Giant Plasma Membrane Vesicles: Models for Understanding Membrane Organization

Current Topics in Membranes

Volumn 75, Issue , 2015, Pages 25-57

  Levental, Kandice R ^a   Levental, Ilya ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

GPMV; Microdomain; Model membrane; Partitioning; Phase separation; Plasma membrane; Plasma membrane vesicle; Raft

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; CYTOPLASM VESICLE; HUMAN; MEMBRANE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL MEMBRANE; CYTOPLASMIC VESICLES; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANES; MODELS, BIOLOGICAL;

EID: 84946229501     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctm.2015.03.009     Document Type: Article

References (124)

1. Ahmed S.N., Brown D.A., London E. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry 1997, 36(36):10944-10953.
2. Atilla-Gokcumen G.E., Muro E., Relat-Goberna J., Sasse S., Bedigian A., Coughlin M.L., et al. Dividing cells regulate their lipid composition and localization. Cell 2014, 156(3):428-439.
3. Barros L.F., Kanaseki T., Sabirov R., Morishima S., Castro J., Bittner C.X., et al. Apoptotic and necrotic blebs in epithelial cells display similar neck diameters but different kinase dependency. Cell Death & Differentiation 2003, 10(6):687-697.
4. Bauer B., Davidson M., Orwar O. Direct reconstitution of plasma membrane lipids and proteins in nanotube-vesicle networks. Langmuir 2006, 22(22):9329-9332.
5. Baumgart T., Hammond A.T., Sengupta P., Hess S.T., Holowka D.A., Baird B.A., et al. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(9):3165-3170.
6. Belkin M., Hardy W.G. Relation between water permeability and integrity of sulfhydryl groups in malignant and normal cells. Journal of Biophysical and Biochemical Cytology 1961, 9(4):733-745.
7. Bezlyepkina N., Gracia R.S., Shchelokovskyy P., Lipowsky R., Dimova R. Phase diagram and tie-line determination for the ternary mixture DOPC/eSM/cholesterol. Biophysical Journal 2013, 104(7):1456-1464.
8. Brown D.A. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 2006, 21:430-439.
9. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annual Review of Cell and Developmental Biology 1998, 14:111-136.
10. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 1992, 68(3):533-544.
11. Calleros L., Lasa M., Rodriguez-Alvarez F.J., Toro M.J., Chiloeches A. RhoA and p38 MAPK mediate apoptosis induced by cellular cholesterol depletion. Apoptosis 2006, 11(7):1161-1173.
12. Cantor R.S. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 1997, 36(9):2339-2344.
13. Charras G.T. A short history of blebbing. Journal of Microscopy 2008, 231(3):466-478.
14. Cheng H.T., Megha, London E. Preparation and properties of asymmetric vesicles that mimic cell membranes: effect upon lipid raft formation and transmembrane helix orientation. Journal of Biological Chemistry 2009, 284(10):6079-6092.
15. Chen X., Resh M.D. Cholesterol depletion from the plasma membrane triggers ligand-independent activation of the epidermal growth factor receptor. Journal of Biological Chemistry 2002, 277(51):49631-49637.
16. Cohen S., Ushiro H., Stoscheck C., Chinkers M. A native 170,000 epidermal growth factor receptor-kinase complex from shed plasma membrane vesicles. Journal of Biological Chemistry 1982, 257(3):1523-1531.
17. Collins M.D., Keller S.L. Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(1):124-128.
18. Coskun U., Grzybek M., Drechsel D., Simons K. Regulation of human EGF receptor by lipids. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(22):9044-9048.
19. Costello D.A., Hsia C.Y., Millet J.K., Porri T., Daniel S. Membrane fusion-competent virus-like proteoliposomes and proteinaceous supported bilayers made directly from cell plasma membranes. Langmuir 2013, 29(21):6409-6419.
20. Curthoys N.M., Parent M., Mlodzianoski M., Nelson A.J., Lilieholm J., Butler M.B., et al. Dances with Membranes: Breakthroughs from Super-resolution Imaging. Current Topics in Membranes 2015, 75:59-124.
