Membrane microdomains: From seeing to understanding

Frontiers in Plant Science

Volumn 5, Issue FEB, 2014, Pages

  Truong Quang, Binh An ^a   Lenne, Pierre François ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Multiscale organization; Plasma membrane microdomains; Protein clusters; Quantitative imaging; Suppersolution

Indexed keywords

EID: 84901022255     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00018     Document Type: Review

References (187)

1. Aaron, J. S., Carson, B. D., and Timlin, J. A. (2012). Characterization of differential Toll-like receptor responses below the optical diffraction limit. Small 8, 3041-3049. doi: 10.1002/smll.201200106
2. Abbe, E. (1873). Beiträge zur theorie des mikroskops und der mikroskopischen Wahrnehmung: I. Die construction von mikroskopen auf grund der theorie. Arch. Für Mikrosk. Anat. 9, 413-418. doi: 10.1007/BF02956173
3. Ando, R., Mizuno, H., and Miyawaki, A. (2004). Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306, 1370-1373. doi: 10.1126/science.1102506
4. Annibale, P., Vanni, S., Scarselli, M., Rothlisberger, U., and Radenovic, A. (2011). Identification of clustering artifacts in photoactivated localization microscopy. Nat. Methods 8, 527-528. doi: 10.1038/nmeth.1627
5. Baddeley, D., Jayasinghe, I. D., Lam, L., Rossberger, S., Cannell, M. B., and Soeller, C. (2009). Optical single-channel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A. 106, 22275-22280. doi: 10.1073/pnas.0908971106
6. Bar-On, D., Wolter, S., van de Linde, S., Heilemann, M., Nudelman, G., Nachliel, E., et al. (2012). Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters. J. Biol. Chem. 287, 27158-27167. doi: 10.1074/jbc.M112.353250
7. Batada, N. N., Shepp, L. A., and Siegmund, D. O. (2004). Stochastic model of protein-protein interaction: why signaling proteins need to be colocalized. Proc. Natl. Acad. Sci. U.S.A. 101, 6445-6449. doi: 10.1073/pnas.0401314101
8. Beheiry, M. E., and Dahan, M. (2013). ViSP: representing single-particle localizations in three dimensions. Nat. Methods 10, 689-690. doi: 10.1038/nmeth.2566
9. Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifacino, J. S., et al. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645. doi: 10.1126/science.1127344
10. Blagoev, B., Kratchmarova, I., Ong, S.-E., Nielsen, M., Foster, L. J., and Mann, M. (2003). A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat. Biotechnol. 21, 315-318. doi: 10.1038/nbt790
11. Brown, D. A., and Rose, J. K. (1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544. doi: 10.1016/0092-8674(92)90189-J
12. Cannell, M. B., Cheng, H., and Lederer, W. J. (1995). The control of calcium release in heart muscle. Science 268, 1045-1049. doi: 10.1126/science.7754384
13. Cavey, M., Rauzi, M., Lenne, P.-F., and Lecuit, T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453, 751-756. doi: 10.1038/nature06953
14. Cerneus, D. P., Ueffing, E., Posthuma, G., Strous, G. J., and van der Ende, A. (1993). Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J. Biol. Chem. 268, 3150-3155.
15. Chacko, J. V., Canale, C., Harke, B., and Diaspro, A. (2013). Sub-diffraction nano manipulation using STED AFM. PLoS ONE 8:e66608. doi: 10.1371/journal.pone.0066608
16. Chang, H., Zhang, M., Ji, W., Chen, J., Zhang, Y., Liu, B., et al. (2012). A unique series of reversibly switchable fluorescent proteins with beneficial properties for various applications. Proc. Natl. Acad. Sci. U.S.A. 109, 4455-4460. doi: 10.1073/pnas.1113770109
17. Chojnacki, J., Staudt, T., Glass, B., Bingen, P., Engelhardt, J., Anders, M., et al. (2012). Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 338, 524-528. doi: 10.1126/science.1226359
18. Cox, S., Rosten, E., Monypenny, J., Jovanovic-Talisman, T., Burnette, D. T., Lippincott-Schwartz, J., et al. (2012). Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat. Methods 9, 195-200. doi: 10.1038/nmeth.1812
