Dynamics in the plasma membrane: How to combine fluidity and order

EMBO Journal

Volumn 25, Issue 15, 2006, Pages 3446-3457

  Marguet, Didier ^a,b,c   Lenne, Pierre François ^c,d   Rigneault, Hervé ^c,d   He, Hai Tao ^a,b,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b INSERM   (France)

^c CNRS   (France)

^d AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Actin meshwork; Cell membrane; Fluorescence microscopy; Lateral diffusion; Membrane microdomain

Indexed keywords

CELL FUNCTION; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CHEMICAL REACTION; DIFFUSION; FLUORESCENCE; MEMBRANE MODEL; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SUPRAMOLECULAR CHEMISTRY;

ANIMALS; CELL MEMBRANE; HUMANS; KINETICS; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE;

EID: 33747591249     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601204     Document Type: Review

References (76)

1. Almeida PF, Pokorny A, Hinderliter A (2005) Thermodynamics of membrane domains. Biochim Biophys Acta 1720: 1-13
2. Axelrod D (2001) Total internal reflection fluorescence microscopy in cell biology. Traffic 2: 764-774
3. Bacia K, Kim SA, Schwille P (2006) Fluorescence cross-correlation spectroscopy in living cells. Nat Methods 3: 83-89
4. Bacia K, Scherfeld D, Kahya N, Schwille P (2004) Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys J 87: 1034-1043
5. Berg HC (1983) Random Walks in Biology. Princeton: Princeton University Press
6. Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275: 17221-17224
7. Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, Barr VA, Samelson LE (2002) T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 158: 1263-1275
8. Cho H, Kim YA, Yoon JY, Lee D, Kim JH, Lee SH, Ho WK (2005) Low mobility of phosphatidylinositol 4,5-bisphosphate underlies receptor specificity of Gq-mediated ion channel regulation in atrial myocytes. Proc Natl Acad Sci USA 102: 15241-15246
9. Cognet L, Tardin C, Boyer D, Choquet D, Tamarat P, Lounis B (2003) Single metallic nanoparticle imaging for protein detection in cells. Proc Natl Acad Sci USA 100: 11350-11355
10. Cole NB, Smith CL, Sciaky N, Terasaki M, Edidin M, Lippincott-Schwartz J (1996) Diffusional mobility of Golgi proteins in membranes of living cells. Science 273: 797-801
11. Costantino S, Comeau JW, Kolin DL, Wiseman PW (2005) Accuracy and dynamic range of spatial image correlation and cross-correlation spectroscopy. Biophys J 89: 1251-1260
12. Cuatrecasas P (1974) Membrane receptors. Annu Rev Biochem 43: 169-214
13. Dahan M, Levi S, Luccardini C, Rostaing P, Riveau B, Triller A (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302: 442-445
14. Dietrich C, Bagatolli LA, Volovyk ZN, Thompson NL, Levi M, Jacobson K, Gratton E (2001) Lipid rafts reconstituted in model membranes. Biophys J 80: 1417-1428
15. Digman MA, Brown CM, Sengupta P, Wiseman PW, Horwitz AR, Gratton E (2005) Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophys J 89: 1317-1327
16. Douglass AD, Vale RD (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121: 937-950
17. Edidin M (2003) The State of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32: 257-283
18. Edidin M, Zuniga MC, Sheetz MP (1994) Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc Natl Acad Sci USA 91: 3378-3382
19. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438: 578-580
20. Frye LD, Edidin M (1970) The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons. J Cell Sci 7: 319-335
21. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157: 1071-1081
22. Gambin Y, Lopez-Esparza R, Reffay M, Sierecki E, Gov NS, Genest M, Hodges RS, Urbach W (2006) Lateral mobility of proteins in liquid membranes revisited. Proc Natl Acad Sci USA 103: 2098-2102
