiani M., Luetterforst R., Kirkham M., Kirkham A., Nixon S.J., et al. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 2008, 132:113-124.
23. Wilbur J.D., Hwang P.K., Brodsky F.M. New faces of the familiar clathrin lattice. Traffic 2005, 6:346-350.
24. Bauer M., Pelkmans L. A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett 2006, 580:5559-5564.
25. Doherty G.J., McMahon H.T. Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu Rev Biophys 2008, 37:65-95.
26. Kirchhausen T. Imaging endocytic clathrin structures in living cells. Trends Cell Biol 2009, 19:596-605.
27. Mercer J., Schelhaas M., Helenius A. Virus entry by endocytosis. Annu Rev Biochem 2010, 79:803-833.
28. Suetsugu S., Toyooka K., Senju Y. Subcellular membrane curvature mediated by the BAR domain superfamily proteins. Semin Cell Dev Biol 2010, 21:340-349.
29. McMahon H.T., Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011, 12:517-533.
30. Saxton M.J., Jacobson K. Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct 1997, 26:373-399.
31. Murakoshi H., Iino R., Kobayashi T., Fujiwara T., Ohshima C., Yoshimura A., et al. Single-molecule imaging analysis of Ras activation in living cells. Proc Natl Acad Sci USA 2004, 101:7317-7322.
32. Toomre D., Bewersdorf J. A new wave of cellular imaging. Annu Rev Cell Dev Biol 2010, 26:285-314.
33. Dustin M.L., Depoil D. New insights into the T cell synapse from single molecule techniques. Nat Rev Immunol 2011, 11:672-684.
34. Kusumi A, Fujiwara TK, Chadda R, Xie M, Tsunoyama TA, Kalay Z, et al. Organizing principles of the plasma membrane for signal transduction: membrane mechanisms by the three-tiered hierarchical meso-scale domain architecture. Ann Rev Cell Dev Biol, in press.
35. Murase K., Fujiwara T., Umemura Y., Suzuki K., Iino R., Yamashita H., et al. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys J 2004, 86:4075-4093.
36. 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 1993, 65:2021-2040.
37. Suzuki K., Ritchie K., Kajikawa E., Fujiwara T., Kusumi A. Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys J 2005, 88:3659-3680.
38. Powles J.G., Mallett M.J.D., Rickayzen G., Evans W.A.B. Exact analytic solutions for diffusion impeded by an infinite array of partially permeable barriers. Proc R Soc A 1992, 436:391-403.
39. Fujiwara T., Ritchie K., Murakoshi H., Jacobson K., Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 2002, 157:1071-1081.
40. Kusumi A., Ike H., Nakada C., Murase K., Fujiwara T. Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules. Semin Immunol 2005, 17:3-21.
41. Sako Y., Kusumi A. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J Cell Biol 1994, 125:1251-1264.
42. Umemura Y.M., Vrljic M., Nishimura S.Y., Fujiwara T.K., Suzuki K.G.N., Kusumi A. Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking. Biophys J 2008, 95:435-450.
43. Kusumi A., Shirai Y.M., Koyama-Honda I., Suzuki K.G.N., Fujiwara T.K. Hierarchical organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett 2010, 584:1814-1823.
44. Morone N., Fujiwara T., Murase K., Kasai R.S., Ike H., Yuasa S., et al. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol 2006, 174:851-862.
45. Peters R., Cherry R.J. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbrück equations. Proc Natl Acad Sci USA 1982, 79:4317-4321.
46. Vaz W.L.C., Criado M., Madeira V.M.C., Schoellmann G., Jovin T.M. Size dependence of the translational diffusion of large integral membrane-proteins in liquid-crystalline phase lipid bilayers - a study using fluorescence recovery after photobleaching. Biochemistry 1982, 21:5608-5612.
47. Frick M., Schmidt K., Nichols B.J. Modulation of lateral diffusion in the plasma membrane by protein density. Curr Biol 2007, 17:462-467.