19. Daleke, D. L. (2003). Regulation of transbilayer plasma membrane phospholipid asymmetry. J. Lipid Res. 44, 233-242. doi: 10.1194/jlr.R200019-JLR200
20. D'Amico, F., and Skarmoutsou, E. (2008). Quantifying immunogold labelling in transmission electron microscopy. J. Microsc. 230, 9-15. doi: 10.1111/j.1365-2818.2008.01949.x
21. Damjanovich, S., Gáspár, J., and Pieri, C. (1997). Dynamic receptor superstructures at the plasma membrane. Q. Rev. Biophys. 30, 67-106. doi: 10.1017/S0033583596003307
22. Davis, D. M., Chiu, I., Fassett, M., Cohen, G. B., Mandelboim, O., and Strominger, J. L. (1999). The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. U.S.A. 96, 15062-15067. doi: 10.1073/pnas.96.26.15062
23. Demir, F., Horntrich, C., Blachutzik, J. O., Scherzer, S., Reinders, Y., Kierszniowska, S., et al. (2013). Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc. Natl. Acad. Sci. U.S.A. 110, 8296-8301. doi: 10.1073/pnas.1211667110
24. Douglass, A. D., and Vale, R. D. (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. doi: 10.1016/j.cell.2005.04.009
25. 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
26. Dykstra, M., Cherukuri, A., Sohn, H. W., Tzeng, S.-J., and Pierce, S. K. (2003). Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21, 457-481. doi: 10.1146/annurev.immunol.21.120601.141021
27. 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, 1159-1162. doi: 10.1038/nature07596
28. Fahey, P. F., Koppel, D. E., Barak, L. S., Wolf, D. E., Elson, E. L., and Webb, W. W. (1977). Lateral diffusion in planar lipid bilayers. Science 195, 305-306. doi: 10.1126/science.831279
29. Fiche, J.-B., Cattoni, D. I., Diekmann, N., Langerak, J. M., Clerte, C., Royer, C. A., et al. (2013). Recruitment, assembly, and molecular architecture of the SpoIIIE DNA pump revealed by superresolution microscopy. PLoS Biol. 11:e1001557. doi: 10.1371/journal.pbio.1001557
30. Fiorini, R. M., Valentino, M., Glaser, M., Gratton, E., and Curatola, G. (1988). Fluorescence lifetime distributions of 1,6-diphenyl-1,3,5-hexatriene reveal the effect of cholesterol on the microheterogeneity of erythrocyte membrane. Biochim. Biophys. Acta 939, 485-492. doi: 10.1016/0005-2736(88)90095-8
31. Fitzgibbon, J., Bell, K., King, E., and Oparka, K. (2010). Super-resolution imaging of plasmodesmata using three-dimensional structured illumination microscopy1[W]. Plant Physiol. 153, 1453-1463. doi: 10.1104/pp.110.157941
32. Gandhavadi, M., Allende, D., Vidal, A., Simon, S. A., and McIntosh, T. J. (2002). Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts. Biophys. J. 82, 1469-1482. doi: 10.1016/S0006-3495(02)75501-X
33. Ge, M., Gidwani, A., Brown, H. A., Holowka, D., Baird, B., and Freed, J. H. (2003). Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells. An ESR Study. Biophys. J. 85, 1278-1288. doi: 10.1016/S0006-3495(03)74563-9
34. Gowrishankar, K., Ghosh, S., Saha, S., C, R., Mayor, 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
35. Greenfield, D., McEvoy, A. L., Shroff, H., Crooks, G. E., Wingreen, N. S., Betzig, E., et al. (2009). Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol. 7:e1000137. doi: 10.1371/journal.pbio.1000137
36. 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 clustered membrane protein influenza hemagglutinin. Biophys. J. 104, 2182-2192. doi: 10.1016/j.bpj.2013.03.054
37. Gurskaya, N. G., Verkhusha, V. V., Shcheglov, A. S., Staroverov, D. B., Chepurnykh, T. V., Fradkov, A. F., et al. (2006). Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465. doi: 10.1038/nbt1191
38. 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
39. Gustafsson, M. G. L. (2005). Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Proc. Natl. Acad. Sci. U.S.A. 102, 13081-13086. doi: 10.1073/pnas.0406877102
40. Gustafsson, M. G. L., Shao, L., Carlton, P. M., Wang, C. J. R., Golubovskaya, I. N., Cande, W. Z., et al. (2008). Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957-4970. doi: 10.1529/biophysj.107.120345
