Fluorescence Correlation Methods for Imaging Cellular Behavior of Sphingolipid-Interacting Probes

Methods in Cell Biology

Volumn 108, Issue , 2012, Pages 395-427

  Kraut, Rachel ^a   Bag, Nirmalya ^b   Wohland, Thorsten ^b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Analog; Correlation; Diffusion; Domain; Perturbation; Sphingolipid

Indexed keywords

EID: 84856716155     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386487-1.00018-3     Document Type: Chapter

References (117)

1. Axelrod D. Total internal reflection fluorescence microscopy in cell biology. Methods Enzymol. 2003, 361:1-33.
2. Bacia K., Kim S.A., et al. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 2006, 3(2):83-89.
3. Bakht O., London E. Detecting ordered domain formation (lipid rafts) in model membranes using Tempo. Methods Mol. Biol. 2007, 398:29-40.
4. Bakrac B., Kladnik A., et al. A toxin-based probe reveals cytoplasmic exposure of golgi sphingomyelin. J. Biol. Chem. 2010, 285:22186-22195.
5. Baumgart T., Hammond A.T., et al. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc. Natl. Acad. Sci. 2007, 104(9):3165-3170.
6. Benda A., Benes M., et al. How to determine diffusion coefficients in planar phospholipid systems by confocal fluorescence correlation spectroscopy. Langmuir 2003, 19(10):4120-4126.
7. Bhagatji P., Leventis R., et al. Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins. J. Cell Biol. 2009, 186(4):615-628.
8. Brinkmeier M., Dorre K., et al. Two-beam cross-correlation: a method to characterize transport phenomena in micrometer-sized structures. Analyt. Chem. 1999, 71(3):609-616.
9. Brown R. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 1998, 111(1):1-9.
10. Burkhardt M., Schwille P. Electron multiplying CCD based detection for spatially resolved fluorescence correlation spectroscopy. Opt. Express 2006, 14(12):5013-5020.
11. Burns A.R., Frankel D.J., et al. Local mobility in lipid domains of supported bilayers characterized by atomic force microscopy and fluorescence correlation spectroscopy. Biophys. J. 2005, 89(2):1081-1093.
12. Chadda R., Howes M.T., et al. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 2007, 8(6):702-717.
13. Chen C., Fu Z., et al. Gangliosides as high affinity receptors for tetanus neurotoxin. J. Biol. Chem. 2009, 284(39):26569-26577.
14. Chiantia S., Ries J., et al. Role of ceramide in membrane protein organization investigated by combined AFM and FCS. Biochim. Biophys. Acta 2008, 1778(5):1356-1364.
15. Chichili G.R., Rodgers W. Clustering of membrane raft proteins by the actin cytoskeleton. J. Biol. Chem 2007, 282(50):36682-36691.
16. Critchley P., Kazlauskaite J., et al. Binding of prion proteins to lipid membranes. Biochem. Biophys. Res. Commun. 2004, 313(3):559-567.
17. Daumas F., Destainville N., et al. Confined diffusion without fences of a G-protein-coupled receptor as revealed by single particle tracking. Biophys J. 2003, 84(1):356-366.
18. Destainville N., Dumas F., et al. What do diffusion measurements tell us about membrane compartmentalisation? Emergence of the role of interprotein interactions. J. Chem. Biol. 2008, 1(1-4):37-48.
19. Digman M.A., Gratton E. Imaging barriers to diffusion by pair correlation functions. Biophys. J. 2009, 97(2):665-673.
20. Eggeling C., Ringemann C., et al. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 2008, 457(7233):1159-1162.
21. Engelman D.M. Membranes are more mosaic than fluid. Nature 2005, 438(7068):578-580.
22. Epand R.M. Do proteins facilitate the formation of cholesterol-rich domains?. Biochim. Biophys. Acta 2004, 1666(1-2):227-238.
23. Ewers H., Romer W., et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell Biol. 2009, 12(1):11-18.
24. Fantini J. Interaction of proteins with lipid rafts through glycolipid-binding domains: biochemical background and potential therapeutic applications. Curr. Med. Chem. 2007, 14(27):2911-2917.
