Molecular probes to visualize the location, organization and dynamics of lipids

Journal of Cell Science

Volumn 127, Issue 22, 2014, Pages 4801-4812

  Maekawa, Masashi ^a   Fairn, Gregory D ^a,b,c  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Electron microscopy; Imaging; Lipid; Superresolution

Indexed keywords

ANTIBODY; CHOLERA TOXIN B SUBUNIT; CHOLESTEROL; FAT DROPLET; GLYCEROLIPID; LIPID; MEMBRANE PROTEIN; PHOSPHOLIPID; SPHINGOMYELIN; TOXIN; MOLECULAR PROBE;

AUTOPHAGOSOME; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; ENDOSOME; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOLOGY; LIPID ANALYSIS; LIPID BILAYER; MICROSCOPY; MOLECULAR PROBE; NONHUMAN; NOTE; PROTEIN DOMAIN; CHEMISTRY; PROCEDURES;

HUMANS; LIPIDS; MICROSCOPY, ELECTRON; MOLECULAR PROBES;

EID: 84911978116     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.150524     Document Type: Note

References (118)

1. Abrams, F. S. and London, E. (1993). Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 32, 10826-10831.
2. Alving, C. R. and Richards, R. L. (1977). Immune reactivities of antibodies against glycolipids-II. Comparative properties, using liposomes, of purified antibodies against mono-, di-and trihexosyl ceramide haptens. Immunochemistry 14, 383-389.
3. Andree, H. A., Reutelingsperger, C. P., Hauptmann, R., Hemker, H. C., Hermens, W. T. and Willems, G. M. (1990). Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J. Biol. Chem. 265, 4923-4928.
4. Axelrod, D. (2001). Total internal reflection fluorescence microscopy in cell biology. Traffic 2, 764-774.
5. Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. and Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055-1069.
6. Baumgart, T., Hunt, G., Farkas, E. R., Webb, W. W. and Feigenson, G. W. (2007). Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. Biochim. Biophys. Acta 1768, 2182-2194.
7. Bohdanowicz, M., Schlam, D., Hermansson, M., Rizzuti, D., Fairn, G. D., Ueyama, T., Somerharju, P., Du, G. and Grinstein, S. (2013). Phosphatidic acid is required for the constitutive ruffling and macropinocytosis of phagocytes. Mol. Biol. Cell 24, 1700-1712, S1-S7.
8. Bornig, H. and Geyer, G. (1974). Staining of cholesterol with the fluorescent antibiotic "filipin". Acta Histochem. 50, 110-115.
9. Chattopadhyay, A. and London, E. (1987). Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 26, 39-45.
10. Cheng, J., Fujita, A., Yamamoto, H., Tatematsu, T., Kakuta, S., Obara, K., Ohsumi, Y. and Fujimoto, T. (2014). Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries. Nat. Commun. 5, 3207.
11. Choung, S. Y., Kobayashi, T., Takemoto, K., Ishitsuka, H. and Inoue, K. (1988). Interaction of a cyclic peptide, Ro09-0198, with phosphatidylethanolamine in liposomal membranes. Biochim. Biophys. Acta 940, 180-187.
12. Colón-González, F. and Kazanietz, M. G. (2006). C1 domains exposed: from diacylglycerol binding to protein-protein interactions. Biochim. Biophys. Acta 1761, 827-837.
13. Corbett-Nelson, E. F., Mason, D., Marshall, J. G., Collette, Y. and Grinstein, S. (2006). Signaling-dependent immobilization of acylated proteins in the inner monolayer of the plasma membrane. J. Cell Biol. 174, 255-265.
14. Cornett, D. S., Reyzer, M. L., Chaurand, P. and Caprioli, R. M. (2007). MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat. Methods 4, 828-833.
15. Dowler, S., Currie, R. A., Campbell, D. G., Deak, M., Kular, G., Downes, C. P. and Alessi, D. R. (2000). Identification of pleckstrin-homology-domaincontaining proteins with novel phosphoinositide-binding specificities. Biochem. J. 351, 19-31.
16. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., Belov, V. N., Hein, B., von Middendorff, C., Schönle, A. et al. (2009). Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457, 1159-1162.
17. Ellson, C. D., Gobert-Gosse, S., Anderson, K. E., Davidson, K., Erdjument-Bromage, H., Tempst, P., Thuring, J. W., Cooper, M. A., Lim, Z. Y., Holmes, A. B. et al. (2001). PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox). Nat. Cell Biol. 3, 679-682.
18. Elvington, S. M. and Nichols, J. W. (2007). Spontaneous, intervesicular transfer rates of fluorescent, acyl chain-labeled phosphatidylcholine analogs. Biochim. Biophys. Acta 1768, 502-508.
19. Emoto, K., Kobayashi, T., Yamaji, A., Aizawa, H., Yahara, I., Inoue, K. and Umeda, M. (1996). Redistribution of phosphatidylethanolamine at the cleavage furrow of dividing cells during cytokinesis. Proc. Natl. Acad. Sci. USA 93, 12867-12872.
20. 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.
21. Fairn, G. D., Curwin, A. J., Stefan, C. J. and McMaster, C. R. (2007). The oxysterol binding protein Kes1p regulates Golgi apparatus phosphatidylinositol-4-phosphate function. Proc. Natl. Acad. Sci. USA 104, 15352-15357.
22. Fairn, G. D., Hermansson, M., Somerharju, P. and Grinstein, S. (2011a). Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat. Cell Biol. 13, 1424-1430.
23. Fairn, G. D., Schieber, N. L., Ariotti, N., Murphy, S., Kuerschner, L., Webb, R. I., Grinstein, S. and Parton, R. G. (2011b). High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J. Cell Biol. 194, 257-275.
24. Fernández-Suárez, M. and Ting, A. Y. (2008). Fluorescent probes for superresolution imaging in living cells. Nat. Rev. Mol. Cell Biol. 9, 929-943.
25. Flannagan, R. S., Harrison, R. E., Yip, C. M., Jaqaman, K. and Grinstein, S. (2010). Dynamic macrophage "probing" is required for the efficient capture of phagocytic targets. J. Cell Biol. 191, 1205-1218.
26. Fujimoto, T., Yamamoto, H. and Ohsumi, Y. (2014). Different phosphatidylinositol 3-phosphate asymmetries in yeast and mammalian autophagosomes revealed by a new electron microscopy technique. Autophagy 10, 933-935.
27. Fujita, A., Cheng, J., Tauchi-Sato, K., Takenawa, T. and Fujimoto, T. (2009). A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc. Natl. Acad. Sci. USA 106, 9256-9261.
28. Galbraith, C. G. and Galbraith, J. A. (2011). Super-resolution microscopy at a glance. J. Cell Sci. 124, 1607-1611.
29. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G. and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
30. Godi, A., Di Campli, A., Konstantakopoulos, A., Di Tullio, G., Alessi, D. R., Kular, G. S., Daniele, T., Marra, P., Lucocq, J. M. and De Matteis, M. A. (2004). FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6, 393-404.
31. Golebiewska, U., Nyako, M., Woturski, W., Zaitseva, I. and McLaughlin, S. (2008). Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol. Biol. Cell 19, 1663-1669.
32. Golebiewska, U., Kay, J. G., Masters, T., Grinstein, S., Im, W., Pastor, R. W., Scarlata, S. and McLaughlin, S. (2011). Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5-bisphosphate out of the forming phagosomes of macrophages. Mol. Biol. Cell 22, 3498-3507.
33. Gray, A., Van Der Kaay, J. and Downes, C. P. (1999). The pleckstrin homology domains of protein kinase B and GRP1 (general receptor for phosphoinositides-1) are sensitive and selective probes for the cellular detection of phosphatidylinositol 3,4-bisphosphate and/or phosphatidylinositol 3,4,5-trisphosphate in vivo. Biochem. J. 344, 929-936.