41. Hagan, I. M., and Palazzo, R. E. (2006). Warming up at the poles. EMBO Rep. 7, 364-371.
42. Hammonds, J., Ding, L., Chu, H., Geller, K., Robbins, A., Wang, J.-J., et al. (2012). The tetherin/BST-2 coiled-coil ectodomain mediates plasma membrane microdomain localization and restriction of particle release. J. Virol. 86, 2259-2272. doi: 10.1128/JVI.05906-11
43. Harke, B., Ullal, C. K., Keller, J., and Hell, S. W. (2008). Three-dimensional nanoscopy of colloidal crystals. Nano Lett. 8, 1309-1313. doi: 10.1021/nl073164n
44. Hartmann, W., Galla, H.-J., and Sackmann, E. (1977). Direct evidence of charge-induced lipid domain structure in model membranes. FEBS Lett. 78, 169-172. doi: 10.1016/0014-5793(77)80298-6
45. Hedde, P. N., Fuchs, J., Oswald, F., Wiedenmann, J., and Nienhaus, G. U. (2009). Online image analysis software for photoactivation localization microscopy. Nat. Methods 6, 689-690. doi: 10.1038/nmeth1009-689
46. Heerklotz, H. (2002). Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83, 2693-2701. doi: 10.1016/S0006-3495(02)75278-8
47. Heilemann, M., van de Linde, S., Mukherjee, A., and Sauer, M. (2009). Super-resolution imaging with small organic fluorophores. Angew. Chem. Int. Ed. 48, 6903-6908. doi: 10.1002/anie.200902073
48. Heilemann, M., van de Linde, S., Schüttpelz, M., Kasper, R., Seefeldt, B., Mukherjee, A., et al. (2008). Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. 47, 6172-6176. doi: 10.1002/anie.200802376
49. 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
50. Hein, B., Willig, K. I., Wurm, C. A., Westphal, V., Jakobs, S., and Hell, S. W. (2010). Stimulated emission depletion nanoscopy of living cells using SNAP-tag fusion proteins. Biophys. J. 98, 158-163. doi: 10.1016/j.bpj.2009.09.053
51. 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/OL.19.000780
52. Henriques, R., Lelek, M., Fornasiero, E. F., Valtorta, F., Zimmer, C., and Mhlanga, M. M. (2010). QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat. Methods 7, 339-340. doi: 10.1038/nmeth0510-339
53. 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
54. Hess, S. T., Kumar, M., Verma, A., Farrington, J., Kenworthy, A., and Zimmerberg, J. (2005). Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin. J. Cell Biol. 169, 965-976. doi: 10.1083/jcb.200412058
55. Hoeller, D., Volarevic, S., and Dikic, I. (2005). Compartmentalization of growth factor receptor signalling. Curr. Opin. Cell Biol. 17, 107-111. doi: 10.1016/j.ceb.2005.01.001
56. Holden, S. J., Uphoff, S., and Kapanidis, A. N. (2011). DAOSTORM: an algorithm for high-density super-resolution microscopy. Nat. Methods 8, 279-280. doi: 10.1038/nmeth0411-279
57. 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
58. Hooke, R. (1665). Micrographia: or Some Physiological Descriptions of Minute Bodies Made by Magnifying Glasses, with Observations and Inquiries There Upon. London: Courier Dover Publications. doi: 10.5962/bhl.title.904
59. Huang, B., Wang, W., Bates, M., and Zhuang, X. (2008). Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813. doi: 10.1126/science.1153529
60. Hui, S. W., and Parsons, D. F. (1975). Direct observation of domains in wet lipid bilayers. Science 190, 383-384. doi: 10.1126/science.1179216
61. Ichinose, J., Murata, M., Yanagida, T., and Sako, Y. (2004). EGF signalling amplification induced by dynamic clustering of EGFR. Biochem. Biophys. Res. Commun. 324, 1143-1149. doi: 10.1016/j.bbrc.2004.09.173
62. Israelachvili, J. N. (1985). Intermolecular and Surface Forces. Fort Worth: Saunders College Publishing/Harcourt Brace.
63. Izeddin, I., Specht, C. G., Lelek, M., Darzacq, X., Triller, A., Zimmer, C., et al. (2011). Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe. PLoS ONE 6:e15611. doi:10.1371/journal.pone.0015611
64. Jacobson, K., Sheets, E. D., and Simson, R. (1995). Revisiting the fluid mosaic model of membranes. Science 268, 1441-1442. doi: 10.1126/science.7770769
65. Jaqaman, K., Kuwata, H., Touret, N., Collins, R., Trimble, W. S., Danuser, G., et al. (2011). Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 146, 593-606. doi: 10.1016/j.cell.2011.06.049
66. Jones, R. B., Gordus, A., Krall, J. A., and MacBeath, G. (2006). A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 439, 168-174. doi: 10.1038/nature04177
67. Jones, S. A., Shim, S.-H., He, J., and Zhuang, X. (2011). Fast, three-dimensional super-resolution imaging of live cells. Nat. Methods 8, 499-505. doi: 10.1038/nmeth.1605
68. Juette, M. F., Gould, T. J., Lessard, M. D., Mlodzianoski, M. J., Nagpure, B. S., Bennett, B. T., et al. (2008). Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat. Methods 5, 527-529. doi: 10.1038/nmeth.1211
69. Kanchanawong, P., Shtengel, G., Pasapera, A. M., Ramko, E. B., Davidson, M. W., Hess, H. F., et al. (2010). Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584. doi: 10.1038/nature09621
70. Karnovsky, M. J., Kleinfeld, A. M., Hoover, R. L., and Klausner, R. D. (1982). The concept of lipid domains in membranes. J. Cell Biol. 94, 1-6. doi: 10.1083/jcb.94.1.1
71. Kechkar, A., Nair, D., Heilemann, M., Choquet, D., and Sibarita, J.-B. (2013). Real-time analysis and visualization for single-molecule based super-resolution microscopy. PLoS ONE 8:e62918. doi: 10.1371/journal.pone.0062918
72. Kempf, C., Staudt, T., Bingen, P., Horstmann, H., Engelhardt, J., Hell, S. W., et al. (2013). Tissue multicolor STED nanoscopy of presynaptic proteins in the calyx of held. PLoS ONE 8:e62893. doi: 10.1371/journal.pone.0062893
73. Khursigara, C. M., Lan, G., Neumann, S., Wu, X., Ravindran, S., Borgnia, M. J., et al. (2011). Lateral density of receptor arrays in the membrane plane influences sensitivity of the E. coli chemotaxis response. EMBO J. 30, 1719-1729. doi: 10.1038/emboj.2011.77
74. Klaasse, E. C., Ijzerman, A. P., de Grip, W. J., and Beukers, M. W. (2008). Internalization and desensitization of adenosine receptors. Purinergic Signal. 4, 21-37. doi: 10.1007/s11302-007-9086-7
75. Klar, T. A., Jakobs, S., Dyba, M., Egner, A., and Hell, S. W. (2000). Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl. Acad. Sci. U.S.A. 97, 8206-8210. doi: 10.1073/pnas.97.15.8206
76. Klausner, R. D., Kleinfeld, A. M., Hoover, R. L., and Karnovsky, M. J. (1980). Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. J. Biol. Chem. 255, 1286-1295.