48. Lindblom G., Johansson L.B., Arvidson G. Effect of cholesterol in membranes. Pulsed nuclear magnetic resonance measurements of lipid lateral diffusion. Biochemistry 1981, 20:2204-2207.
49. 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 2001, 98:10642-10647.
50. Sheetz M.P., Schindler M., Koppel D.E. Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature 1980, 285:510-511.
51. 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 1986, 25:6133-6139.
52. 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 1988, 27:7447-7452.
53. Saffman P.G., Delbrück M. Brownian-motion in biological-membranes. Proc Natl Acad Sci USA 1975, 72:3111-3113.
54. Gambin Y., Lopez-Esparza R., Reffay M., Sierecki E., Gov N.S., Genest M., et al. Lateral mobility of proteins in liquid membranes revisited. Proc Natl Acad Sci USA 2006, 103:2098-2102.
55. Niehaus A.M., Vlachos D.G., Edwards J.S., Plechac P., Tribe R. Microscopic simulation of membrane molecule diffusion on corralled membrane surfaces. Biophys J 2008, 94:1551-1564.
56. Kenkre V.M., Giuggioli L., Kalay Z. Molecular motion in cell membranes: analytic study of fence-hindered random walks. Phys Rev E 2008, 77.
57. Kalay Z., Parris P.E., Kenkre V.M. Effects of disorder in location and size of fence barriers on molecular motion in cell membranes. J Phys: Condens Matter 2008, 20.
58. Novikov D.S., Fieremans E., Jensen J.H., Helpern J.A. Random walk with barriers. Nat Phys 2011, 7:508-514.
59. Kusumi A., Sako Y. Cell surface organization by the membrane skeleton. Curr Opin Cell Biol 1996, 8:566-574.
60. 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 1998, 142:989-1000.
61. Ehrlich M., Boll W., van Oijen A., Hariharan R., Chandran K., Nibert M.L., et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004, 118:591-605.
62. Lommerse P.H., Snaar-Jagaiska B.E., Spaink H.P., Schmidt T. Single-molecule diffusion measurements of H-Ras at the plasma membrane of live cells reveal microdomain localization upon activation. J Cell Sci 2005, 118:1799-1809.
63. Schaaf M.J., Koopmans W.J., Meckel T., van Noort J., Snaar-Jagalska B.E., Schmidt T.S., et al. Single-molecule microscopy reveals membrane microdomain organization of cells in a living vertebrate. Biophys J 2009, 97:1206-1214.
64. Jaqaman K., Kuwata H., Touret N., Collins R., Trimble W.S., Danuser G., et al. Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 2011, 146:593-606.
65. Saxton M.J. Lateral diffusion in an archipelago. The effect of mobile obstacles. Biophys J 1987, 52:989-997.
66. Saxton M.J. Lateral diffusion in a mixture of mobile and immobile particles. A Monte Carlo study. Biophys J 1990, 58:1303-1306.
67. Bussell S.J., Hammer D.A., Koch D.L. The effect of hydrodynamic interactions on the tracer and gradient diffusion of integral membrane-proteins in lipid bilayers. J Fluid Mech 1994, 258:167-190.
68. 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 1995, 68:1836-1849.
69. Bussell S.J., Koch D.L., Hammer D.A. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: tracer diffusion in organelle and reconstituted membranes. Biophys J 1995, 68:1828-1835.
70. 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 1995, 293:147-180.
71. Nicolau D.V., Hancock J.F., Burrage K. Sources of anomalous diffusion on cell membranes: a Monte Carlo study. Biophys J 2007, 92:1975-1987.
72. Kusumi A., Koyama-Honda I., Suzuki K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 2004, 5:213-230.
73. Kusumi A., Suzuki K.G.N., Kasai R.S., Ritchie K., Fujiwara T.K. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 2011, 36:604-615.
74. de Monvel J.B., Brownell W.E., Ulfendahl M. Lateral diffusion anisotropy and membrane lipid/skeleton interaction in outer hair cells. Biophys J 2006, 91:364-381.
75. Boucrot E., Saffarian S., Massol R., Kirchhausen T., Ehrlich M. Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 2006, 312:4036-4048.
