Imaging lipid domains in cell membranes: The advent of super-resolution fluorescence microscopy

Frontiers in Plant Science

Volumn 4, Issue DEC, 2013, Pages

  Owen, Dylan M ^a   Gaus, Katharina ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Cell membranes; Fluorescence; Lipid rafts; Membrane microdomains; Super resolution

Indexed keywords

EID: 84901056407     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00503     Document Type: Article

References (96)

1. Bacia, K., Scherfeld, D., Kahya, N., and Schwille, P. (2004). Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87, 1034-1043. doi: 10.1529/biophysj.104.040519
2. Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifa-Cino, J. S., et al. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science 313,1642-1645. doi: 10.1126/science.1127344
3. Bezlyepkina, N., Gracia, R. S., Shchelokovskyy, P., Lipowsky, R., and Dimova, R. (2013). Phase diagram and tie-line determination for the ternary mixture DOPC/eSM/cholesterol. Biophys. J. 104, 1456-1464. doi: 10.1016/j.bpj.2013.02.024
4. Borner, G. H. H., Sherrier, D. J., Weimar, T., Michaelson, L. V., Hawkins, N. D., MacAskill, A., et al. (2005). Analysis of detergent-resistant membranes in Ara- bidopsis. Evidence for plasma membrane lipid rafts. PlantPhysiol 137,104-116. doi: 10.1104/pp.104.053041
5. Brown, A. C. N., Oddos, S., Dobbie, I.M., Alakoskela, J.-M., Parton, R. M., Eissmann, P., et al. (2011). Remodelling ofcortical actinwhere lytic granules dockatnatural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol. 9:e1001152. doi: 10.1371/journal.pbio.1001152
6. Brown, D. A. (2006). Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21, 430-439. doi: 10.1152/physiol.00032.2006
7. Carrasco, M., Amorim, M. J., and Digard, P. (2004). Lipid raft-dependent targeting of the influenza A virus nucleoprotein to the apical plasma membrane. Traffic 5, 979-992. doi: 10.1111/j.1600-0854.2004.00237.x
8. Chaudhuri, A., Bhattacharya, B., Gowrishankar, K., Mayor, S., and Rao, M. (2011). Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc. Natl. Acad. Sci. 108,14825-14830. doi: 10.1073/pnas.1100007108
9. Chen, Y., Qin, J., Cai, J., and Chen, Z.W. (2009). Coldinducesmicro- andnano-scale reorganization of lipid raft markers at mounds of T-cell membrane fluctuations. PLoS ONE 4:e5386. doi: 10.1371/journal.pone.0005386
10. Dinic, J., Ashrafzadeh, P., and Parmryd, I. (2013). Actin filaments attachment at the plasma membrane in live cells cause the formation of ordered lipid domains. Biochim. Biophys. Acta 1828, 1102-1111. doi: 10.1016/j.bbamem.2012.12. 004
11. Dodelet-Devillers, A., Cayrol, R., van Horssen, J., Haqqani, A., de Vries, H., Engel- hardt, B., et al. (2009). Functions of lipid raft membrane microdomains at the blood-brainbarrier. J. Mol. Med. 87, 765-774. doi: 10.1007/s00109-009-0488-6
12. Dupuy, A. D., and Engelman, D. M. (2008). Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 105, 2848-2852. doi: 10.1073/pnas.0712379105
13. Edidin, M. (2006). Switching sides: the actin/membrane lipid connection. Biophys. J. 91, 3963. doi: 10.1529/biophysj.106.094078
14. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., et al. (2009). Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457, 1159-1163. doi: 10.1038/nature07596
15. Fitzgibbon, J., Bell, K., King, E., and Oparka, K. (2010). Super-resolution imaging of plasmodesmata using three-dimensional structured illumination microscopy. PlantPhysiol. 153,1453-1463. doi: 10.1104/pp.110.157941
16. Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K., and Kusumi, A. (2002). Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. CellBiol. 157, 1071-1082. doi: 10.1083/jcb.200202050
17. Gaus, K., Gratton, E., Kable, E. P. W., Jones, A. S., Gelissen, I., Kritharides, L., et al. (2003). Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. U.S.A. 100, 15554-15559. doi: 10.1073/pnas.2534386100