34. Hammond, G. R., Schiavo, G. and Irvine, R. F. (2009a). Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P(2). Biochem. J. 422, 23-35.
35. Hammond, G. R., Sim, Y., Lagnado, L. and Irvine, R. F. (2009b). Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J. Cell Biol. 184, 297-308.
36. Hammond, G. R., Machner, M. P. and Balla, T. (2014). A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J. Cell Biol. 205, 113-126.
37. Han, X. and Gross, R. W. (2003). Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J. Lipid Res. 44, 1071-1079.
38. Hao, M., Lin, S. X., Karylowski, O. J., Wüstner, D., McGraw, T. E. and Maxfield, F. R. (2002). Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J. Biol. Chem. 277, 609-617.
39. Haustein, E. and Schwille, P. (2007). Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct. 36, 151-169.
40. Holthuis, J. C. and Levine, T. P. (2005). Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6, 209-220.
41. Hölttä-Vuori, M., Uronen, R. L., Repakova, J., Salonen, E., Vattulainen, I., Panula, P., Li, Z., Bittman, R. and Ikonen, E. (2008). BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic 9, 1839-1849.
42. Hyslop, P. A., Morel, B. and Sauerheber, R. D. (1990). Organization and interaction of cholesterol and phosphatidylcholine in model bilayer membranes. Biochemistry 29, 1025-1038.
43. Ikonen, E. (2008). Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138.
44. Jaqaman, K., Loerke, D., Mettlen, M., Kuwata, H., Grinstein, S., Schmid, S. L. and Danuser, G. (2008). Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5, 695-702.
45. Jaqaman, K., Kuwata, H., Touret, N., Collins, R., Trimble, W. S., Danuser, G. and Grinstein, S. (2011). Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 146, 593-606.
46. Kaiser, R. D. and London, E. (1998). Determination of the depth of BODIPY probes in model membranes by parallax analysis of fluorescence quenching. Biochim. Biophys. Acta 1375, 13-22.
47. Kavran, J. M., Klein, D. E., Lee, A., Falasca, M., Isakoff, S. J., Skolnik, E. Y. and Lemmon, M. A. (1998). Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508.
48. Kay, J. G., Koivusalo, M., Ma, X., Wohland, T. and Grinstein, S. (2012). Phosphatidylserine dynamics in cellular membranes. Mol. Biol. Cell 23, 2198-2212.
49. Kleusch, C., Hersch, N., Hoffmann, B., Merkel, R. and Csiszár, A. (2012). Fluorescent lipids: functional parts of fusogenic liposomes and tools for cell membrane labeling and visualization. Molecules 17, 1055-1073.
50. Knight, J. D. and Falke, J. J. (2009). Single-molecule fluorescence studies of a PH domain: new insights into the membrane docking reaction. Biophys. J. 96, 566-582.
51. Knott, G. and Genoud, C. (2013). Is EM dead? J. Cell Sci. 126, 4545-4552.
52. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G. and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
53. 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. USA 96, 8461-8466.
54. Kraft, M. L. and Klitzing, H. A. (2014). Imaging lipids with secondary ion mass spectrometry. Biochim. Biophys. Acta 1841, 1108-1119.
55. Krishnamurthy, K., Dasgupta, S. and Bieberich, E. (2007). Development and characterization of a novel anti-ceramide antibody. J. Lipid Res. 48, 968-975.
56. Kusumi, A., Suzuki, K. G., Kasai, R. S., Ritchie, K. and Fujiwara, T. K. (2011). Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36, 604-615.
57. Lemmon, M. A., Ferguson, K. M., O'Brien, R., Sigler, P. B. and Schlessinger, J. (1995). Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. USA. 92, 10472-10476.
58. Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
59. Li, Z., Mintzer, E. and Bittman, R. (2006). First synthesis of free cholesterol-BODIPY conjugates. J. Org. Chem. 71, 1718-1721.