21. Dai J., Sheetz M.P. Membrane tether formation from blebbing cells. Biophysical Journal 1999, 77(6):3363-3370.
22. Del Piccolo N., Placone J., He L., Agudelo S.C., Hristova K. Production of plasma membrane vesicles with chloride salts and their utility as a cell membrane mimetic for biophysical characterization of membrane protein interactions. Analytical Chemistry 2012, 84(20):8650-8655.
23. Diaz-Rohrer B., Levental K., Simons K., Levental I. Membrane raft association is a determinant of plasma membrane localization. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(23).
24. Dietrich C., Bagatolli L.A., Volovyk Z.N., Thompson N.L., Levi M., Jacobson K., et al. Lipid rafts reconstituted in model membranes. Biophysical Journal 2001, 80(3):1417-1428.
25. Dietrich C., Volovyk Z.N., Levi M., Thompson N.L., Jacobson K. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(19):10642-10647.
26. Dubavik A., Sezgin E., Lesnyak V., Gaponik N., Schwille P., Eychmuller A. Penetration of amphiphilic quantum dots through model and cellular plasma membranes. ACS Nano 2012, 6(3):2150-2156.
27. Dupuy A.D., Engelman D.M. Protein area occupancy at the center of the red blood cell membrane. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(8):2848-2852.
28. Eggeling C., Ringemann C., Medda R., Schwarzmann G., Sandhoff K., Polyakova S., et al. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 2009, 457(7233):1159-1162.
29. Engel S., Scolari S., Thaa B., Krebs N., Korte T., Herrmann A., et al. FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochemical Journal 2010, 425(3):567-573.
30. Fadeel B., Xue D. The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Critical Reviews in Biochemistry and Molecular Biology 2009, 44(5):264-277.
31. Feigenson G.W., Buboltz J.T. Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol. Biophysical Journal 2001, 80(6):2775-2788.
32. Fridriksson E.K., Shipkova P.A., Sheets E.D., Holowka D., Baird B., McLafferty F.W. Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry 1999, 38(25):8056-8063.
33. Garcia-Saez A.J., Chiantia S., Schwille P. Effect of line tension on the lateral organization of lipid membranes. Journal of Biological Chemistry 2007, 282(46):33537-33544.
34. Gaus K., Rodriguez M., Ruberu K.R., Gelissen I., Sloane T.M., Kritharides L., et al. Domain-specific lipid distribution in macrophage plasma membranes. Journal of Lipid Research 2005, 46(7):1526-1538.
35. Ge M., Gidwani A., Brown H.A., Holowka D., Baird B., Freed J.H. Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells. An ESR study. Biophysical Journal 2003, 85(2):1278-1288.
36. Gerl M.J., Sampaio J.L., Urban S., Kalvodova L., Verbavatz J.M., Binnington B., et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. Journal of Cell Biology 2012, 196(2):213-221.
37. Goh S.L., Amazon J.J., Feigenson G.W. Toward a better raft model: modulated phases in the four-component bilayer, DSPC/DOPC/POPC/CHOL. Biophysical Journal 2013, 104(4):853-862.
38. Goswami D., Gowrishankar K., Bilgrami S., Ghosh S., Raghupathy R., Chadda R., et al. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008, 135(6):1085-1097.
39. Gowrishankar K., Ghosh S., Saha S., R.C., Mayor S., Rao M. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 2012, 149(6):1353-1367.
40. Gray E., Karslake J., Machta B.B., Veatch S.L. Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophysical Journal 2013, 105(12):2751-2759.
41. Griffié J., Burn G., Owen D.M. The Nanoscale Organization of Signaling Domains at the Plasma Membrane. Current Topics in Membranes 2015, 75:125-166.
42. Groves J.T. Cell membranes: glycans' imprints. Nat Mater 2013, 12(2):96-97.
43. Haines T.H. Do sterols reduce proton and sodium leaks through lipid bilayers?. Progress in Lipid Research 2001, 40(4):299-324.