76. Saxton M.J. A biological interpretation of transient anomalous subdiffusion. I. Qualitative model. Biophys J 2007, 92:1178-1191.
77. Murcia M.J., Minner D.E., Mustata G.M., Ritchie K., Naumann C.A. Design of quantum dot-conjugated lipids for long-term, high-speed tracking experiments on cell surfaces. J Am Chem Soc 2008, 130:15054-15062.
78. Petrini E.M., Marchionni I., Zacchi P., Sieghart W., Cherubini E. Clustering of extrasynaptic GABA(A) receptors modulates tonic inhibition in cultured hippocampal neurons. J Biol Chem 2004, 279:45833-45843.
79. Minguet S., Swamy M., Alarcon B., Luescher I.F., Schamel W.W.A. Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity 2007, 26:43-54.
80. Briegel A., Ortega D.R., Tocheva E.I., Wuichet K., Li Z., Chen S., et al. Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 2009, 106:17181-17186.
81. Nikolaev V.O., Moshkov A., Lyon A.R., Miragoli M., Novak P., et al. Beta(2)-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 2010, 327:1653-1657.
82. Wang J., Chen H., Brown E.J. L-plastin peptide activation of alpha(v)beta(3)-mediated adhesion requires integrin conformational change and actin filament disassembly. J Biol Chem 2001, 276:14474-14481.
83. Boggs J.M., Wang H.M. Co-clustering of galactosylceramide and membrane proteins in oligodendrocyte membranes on interaction with polyvalent carbohydrate and prevention by an intact cytoskeleton. J Neurosci Res 2004, 76:342-355.
84. Lajoie P., Partridge E.A., Guay G., Goetz J.G., Pawling J., Lagana A., et al. Plasma membrane domain organization regulates EGFR signaling in tumor cells. J Cell Biol 2007, 179:341-356.
85. Chung I., Akita R., Vandlen R., Toomre D., Schlessinger J., Mellman I. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 2010, 464:783-787.
86. Treanor B., Depoil D., Gonzalez-Granja A., Barral P., Weber M., Dushek O., et al. The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 2010, 32:187-199.
87. Grecco H.E., Schmick M., Bastiaens P.I. Signaling from the living plasma membrane. Cell 2011, 144:897-909.
88. Rodgers W., Zavzavadjian J. Glycolipid-enriched membrane domains are assembled into membrane patches by associating with the actin cytoskeleton. Exp Cell Res 2001, 267:173-183.
89. Gomez-Mouton C., Abad J.L., Mira E., Lacalle R.A., Gallardo E., Jimenez-Baranda S., et al. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 2001, 98:9642-9647.
90. Baumgartner W., Schutz G.J., Wiegand J., Golenhofen N., Drenckhahn D. Cadherin function probed by laser tweezer and single molecule fluorescence in vascular endothelial cells. J Cell Sci 2003, 116:1001-1011.
91. 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 2001, 80:2667-2677.
92. Liu C.H., Paprica A., Petersen N.O. Effects of size of macrocyclic polyamides on their rate of diffusion in model membranes. Biophys J 1997, 73:2580-2587.
93. Kobayashi T., Storrie B., Simons K., Dotti C.G. A functional barrier to movement of lipids in polarized neurons. Nature 1992, 359:647-650.
94. Winckler B., Forscher P., Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 1999, 397:698-701.
95. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., et al. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat Cell Biol 2003, 5:626-632.
96. Nishimura S.Y., Vrljic M., Klein L.O., McConnell H.M., Moerner W.E. Cholesterol depletion induces solid-like regions in the plasma membrane. Biophys J 2006, 90:927-938.
97. Winckler B., Poo M.M. No diffusion barrier at axon hillock. Nature 1996, 379:213.
98. Boiko T., Vakulenko M., Ewers H., Yap C.C., Norden C., Winckler B. Ankyrin-dependent and independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J Neurosci 2007, 27:590-603.
99. Brachet A., Leterrier C., Irondelle M., Fache M.P., Racine V., Sibarita J.B., et al. Ankyrin G restricts ion channel diffusion at the axonal initial segment before the establishment of the diffusion barrier. J Cell Biol 2010, 191:383-395.