60. Li, X., Wang, X., Zhang, X., Zhao, M., Tsang, W. L., Zhang, Y., Yau, R. G., Weisman, L. S. and Xu, H. (2013). Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc. Natl. Acad. Sci. USA 110, 21165-21170.
61. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
62. Lippincott-Schwartz, J. and Patterson, G. H. (2003). Development and use of fluorescent protein markers in living cells. Science 300, 87-91.
63. Lippincott-Schwartz, J., Altan-Bonnet, N. and Patterson, G. H. (2003). Photobleaching and photoactivation: following protein dynamics in living cells. Nat. Cell Biol. Suppl., S7-S14.
64. Makino, A., Baba, T., Fujimoto, K., Iwamoto, K., Yano, Y., Terada, N., Ohno, S., Sato, S. B., Ohta, A., Umeda, M. et al. (2003). Cinnamycin (Ro 09-0198) promotes cell binding and toxicity by inducing transbilayer lipid movement. J. Biol. Chem. 278, 3204-3209.
65. Martin, O. C. and Pagano, R. E. (1987). Transbilayer movement of fluorescent analogs of phosphatidylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. Evidence for a protein-mediated and ATPdependent process(es). J. Biol. Chem. 262, 5890-5898.
66. Martin, O. C. and Pagano, R. E. (1994). Internalization and sorting of a fluorescent analogue of glucosylceramide to the Golgi apparatus of human skin fibroblasts: utilization of endocytic and nonendocytic transport mechanisms. J. Cell Biol. 125, 769-781.
67. Martin, D. S., Forstner, M. B. and Käs, J. A. (2002). Apparent subdiffusion inherent to single particle tracking. Biophys. J. 83, 2109-2117.
68. Miller, R. G. (1984). The use and abuse of filipin to localize cholesterol in membranes. Cell Biol. Int. Rep. 8, 519-535.
69. Mizuno, H., Abe, M., Dedecker, P., Makino, A., Rocha, S., Ohno-Iwashita, Y., Hofkens, J., Kobayashi, T. and Miyawaki, A. (2011). Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem. Sci. 2, 1548-1553.
70. Mobius, W., Ohno-Iwashita, Y., van Donselaar, E. G., Oorschot, V. M., Shimada, Y., Fujimoto, T., Heijnen, H. F., Geuze, H. J. and Slot, J. W. (2002). Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J. Histochem. Cytochem. 50, 43-55.
71. Mondal, M., Mesmin, B., Mukherjee, S. and Maxfield, F. R. (2009). Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol. Biol. Cell 20, 581-588.
72. Mueller, V., Ringemann, C., Honigmann, A., Schwarzmann, G., Medda, R., Leutenegger, M., Polyakova, S., Belov, V. N., Hell, S. W. and Eggeling, C. (2011). STED nanoscopy reveals molecular details of cholesterol-and cytoskeleton-modulated lipid interactions in living cells. Biophys. J. 101, 1651-1660.
73. Mukherjee, S., Zha, X., Tabas, I. and Maxfield, F. R. (1998). Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75, 1915-1925.
74. Navarro, J., Chabot, J., Sherrill, K., Aneja, R., Zahler, S. A. and Racker, E. (1985). Interaction of duramycin with artificial and natural membranes. Biochemistry 24, 4645-4650.
75. Ohno-Iwashita, Y., Shimada, Y., Hayashi, M. and Inomata, M. (2010a). Plasma membrane microdomains in aging and disease. Geriatr. Gerontol. Int. 10 Suppl., S41-S52.
76. Ohno-Iwashita, Y., Shimada, Y., Hayashi, M., Iwamoto, M., Iwashita, S. and Inomata, M. (2010b). Cholesterol-binding toxins and anti-cholesterol antibodies as structural probes for cholesterol localization. Subcell. Biochem. 51, 597-621.