25. Fantini J., Garmy N., et al. Prediction of glycolipid-binding domains from the amino acid sequence of lipid raft-associated proteins: application to HpaA, a protein involved in the adhesion of helicobacter pylori to gastrointestinal cells. Biochemistry 2006, 45(36):10957-10962.
26. Feigenson G.W. Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures. Biochim. Biophys. Acta 2009, 1788(1):47-52.
27. Fotinou C., Emsley P., et al. The crystal structure of tetanus toxin Hc fragment complexed with a synthetic GT1b analogue suggests cross-linking between ganglioside receptors and the toxin. J. Biol. Chem. 2001, 276(34):32274-32281.
28. Fu Z., Chen C., et al. Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype F. Biochemistry 2009, 48(24):5631-5641.
29. Ginalski K., Venclovas C., et al. Structure-based sequence alignment for the beta-trefoil subdomain of the clostridial neurotoxin family provides residue level information about the putative ganglioside binding site. FEBS Lett. 2000, 482(1-2):119-124.
30. Glebov O.O., Nichols B.J. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat. Cell Biol. 2004, 6(3):238-243.
31. Golebiewska U., Nyako M., et al. Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol. Biol. Cell 2008, 19(4):1663-1669.
32. Gösch M., Serov A., Anhut T., Lasser T., Rochas A., Besse P.A., Popovic R.S., Blom H., Rigler R. Parallel single molecule detection with a fully integrated single-photon 2×2 CMOS detector array. J. Biomed. Opt. 2004, 9(5):913-921.
33. Goswami D., Gowrishankar K., et al. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008, 135(6):1085-1097.
34. Guo L., Har J.Y., et al. Molecular Diffusion Measurement in Lipid Bilayers over Wide Concentration Ranges: A Comparative Study. ChemPhysChem 2008, 9(5):721-728.
35. Halpern J.L., Loftus A. Characterization of the receptor-binding domain of tetanus toxin. J. Biol. Chem. 1993, 268(15):11188-11192.
36. Haustein E., Schwille P. Fluorescence correlation spectroscopy: novel variations of an established technique. Annu. Rev. Biophys. Biomol. Struct. 2007, 36:151-169.
37. Hebbar S., Lee E., et al. A fluorescent sphingolipid binding domain peptide probe interacts with sphingolipids and cholesterol-dependent raft domains. J. Lipid Res. 2008, 49(5):1077-1089.
38. Hebert B., Costantino S., et al. Spatiotemporal image correlation spectroscopy (STICS) theory, verification, and application to protein velocity mapping in living CHO cells. Biophys. J. 2005, 88(5):3601-3614.
39. Honigmann A., Walter C., et al. Characterization of horizontal lipid bilayers as a model system to study lipid phase separation. Biophys J 2010, 98(12):2886-2894.
40. Ikeda K., Matsuzaki K. Driving force of binding of amyloid [beta]-protein to lipid bilayers. Biochem. Biophys. Res. Commun. 2008, 370(3):525-529.
41. Ishitsuka R., Kobayashi T. Lysenin: a new tool for investigating membrane lipid organization. Anat. Sci. Int. 2004, 79(4):184-190.
42. Johannes L., Mayor S. Induced domain formation in endocytic invagination. Lipid Sorting, and Scission. 2010, 142(4):507-510.
43. Kaiser R.D., London E. Determination of the depth of BODIPY probes in model membranes by parallax analysis of fluorescence quenching. Biochim. Biophys. Acta 1998, 1375(1-2):13-22.
44. Kamata Y., Yoshimoto M., et al. Interaction between botulinum neurotoxin type a and ganglioside: ganglioside inactivates the neurotoxin and quenches its tryptophan fluorescence. Toxicon 1997, 35(8):1337-1340.
45. Kannan B., Guo L., et al. Spatially resolved total internal reflection fluorescence correlation microscopy using an electron multiplying charge-coupled device camera. Anal. Chem. 2007, 79(12):4463-4470.
46. Kannan B., Har J.Y., et al. Electron multiplying charge-coupled device camera based fluorescence correlation spectroscopy. Anal. Chem. 2006, 78(10):3444-3451.