100. Katsuki T., Joshi R., Ailani D., Hiromi Y. Compartmentalization within neurites: its mechanisms and implications. Dev Neurobiol 2011, 71:458-473.
101. Cowan A.E., Myles D.G., Koppel D.E. Lateral diffusion of the Ph-20 protein on guinea-pig sperm - evidence that barriers to diffusion maintain plasma-membrane domains in mammalian sperm. J Cell Biol 1987, 104:917-923.
102. Arts E.G., Jager S., Hoekstra D. Evidence for the existence of lipid-diffusion barriers in the equatorial segment of human spermatozoa. Biochem J 1994, 304:211-218.
103. Ihara M., Kinoshita A., Yamada S., Tanaka H., Tanigaki A., Kitano A., et al. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell 2005, 8:343-352.
104. Kwitny S., Klaus A.V., Hunnicutt G.R. The annulus of the mouse sperm tail is required to establish a membrane diffusion barrier that is engaged during the late steps of spermiogenesis. Biol Reprod 2010, 82:669-678.
105. Selvaraj V., Asano A., Buttke D.E., Sengupta P., Weiss R.S., Travis A.J. Mechanisms underlying the micron-scale segregation of sterols and GM1 in live mammalian sperm. J Cell Physiol 2009, 218:522-536.
106. Xie Y.L., Vessey J.P., Konecna A., Dahm R., Macchi P., Kiebler M.A. The GTP-binding protein septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr Biol 2007, 17:1746-1751.
107. Tada T., Simonetta A., Batterton M., Kinoshita M., Edbauer D., Sheng M. Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr Biol 2007, 17:1752-1758.
108. Francis S.S., Sfakianos J., Lo B., Mellman I. A hierarchy of signals regulates entry of membrane proteins into the ciliary membrane domain in epithelial cells. J Cell Biol 2011, 193:219-233.
109. Hu Q., Milenkovic L., Jin H., Scott M.P., Nachury M.V., Spiliotis E.T., et al. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 2010, 329:436-439.
110. Nachury M.V., Seeley E.S., Jin H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier. Annu Rev Cell Dev Biol 2010, 26:59-87.
111. Takizawa P.A., DeRisi J.L., Wilhelm J.E., Vale R.D. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 2000, 290:341-344.
112. Schmidt K., Nichols B.J. A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr Biol 2004, 14:1002-1006.
113. Caudron F., Barral Y. Septins and the lateral compartmentalization of eukaryotic membranes. Dev Cell 2009, 16:493-506.
114. Saxton M.J. Chemically limited reactions on a percolation cluster. J Chem Phys 2002, 116:203-208.
115. Haggie P.M., Kim J.K., Lukacs G.L., Verkman A.S. Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. Mol Biol Cell 2006, 17:4937-4945.
116. Shibata S.C., Hibino K., Mashimo T., Yanagida T., Sako Y. Formation of signal transduction complexes during immobile phase of NGFR movements. Biochem Biophys Res Commun 2006, 342:316-322.
117. 2+ signaling: single-molecule tracking study 2. J Cell Biol 2007, 177:731-742.
118. Suzuki K.G.N., Fujiwara T.K., Sanematsu F., Iino R., Edidin M., Kusumi A. GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J Cell Biol 2007, 177:717-730.
119. Co C., Wong D.T., Gierke S., Chang V., Taunton J. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 2007, 128:901-913.
120. Subczynski W.K., Antholine W.E., Hyde J.S., Kusumi A. Microimmiscibility and three-dimensional dynamic structures of phosphatidylcholine-cholesterol membranes: translational diffusion of a copper complex in the membrane. Biochemistry 1990, 29:7936-7945.
121. Pasenkiewicz-Gierula M., Subczynski W.K., Kusumi A. Influence of phospholipid unsaturation on the cholesterol distribution in membranes. Rev Biochim 1991, 73:1311-1316.
122. 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: Biomem 2003, 1610:231-243.