23. Gaus K, Chklovskaia E, Fazekas de St Groth B, Jessup W, Harder T (2005) Condensation of the plasma membrane at the site of T lymphocyte activation. J Cell Biol 171: 121-131
24. Gheber LA, Edidin M (1999) A model for membrane patchiness: lateral diffusion in the presence of barriers and vesicle traffic. Biophys J 77: 3163-3175
25. Hell S, Stelzer EHK (1992) Properties of a 4Pi confocal fluorescence microscope. J Opt Soc Am A 9: 2159-2166
26. Hofmann M, Eggeling C, Jakobs S, Hell SW (2005) Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci USA 102: 17565-17569
27. Hwang J, Gheber LA, Margolis L, Edidin M (1998) Domains in cell plasma membranes investigated by near-field scanning optical microscopy. Biophys J 74: 2184-2190
28. Ianoul A, Grant DD, Rouleau Y, Bani-Yaghoub M, Johnston LJ, Pezacki JP (2005) Imaging nanometer domains of beta-adrenergic receptor complexes on the surface of cardiac myocytes. Nat Chem Biol 1: 196-202
29. Karnovsky MJ, Kleinfeld AM, Hoover RL, Klausner RD (1982) The concept of lipid domains in membranes. J Cell Biol 94: 1-6
30. Kenworthy AK, Nichols BJ, Remmert CL, Hendrix GM, Kumar M, Zimmerberg J, Lippincott-Schwartz J (2004) Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165: 735-746
31. Klar TA, Jakobs S, Dyba M, Egner A, Hell SW (2000) Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci USA 97: 8206-8210
32. Korlach J, Schwille P, Webb WW, Feigenson GW (1999) Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc Natl Acad Sci USA 96: 8461-8466
33. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (2005) 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: 351-378
34. Lagerholm BC, Weinreb GE, Jacobson K, Thompson NL (2005) Detecting microdomains in intact cell membranes. Annu Rev Phys Chem 56: 309-336
35. Larson DR, Gosse JA, Holowka DA, Baird BA, Webb WW (2005) Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. J Cell Biol 171: 527-536
36. Lenne PF, Wawrezinieck L, Conchonaud F, Wurtz O, Boned A, Guo XJ, Rigneault H, He HT, Marguet D (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J (in press)
37. Li L, Wang H, Cheng JX (2005) Quantitative coherent anti-stokes Raman scattering imaging of lipid distribution in coexisting domains. Biophys J 89: 3480-3490
38. Lidke DS, Lidke KA, Rieger B, Jovin TM, Arndt-Jovin DJ (2005) Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J Cell Biol 170: 619-626
39. Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16: 557-589
40. Lommerse PH, Blab GA, Cognet L, Harms GS, Snaar-Jagalska BE, Spaink HP, Schmidt T (2004) Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. Biophys J 86: 609-616
41. London E (2005) How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells. Biochim Biophys Acta 1746: 203-220
42. Marguet D, Spiliotis ET, Pentcheva T, Lebowitz M, Schneck J, Edidin M (1999) Lateral diffusion of GFP-tagged H2Ld molecules and of GFP-TAP1 reports on the assembly and retention of these molecules in the endoplasmic reticulum. Immunity 11: 231-240
43. McConnell HM, Vrljic M (2003) Liquid-liquid immiscibility in membranes. Annu Rev Biophys Biomol Struct 32: 469-492
44. Meder D, Moreno MJ, Verkade P, Vaz WL, Simons K (2006) Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc Natl Acad Sci USA 103: 329-334
45. Medintz IL, Uyeda HT, Goldman ER, Mattoussi H (2005) Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater 4: 435-446
46. Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, Sundaresan G, Wu AM, Gambhir SS, Weiss S (2005) Quantum dots for live cells, in vivo imaging, and diagnostics. Science 307: 538-544
47. Nicolini C, Baranski J, Schlummer S, Palomo J, Lumbierres-Burgues M, Kahms M, Kuhlmann J, Sanchez S, Gratton E, Waldmann H, Winter R (2006) Visualizing association of N-Ras in lipid microdomains: influence of domain structure and interfacial adsorption. J Am Chem Soc 128: 192-201