44. Hammond A.T., Heberle F.A., Baumgart T., Holowka D., Baird B., Feigenson G.W. Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(18):6320-6325.
45. Hao M., Mukherjee S., Maxfield F.R. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(23):13072.
46. Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. Journal of Cell Biology 1998, 141(4):929-942.
47. Heberle F.A., Petruzielo R.S., Pan J., Drazba P., Kucerka N., Standaert R.F., et al. Bilayer thickness mismatch controls domain size in model membranes. Journal of the American Chemical Society 2013, 135(18):6853-6859.
48. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophysical Journal 2002, 83(5):2693-2701.
49. Hess S.T., Gould T.J., Gudheti M.V., Maas S.A., Mills K.D., Zimmerberg J. Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(44):17370-17375.
50. Holowka D., Baird B. Structural studies on the membrane-bound immunoglobulin E-receptor complex. 1. Characterization of large plasma membrane vesicles from rat basophilic leukemia cells and insertion of amphipathic fluorescent probes. Biochemistry 1983, 22(14):3466-3474.
51. Honerkamp-Smith A.R., Veatch S.L., Keller S.L. An introduction to critical points for biophysicists; observations of compositional heterogeneity in lipid membranes. Biochimica et Biophysica Acta 2009, 1788(1):53-63.
52. Honigmann A., Sadeghi S., Keller J., Hell S.W., Eggeling C., Vink R. A lipid bound actin meshwork organizes liquid phase separation in model membranes. eLife 2014, 3:e01671.
53. Ipsen J.H., Karlstrom G., Mouritsen O.G., Wennerstrom H., Zuckermann M.J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochimica et Biophysica Acta 1987, 905(1):162-172.
54. Janmey P.A., Lindberg U. Cytoskeletal regulation: rich in lipids. Nature Reviews Molecular Cell Biology 2004, 5(8):658-666.
55. Johnson S.A., Stinson B.M., Go M.S., Carmona L.M., Reminick J.I., Fang X., et al. Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochimica et Biophysica Acta 2010, 1798(7):1427-1435.
56. Kahya N., Brown D.A., Schwille P. Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles. Biochemistry 2005, 44(20):7479-7489.
57. Kaiser H.J., Lingwood D., Levental I., Sampaio J.L., Kalvodova L., Rajendran L., et al. Order of lipid phases in model and plasma membranes. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(39):16645-16650.
58. Keller S.L., Anderson T.G., McConnell H.M. Miscibility critical pressures in monolayers of ternary lipid mixtures. Biophysical Journal 2000, 79:2033-2042.
59. Keller H., Lorizate M., Schwille P. PI(4,5)P2 degradation promotes the formation of cytoskeleton-free model membrane systems. ChemPhysChem 2009, 10(16):2805-2812.
60. Keller S.L., Pitcher W.H., Huestis W.H., McConnell H.M. Red blood cell lipids form immiscible liquids. Physical Review Letters 1998, 81(22):5019.
61. Kelly C.V., Kober M.M., Kinnunen P., Reis D.A., Orr B.G., Banaszak Holl M.M. Pulsed-laser creation and characterization of giant plasma membrane vesicles from cells. Journal of Biological Physics 2009, 35(3):279-295.
62. Kenworthy A.K. Fluorescence recovery after photobleaching studies of lipid rafts. Methods in Molecular Biology 2007, 398:179-192.
63. Kim H.M., Choo H.J., Jung S.Y., Ko Y.G., Park W.H., Jeon S.J., et al. A two-photon fluorescent probe for lipid raft imaging: C-laurdan. Chembiochem 2007, 8(5):553-559.
64. Klose C., Ejsing C.S., Garcia-Saez A.J., Kaiser H.J., Sampaio J.L., Surma M.A., et al. Yeast lipids can phase-separate into micrometer-scale membrane domains. Journal of Biological Chemistry 2010, 285(39):30224-30232.
