With or without rafts? Alternative views on cell membranes

BioEssays

Volumn 38, Issue 2, 2016, Pages 129-139

  Sevcsik, Eva ^a   Schütz, Gerhard J ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Lipids; Membrane heterogeneity; Membrane proteins; Membrane rafts; Phase separation; Plasma membrane; Raft hypothesis

Indexed keywords

CELL MEMBRANE; EXPERIMENTAL MODEL; THEORETICAL MODEL; METABOLISM; PHYSIOLOGY;

MEMBRANE LIPID; MEMBRANE PROTEIN;

CELL MEMBRANE; MEMBRANE LIPIDS; MEMBRANE PROTEINS;

EID: 84956630806     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201500150     Document Type: Article

References (140)

1. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387: 569-72.
2. Sharma P, Varma R, Sarasij R, Ira, et al. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-89.
3. Douglass AD, Vale RD. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121: 937-50.
4. Eggeling C, Ringemann C, Medda R, Schwarzmann G, et al. 2009. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457: 1159-62.
5. Schütz GJ, Kada G, Pastushenko VP, Schindler H. 2000. Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J 19: 892-901.
6. Gaus K, Gratton E, Kable EP, Jones AS, et al. 2003. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc Natl Acad Sci USA 100: 15554-9.
7. Dietrich C, Yang B, Fujiwara T, Kusumi A, et al. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys J 82: 274-84.
8. Dahan M, Levi S, Luccardini C, Rostaing P, et al. 2003. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302: 442-5.
9. Suzuki KG, Kasai RS, Hirosawa KM, Nemoto YL, et al. 2012. Transient GPI-anchored protein homodimers are units for raft organization and function. Nat Chem Biol 8: 774-83.
10. Brameshuber M, Weghuber J, Ruprecht V, Gombos I, et al. 2010. Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane. J Biol Chem 285: 41765-71.
11. Simons K, Ehehalt R. 2002. Cholesterol, lipid rafts, and disease. J Clin Invest 110: 597-603.
12. Schroeder R, London E, Brown D. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc Natl Acad Sci USA 91: 12130-4.
13. Veatch SL, Keller SL. 2003. A closer look at the canonical 'Raft Mixture' in model membrane studies. Biophys J 84: 725-6.
14. Baumgart T, Hammond AT, Sengupta P, Hess ST, et al. 2007. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci USA 104: 3165-70.
15. Brown DA, Crise B, Rose JK. 1989. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245: 1499-501.
16. Honigmann A, Mueller V, Ta H, Schoenle A, et al. 2014. Scanning STED-FCS reveals spatiotemporal heterogeneity of lipid interaction in the plasma membrane of living cells. Nat Commun 5.
17. Lin WC, Iversen L, Tu HL, Rhodes C, et al. 2014. H-Ras forms dimers on membrane surfaces via a protein-protein interface. Proc Natl Acad Sci USA 111: 2996-3001.
18. Raghupathy R, Anilkumar AA, Polley A, Singh PP, et al. 2015. Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins. Cell 161: 581-94.
19. Triffo S, Huang H, Smith A, Chou E, et al. 2012. Monitoring lipid anchor organization in cell membranes by PIE-FCCS. J Am Chem Soc 134: 10833-42.
20. van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, et al. 2011. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479: 552-5.
21. Zhou Y, Wong CO, Cho KJ, van der Hoeven D, et al. 2015. SIGNAL TRANSDUCTION. Membrane potential modulates plasma membrane phospholipid dynamics and K-Ras signaling. Science 349: 873-6.
22. Frisz JF, Klitzing HA, Lou K, Hutcheon ID, et al. 2013. Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol. J Biol Chem 288: 16855-61.
23. Frisz JF, Lou K, Klitzing HA, Hanafin WP, et al. 2013. Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts. Proc Natl Acad Sci USA 110: E613-E22.
24. Sevcsik E, Brameshuber M, Folser M, Weghuber J, et al. 2015. GPI-anchored proteins do not reside in ordered domains in the live cell plasma membrane. Nat Commun 6: 6969.
25. Pike LJ. 2006. Rafts defined. J Lipid Res 47: 1597-8.
26. Munro S. 2003. Lipid rafts: elusive or illusive? Cell 115: 377-88.
27. Kraft M. 2013. Plasma membrane organization and function: moving past lipid rafts. Mol Biol Cell 24: 2765-8.