77. Korlach, J., Schwille, P., Webb, W. W., and Feigenson, G. W. (1999). Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 8461-8466. doi: 10.1073/pnas.96.15.8461
78. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., et al. (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. doi: 10.1146/annurev.biophys.34.040204.144637
79. Kusumi, A., Sako, Y., and Yamamoto, M. (1993). Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021-2040. doi: 10.1016/S0006-3495(93)81253-0
80. Lau, L., Lee, Y. L., Sahl, S. J., Stearns, T., and Moerner, W. E. (2012). STED microscopy with optimized labeling density reveals 9-fold arrangement of a centriole protein. Biophys. J. 102, 2926-2935. doi: 10.1016/j.bpj.2012.05.015
81. Lawo, S., Hasegan, M., Gupta, G. D., and Pelletier, L. (2012). Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat. Cell Biol. 14, 1148-1158. doi: 10.1038/ncb2591
82. Lee, S. F., Thompson, M. A., Schwartz, M. A., Shapiro, L., and Moerner, W. E. (2011). Super-resolution imaging of the nucleoid-associated protein HU in Caulobacter crescentus. Biophys. J. 100, L31-L33. doi: 10.1016/j.bpj.2011.02.022
83. Lee, S. F., Vérolet, Q., and Fürstenberg, A. (2013). Improved super-resolution microscopy with oxazine fluorophores in heavy water. Angew. Chem. Int. Ed. 52, 8948-8951. doi: 10.1002/anie.201302341
84. Lehmann, M., Rocha, S., Mangeat, B., Blanchet, F., Uji-i, H., Hofkens, J., et al. (2011). Quantitative multicolor super-resolution microscopy reveals tetherin HIV-1 Interaction. PLoS Pathog. 7:e1002456. doi: 10.1371/journal.ppat.1002456
85. Lenne, P.-F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.-J., et al. (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
86. Leutenegger, M., Ringemann, C., Lasser, T., Hell, S. W., and Eggeling, C. (2012). Fluorescence correlation spectroscopy with a total internal reflection fluorescence STED microscope (TIRF-STED-FCS). Opt. Express 20, 5243-5263. doi: 10.1364/OE.20.005243
87. Levayer, R., Pelissier-Monier, A., and Lecuit, T. (2011). Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529-540. doi: 10.1038/ncb2224
88. Lillemeier, B. F., Mörtelmaier, M. A., Forstner, M. B., Huppa, J. B., Groves, J. T., and Davis, M. M. (2010). TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 11, 90-96. doi: 10.1038/ni.1832
89. Lin, J., and Shaw, A. S. (2005). Getting downstream without a Raft. Cell 121, 815-816. doi: 10.1016/j.cell.2005.06.001
90. Lingwood, D., and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50. doi: 10.1126/science.1174621
91. Lukinavičius, G., Umezawa, K., Olivier, N., Honigmann, A., Yang, G., Plass, T., et al. (2013). A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat. Chem. 5, 132-139. doi: 10.1038/nchem.1546
92. Mabrey, S., and Sturtevant, J. M. (1976). Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry. Proc. Natl. Acad. Sci. U.S.A. 73, 3862-3866. doi: 10.1073/pnas.73.11.3862
93. Maheshwari, G., Brown, G., Lauffenburger, D. A., Wells, A., and Griffith, L. G. (2000). Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113(Pt 10), 1677-1686.
