STED nanoscopy reveals molecular details of cholesterol- and cytoskeleton-modulated lipid interactions in living cells.

Details about molecular membrane dynamics in living cells, such as lipid-protein interactions, are often hidden from the observer because of the limited spatial resolution of conventional far-field optical microscopy. The superior spatial resolution of stimulated emission depletion (STED) nanoscopy can provide new insights into this process. The application of fluorescence correlation spectroscopy (FCS) in focal spots continuously tuned down to 30 nm in diameter distinguishes between free and anomalous molecular diffusion due to, for example, transient binding of lipids to other membrane constituents, such as lipids and proteins. We compared STED-FCS data recorded on various fluorescent lipid analogs in the plasma membrane of living mammalian cells. Our results demonstrate details about the observed transient formation of molecular complexes. The diffusion characteristics of phosphoglycerolipids without hydroxyl-containing headgroups revealed weak interactions. The strongest interactions were observed with sphingolipid analogs, which showed cholesterol-assisted and cytoskeleton-dependent binding. The hydroxyl-containing headgroup of gangliosides, galactosylceramide, and phosphoinositol assisted binding, but in a much less cholesterol- and cytoskeleton-dependent manner. The observed anomalous diffusion indicates lipid-specific transient hydrogen bonding to other membrane molecules, such as proteins, and points to a distinct connectivity of the various lipids to other membrane constituents. This strong interaction is different from that responsible for forming cholesterol-dependent, liquid-ordered domains in model membranes.

[1]  Jonas Ries,et al.  Studying slow membrane dynamics with continuous wave scanning fluorescence correlation spectroscopy. , 2006, Biophysical journal.

[2]  Christian Eggeling,et al.  Fluorescence fluctuation spectroscopy in subdiffraction focal volumes. , 2005, Physical review letters.

[3]  J. Schlessinger,et al.  Ganglioside-mediated modulation of cell growth. Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor. , 1986, The Journal of biological chemistry.

[4]  Christian Eggeling,et al.  Red-emitting rhodamine dyes for fluorescence microscopy and nanoscopy. , 2010, Chemistry.

[5]  S. Nishimura,et al.  Cholesterol depletion induces solid-like regions in the plasma membrane. , 2006, Biophysical journal.

[6]  Davide Mazza,et al.  Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. , 2009, Biophysical journal.

[7]  S. Hell,et al.  Direct observation of the nanoscale dynamics of membrane lipids in a living cell , 2009, Nature.

[8]  Enrico Gratton,et al.  Laurdan and Prodan as Polarity-Sensitive Fluorescent Membrane Probes , 1998, Journal of Fluorescence.

[9]  Hervé Rigneault,et al.  Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. , 2005, Biophysical journal.

[10]  P. Fahey,et al.  Lateral diffusion in planar lipid bilayers. , 1977, Science.

[11]  Kai Simons,et al.  Plasma membranes are poised for activation of raft phase coalescence at physiological temperature , 2008, Proceedings of the National Academy of Sciences.

[12]  Akihiro Kusumi,et al.  Phospholipids undergo hop diffusion in compartmentalized cell membrane , 2002, The Journal of cell biology.

[13]  K. Sandhoff,et al.  Lysogangliosides: synthesis and use in preparing labeled gangliosides. , 1987, Methods in enzymology.

[14]  Christian Eggeling,et al.  Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids , 2010, Proceedings of the National Academy of Sciences.

[15]  S. Hakomori,et al.  Ganglioside-mediated modulation of cell growth. Specific effects of GM3 and lyso-GM3 in tyrosine phosphorylation of the epidermal growth factor receptor. , 1988, The Journal of biological chemistry.

[16]  D. Marguet,et al.  Spot variation fluorescence correlation spectroscopy allows for superresolution chronoscopy of confinement times in membranes. , 2011, Biophysical journal.

[17]  Hai-Tao He,et al.  Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. , 2008, Nature chemical biology.

[18]  K. Sandhoff,et al.  Direct evidence by carbon-13 NMR spectroscopy for the erythro configuration of the sphingoid moiety in Gaucher cerebroside and other natural sphingolipids. , 1985, European journal of biochemistry.

[19]  I. Vattulainen,et al.  Effect of sphingomyelin headgroup size on molecular properties and interactions with cholesterol. , 2010, Biophysical journal.

[20]  L. Pike Rafts defined: a report on the Keystone symposium on lipid rafts and cell function Published, JLR Papers in Press, April 27, 2006. , 2006, Journal of Lipid Research.

[21]  J. Hancock,et al.  Lipid rafts and membrane traffic , 2007, FEBS letters.

[22]  Yves Mély,et al.  Switchable nile red-based probe for cholesterol and lipid order at the outer leaflet of biomembranes. , 2010, Journal of the American Chemical Society.

[23]  W. Webb,et al.  Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. , 2007, Biochimica et biophysica acta.