28. Kenworthy AK. 2008. Have we become overly reliant on lipid rafts? Talking point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9: 531-5.
29. Shaw AS. 2006. Lipid rafts: now you see them, now you don't. Nat Immunol 7: 1139-42.
30. Klotzsch E, Schütz GJ. 2013. A critical survey of methods to detect plasma membrane rafts. Phil Trans R Soc B 368: 20120033.
31. Box GEP, Draper NR. 1987. Empirical Model Building and Response Surfaces. New York, NY: John Wiley & Son.
32. Brown DA, Rose JK. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533-44.
33. Shogomori H, Brown DA. 2003. Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol Chem 384: 1259-63.
34. Legler DF, Doucey MA, Schneider P, Chapatte L, et al. 2005. Differential insertion of GPI-anchored GFPs into lipid rafts of live cells. FASEB J 19: 73-5.
35. Heerklotz H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys J 83: 2693-701.
36. Pathak P, London E. 2011. Measurement of lipid nanodomain (raft) formation and size in sphingomyelin/POPC/cholesterol vesicles shows TX-100 and transmembrane helices increase domain size by coalescing preexisting nanodomains but do not induce domain formation. Biophys J 101: 2417-25.
37. van Meer G, Simons K. 1982. Viruses budding from either the apical or the basolateral plasma membrane domain of MDCK cells have unique phospholipid compositions. EMBO J 1: 847-52.
38. Pang S, Urquhart P, Hooper NM. 2004. N-glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI-anchored protein in polarised epithelial cells. J Cell Sci 117: 5079-86.
39. Benting JH, Rietveld AG, Simons K. 1999. N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J Cell Biol 146: 313-20.
40. Paladino S, Sarnataro D, Pillich R, Tivodar S, et al. 2004. Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. J Cell Biol 167: 699-709.
41. Lipardi C, Nitsch L, Zurzolo C. 2000. Detergent-insoluble GPI-anchored proteins are apically sorted in fischer rat thyroid cells, but interference with cholesterol or sphingolipids differentially affects detergent insolubility and apical sorting. Mol Biol Cell 11: 531-42.
42. Paladino S, Lebreton S, Tivodar S, Formiggini F, et al. 2014. Golgi sorting regulates organization and activity of GPI proteins at apical membranes. Nat Chem Biol 10: 350-7.
43. Imjeti NS, Lebreton S, Paladino S, de la Fuente E, et al. 2011. N-Glycosylation instead of cholesterol mediates oligomerization and apical sorting of GPI-APs in FRT cells. Mol Biol Cell 22: 4621-34.
44. Jaensch N, Correa IR, Jr., Watanabe R. 2014. Stable cell surface expression of GPI-anchored proteins, but not intracellular transport, depends on their fatty acid structure. Traffic 15: 1305-29.
45. Harder T, Scheiffele P, Verkade P, Simons K. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-42.
46. Yetukuri L, Ekroos K, Vidal-Puig A, Oresic M. 2008. Informatics and computational strategies for the study of lipids. Mol Biosyst 4: 121-7.
47. Veatch SL, Keller SL. 2005. Seeing spots: complex phase behavior in simple membranes. Biochim Biophys Acta 1746: 172-85.
48. Dupuy AD, Engelman DM. 2008. Protein area occupancy at the center of the red blood cell membrane. Proc Natl Acad Sci USA 105: 2848-52.
49. Contreras FX, Ernst AM, Haberkant P, Bjorkholm P, et al. 2012. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 481: 525-9.
50. Fantini J, Barrantes FJ. 2013. How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front Physiol 4: 31.
51. Hansen SB, Tao X, MacKinnon R. 2011. Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477: 495-8.
52. Anderson RG, Jacobson K. 2002. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296: 1821-5.
53. Niemela PS, Miettinen MS, Monticelli L, Hammaren H, et al. 2010. Membrane proteins diffuse as dynamic complexes with lipids. J Am Chem Soc 132: 7574-5.
54. Hammond GR, Fischer MJ, Anderson KE, Holdich J, et al. 2012. PI4P and PI(4, 5)P2 are essential but independent lipid determinants of membrane identity. Science 337: 727-30.
55. Yeung T, Gilbert GE, Shi J, Silvius J, et al. 2008. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319: 210-3.
56. Scheve C, Gonzales P, Momin N, Stachowiak J. 2013. Steric pressure between membrane-bound proteins opposes lipid phase separation. J Am Chem Soc 135: 1185-8.
57. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, et al. 2008. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135: 1085-97.
58. Gowrishankar K, Ghosh S, Saha S, Rumamol C, et al. 2012. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149: 1353-67.
59. Wang TY, Leventis R, Silvius JR. 2005. Artificially lipid-anchored proteins can elicit clustering-induced intracellular signaling events in Jurkat T-lymphocytes independent of lipid raft association. J Biol Chem 280: 22839-46.
60. Saka SK, Honigmann A, Eggeling C, Hell SW, et al. 2014. Multi-protein assemblies underlie the mesoscale organization of the plasma membrane. Nat Commun 5: 4509.
61. van Zanten TS, Gomez J, Manzo C, Cambi A, et al. 2010. Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc Natl Acad Sci USA 107: 15437-42.
62. Lenne PF, Wawrezinieck L, Conchonaud F, Wurtz O, et al. 2006. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J 25: 3245-56.
63. Zidovetzki R, Levitan I. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim Biophys Acta 1768: 1311-24.
64. Jamur MC, Oliver C. 2010. Permeabilization of cell membranes. Methods Mol Biol 588: 63-6.
65. Neuvonen M, Manna M, Mokkila S, Javanainen M, et al. 2014. Enzymatic oxidation of cholesterol: properties and functional effects of cholestenone in cell membranes. PLoS ONE 9: e103743.
66. Owicki JC, McConnell HM. 1980. Lateral diffusion in inhomogeneous membranes. Model membranes containing cholesterol. Biophys J 30: 383-97.
67. Grunze M, Deuticke B. 1974. Changes of membrane permeability due to extensive cholesterol depletion in mammalian erythrocytes. Biochim Biophys Acta 356: 125-30.
68. Finkelstein A. 1976. Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol 68: 127-35.
69. Sieber JJ, Willig KI, Kutzner C, Gerding-Reimers C, et al. 2007. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317: 1072-6.
70. Kwik J, Boyle S, Fooksman D, Margolis L, et al. 2003. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4, 5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100: 13964-9.
71. Mayinger P. 2012. Phosphoinositides and vesicular membrane traffic. Biochim Biophys Acta 1821: 1104-13.
72. Chadda R, Howes MT, Plowman SJ, Hancock JF, et al. 2007. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8: 702-17.
73. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, et al. 2011. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36: 604-15.
74. Zocher M, Zhang C, Rasmussen SG, Kobilka BK, et al. 2012. Cholesterol increases kinetic, energetic, and mechanical stability of the human beta2-adrenergic receptor. Proc Natl Acad Sci USA 109: E3463-72.
75. Hoop CL, Sivanandam VN, Kodali R, Srnec MN, et al. 2012. Structural characterization of the caveolin scaffolding domain in association with cholesterol-rich membranes. Biochemistry 51: 90-9.
76. Sheng R, Chen Y, Yung Gee H, Stec E, et al. 2012. Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Nat Commun 3: 1249.
77. Wang PY, Weng J, Anderson RG. 2005. OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation. Science 307: 1472-6.
78. Maxfield FR, Mayor S. 1997. Cell surface dynamics of GPI-anchored proteins. Adv Exp Med Biol 419: 355-64.
79. Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, et al. 1991. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254: 1016-9.
80. Mitchell JS, Kanca O, McIntyre BW. 2002. Lipid microdomain clustering induces a redistribution of antigen recognition and adhesion molecules on human T lymphocytes. J Immunol 168: 2737-44.
81. Mrowczynska L, Hagerstrand H. 2008. Patching of ganglioside(M1) in human erythrocytes - distribution of CD47 and CD59 in patched and curved membrane. Mol Membr Biol 25: 258-65.
82. Favoreel HW, Mettenleiter TC, Nauwynck HJ. 2004. Copatching and lipid raft association of different viral glycoproteins expressed on the surfaces of pseudorabies virus-infected cells. J Virol 78: 5279-87.
83. Hogue IB, Grover JR, Soheilian F, Nagashima K, et al. 2011. Gag induces the coalescence of clustered lipid rafts and tetraspanin-enriched microdomains at HIV-1 assembly sites on the plasma membrane. J Virol 85: 9749-66.