18. Gaus, K., Le Lay, S., Balasubramanian, N., and Schwartz, M. A. (2006). Integrin- mediated adhesion regulates membrane order. J. Cell Biol. 174, 725-734. doi: 10.1083/jcb.200603034
19. Glebov, O. O., and Nichols, B. J. (2004). Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat. Cell Biol. 6, 238-243. doi: 10.1038/ncb1103
20. Gomez-Mouton, C., Lacalle, R. A., Mira, E., Jimenez-Baranda, S., Barber, D. F., Carrera, A. C., et al. (2004). Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J. Cell Biol. 164, 759-768. doi: 10.1083/jcb.200309101
21. Gowrishankar, K., Ghosh, S., Saha, S., Mayor, R. C. S., and Rao, M. (2012). Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149,1353-1367. doi: 10.1016/j.cell.2012.05.008
22. Grennan, A. K. (2007). Lipid rafts in plants. Plant Physiol. 143, 1083-1085. doi: 10.1104/pp.104.900218
23. Gudheti, M. V., Curthoys, N. M., Gould, T. J., Kim, D., Gunewardene, M. S., Gabor, K. A., et al. (2013). Actin mediates the nanoscale membrane organization of the clusteredmembraneproteininfluenzahemagglutinin. Biophys. J. 104,2182-2192. doi: 10.1016/j.bpj.2013.03.054
24. Gupta, N., and DeFranco, A. L. (2007). Lipid rafts and B cell signaling. Semin. Cell Dev. Biol. 18,616-626. doi: 10.1016/j.semcdb.2007.07.009
25. Gustafsson, M. G. L. (2000). Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198, 82-87. doi: 10.1046/j.1365-2818.2000.00710.x
26. Hancock, J. F. (2006). Lipidrafts: contentious onlyfromsimplistic standpoints. Nat. Rev.Mol. CellBiol. 7,456-462.doi: 10.1038/nrm1925
27. Hein, B., Willig, K. I., and Hell, S. W. (2008). Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell. Proc. Natl. Acad. Sci. U.S.A. 105,14271-14276. doi: 10.1073/pnas.0807705105
28. Heinemann, F., Vogel, S. K., and Schwille, P. (2013). Lateral membrane diffusion modulated by a minimal actin cortex. Biophys. J. 104, 1465-1475. doi: 10.1016/j.bpj.2013.02.042
29. Hell, S. W., and Wichmann, J. (1994). Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780-782. doi: 10.1364/0L.19.000780
30. Hess, S. T., Gould, T. J., Gudheti, M. V., Maas, S. A., Mills, K. D., and Zimmerberg, J. (2007). Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl. Acad. Sci. U.S.A. 104, 17370-17375. doi: 10.1073/pnas.0708066104
31. Honigmann, A., Mueller, V., Hell, S. W., and Eggeling, C. (2013). STED microscopy detects and quantifies liquid phase separation in lipid membranes using a new far-red emitting fluorescent phosphoglycerolipid analogue. Faraday Discuss. 161, 77-89. doi: 10.1039/c2fd20107k
32. Jacobson, K., Mouritsen, O. G., and Anderson, R. G. W. (2007). Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9, 7-14. doi: 10.1038/ncb0107-7
33. Jin, L., Millard, A. C., Wuskell, J. P., Dong, X., Wu, D., Clark, H. A., et al. (2006). Characterization and application of a new optical probe for membrane lipid domains. Biophys. J. 90, 2563-2575. doi: 10.1529/biophysj.105. 072884
34. Jury, E. C., Flores-Borja, F., and Kabouridis, P. S. (2007). Lipid rafts in T cell signalling and disease. Semin. Cell Dev. Biol. 18, 608-615. doi: 10.1016/j.semcdb.2007.08.002
35. Kaiser, H.-J., Lingwood, D., Levental, I., Sampaio, J. L., Kalvodova, L., Rajendran, L., et al. (2009). Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. U.S.A. 106,16645-16650. doi: 10.1073/pnas.0908987106
36. Kaiser, H.-J., Surma, M. A., Mayer, F., Levental, I., Grzybek, M., Klemm, R. W., et al. (2011). Molecular convergence of bacterial and eukaryotic surface order. J. Biol. Chem. 286, 40631-40637. doi: 10.1074/jbc.M111.276444
37. Khurana, S., Krementsov, D. N., de Parseval, A., Elder, J. H., Foti, M., and Thali, M. (2007). Human immunodeficiency virus type 1 and influenza virus exit via different membrane microdomains. J. Virol. 81, 12630-12640. doi: 10.1128/JVI.01255-07
38. Klein, T., Loschberger, A., Proppert, S., Wolter, S., van de Linde, S., and Sauer, M. (2011). Live-cell dSTORM with SNAP-tag fusion proteins. Nat. Methods 8, 7-9. doi: 10.1038/nmeth0111-7b