94. Mañes, S., del Real, G., and Martínez-A, C. (2003). Pathogens: raft hijackers. Nat. Rev. Immunol. 3, 557-568. doi: 10.1038/nri1129
95. Manley, S., Gillette, J. M., Patterson, G. H., Shroff, H., Hess, H. F., Betzig, E., et al. (2008). High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155-157. doi: 10.1038/nmeth.1176
96. Marsh, D., Watts, A., Pates, R. D., Uhl, R., Knowles, P. F., and Esmann, M. (1982). ESR spin-label studies of lipid-protein interactions in membranes. Biophys. J. 37, 265-274. doi: 10.1016/S0006-3495(82)84675-4
97. McGill, M. A., McKinley, R. F. A., and Harris, T. J. C. (2009). Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions. J. Cell Biol. 185, 787-796. doi: 10.1083/jcb.200812146
98. McKinney, S. A., Murphy, C. S., Hazelwood, K. L., Davidson, M. W., and Looger, L. L. (2009). A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6, 131-133. doi: 10.1038/nmeth.1296
99. Meilhac, N., and Destainville, N. (2011). Clusters of proteins in biomembranes: insights into the roles of interaction potential shapes and of protein diversity. J. Phys. Chem. B 115, 7190-7199. doi: 10.1021/jp1099865
100. Melchior, D. L. (1986). Lipid domains in fluid membranes: a quick-freeze differential scanning calorimetry study. Science 234, 1577-1580. doi: 10.1126/science.3787264
101. Mennella, V., Keszthelyi, B., McDonald, K. L., Chhun, B., Kan, F., Rogers, G. C., et al. (2012). Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14, 1159-1168. doi: 10.1038/ncb2597
102. Metcalf, T. N., Wang, J. L., and Schindler, M. (1986). Lateral diffusion of phospholipids in the plasma membrane of soybean protoplasts: evidence for membrane lipid domains. Proc. Natl. Acad. Sci. U.S.A. 83, 95-99. doi: 10.1073/pnas.83.1.95
103. Meyer, T., and Schindler, H. (1988). Particle counting by fluorescence correlation spectroscopy. Simultaneous measurement of aggregation and diffusion of molecules in solutions and in membranes. Biophys. J. 54, 983-993. doi: 10.1016/S0006-3495(88)83036-4
104. Mitrakos, P., and MacDonald, P. M. (1996). DNA-induced lateral segregation of cationic amphiphiles in lipid bilayer membranes as detected via 2H NMR. Biochemistry (Mosc.) 35, 16714-16722.
105. Mitrakos, P., and MacDonald, P. M. (1997). Domains in cationic lipid plus polyelectrolyte bilayer membranes: detection and characterization via 2H nuclear magnetic resonance. Biochemistry (Mosc.) 36, 13646-13656.
106. Mizuno, H., Abe, M., Dedecker, P., Makino, A., Rocha, S., Ohno-Iwashita, Y., et al. (2011). Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem. Sci. 2, 1548-1553. doi: 10.1039/c1sc00169h
107. Mongrand, S., Stanislas, T., Bayer, E. M. F., Lherminier, J., and Simon-Plas, F. (2010). Membrane rafts in plant cells. Trends Plant Sci. 15, 656-663. doi: 10.1016/j.tplants.2010.09.003
108. Monks, C. R. F., Freiberg, B. A., Kupfer, H., Sciaky, N., and Kupfer, A. (1998). Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86. doi: 10.1038/25764
109. 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 lipid interactions in living cells. Biophys. J. 101, 1651-1660. doi: 10.1016/j.bpj.2011.09.006
110. Mukamel, E. A., Babcoc, K. H., and Zhuang, X. (2012). Statistical deconvolution for superresolution fluorescence microscopy. Biophys. J. 102, 2391-2400. doi: 10.1016/j.bpj.2012.03.070
111. Muranyi, W., Malkusch, S., Müller, B., Heilemann, M., and Kräusslich, H.-G. (2013). Super-resolution microscopy reveals specific recruitment of HIV-1 envelope proteins to viral assembly sites dependent on the envelope C-terminal tail. PLoS Pathog. 9:e1003198. doi: 10.1371/journal.ppat.1003198
112. Olivier, N., Keller, D., Gonczy, P., and Manley, S. (2013a). Resolution doubling in 3D-STORM imaging through improved buffers. PLoS ONE 8:e69004. doi: 10.1371/journal.pone.0069004
113. Olivier, N., Keller, D., Rajan, V. S., Gonczy, P., and Manley, S. (2013b). Simple buffers for 3D STORM microscopy. Biomed. Opt. Express 4, 885-899. doi: 10.1364/BOE.4.000885
114. Owen, D. M., Williamson, D. J., Magenau, A., and Gaus, K. (2012). Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nat. Commun. 3:1256. doi: 10.1038/ncomms2273
115. Parthasarathy, R. (2012). Rapid, accurate particle tracking by calculation of radial symmetry centers. Nat. Methods 9, 724-726. doi: 10.1038/nmeth.2071
116. Pawson, T. (2004). Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203. doi: 10.1016/S0092-8674(03)01077-8
117. Prior, I. A. (2003). Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160, 165-170. doi: 10.1083/jcb.200209091
118. Prior, I. A., Muncke, C., Parton, R. G., and Hancock, J. F. (2003). Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160, 165-170. doi: 10.1083/jcb.200209091
119. Purbhoo, M. A., Liu, H., Oddos, S., Owen, D. M., Neil, M. A. A., Pageon, S. V., et al. (2010). Dynamics of subsynaptic vesicles and surface microclusters at the immunological synapse. Sci. Signal. 3:ra36. doi: 10.1126/scisignal.2000645
120. Rauzi, M., Lenne, P.-F., and Lecuit, T. (2010). Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114. doi: 10.1038/nature09566
121. Rayleigh, L. (1874). On the Manufacture and Theory of Diffraction Gratings (Fabrication et théorie des réseaux de diffraction); Philosophical Magazine, février et mars 1874. p. 81 et 193. J. Phys. Théor. Appl. 3, 320-324.