84. Larive RM, Baisamy L, Urbach S, Coopman P, et al. 2010. Cell membrane extensions, generated by mechanical constraint, are associated with a sustained lipid raft patching and an increased cell signaling. Biochim Biophys Acta 1798: 389-400.
85. Glebov O, Nichols B. 2004. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat Cell Biol 6: 238-43.
86. Sezgin E, Kaiser HJ, Baumgart T, Schwille P, et al. 2012. Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7: 1042-51.
87. Simons K, Gerl MJ. 2010. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688-99.
88. Llorente A, Skotland T, Sylvanne T, Kauhanen D, et al. 2013. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta 1831: 1302-9.
89. Liu AP, Fletcher DA. 2006. Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys J 91: 4064-70.
90. Veksler A, Gov NS. 2009. Calcium-actin waves and oscillations of cellular membranes. Biophys J 97: 1558-68.
91. Chen D, Santore MM. 2014. Large effect of membrane tension on the fluid-solid phase transitions of two-component phosphatidylcholine vesicles. Proc Natl Acad Sci USA 111: 179-84.
92. Levental I, Grzybek M, Simons K. 2011. Raft domains of variable properties and compositions in plasma membrane vesicles. Proc Natl Acad Sci USA 108: 11411-6.
93. Johnson SA, Stinson BM, Go MS, Carmona LM, et al. 2010. Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim Biophys Acta 1798: 1427-35.
94. Marsh D. 2008. Protein modulation of lipids, and vice-versa, in membranes. Biochim Biophys Acta 1778: 1545-75.
95. Kaiser HJ, Orlowski A, Rog T, Nyholm TK, et al. 2011. Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching. Proc Natl Acad Sci USA 108: 16628-33.
96. Killian JA. 1998. Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta 1376: 401-15.
97. Ewers H, Helenius A. 2011. Lipid-mediated endocytosis. Cold Spring Harb Perspect Biol 3: a004721.
98. Suetsugu S, Kurisu S, Takenawa T. 2014. Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins. Physiol Rev 94: 1219-48.
99. Tu-Sekine B, Goldschmidt H, Raben DM. 2015. Diacylglycerol, phosphatidic acid, and their metabolic enzymes in synaptic vesicle recycling. Adv Biol Regul 57: 147-52.
100. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, et al. 2012. Membrane bending by protein-protein crowding. Nat Cell Biol 14: 944-9.
101. Heinrich M, Tian A, Esposito C, Baumgart T. 2010. Dynamic sorting of lipids and proteins in membrane tubes with a moving phase boundary. Proc Natl Acad Sci USA 107: 7208-13.
102. Elbaz Y, Schuldiner M. 2011. Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci 36: 616-23.
103. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, et al. 2011. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144: 389-401.
104. Kusumi A, Sako Y. 1996. Cell surface organization by the membrane skeleton. Curr Opin Cell Biol 8: 566-74.
105. Trimble WS, Grinstein S. 2015. Barriers to the free diffusion of proteins and lipids in the plasma membrane. J Cell Biol 208: 259-71.
106. Contreras FX, Ernst AM, Wieland F, Brugger B. 2011. Specificity of intramembrane protein-lipid interactions. Cold Spring Harb Perspect Biol 3: a004705.
107. Sonnino S, Prinetti A. 2010. Lipids and membrane lateral organization. Front Physiol 1: 153.
108. Goni FM. 2014. The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. Biochim Biophys Acta 1838: 1467-76.
109. Huang S. 2013. When peers are not peers and don't know it: the Dunning-Kruger effect and self-fulfilling prophecy in peer-review. BioEssays 35: 414-6.
110. Sengupta P, Jovanovic-Talisman T, Skoko D, Renz M, et al. 2011. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat Methods 8: 969-75.
111. Mouritsen OG. 2010. The liquid-ordered state comes of age. Biochim Biophys Acta 1798: 1286-8.
112. Mueller V, Ringemann C, Honigmann A, Schwarzmann G, et al. 2011. STED nanoscopy reveals molecular details of cholesterol- and cytoskeleton-modulated lipid interactions in living cells. Biophys J 101: 1651-60.
113. Owen DM, Williamson DJ, Magenau A, Gaus K. 2012. Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nat Commun 3: 1256.