48. Petersen NO, Hoddelius PL, Wiseman PW, Seger O, Magnusson KE (1993) Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application. Biophys J 65: 1135-1146
49. Pons T, Moreaux L, Mongin O, Blanchard-Desce M, Mertz J (2003) Mechanisms of membrane potential sensing with second-harmonic generation microscopy. J Biomed Opt 8: 428-431
50. Potma EO, Xie XS (2005) Direct visualization of lipid phase segregation in single lipid bilayers with coherent anti-stokes Raman scattering microscopy. Chem Phys Chem 6: 77-79
51. Pralle A, Keller P, Florin EL, Simons K, Horber JK (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148: 997-1008
52. Pucadyil TJ, Kalipatnapu S, Harikumar KG, Rangaraj N, Karnik SS, Chattopadhyay A (2004) G-protein-dependent cell surface dynamics of the human serotonin1A receptor tagged to yellow fluorescent protein. Biochemistry 43: 15852-15862
53. Roke S, Schins J, Muller M, Bonn M (2003) Vibrational spectroscopic investigation of the phase diagram of a biomimetic lipid monolayer. Phys Rev Lett 90: 128101
54. Saffman PG, Delbruck M (1975) Brownian motion in biological membranes. Proc Natl Acad Sci USA 72: 3111-3113
55. Sako Y, Kusumi A (1994) Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J Cell Biol 125: 1251-1264
56. Sanchez-Andres A, Chen Y, Muller JD (2005) Molecular brightness determined from a generalized form of Mandel's Q-parameter. Biophys J 89: 3531-3547
57. Sawano A, Takayama S, Matsuda M, Miyawaki A (2002) Lateral propagation of EGF signaling after local stimulation is dependent on receptor density. Dev Cell 3: 245-257
58. Saxton MJ (1989) The spectrin network as a barrier to lateral diffusion in erythrocytes. A percolation analysis. Biophys J 55: 21-28
59. Saxton MJ, Jacobson K (1997) Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26: 373-399
60. Schutz GJ, Kada G, Pastushenko VP, Schindler H (2000) Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J 19: 892-901
61. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909
62. Sheetz MP, Schindler M, Koppel DE (1980) Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature 285: 510-511
63. Shinbrot T, Muzzio FJ (2001) Noise to order. Nature 410: 251-258
64. Shvartsman DE, Kotler M, Tall RD, Roth MG, Henis YI (2003) Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J Cell Biol 163: 879-888
65. Simons K, Vaz WL (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33: 269-295
66. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720-731
67. Sprong H, van Der Sluijs P, van Meer G (2001) How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol 2: 504-513
68. Tang Q, Edidin M (2001) Vesicle trafficking and cell surface membrane patchiness. Biophys J 81: 196-203
69. Tardin C, Cognet L, Bats C, Lounis B, Choquet D (2003) Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 22: 4656-4665
70. Turner MS, Sens P, Socci ND (2005) Nonequilibrium raftlike membrane domains under continuous recycling. Phys Rev Lett 95: 168301
71. van Meer G (2005) Cellular lipidomics. EMBO J 24: 3159-3165
72. Verveer PJ, Wouters FS, Reynolds AR, Bastiaens PI (2000) Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. Science 290: 1567-1570
73. Wawrezinieck L, Rigneault H, Marguet D, Lenne P-F (2005) Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys J 89: 4029-4042
74. Wurpel GW, Rinia HA, Muller M (2005) Imaging orientational order and lipid density in multilamellar vesicles with multiplex CARS microscopy. J Microsc 218: 37-45
75. Yechiel E, Edidin M (1987) Micrometer-scale domains in fibroblast plasma membranes. J Cell Biol 105: 755-760
76. Zumbusch A, Holtom GR, Xie XS (1999) Vibrationnal microscopy using coherent anti-stokes Raman scattering. Phys Rev Lett 82: 4014-4017