47. Kenworthy A.K., Nichols B.J., et al. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 2004, 165(5):735-746.
48. Kim S.A., Heinze K.G., et al. Fluorescence correlation spectroscopy in living cells. Nat. Methods 2007, 4(11):963-973.
49. Kitamura M., Iwamori M., et al. Interaction between Clostridium botulinum neurotoxin and gangliosides. Biochim. Biophys. Acta 1980, 628(3):328-335.
50. Kolin D.L., Wiseman P.W. Advances in image correlation spectroscopy: measuring number densities, aggregation states, and dynamics of fluorescently labeled macromolecules in cells. Cell Biochem. Biophys. 2007, 49(3):141-164.
51. Kusumi A., Shirai Y.M., et al. Hierarchical organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett. 2010, 584(9):1814-1823.
52. Lagerholm B.C., Weinreb G.E., et al. Detecting microdomains in intact cell membranes. Annu Rev. Phys. Chem. 2005, 56:309-336.
53. Lai A.L., Tamm L.K., et al. Synaptotagmin 1 Modulates Lipid Acyl Chain Order in Lipid Bilayers by Demixing Phosphatidylserine. J. Biol. Chem. 2011, 286(28):25291-25300.
54. Lasserre R., Guo X.J., et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat. Chem. Biol. 2008, 4(9):538-547.
55. Lencer W.I., Saslowsky D. Raft trafficking of AB5 subunit bacterial toxins. Biochim. Biophys. Acta 2005, 1746(3):314-321.
56. Lenne P.F., Wawrezinieck L., et al. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 2006, 25(14):3245-3256.
57. Lingwood D., Kaiser H.-J., et al. Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 2009, 037(5):955-960.
58. Lingwood D., Ries J., et al. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(29):10005-10010.
59. Liu A.P., Fletcher D.A. Actin Polymerization Serves as a Membrane Domain Switch in Model Lipid Bilayers. Biophys. J. 2006, 91(11):4064-4070.
60. Longo M.L., Blanchette C.D. Imaging cerebroside-rich domains for phase and shape characterization in binary and ternary mixtures. Biochimica et Biophysica Acta (BBA) - Biomembranes 2007, 1798(7):1357-1367.
61. Louch H.A., Buczko E.S., et al. Identification of a binding site for ganglioside on the receptor binding domain of tetanus toxin. Biochemistry 2002, 41(46):13644-13652.
62. Machan R., Hof M. Recent Developments in Fluorescence Correlation Spectroscopy for Diffusion Measurements in Planar Lipid Membranes. Int. J. Mol. Sci. 2010, 11(2):427-457.
63. Mahfoud R., Garmy N., et al. Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J. Biol. Chem. 2002, 277(13):11292-11296.
64. Maier O., Oberle V., et al. Fluorescent lipid probes: some properties and applications (a review). Chem. Phys. Lipids 2002, 116(1-2):3-18.
65. Martin O.C., Pagano R.E. 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. 1994, 125(4):769-781.
66. Masuda A., Ushida K., et al. New fluorescence correlation spectroscopy enabling direct observation of spatiotemporal dependence of diffusion constants as an evidence of anomalous transport in extracellular matrices. Biophys. J. 2005, 88(5):3584-3591.
67. Merrill A.H. De Novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J. Biol. Chem. 2002, 277(29):25843-25846.
68. Merrill A.H., van Echten G., et al. Fumonisin B1 inhibits sphingosine (sphinganine) N-acyltransferase and de novo sphingolipid biosynthesis in cultured neurons in situ. J. Biol. Chem. 1993, 268(36):27299-27306.
69. Pagano R.E. Endocytic trafficking of glycosphingolipids in sphingolipid storage diseases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358(1433):885-891.
70. Pan X., Foo W., et al. Multifunctional fluorescence correlation microscope for intracellular and microfluidic measurements. Rev. Sci. Instrum. 2007, 78(5):053711.
71. Petersen N.O. Scanning fluorescence correlation spectroscopy. I. Theory and simulation of aggregation measurements. Biophys. J. 1986, 49(4):809-815.