65. Korlach J., Schwille P., Webb W.W., Feigenson G.W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 1999, 96(15):8461.
66. LaRocca T.J., Pathak P., Chiantia S., Toledo A., Silvius J.R., Benach J.L., et al. Proving lipid rafts exist: membrane domains in the prokaryote Borrelia burgdorferi have the same properties as eukaryotic lipid rafts. PLoS Pathogens 2013, 9(5):e1003353.
67. Levental I., Byfield F.J., Chowdhury P., Gai F., Baumgart T., Janmey P.A. Cholesterol-dependent phase separation in cell-derived giant plasma-membrane vesicles. Biochemical Journal 2009, 424(2):163-167.
68. Levental I., Grzybek M., Simons K. Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 2010, 49(30):6305-6316.
69. Levental I., Grzybek M., Simons K. Raft domains of variable properties and compositions in plasma membrane vesicles. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(28):11411-11416.
70. Levental K.R., Levental I. Isolation of giant plasma membrane vesicles for evaluation of plasma membrane structure and protein partitioning. Methods in Molecular Biology 2015, 1232:65-77.
71. Levental I., Lingwood D., Grzybek M., Coskun U., Simons K. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(51):22050-22054.
72. Lin Q., London E. Altering hydrophobic sequence lengths shows that hydrophobic mismatch controls affinity for ordered lipid domains (rafts) in the multitransmembrane strand protein perfringolysin O. Journal of Biological Chemistry 2013, 288(2):1340-1352.
73. Lingwood D., Ries J., Schwille P., Simons K. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(29):10005-10010.
74. Lingwood D., Simons K. Lipid rafts as a membrane-organizing principle. Science 2010, 327(5961):46-50.
75. Machta B.B., Papanikolaou S., Sethna J.P., Veatch S.L. Minimal model of plasma membrane heterogeneity requires coupling cortical actin to criticality. Biophysical Journal 2011, 100(7):1668-1677.
76. Mahammad S., Dinic J., Adler J., Parmryd I. Limited cholesterol depletion causes aggregation of plasma membrane lipid rafts inducing T cell activation. Biochimica et Biophysica Acta 2010, 1801(6):625-634.
77. Manni M.M., Sot J., Goni F.M. Interaction of C. perfringens epsilon-toxin with biological and model membranes: a putative protein receptor in cells. Biochimica et Biophysica Acta 2015, 1848(3):797-804.
78. McConnell H.M., Vrljic M. Liquid-liquid immiscibility in membranes. Annual Review of Biophysics and Biomolecular Structure 2003, 32:469-492.
79. Meder D., Moreno M.J., Verkade P., Vaz W.L., Simons K. Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(2):329-334.
80. Mouritsen O.G., Bloom M. Mattress model of lipid-protein interactions in membranes. Biophysical Journal 1984, 46(2):141-153.
81. Nikolaus J., Scolari S., Bayraktarov E., Jungnick N., Engel S., Pia Plazzo A., et al. Hemagglutinin of influenza virus partitions into the nonraft domain of model membranes. Biophysical Journal 2010, 99(2):489-498.
82. Norman L.L., Oetama R.J., Dembo M., Byfield F., Hammer D.A., Levitan I., et al. Modification of cellular cholesterol content affects traction force, adhesion and cell spreading. Cellular and Molecular Bioengineering 2010, 3(2):151-162.
83. Ostrom R.S., Liu X. Detergent and detergent-free methods to define lipid rafts and caveolae. Methods in Molecular Biology 2007, 400:459-468.
84. Owen D.M., Rentero C., Magenau A., Abu-Siniyeh A., Gaus K. Quantitative imaging of membrane lipid order in cells and organisms. Nature Protocols 2011, 7(1):24-35.
85. Owen D.M., Williamson D.J., Magenau A., Gaus K. Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nature Communications 2012, 3:1256.