123. 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 2000, 11:1645-1655.
124. Kawasaki K., Yin J.J., Subczynski W.K., Hyde J.S., Kusumi A. Pulse EPR detection of lipid exchange between protein-rich raft and bulk domains in the membrane: methodology development and its application to studies of influenza viral membrane. Biophys J 2001, 80:738-748.
125. Varma R., Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 1998, 394:798-801.
126. Meder D., Moreno M.J., Verkade P., Vaz W.L., Simons K. Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc Natl Acad Sci USA 2006, 103:329-334.
127. Baumgart T., Hammond A.T., Sengupta P., Hess S.T., Holowka D.A., Baird B.A., et al. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci USA 2007, 104:3165-3170.
128. Lingwood D., Ries J., Schwille P., Simons K. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc Natl Acad Sci USA 2008, 105:10005-10010.
129. Kaiser H.J., Lingwood D., Levental I., Sampaio J.L., Kalvodova L., Rajendran L., et al. Order of lipid phases in model and plasma membranes. Proc Natl Acad Sci USA 2009, 106:16645-16650.
130. Thomas J.L., Holowka D., Baird B., Webb W.W. Large-scale co-aggregation of fluorescent lipid probes with cell surface proteins. J Cell Biol 1994, 125:795-802.
131. Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 1998, 141:929-942.
132. Janes P.W., Ley S.C., Magee A.I. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol 1999, 147:447-461.
133. Sheets E.D., Holowka D., Baird B. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of Fc epsilon RI and their association with detergent-resistant membranes. J Cell Biol 1999, 145:877-887.
134. Pierini L.M., Maxfield F.R. Flotillas of lipid rafts fore and aft. Proc Natl Acad Sci USA 2001, 98:9471-9473.
135. Matko J., Bodnar A., Vereb G., Bene L., Vamosi G., Szentesi G., et al. GPI-microdomains (membrane rafts) and signaling of the multi-chain interleukin-2 receptor in human lymphoma/leukemia T cell lines. Eur J Biochem 2002, 269:1199-1208.
136. Stoddart A., Dykstra M.L., Brown B.K., Song W.X., Pierce S.K., Brodsky F.M. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 2002, 17:451-462.
137. Dykstra M., Cherukuri A., Sohn H.W., Tzeng S.J., Pierce S.K. Location is everything: lipid rafts and immune cell signaling. Annu Rev Immunol 2003, 21:457-481.
138. Mayor S., Rothberg K.G., Maxfield F.R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 1994, 264:1948-1951.
139. Tanaka K.A., Suzuki K.G.N., Shirai Y.M., Shibutani S.T., Miyahara M.S., Tsuboi H., et al. Membrane molecules mobile even after chemical fixation. Nat Methods 2010, 7:865-866.
140. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys J 2002, 83:2693-2701.
141. 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 2003, 329:793-799.
142. Kusumi A., Suzuki K. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim Biophys Acta Mol Cell Res 2005, 1746:234-251.
143. Morris R.J. Ionic control of the metastable inner leaflet of the plasma membrane: fusions natural and artefactual. FEBS Lett 2010, 584:1665-1669.
144. Morris R.J., Jen A., Warley A. Isolation of nano-meso scale detergent resistant membrane that has properties expected of lipid 'rafts'. J Neurochem 2011, 116:671-677.
145. Pralle A., Keller P., Florin E.L., Simons K., Horber J.K.H. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 2000, 148:997-1007.
146. Warren G.B., Houslay M.D., Metcalfe J.C., Birdsall N.J.M. Cholesterol is excluded from phospholipid annulus surrounding an active calcium-transport protein. Nature 1975, 255:684-687.
147. 2+)-ATPase. Biochim Biophys Acta 1982, 693:398-406.
148. Subczynski W.K., Hyde J.S., Kusumi A. Effect of alkyl chain unsaturation and cholesterol intercalation on oxygen transport in membranes: a pulse ESR spin labeling study. Biochemistry 1991, 30:8578-8590.