72. Petersen N.O., Hoddelius P.L., et al. Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application. Biophys. J. 1993, 65(3):1135-1146.
73. Petersen N.O., Johnson D.C., et al. Scanning fluorescence correlation spectroscopy. II. Application to virus glycoprotein aggregation. Biophys. J. 1986, 49(4):817-820.
74. Petrasek Z., Schwille P. Scanning fluorescence correlation spectroscopy. "Single Molecules and Nanotechnology" 2008, 83-105. Springer, Berlin. R.R. Rigler, H. Vogel (Eds.).
75. Pinaud F., Michalet X., et al. Dynamic partitioning of a glycosyl-phosphatidylinositol-anchored protein in glycosphingolipid-rich microdomains imaged by single-quantum dot tracking. Traffic 2009, 10(6):691-712.
76. Platt F.M., Neises G.R., et al. N-butyldeoxynojirimycin is a novel inhibitor of glycolipid biosynthesis. J. Biol. Chem. 1994, 269(11):8362-8365.
77. Polyakova S.M., Belov V.N., et al. New GM1 ganglioside derivatives for selective single and double labelling of the natural glycosphingolipid skeleton. Eur. J. Org. Chem. 2009, 2009(30):5162-5177.
78. Prinetti A., Loberto N., et al. Glycosphingolipid behaviour in complex membranes. Biochim. Biophys. Acta 2009, 1788(1):184-193.
79. Reyes Mateo C., Brochon J.C., et al. Lipid clustering in bilayers detected by the fluorescence kinetics and anisotropy of trans-parinaric acid. Biophys. J. 1993, 65(5):2237-2247.
80. Ries J., Petrasek Z., Garcia-Saez A.J., Scwille P. A comprehensive framework for fluorescence cross-correlation spectroscopy. New J. Phys. 2010, 12:113009. (November 2010).
81. Romer W., Berland L., et al. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 2007, 450(7170):670-675.
82. Rummel A., Mahrhold S., et al. The HCC-domain of botulinum neurotoxins A and B exhibits a singular ganglioside binding site displaying serotype specific carbohydrate interaction. Mol. Microbiol. 2004, 51(3):631-643.
83. Ruprecht V., Wieser S., et al. Spot variation fluorescence correlation spectroscopy allows for superresolution chronoscopy of confinement times in membranes. Biophys. J. 2011, 100(11):2839-2845.
84. Sahl S.J., Leutenegger M., et al. Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids. Proc. Natl. Acad. Sci. 2010, 107(15):6829-6834.
85. Sankaran J., Manna M., et al. Diffusion, transport, and cell membrane organization investigated by imaging fluorescence cross-correlation spectroscopy. Biophys. J. 2009, 97(9):2630-2639.
86. Sankaran J., Shi X., et al. ImFCS: a software for imaging FCS data analysis and visualization. Opt. Express 2010, 18(25):25468-25481.
87. Schwarzmann G., Wendeler M., et al. Synthesis of novel NBD-GM1 and NBD-GM2 for the transfer activity of GM2-activator protein by a FRET-based assay system. Glycobiology 2005, 15(12):1302-1311.
88. Sengupta P., Garai K., et al. Measuring size distribution in highly heterogeneous systems with fluorescence correlation spectroscopy. Biophys. J. 2003, 84(3):1977-1984.
89. Shapiro R.E., Specht C.D., et al. Identification of a ganglioside recognition domain of tetanus toxin using a novel ganglioside photoaffinity ligand. J. Biol. Chem. 1997, 272(48):30380-30386.
90. Sharma P., Varma R., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 2004, 116(4):577-589.
91. Shi X., Teo L.S., et al. Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy. Dev. Dyn. 2009, 238(12):3156-3167.
92. Shi X., Wohland T. Fluorescence Correlation Spectroscopy. Nanoscopy and Multidimensional Optical Fluorescence Microscopy 2010, CRC Press, Boca Raton. A. Diaspro (Ed.).
93. Simons K., Gerl M.J. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 2010, 11(10):688-699.
94. Sisan D.R., Arevalo R., et al. Spatially resolved fluorescence correlation spectroscopy using a spinning disk confocal microscope. Biophys. J. 2006, 91(11):4241-4252.