122. Rego, E. H., Shao, L., Macklin, J. J., Winoto, L., Johansson, G. A., Kamps-Hughes, N., et al. (2012). Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution. Proc. Natl. Acad. Sci. U.S.A. 109, E135-E143. doi: 10.1073/pnas.1107547108
123. Renz, M., Daniels, B. R., Vámosi, G., Arias, I. M., and Lippincott-Schwartz, J. (2012). Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc. Natl. Acad. Sci. U.S.A. 109, E2989-E2997. doi: 10.1073/pnas.1211753109
124. Ries, J., Kaplan, C., Platonova, E., Eghlidi, H., and Ewers, H. (2012). A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 9, 582-584. doi: 10.1038/nmeth.1991
125. Roca-Cusachs, P., Gauthier, N. C., Del Rio, A., and Sheetz, M. P. (2009). Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc. Natl. Acad. Sci. U.S.A. 106, 16245-16250. doi: 10.1073/pnas.0902818106
126. Rönnlund, D., Gad, A. K. B., Blom, H., Aspenström, P., and Widengren, J. (2013). Spatial organization of proteins in metastasizing cells. Cytometry 83, 855-865. doi: 10.1002/cyto.a.22304
127. Rossi, A., Moritz, T. J., Ratelade, J., and Verkman, A. S. (2012). Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes. J. Cell Sci. 125, 4405-4412. doi: 10.1242/jcs.109603
128. Rothman, J. E., and Lenard, J. (1977). Membrane asymmetry. Science 195, 743-753. doi: 10.1126/science.402030
129. Roy, N. H., Chan, J., Lambelé, M., and Thali, M. (2013). Clustering and mobility of HIV-1 Env at viral assembly sites predict its propensity to induce cell-cell fusion. J. Virol. 87, 7516-7525. doi: 10.1128/JVI.00790-13
130. Rust, M. J., Bates, M., and Zhuang, X. (2006). Stochastic optical reconstruction microscopy (STORM) provides sub-diffraction-limit image resolution. Nat. Methods 3, 793-795. doi: 10.1038/nmeth929
131. Saha, N., Himanen, J.-P., and Nikolov, D. B. (2007). Cell-cell signaling via Eph receptors and ephrins. Curr. Opin. Cell Biol. 19, 534-542. doi: 10.1016/j.ceb.2007.08.004
132. Sako, Y., and 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. doi: 10.1083/jcb.125.6.1251
133. Scarselli, M., Annibale, P., Gerace, C., and Radenovic, A. (2013). Enlightening G-protein-coupled receptors on the plasma membrane using super-resolution photoactivated localization microscopy. Biochem. Soc. Trans. 41, 191-196. doi: 10.1042/BST20120250
134. Scarselli, M., Annibale, P., and Radenovic, A. (2012). Cell type-specific β2-adrenergic receptor clusters identified using photoactivated localization microscopy are not lipid raft related, but depend on actin cytoskeleton integrity. J. Biol. Chem. 287, 16768-16780. doi: 10.1074/jbc.M111.329912
135. Schutz, G. J., Kada, G., Pastushenko, V. P., and Schindler, H. (2000). Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J. 19, 892-901. doi: 10.1093/emboj/19.5.892
136. Schwille, P., Korlach, J., and Webb, W. W. (1999). Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes. Cytometry 36, 176-182. doi: 10.1002/(SICI)1097-0320(19990701)36:3<176::AID-CYTO5>3.0.CO;2-F
137. Seiradake, E., Harlos, K., Sutton, G., Aricescu, A. R., and Jones, E. Y. (2010). An extracellular steric seeding mechanism for Eph-ephrin signaling platform assembly. Nat. Struct. Mol. Biol. 17, 398-402. doi: 10.1038/nsmb.1782
138. Selhuber-Unkel, C., Erdmann, T., López-García, M., Kessler, H., Schwarz, U. S., and Spatz, J. P. (2010). Cell adhesion strength is controlled by intermolecular spacing of adhesion receptors. Biophys. J. 98, 543-551. doi: 10.1016/j.bpj.2009.11.001
139. Sengupta, P., Jovanovic-Talisman, T., and Lippincott-Schwartz, J. (2013). Quantifying spatial organization in point-localization superresolution images using pair correlation analysis. Nat. Protoc. 8, 345-354. doi: 10.1038/nprot.2013.005
140. 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
141. 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.