149. Garg S., Tang J.X., Ruhe J., Naumann C.A. Actin-induced perturbation of PS lipid-cholesterol interaction: a possible mechanism of cytoskeleton-based regulation of membrane organization. J Struct Biol 2009, 168:11-20.
150. Lasserre R., Guo X.J., Conchonaud F., Hamon Y., Hawchar O., Bernard A.M., et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 2008, 4:538-547.
151. Ehrig J., Petrov E.P., Schwille P. Near-critical fluctuations and cytoskeleton-assisted phase separation lead to subdiffusion in cell membranes. Biophys J 2011, 100:80-89.
152. Tavano R., Contento R.L., Baranda S.J., Soligo M., Tuosto L., Manes S., et al. CD28 interaction with filamin-A controls lipid raft accumulation at the T-cell immunological synapse. Nat Cell Biol 2006, 8:1270-1276.
153. Viola A., Gupta N. Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins. Nat Rev Immunol 2007, 7:889-896.
154. Chaudhuri A., Bhattacharya B., Gowrishankar K., Mayor S., Rao M. Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc Natl Acad Sci USA 2011, 108:14825-14830.
155. Zanoni I., Ostuni R., Capuano G., Collini M., Caccia M., Ronchi A.E., et al. CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 2009, 460:264-268.
156. Paladino S., Lebreton S., Tivodar S., Campana V., Tempre R., Zurzolo C. Different GPI-attachment signals affect the oligomerisation of GPI-anchored proteins and their apical sorting. J Cell Sci 2008, 121:4001-4007.
157. Imjeti N.S., Lebreton S., Paladino S., de la Fuente E., Gonzales A., Zurzolo C. N-Glycosylation instead of cholesterol mediates oligomerization and apical sorting of GPI-APs in FRT cells. Mol Biol Cell 2011, 22:4621-4634.
158. Kenworthy A.K., Nichols B.J., Remmert C.L., Hendrix G.M., Kumar M., et al. Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 2004, 165:735-746.
159. Hess S.T., Gould T.J., Gudheti M.V., Maas S.A., Mills K.D., Zimmerberg J. Dynamic clustered distribution of hemagglutinin resolved at 40nm in living cell membranes discriminates between raft theories. Proc Natl Acad Sci USA 2007, 104:17370-17375.
160. Levental I., Lingwood D., Grzybek M., Coskun U., Simons K. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci USA 2010, 107:22050-22054.
161. Sohn H.W., Tolar P., Jin T., Pierce S.K. Fluorescence resonance energy transfer in living cells reveals dynamic membrane changes in the initiation of B cell signaling. Proc Natl Acad Sci USA 2006, 103:8143-8148.
162. Sohn H.W., Tolar P., Pierce S.K. Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. J Cell Biol 2008, 182:367-379.
163. Chen Y., Veracini L., Benistant C., Jacobson K. The transmembrane protein CBP plays a role in transiently anchoring small clusters of Thy-1, a GPI-anchored protein, to the cytoskeleton. J Cell Sci 2009, 122:3966-3972.
164. Runeberg-Roos P., Saarma M. Neurotrophic factor receptor RET: structure, cell biology, and inherited diseases. Ann Med 2007, 39:572-580.
165. Field K.A., Holowka D., Baird B. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem 1997, 272:4276-4280.
166. Wu M., Holowka D., Craighead H.G., Baird B. Visualization of plasma membrane compartmentalization with patterned lipid bilayers. Proc Natl Acad Sci USA 2004, 101:13798-13803.
167. Larson D.R., Gosse J.A., Holowka D.A., Baird B.A., Webb W.W. Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. J Cell Biol 2005, 171:527-536.
168. Shvartsman D.E., Donaldson J.C., Diaz B., Gutman O., Martin G.S., Henis Y.I. Src kinase activity and SH2 domain regulate the dynamics of Src association with lipid and protein targets. J Cell Biol 2007, 178:675-686.
169. Tolar P., Sohn H.W., Pierce S.K. The initiation of antigen-induced B cell antigen receptor signaling viewed in living cells by fluorescence resonance energy transfer. Nat Immunol 2005, 6:1168-1176.