[24]  E. Gratton,et al.  Spatial-temporal studies of membrane dynamics: scanning fluorescence correlation spectroscopy (SFCS). , 2004, Biophysical journal.

[25]  Hai-Tao He,et al.  Detecting nanodomains in living cell membrane by fluorescence correlation spectroscopy. , 2011, Annual review of physical chemistry.

[26]  P. Schwille,et al.  Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. , 2006, Biophysical journal.

[27]  G. Schwarzmann,et al.  Synthesis of fluorescent and radioactive analogues of two lactosylceramides and glucosylceramide containing beta-thioglycosidic bonds that are resistant to enzymatic degradation. , 1995, Carbohydrate research.

[28]  J. Korlach,et al.  Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes. , 1999, Cytometry.

[29]  Akihiro Kusumi,et al.  Hierarchical organization of the plasma membrane: Investigations by single‐molecule tracking vs. fluorescence correlation spectroscopy , 2010, FEBS letters.

[30]  T. Buranda,et al.  Local mobility in lipid domains of supported bilayers characterized by atomic force microscopy and fluorescence correlation spectroscopy. , 2005, Biophysical journal.

[31]  I. Pascher Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. , 1976, Biochimica et biophysica acta.

[32]  Carlo Manzo,et al.  Nanoscale fluorescence correlation spectroscopy on intact living cell membranes with NSOM probes. , 2011, Biophysical journal.

[33]  Tian-yun Wang,et al.  Different sphingolipids show differential partitioning into sphingolipid/cholesterol-rich domains in lipid bilayers. , 2000, Biophysical journal.

[34]  E. Joly Hypothesis: could the signalling function of membrane microdomains involve a localized transition of lipids from liquid to solid state? , 2004, BMC Cell Biology.

[35]  I. Spector,et al.  Effects of Jasplakinolide on the Kinetics of Actin Polymerization , 2000, The Journal of Biological Chemistry.

[36]  C. Eggeling,et al.  Characterization of horizontal lipid bilayers as a model system to study lipid phase separation. , 2010, Biophysical journal.

[37]  F. Zilliken,et al.  Substrate Specificity of Neuraminidase from Erysipelothrix rhusiopathiae , 1978, Hoppe-Seyler's Zeitschrift fur physiologische Chemie.

[38]  D. Lingwood,et al.  Order of lipid phases in model and plasma membranes , 2009, Proceedings of the National Academy of Sciences.

[39]  M. Ameloot,et al.  Probing diffusion laws within cellular membranes by Z-scan fluorescence correlation spectroscopy. , 2006, Biophysical journal.

[40]  Watt W. Webb,et al.  Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles , 2007, Proceedings of the National Academy of Sciences.

[41]  Megha,et al.  Ceramide Selectively Displaces Cholesterol from Ordered Lipid Domains (Rafts) , 2004, Journal of Biological Chemistry.

[42]  Petra Schwille,et al.  Fluorescence correlation spectroscopy relates rafts in model and native membranes. , 2004, Biophysical journal.

[43]  Christian Eggeling,et al.  Exploring single-molecule dynamics with fluorescence nanoscopy , 2009 .

[44]  Kai Simons,et al.  Regulation of human EGF receptor by lipids , 2011, Proceedings of the National Academy of Sciences.

[45]  Kai Simons,et al.  Lipid Rafts As a Membrane-Organizing Principle , 2010, Science.

[46]  Hervé Rigneault,et al.  Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork , 2006, The EMBO journal.

[47]  F. Goñi,et al.  Giant unilamellar vesicles electroformed from native membranes and organic lipid mixtures under physiological conditions. , 2007, Biophysical journal.

[48]  L. Tamm,et al.  Coupling of cholesterol-rich lipid phases in asymmetric bilayers. , 2008, Biochemistry.

[49]  R. Kraut,et al.  Diffusion, transport, and cell membrane organization investigated by imaging fluorescence cross-correlation spectroscopy. , 2009, Biophysical journal.

[50]  S. Hell Microscopy and its focal switch , 2008, Nature Methods.

[51]  M. Rao,et al.  Nanoclusters of GPI-Anchored Proteins Are Formed by Cortical Actin-Driven Activity , 2008, Cell.

[52]  S. Hell,et al.  Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. , 1994, Optics letters.

[53]  R. Epand,et al.  Correlated fluorescence-atomic force microscopy of membrane domains: structure of fluorescence probes determines lipid localization. , 2006, Biophysical journal.

[54]  Richard G. W. Anderson,et al.  Lipid rafts: at a crossroad between cell biology and physics , 2007, Nature Cell Biology.

[55]  K. Itoh,et al.  Tyrosine Kinase Activity of Epidermal Growth Factor Receptor Is Regulated by GM3 Binding through Carbohydrate to Carbohydrate Interactions* , 2009, Journal of Biological Chemistry.

[56]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.