77. Pagano, R. E., Martin, O. C., Kang, H. C. and Haugland, R. P. (1991). A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113, 1267-1279.
78. Palade, G. E. (1952). A study of fixation for electron microscopy. J. Exp. Med. 95, 285-298.
79. Palade, G. E. and Porter, K. R. (1954). Studies on the endoplasmic reticulum. I. Its identification in cells in situ. J. Exp. Med. 100, 641-656.
80. Puri, V., Watanabe, R., Dominguez, M., Sun, X., Wheatley, C. L., Marks, D. L. and Pagano, R. E. (1999). Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1, 386-388.
81. Puri, V., Watanabe, R., Singh, R. D., Dominguez, M., Brown, J. C., Wheatley, C. L., Marks, D. L. and Pagano, R. E. (2001). Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 154, 535-548.
82. Ries, J., Chiantia, S. and Schwille, P. (2009). Accurate determination of membrane dynamics with line-scan FCS. Biophys. J. 96, 1999-2008.
83. Ritchie, K., Shan, X. Y., Kondo, J., Iwasawa, K., Fujiwara, T. and Kusumi, A. (2005). Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophys. J. 88, 2266-2277.
84. Rogers, J., Lee, A. G. and Wilton, D. C. (1979). The organisation of cholesterol and ergosterol in lipid bilayers based on studies using non-perturbing fluorescent sterol probes. Biochim. Biophys. Acta 552, 23-37.
85. Roy, A. and Levine, T. P. (2004). Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J. Biol. Chem. 279, 44683-44689.
86. Sarantis, H. and Grinstein, S. (2012). Subversion of phagocytosis for pathogen survival. Cell Host Microbe 12, 419-431.
87. Saxton, M. J. and Jacobson, K. (1997). Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26, 373-399.
88. Schlam, D., Bohdanowicz, M., Chatgilialoglu, A., Steinberg, B. E., Ueyama, T., Du, G., Grinstein, S. and Fairn, G. D. (2013). Diacylglycerol kinases terminate diacylglycerol signaling during the respiratory burst leading to heterogeneous phagosomal NADPH oxidase activation. J. Biol. Chem. 288, 23090-23104.
89. Schuster, B. G., Neidig, M., Alving, B. M. and Alving, C. R. (1979). Production of antibodies against phosphocholine, phosphatidylcholine, sphingomyelin, and lipid A by injection of liposomes containing lipid A. J. Immunol. 122, 900-905.
90. Schwille, P., Haupts, U., Maiti, S. and Webb, W. W. (1999). Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one-and two-photon excitation. Biophys. J. 77, 2251-2265.
91. Sezgin, E., Levental, I., Grzybek, M., Schwarzmann, G., Mueller, V., Honigmann, A., Belov, V. N., Eggeling, C., Coskun, U., Simons, K. et al. (2012). Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta 1818, 1777-1784.
92. Shimada, Y., Maruya, M., Iwashita, S. and Ohno-Iwashita, Y. (2002). The Cterminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur. J. Biochem. 269, 6195-6203.
93. 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.
94. Simons, K. and Ehehalt, R. (2002). Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110, 597-603.
95. Simons, K. and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
96. Singer, S. J. and Nicolson, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science 175, 720-731.
97. Solanko, L. M., Honigmann, A., Midtiby, H. S., Lund, F. W., Brewer, J. R., Dekaris, V., Bittman, R., Eggeling, C. and Wüstner, D. (2013). Membrane orientation and lateral diffusion of BODIPY-cholesterol as a function of probe structure. Biophys. J. 105, 2082-2092.
98. Sprong, H., van der Sluijs, P. and van Meer, G. (2001). How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2, 504-513.
99. Stauffer, T. P., Ahn, S. and Meyer, T. (1998). Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr. Biol. 8, 343-346.
100. Steinberg, B. E., Magalhaes, M. A. and Grinstein, S. (2014). Expression of genetically encoded fluorescent probes to monitor phospholipid dynamics in live neutrophils. Methods Mol. Biol. 1124, 269-277.