170. Viola A., Schroeder S., Sakakibara Y., Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999, 283:680-682.
171. Yokosuka T., Saito T. Dynamic regulation of T-cell costimulation through TCR-CD28 microclusters. Immunol Rev 2009, 229:27-40.
172. Huang J., Zarnitsyna V.I., Liu B.Y., Edwards L.J., Jiang N., Evavold B.D., et al. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 2010, 464:932-936.
173. Huppa J.B., Axmann M., Mortelmaier M.A., Lillemeier B.F., Newell E.W., Brameshuber M., et al. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 2010, 463:963-967.
174. Douglass A.D., 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 2005, 121:937-950.
175. Kaizuka Y., Douglass A.D., Vardhana S., Dustin M.L., Vale R.D. The coreceptor CD2 uses plasma membrane microdomains to transduce signals in T cells. J Cell Biol 2009, 185:521-534.
176. Yokosuka T., Saito T. The immunological synapse, TCR microclusters, and T cell activation. Curr Top Microbiol Immunol 2010, 340:81-107.
177. Hartman N.C., Groves J.T. Signaling clusters in the cell membrane. Curr Opin Cell Biol 2011, 23:370-376.
178. Hashimoto-Tane A., Yokosuka T., Sakata-Sogawa K., Sakuma M., Ishihara C., Tokunaga M., et al. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 2011, 34:919-931.
179. 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 1998, 140:1227-1240.
180. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 1999, 397:50-53.
181. Evans E., Ritchie K. Strength of a weak bond connecting flexible polymer chains. Biophys J 1999, 76:2439-2447.
182. Lillemeier B.F., Pfeiffer J.R., Surviladze Z., Wilson B.S., Davis M.M. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc Natl Acad Sci USA 2006, 103:18992-18997.
183. Lillemeier B.F., Mortelmaier M.A., Forstner M.B., Huppa J.B., Groves J.T., Davis M.M. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 2010, 11:90-96.
184. Fahmy T.M., Bieler J.G., Edidin M., Schneck J.P. Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. Immunity 2001, 14:135-143.
185. Schamel W.W., Arechaga I., Risueno R.M., van Santen H.M., Cabezas P., Risco C., et al. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J Exp Med 2005, 202:493-503.
186. James J.R., White S.S., Clarke R.W., Johansen A.M., Dunne P.D., Sleep D.L., et al. Single-molecule level analysis of the subunit composition of the T cell receptor on live T cells. Proc Natl Acad Sci USA 2007, 104:17662-17667.
187. Harding A.S., Hancock J.F. Using plasma membrane nanoclusters to build better signaling circuits. Trends Cell Biol 2008, 18:364-371.
188. Prior I.A., Hancock J.F. Ras trafficking, localization and compartmentalized signalling. Semin Cell Dev Biol 2011.
189. Williamson D.J., Owen D.M., Rossy J., Magenau A., Wehrmann M., Gooding J.J., et al. Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat Immunol 2011, 12:655-662.
190. Kasai R.S., Suzuki K.G.N., Prossnitz E.R., Koyama-Honda I., Nakada C., Fujiwara T.K., et al. Full characterization of GPCR monomer-dimmer dynamic equilibrium by single molecule imaging. J Cell Biol 2011, 192:463-480.
191. Hern J.A., Baig A.H., Mashanov G.I., Birdsall B., Corrie J.E., Lazareno S., et al. Formation and dissociation of M(1) muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc Natl Acad Sci USA 2010, 107:2693-2698.
192. Honerkamp-Smith A.R., Cicuta P., Collins M.D., Veatch S.L., den Nijs M., Schick M., et al. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophys J 2008, 95:236-246.
193. Honerkamp-Smith A.R., Veatch S.L., Keller S.L. An introduction to critical points for biophysicists; observations of compositional heterogeneity in lipid membranes. Biochim Biophys Acta 2009, 1788:53-63.
194. Martin R.B., Yeagle P.L. Models for lipid organization in cholesterol-phospholipid bilayers including cholesterol dimer formation. Lipids 1978, 13:594-597.