39. Kleine-Vehn, J., Wabnik, K., Martiniere, A., Langowski, L., Willig, K., Naramoto, S., et al. (2011). Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7, 540. doi: 10.1038/msb.2011.72
40. Kner, P., Chhun, B. B., Griffis, E. R., Winoto, L., and Gustafsson, M. G. L. (2009). Super-resolution video microscopy of live cells by structured illumination. Nat. Methods 6, 339-342. doi: 10.1038/nmeth.1324
41. Kusumi, A., Koyama-Honda, I., and Suzuki, K. (2004). Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5,213-230. doi: 10.1111/j.1600-0854.2004.0178.x
42. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., etal. (2005). Paradigm shift of the plasma membrane concept from the twodimensional continuum fluid to the partitioned fluid: high-speed single-molecule trackingofmembranemolecules. Annu. Rev. Biophys. Biomol. Struct. 34,351-378. doi: 10.1146/annurev.biophys.34.040204.144637
43. Lasserre, R., Guo, X.-J., Conchonaud, F., Hamon, Y., Hawchar, O., Bernard, A.-M., et al. (2008). Raft nanodomains contribute toAkt/PKB plasmamembrane recruitment and activation. Nat. Chem. Biol. 4, 538-547. doi: 10.1038/nchem- bio.103
44. Lenne, P.-F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.-J., etal. (2006). Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25, 3245-3256. doi: 10.1038/sj.emboj.7601214
45. Levental, I., Grzybek, M., and Simons, K. (2010). Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49, 6305-6316. doi: 10.1021/bi100882y
46. Lingwood, D., Ries, J., Schwille, P., and Simons, K. (2008). Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. U.S.A. 105, 10005-10010. doi: 10.1073/pnas.0804374105
47. London, E., and Brown, D. A. (2000). Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta 1508, 182-195. doi: 10.1016/S0304-4157(00)00007-1
48. Lorizate, M., Brugger, B., Akiyama, H., Glass, B., Muller, B., Anderluh, G., et al. (2009). Probing HIV-1 membrane liquid order by Laurdan staining reveals producer cell-dependent differences. J. Biol. Chem. 284, 22238-22247. doi: 10.1074/jbc.M109.029256
49. Machta, B., Papanikolaou, S., Sethna, J. P., and Veatch, S. L. (2011). Minimal model of plasma membrane heterogeneity requires coupling cortical actin to criticality. Biophys.J. 100, 1668-1677. doi: 10.1016/j.bpj.2011.02.029
50. Magee, A. I., Adler, J., and Parmryd, I. (2005). Cold-induced coalescence of T-cell plasma membrane microdomains activates signalling pathways. J. Cell Sci. 118, 3141-3151. doi: 10.1242/jcs.02442
51. Manes, S., del Real, G., Lacalle, R. A., Lucas, P., Gomez-Mouton, C., Sanchez-Palomino, S., et al. (2000). Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1, 190-196. doi: 10.1093/embo-reports/kvd025
52. Manzo, C., van Zanten, T. S., and Garcia-Parajo, M. F. (2011). Nanoscale fluorescence correlation spectroscopy on intact living cell membranes with NSOM probes. Biophys. J. 100, L8-L10. doi: 10.1016/j.bpj.2010.12.3690
53. Marquez, D. C., Chen, H.-W., Curran, E. M., Welshons, W. V., and Pietras, R. J. (2006). Estrogen receptors in membrane lipid rafts and signal transduction in breast cancer. Mol. Cell. Endocrinol. 246, 91-100. doi: 10.1016/j.mce.2005.11.020
54. Martin, S. W., Glover, B. J., and Davies, J. M. (2005). Lipid microdomains - plant membranes get organized. Trends Plant Sci. 10, 263-265. doi: 10.1016/j.tplants.2005.04.004
55. Mattila, P. K., Feest, C., Depoil, D., Treanor, B., Montaner, B., Otipoby, K. L., et al. (2013). The actin and tetraspanin networks organize receptor nanoclusters to regulate B cell receptor-mediated signaling. Immunity 38, 461-474. doi: 10.1016/j.immuni.2012.11.019
56. Miguel, L., Owen, D. M., Lim, C., Liebig, C., Evans, J., Magee, A. I., et al. (2011). Primary human CD4+ T cells have diverse levels of membrane lipid order that correlate with their function. J. Immunol. 186, 3505-3516. doi: 10.4049/jimmunol.1002980