101. Tanaka, K. A., Suzuki, K. G., Shirai, Y. M., Shibutani, S. T., Miyahara, M. S., Tsuboi, H., Yahara, M., Yoshimura, A., Mayor, S., Fujiwara, T. K. et al. (2010). Membrane molecules mobile even after chemical fixation. Nat. Methods 7, 865-866.
102. Teruel, M. N. and Meyer, T. (2000). Translocation and reversible localization of signaling proteins: a dynamic future for signal transduction. Cell 103, 181-184.
103. Touboul, D., Laprévote, O. and Brunelle, A. (2011). Micrometric molecular histology of lipids by mass spectrometry imaging. Curr. Opin. Chem. Biol. 15, 725-732.
104. van den Bogaart, G., Meyenberg, K., Risselada, H. J., Amin, H., Willig, K. I., Hubrich, B. E., Dier, M., Hell, S. W., Grubmüller, H., Diederichsen, U. et al. (2011). Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555.
105. van Genderen, I. L., van Meer, G., Slot, J. W., Geuze, H. J. and Voorhout, W. F. (1991). Subcellular localization of Forssman glycolipid in epithelial MDCK cells by immuno-electronmicroscopy after freeze-substitution. J. Cell Biol. 115, 1009-1019.
106. van Meer, G., Voelker, D. R. and Feigenson, G. W. (2008). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124.
107. Várnai, P. and Balla, T. (2006). Live cell imaging of phosphoinositide dynamics with fluorescent protein domains. Biochim. Biophys. Acta 1761, 957-967.
108. Várnai, P., Rother, K. I. and Balla, T. (1999). Phosphatidylinositol 3-kinasedependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274, 10983-10989.
109. Voorhout, W., van Genderen, I., van Meer, G. and Geuze, H. (1991). Preservation and immunogold localization of lipids by freeze-substitution and low temperature embedding. Scanning Microsc. Suppl. 5, S17-S24; discussion S24-S25.
110. Wang, J. and Richards, D. A. (2012). Segregation of PIP2 and PIP3 into distinct nanoscale regions within the plasma membrane. Biol. Open 1, 857-862.
111. Watson, A. D. (2006). Thematic review series: systems biology approaches to metabolic and cardiovascular disorders. Lipidomics: a global approach to lipid analysis in biological systems. J. Lipid Res. 47, 2101-2111.
112. Wüstner, D. (2007). Fluorescent sterols as tools in membrane biophysics and cell biology. Chem. Phys. Lipids 146, 1-25.
113. Yachi, R., Uchida, Y., Balakrishna, B. H., Anderluh, G., Kobayashi, T., Taguchi, T. and Arai, H. (2012). Subcellular localization of sphingomyelin revealed by two toxin-based probes in mammalian cells. Genes Cells 17, 720-727.
114. Yamaji, A., Sekizawa, Y., Emoto, K., Sakuraba, H., Inoue, K., Kobayashi, H. and Umeda, M. (1998). Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 273, 5300-5306.
115. Yeung, T., Terebiznik, M., Yu, L., Silvius, J., Abidi, W. M., Philips, M., Levine, T., Kapus, A. and Grinstein, S. (2006). Receptor activation alters inner surface potential during phagocytosis. Science 313, 347-351.
116. Yeung, T., Gilbert, G. E., Shi, J., Silvius, J., Kapus, A. and Grinstein, S. (2008). Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213.
117. Zhao, C., Du, G., Skowronek, K., Frohman, M. A. and Bar-Sagi, D. (2007). Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat. Cell Biol. 9, 707-712.
118. Zhou, Y., Liang, H., Rodkey, T., Ariotti, N., Parton, R. G. and Hancock, J. F. (2014). Signal integration by lipid-mediated spatial cross talk between Ras nanoclusters. Mol. Cell. Biol. 34, 862-876.