142. Sharma, P., Varma, R., Sarasij, R., Ira Gousset, K., Krishnamoorthy, G., Rao, M., et al. (2004). Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577-589. doi: 10.1016/S0092-8674(04)00167-9
143. Sheets, E. (1995). New insights into membrane dynamics from the analysis of cell surface interactions by physical methods. Curr. Opin. Cell Biol. 7, 707-714. doi: 10.1016/0955-0674(95)80113-8
144. Sherman, E., Barr, V., Manley, S., Patterson, G., Balagopalan, L., Akpan, I., et al. (2011). Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. Immunity 35, 705-720. doi: 10.1016/j.immuni.2011.10.004
145. Shroff, H., Galbraith, C. G., Galbraith, J. A., and Betzig, E. (2008). Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat. Methods 5, 417-423. doi: 10.1038/nmeth.1202
146. Shroff, H., Galbraith, C. G., Galbraith, J. A., White, H., Gillette, J., Olenych, S., et al. (2007). Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc. Natl. Acad. Sci. U.S.A. 104, 20308-20313. doi: 10.1073/pnas.0710517105
147. Shtengel, G., Galbraith, J. A., Galbraith, C. G., Lippincott-Schwartz, J., Gillette, J. M., Manley, S., et al. (2009). Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl. Acad. Sci. U.S.A. 106, 3125-3130. doi: 10.1073/pnas.0813131106
148. Sieber, J. J., Willig, K. I., Heintzmann, R., Hell, S. W., and Lang, T. (2006). The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane. Biophys. J. 90, 2843-2851. doi: 10.1529/biophysj.105.079574
149. Sieber, J. J., Willig, K. I., Kutzner, C., Gerding-Reimers, C., Harke, B., Donnert, G., et al. (2007). Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317, 1072-1076. doi: 10.1126/science.1141727
150. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572. doi: 10.1038/42408
151. Simons, K., and Van Meer, G. (1988). Lipid sorting in epithelial cells. Biochemistry (Mosc.) 27, 6197-6202.
152. Simons, K., and Sampaio, J. L. (2011). Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 3:a004697. doi: 10.1101/cshperspect.a004697
153. 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
154. Smith, C. S., Joseph, N., Rieger, B., and Lidke, K. A. (2010). Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods 7, 373-375. doi: 10.1038/nmeth.1449
155. Stier, A., and Sackmann, E. (1973). Spin labels as enzyme substrates Heterogeneous lipid distribution in liver microsomal membranes. Biochim. Biophys. Acta BBA Biomembr. 311, 400-408. doi: 10.1016/0005-2736(73)90320-9
156. Subach, F. V., Patterson, G. H., Manley, S., Gillette, J. M., Lippincott-Schwartz, J., and Verkhusha, V. V. (2009). Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat. Methods 6, 153-159. doi: 10.1038/nmeth.1298
157. Subach, F. V., Patterson, G. H., Renz, M., Lippincott-Schwartz, J., and Verkhusha, V. V. (2010). Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells. J. Am. Chem. Soc. 132, 6481-6491. doi: 10.1021/ja100906g
158. Subach, O. M., Entenberg, D., Condeelis, J. S., and Verkhusha, V. V. (2012). A FRET-facilitated photoswitching using an orange fluorescent protein with the fast photoconversion kinetics. J. Am. Chem. Soc. 134, 14789-14799. doi: 10.1021/ja3034137
159. Suzuki, K. G. N., Kasai, R. S., Hirosawa, K. M., Nemoto, Y. L., Ishibashi, M., Miwa, Y., et al. (2012). Transient GPI-anchored protein homodimers are units for raft organization and function. Nat. Chem. Biol. 8, 774-783. doi: 10.1038/nchembio.1028
160. Svistounov, D., Warren, A., McNerney, G. P., Owen, D. M., Zencak, D., Zykova, S. N., et al. (2012). The relationship between fenestrations, sieve plates and rafts in liver sinusoidal endothelial cells. PLoS ONE 7:e46134. doi: 10.1371/journal.pone.0046134
161. Swamy, M. J., Ciani, L., Ge, M., Smith, A. K., Holowka, D., Baird, B., et al. (2006). Coexisting domains in the plasma membranes of live cells characterized by Spin-label ESR spectroscopy. Biophys. J. 90, 4452-4465. doi: 10.1529/biophysj.105.070839
162. Tanaka, K. A. K., Suzuki, K. G. N., Shirai, Y. M., Shibutani, S. T., Miyahara, M. S. H., Tsuboi, H., et al. (2010). Membrane molecules mobile even after chemical fixation. Nat. Methods 7, 865-866. doi: 10.1038/nmeth.f.314
163. Thompson, R. E., Larson, D. R., and Webb, W. W. (2002). Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82, 2775-2783. doi: 10.1016/S0006-3495(02)75618-X