95. Skakun V.V., Hink M.A., et al. Global analysis of fluorescence fluctuation data. Eur. Biophys. J. 2005, 34(4):323-334.
96. Steinert S., Lee E., et al. A fluorescent glycolipid-binding peptide probe traces cholesterol dependent microdomain-derived trafficking pathways. PLoS ONE 2008, 3(8):e2933.
97. Stenmark P., Dupuy J., et al. Crystal structure of botulinum neurotoxin type A in complex with the cell surface co-receptor GT1b-insight into the toxin-neuron interaction. PLoS Pathog. 2008, 4(8):e1000129.
98. Taieb N., Yahi N., et al. Rafts and related glycosphingolipid-enriched microdomains in the intestinal epithelium: bacterial targets linked to nutrient absorption. Adv. Drug Deliv. Rev. 2004, 56(6):779-794.
99. Thompson T.E., Tillack T.W. Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu. Rev. Biophys. Chem. 1985, 14:361-386.
100. Valdes-Gonzalez T., Inagawa J., et al. Characterization of the interactions of ß-amyloid peptides with glycolipid receptors by surface plasmon resonance. Spectroscopy 2003, 17(2):241-254.
101. van Meer G., Stelzer E., et al. Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J. Cell Biol. 1987, 105(4):1623-1635.
102. van Zanten T.S., Gomez J., et al. Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc. Natl. Acad. Sci. 2010, 107(35):15437-15442.
103. Veatch S.L., Soubias O., et al. Critical fluctuations in domain-forming lipid mixtures. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(45):17650-17655.
104. Waheed A.A., Shimada Y., et al. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). PNAS 2001, 98(9):4926-4931.
105. Wang T.Y., Silvius J.R. Sphingolipid partitioning into ordered domains in cholesterol-free and cholesterol-containing lipid bilayers. Biophys. J. 2003, 84(1):367-378.
106. Wawrezinieck L., Lenne P.-F., et al. Fluorescence correlation spectroscopy to determine diffusion laws: application to live cell membrane. Proc. SPIE 2004, 5462:92-102.
107. Wawrezinieck L., Rigneault H., et al. Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys. J. 2005, 89(6):4029-4042.
108. Weis W.I., Drickamer K. Structural basis of lectin-carbohydrate recognition. Annu. Rev. Biochem. 1996, 65:441-473.
109. Weissman M., Schindler H., et al. Determination of molecular weights by fluctuation spectroscopy: application to DNA. Proc. Natl. Acad. Sci. U. S. A. 1976, 73(8):2776-2780.
110. Westerlund B., Slotte J.P. How the molecular features of glycosphingolipids affect domain formation in fluid membranes. Biochim. Biophys. Acta 2009, 1788(1):194-201.
111. Widengren J., Mets U., et al. Fluorescence correlation spectroscopy of triplet-states in solution - a theoretical and experimental-study. J. Phys. Chem. 1995, 99(36):13368-13379.
112. Widengren J., Mets U., et al. Photodynamic properties of green fluorescent proteins investigated by fluorescence correlation spectroscopy. Chem. Phys. 1999, 250(2):171-186.
113. Wohland T., Shi X., et al. Single plane illumination fluorescence correlation spectroscopy (SPIM-FCS) probes in homogeneous three-dimensional environments. Opt. Express 2010, 18(10):10627-10641.
114. Yanagisawa K. Role of gangliosides in Alzheimer's disease. Biochim. Biophys. Acta 2007, 1768(8):1943-1951.
115. Yanagisawa K., Odaka A., et al. GM1 ganglioside-bound amyloid beta-protein (A beta): a possible form of preamyloid in Alzheimer's disease. Nat. Med. 1995, 1(10):1062-1066.
116. Yu C., Alterman M., et al. Ceramide displaces cholesterol from lipid rafts and decreases the association of the cholesterol binding protein caveolin-1. J. Lipid Res. 2005, 46(8):1678-1691.
117. Zhang Y., Li X., et al. Ceramide-enriched membrane domains - structure and function. Biochim. Biophys. Acta 2009, 1788:178-183.