114. Amaro M, Sachl R, Jurkiewicz P, Coutinho A, et al. 2014. Time-resolved fluorescence in lipid bilayers: selected applications and advantages over steady state. Biophys J 107: 2751-60.
115. Machan R, Jurkiewicz P, Olzynska A, Olsinova M, et al. 2014. Peripheral and integral membrane binding of peptides characterized by time-dependent fluorescence shifts: focus on antimicrobial peptide LAH(4). Langmuir 30: 6171-9.
116. Yeagle PL. 1985. Cholesterol and the cell membrane. Biochim Biophys Acta 822: 267-87.
117. Brown DA, London E. 1998. Structure and origin of ordered lipid domains in biological membranes. J Membr Biol 164: 103-14.
118. Subczynski WK, Kusumi A. 2003. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochim Biophys Acta 1610: 231-43.
119. Ipsen JH, Karlstrom G, Mouritsen OG, Wennerstrom H, et al. 1987. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta 905: 162-72.
120. Paulick MG, Bertozzi CR. 2008. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47: 6991-7000.
121. Robinson PJ. 1997. Signal transduction via GPI-anchored membrane proteins. Adv Exp Med Biol 419: 365-70.
122. Yu J, Fischman DA, Steck TL. 1973. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J Supramol Struct 1: 233-48.
123. Levental I, Lingwood D, Grzybek M, Coskun U, et al. 2010. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci USA 107: 22050-4.
124. van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 112-24.
125. Yu RK, Tsai YT, Ariga T, Yanagisawa M. 2011. Structures, biosynthesis, and functions of gangliosides - an overview. J Oleo Sci 60: 537-44.
126. Barboni E, Rivero BP, George AJ, Martin SR, et al. 1995. The glycophosphatidylinositol anchor affects the conformation of Thy-1 protein. J Cell Sci 108: 487-97.
127. Butikofer P, Malherbe T, Boschung M, Roditi I. 2001. GPI-anchored proteins: now you see 'em, now you don't. FASEB J 15: 545-8.
128. Qu Q, Sharom FJ. 2002. Proximity of bound Hoechst 33342 to the ATPase catalytic sites places the drug binding site of P-glycoprotein within the cytoplasmic membrane leaflet. Biochemistry 41: 4744-52.
129. Rademacher TW, Edge CJ, Dwek RA. 1991. Dropping anchor with the lipophosphoglycans. Curr Biol 1: 41-2.
130. Homans SW, Edge CJ, Ferguson MA, Dwek RA, et al. 1989. Solution structure of the glycosylphosphatidylinositol membrane anchor glycan of Trypanosoma brucei variant surface glycoprotein. Biochemistry 28: 2881-7.
131. Ruprecht V, Brameshuber M, Schütz GJ. 2010. Two-color single molecule tracking combined with photobleaching for the detection of rare molecular interactions in fluid biomembranes. Soft Matter 6: 568-81.
132. Wieser S, Moertelmaier M, Fuertbauer E, Stockinger H, et al. 2007. (Un) Confined diffusion of CD59 in the plasma membrane determined by high-resolution single molecule microscopy. Biophys J 92: 3719-28.
133. Ichimori H, Hata T, Matsuki H, Kaneshina S. 1999. Effect of unsaturated acyl chains on the thermotropic and barotropic phase transitions of phospholipid bilayer membranes. Chem Phys Lipids 100: 151-64.
134. Tada K, Goto M, Tamai N, Matsuki H, et al. 2010. Pressure effect on the bilayer phase transition of asymmetric lipids with an unsaturated acyl chain. Ann N Y Acad Sci 1189: 77-85.
135. Pascher I. 1976. Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim Biophys Acta 455: 433-51.
136. Niemela PS, Hyvonen MT, Vattulainen I. 2009. Atom-scale molecular interactions in lipid raft mixtures. Biochim Biophys Acta 1788: 122-35.
137. Mombelli E, Morris R, Taylor W, Fraternali F. 2003. Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophys J 84: 1507-17.
138. Dinic J, Biverstahl H, Maler L, Parmryd I. 2011. Laurdan and di-4-ANEPPDHQ do not respond to membrane-inserted peptides and are good probes for lipid packing. Biochim Biophys Acta 1808: 298-306.
139. Massey JB, Pownall HJ. 2005. The polar nature of 7-ketocholesterol determines its location within membrane domains and the kinetics of membrane microsolubilization by apolipoprotein A-I. Biochemistry 44: 10423-33.
140. Kulig W, Olzynska A, Jurkiewicz P, Kantola AM, et al. 2015. Cholesterol under oxidative stress - how lipid membranes sense oxidation as cholesterol is being replaced by oxysterols. Free Radic Biol Med 84: 30-41.