57. Morone, N., Fujiwara, T., Murase, K., Kasai, R. S., Ike, H., Yuasa, S., et al. (2006). Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J. Cell Biol. 174, 851-862. doi: 10.1083/jcb.200606007
58. Mueller, V., Ringemann, C., Honigmann, A., Schwarzmann, G., Medda, R., Leutenegger, M., et al. (2011). STED nanoscopy reveals molecular details of cholesterol- and cytoskeleton-modulated lipidinteractions in living cells. Biophys. J. 101, 1651-1660. doi: 10.1016/j.bpj.2011.09.006
59. Munro, S. (2003). Lipid rafts: elusive or illusive? Cell 115, 377-388. doi: 10.1016/S0092-8674(03)00882-1
60. Owen, D.M., Magenau, A., Majumdar, A., and Gaus, K. (2010a). Imagingmembrane lipid order in whole, living vertebrate organisms. Biophys. J. 99, L7-L9. doi: 10.1016/j.bpj.2010.04.022
61. Owen, D. M., Oddos, S., Kumar, S., Davis, D. M., Neil, M. A. A., French, P. M. W., et al. (2010b). High plasma membrane lipid order imaged at the immunological synapse periphery in live T cells. Mol. Membr. Biol. 27, 178-189. doi: 10.3109/09687688.2010.495353
62. Owen, D. M., Rentero, C., Rossy, J., Magenau, A., Williamson, D., Rodriguez, M., et al. (2010c). PALM imaging and cluster analysis of protein heterogeneity at the cell surface. J. Biophotonics 3, 446-454. doi: 10.1002/jbio.200900089
63. Owen, D. M., Magenau, A., Williamson, D., and Gaus, K. (2012a). The lipid raft hypothesis revisited - new insights on raft composition and function from super-resolution fluorescence microscopy. BioEssays 34, 739-747. doi: 10.1002/bies.201200044
64. Owen, D. M., Rentero, C., Magenau, A., Abu-Siniyeh, A., and Gaus, K. (2012b). Quantitative imaging of membrane lipid order in cells and organisms. Nat. Protocols 7, 24-35. doi: 10.1038/nprot.2011.419
65. Owen, D. M., Williamson, D. J., Magenau, A., and Gaus, K. (2012c). Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nat. Commun. 3, 1256. doi: 10.1038/ncomms2273
66. Parton, R., and Simons, K. (1995). Digging into caveolae. Science 269, 1398-1399. doi: 10.1126/science.7660120
67. Peskan, T., Westermann, M., and Oelmuller, R. (2000). Identification of low-density Triton X-100-insoluble plasma membrane microdomains in higher plants. Eur. J. Biochem. 267, 6989-6995. doi: 10.1046/j.1432-1327.2000.01776.x
68. Pike, L. J. (2006). Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 47, 1597-1598. doi: 10.1194/jlr.E600002-JLR200
69. Pralle, A., Keller, P., Florin, E.-L., Simons, K., and Horber, J. K. H. (2000). Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammaliancells. J. CellBiol. 148,997-1008. doi: 10.1083/jcb.148.5.997
70. Rak, G. D., Mace, E. M., Banerjee, P. P., Svitkina, T., and Orange, J. S. (2011). Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol. 9:e1001151. doi: 10.1371/journal.pbio. 1001151
71. Rentero, C., Zech, T., Quinn, C. M., Engelhardt, K., Williamson, D., Gre-Wal, T., et al. (2008). Functional implications of plasma membrane condensation for T cell activation. PLoS ONE 3:e2262. doi: 10.1371/journal.pone. 0002262
72. Rossy, J., Owen, D. M., Williamson, D. J., Yang, Z., and Gaus, K. (2013). Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat. Immunol. 14, 82-89. doi: 10.1038/ni.2488
73. Rust, M. J., Bates, M., and Zhuang, X. (2006). Sub-diffraction-limit imaging by stochastic opticalreconstructionmicroscopy (STORM). Nat. Methods 3,793-796. doi: 10.1038/nmeth929
74. Sengupta, P., Jovanovic-Talisman, T., Skoko, D., Renz, M., Veatch, S. L., and Lippincott-Schwartz, J. (2011). Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat. Methods 8, 969-975. doi: 10.1038/nmeth.1704
75. Sengupta, P., and Lippincott-Schwartz, J. (2012). Quantitative analysis of photoactivated localization microscopy (PALM) datasets using pair-correlation analysis. BioEssays 34, 396-405. doi: 10.1002/bies.201200022
76. Sezgin, E., Levental, I., Grzybek, M., Schwarzmann, G., Mueller, V., Honigmann, A., et al. (2012). Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta 1818, 1777-1784. doi: 10.1016/j.bbamem.2012.03.007