164. Truong-Quang, B.-A., Mani, M., Markova, O., Lecuit, T., and Lenne, P.-F. (2013). Principles of e-cadherin supramolecular organization in vivo. Curr. Biol. 23, 2197-2207. doi: 10.1016/j.cub.2013.09.015
165. Turner, M. S., Sens, P., and Socci, N. D. (2005). Nonequilibrium raftlike membrane domains under continuous recycling. Phys. Rev. Lett. 95, 168301. doi: 10.1103/PhysRevLett.95.168301
166. Ullrich, A., and Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212. doi: 10.1016/0092-8674(90)90801-K
167. van de Linde, S., Löschberger, A., Klein, T., Heidbreder, M., Wolter, S., Heilemann, M., et al. (2011). Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat. Protoc. 6, 991-1009. doi: 10.1038/nprot.2011.336
168. Varma, R., and Mayor, S. (1998). GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801. doi: 10.1038/29563
169. Veatch, S. L., Machta, B. B., Shelby, S. A., Chiang, E. N., Holowka, D. A., and Baird, B. A. (2012). Correlation functions quantify super-resolution images and estimate apparent clustering due to over-counting. PLoS ONE 7:e31457. doi: 10.1371/journal.pone.0031457
170. Veatch, S. L., Polozov, I. V., Gawrisch, K., and Keller, S. L. (2004). Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 86, 2910-2922. doi: 10.1016/S0006-3495(04)74342-8
171. Watanabe, S., Punge, A., Hollopeter, G., Willig, K. I., Hobson, R. J., Davis, M. W., et al. (2011). Protein localization in electron micrographs using fluorescence nanoscopy. Nat. Methods 8, 80-84. doi: 10.1038/nmeth.1537
172. 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
173. Westphal, V., and Hell, S. W. (2005). Nanoscale resolution in the focal plane of an optical microscope. Phys. Rev. Lett. 94, 143903. doi: 10.1103/PhysRevLett.94.143903
174. Wiedenmann, J., Ivanchenko, S., Oswald, F., Schmitt, F., Röcker, C., Salih, A., et al. (2004). EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc. Natl. Acad. Sci. U.S.A. 101, 15905-15910. doi: 10.1073/pnas.0403668101
175. Wildanger, D., Medda, R., Kastrup, L., and Hell, S. W. (2009). A compact STED microscope providing 3D nanoscale resolution. J. Microsc. 236, 35-43. doi: 10.1111/j.1365-2818.2009.03188.x
176. 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
177. Willig, K., Rizzoli, S., Westphal, V., Jahn, R., and Hell, S. (2006). STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440, 935-939. doi: 10.1038/nature04592
178. Wolf, D. E., Kinsey, W., Lennarz, W., and Edidin, M. (1981). Changes in the organization of the sea urchin egg plasma membrane upon fertilization: indications from the lateral diffusion rates of lipid-soluble fluorescent dyes. Dev. Biol. 81, 133-138. doi: 10.1016/0012-1606(81)90355-9
179. Wolf, D. E., Maynard, V. M., McKinnon, C. A., and Melchior, D. L. (1990). Lipid domains in the ram sperm plasma membrane demonstrated by differential scanning calorimetry. Proc. Natl. Acad. Sci. U.S.A. 87, 6893-6896. doi: 10.1073/pnas.87.17.6893
180. Wunderlich, F., Kreutz, W., Mahler, P., Ronai, A., and Heppeler, G. (1978). Thermotropic fluid goes to ordered "discontinuous" phase separation in microsomal lipids of Tetrahymena. An X-ray diffraction study. Biochemistry (Mosc.) 17, 2005-2010.
181. Yang, T. T., Hampilos, P. J., Nathwani, B., Miller, C. H., Sutaria, N. D., and Liao, J.-C. (2013). Superresolution STED microscopy reveals differential localization in primary cilia. Cytoskeleton 70, 54-65. doi: 10.1002/cm.21090
182. Yarden, Y., and Sliwkowski, M. X. (2001). Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137. doi: 10.1038/35052073
183. York, A. G., Chandris, P., Nogare, D. D., Head, J., Wawrzusin, P., Fischer, R. S., et al. (2013). Instant super-resolution imaging in live cells and embryos via analog image processing. Nat. Methods 10, 1122-1126. doi: 10.1038/nmeth.2687
184. Zaidel-Bar, R., Ballestrem, C., Kam, Z., and Geiger, B. (2003). Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613. doi: 10.1242/jcs.00792
185. Zhang, J., Pekosz, A., and Lamb, R. A. (2000). Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 74, 4634-4644. doi: 10.1128/JVI.74.10.4634-4644.2000
186. Zhang, M., Chang, H., Zhang, Y., Yu, J., Wu, L., Ji, W., et al. (2012). Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat. Methods 9, 727-729. doi: 10.1038/nmeth.2021
187. Zhu, L., Zhang, W., Elnatan, D., and Huang, B. (2012). Faster STORM using compressed sensing. Nat. Methods 9, 721-723. doi: 10.1038/nmeth.1978