77. Shao, L., Kner, P., Rego, E. H., and Gustafsson, M. G. L. (2011). Super-resolution 3D microscopy of live whole cells using structured illumination. Nat. Methods 8, 1044-1046. doi: 10.1038/nmeth.1734
78. Shogomori, H., and Brown, D. A. (2003). Use of detergents to study membrane rafts: The good, the bad, and the ugly. Biol. Chem. 384, 1259-1263. doi: 10.1515/BC.2003.139
79. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572. doi: 10.1038/42408
80. Simons, K. and Vaz, W. L. C. (2004). Model systems, lipid rafts and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33, 269-295. doi: 10.1146/annurev.biophys.32.110601.141803
81. Singer, S. J., and Nicolson, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science 175, 720-731. doi: 10.1126/science.175.4023.720
82. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Gr0nborg, M., Riedel, D., et al. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831-846. doi: 10.1016/j.cell.2006.10.030
83. Takeda, M., Leser, G. P., Russell, C. J., and Lamb, R. A. (2003). Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc. Natl. Acad Sci. U.S.A 100,14610-14617. doi: 10.1073/pnas.2235620100
84. Toulmay, A., and Prinz, W. A. (2013). Direct imaging reveals stable, micrometer- scale lipid domains that segregate proteins in live cells. J. Cell. Biol. 202, 35-44. doi: 10.1083/jcb.201301039
85. van Meer, G., Stelzer, E., Wijnaendts-van-Resandt, R., and Simons, K. (1987). Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J. Cell Biol. 105, 1623-1635. doi: 10.1083/jcb.105.4.1623
86. van Zanten, T. S., Cambi, A., Koopman, M., Joosten, B., Figdor, C. G., and Garcia-Parajo, F. M. (2009). Hotspots of GPI-anchored proteins and integrin nanoclusters function as nucleation sites for cell adhesion. Proc. Natl. Acad. Sci. U.S.A 106,18557-18562. doi: 10.1073/pnas.0905217106
87. van Zanten, T. S., Gomez, J., Manzo, C., Cambi, A., Buceta, J., Reigada, R., et al. (2010). Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc. Natl. Acad. Sci. U.S.A 107, 15437-15442. doi: 10.1073/pnas.1003876107
88. Ventimiglia, L. N., and Alonso, M. A. (2013). The role of membrane rafts in Lck transport, regulation and signalling in T-cells. Biochem. J. 454, 169-179. doi: 10.1042/BJ20130468
89. Vicidomini, G., Moneron, G., Han, K.Y., Westphal, V., Ta, H., Reuss, M., et al. (2011). Sharper low-power STED nanoscopy by time gating. Nat. Methods 8, 571-573. doi: 10.1038/nmeth.1624
90. Vobornik, D., Banks, D. S., Lu, Z., Fradin, C., Taylor, R., and Johnston, L. J. (2008). Fluorescence correlation spectroscopy with sub-diffraction-limited resolution using near-field optical probes. App. Phys. Lett. 93, 163904. doi: 10.1063/1.2998602
91. Wawrezinieck, L., Rigneault, H., Marguet, D., and Lenne, P.-F. (2005). Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys. J. 89, 4029-4042. doi: 10.1529/biophysj.105. 067959
92. Williamson, D. J., Owen, D. M., Rossy, J., Magenau, A., Wehrmann, M., Gooding, J. J., et al. (2011). Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat. Immunol. 12, 655-662. doi: 10.1038/ni. 2049
93. Xu, K., Babcock, H. P., and Zhuang, X. (2012). Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat. Methods 9, 185-188. doi: 10.1038/nmeth.1841
94. Xu, K., Zhong, G., and Zhuang, X. (2013). Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339, 452-456. doi: 10.1126/science.1232251
95. Yang, N., Jiang, J., Deng, L., Waters, M. J., Wang, X., and Frank, S. J. (2010). Growth hormone receptor targeting to lipid rafts requires extracellular subdomain 2. Biochem. Biophys. Res. Commun. 391, 414-418. doi: 10.1016/j.bbrc.2009. 11.072
96. Zhong, L., Zeng, G., Lu, X., Wang, R. C., Gong, G., Yan, L., et al. (2009). NSOM/QD- based direct visualization of CD3-induced and CD28-enhanced nanospatial coclustering of TCR and coreceptor in nanodomains in T cell activation. PLoS ONE 4:e5945. doi: 10.1371/journal.pone.0005945