86. Pae J., Saalik P., Liivamagi L., Lubenets D., Arukuusk P., Langel U., et al. Translocation of cell-penetrating peptides across the plasma membrane is controlled by cholesterol and microenvironment created by membranous proteins. Journal of Controlled Release 2014, 192:103-113.
87. Parasassi T., De Stasio G., Ravagnan G., Rusch R.M., Gratton E. Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophysical Journal 1991, 60(1):179-189.
88. Pathak P., London E. 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. Biophysical Journal 2011, 101(10):2417-2425.
89. Prior I.A., Hancock J.F. Ras trafficking, localization and compartmentalized signalling. Seminars in Cell & Developmental Biology 2012, 145-153.
90. Resh M.D. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Science's STKE 2006, 2006(359):re14.
91. Rice P.A., McConnell H.M. Critical shape transitions of monolayer lipid domains. Proceedings of the National Academy of Sciences of the United States of America 1989, 86(17):6445-6448.
92. Saenz J.P., Sezgin E., Schwille P., Simons K. Functional convergence of hopanoids and sterols in membrane ordering. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(35):14236-14240.
93. Sahu S.K., Gummadi S.N., Manoj N., Aradhyam G.K. Phospholipid scramblases: an overview. Archives of Biochemistry and Biophysics 2007, 462(1):103-114.
94. Sampaio J.L., Gerl M.J., Klose C., Ejsing C.S., Beug H., Simons K., et al. Membrane lipidome of an epithelial cell line. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(5):1903-1907.
95. Samsonov A.V., Mihalyov I., Cohen F.S. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophysical Journal 2001, 81(3):1486-1500.
96. Sanchez S.A., Tricerri M.A., Gratton E. Laurdan generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(19):7314-7319.
97. Scheiffele P., Roth M.G., Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO Journal 1997, 16(18):5501-5508.
98. Schuck S., Honsho M., Ekroos K., Shevchenko A., Simons K. Resistance of cell membranes to different detergents. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(10):5795-5800.
99. Schuck S., Simons K. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. Journal of Cell Science 2004, 117(Pt 25):5955-5964.
100. Scott R.E. Plasma membrane vesiculation: a new technique for isolation of plasma membranes. Science 1976, 194(4266):743-745.
101. Scott R.E., Perkins R.G., Zschunke M.A., Hoerl B.J., Maercklein P.B. Plasma membrane vesiculation in 3T3 and SV3T3 cells. I. Morphological and biochemical characterization. Journal of Cell Science 1979, 35:229-243.
102. Sengupta P., Hammond A., Holowka D., Baird B. Structural determinants for partitioning of lipids and proteins between coexisting fluid phases in giant plasma membrane vesicles. Biochimica et Biophysica Acta 2008, 1778(1):20-32.
103. Sezgin, E., Grzybek, M., Buhl, T., Dirkx, R., Gutmann, T., Coskun, U., et al. Adaptive lipid packing and bioactivity in membrane domains. PLoS One, in press.
104. Sezgin E., Levental I., Grzybek M., Schwarzmann G., Mueller V., Honigmann A., et al. Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochimica et Biophysica Acta 2012, 1818(7):1777-1784.
105. Sezgin E., Sadowski T., Simons K. Measuring lipid packing of model and cellular membranes with environment sensitive probes. Langmuir 2014, 30(27):8160-8166.
106. Sheets E.D., Holowka D., Baird B. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes. Journal of Cell Biology 1999, 145(4):877-887.
107. Sheetz M.P., Sable J.E., Dobereiner H.G. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annual Review of Biophysics and Biomolecular Structure 2006, 35:417-434.
108. Shogomori H., Hammond A.T., Ostermeyer-Fay A.G., Barr D.J., Feigenson G.W., London E., et al. Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells. Journal of Biological Chemistry 2005, 280(19):18931-18942.
109. Simons K., Gerl M.J. Revitalizing membrane rafts: new tools and insights. Nature Reviews Molecular Cell Biology 2010, 11(10):688-699.
110. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387(6633):569-572.
111. Simons K., Toomre D. Lipid rafts and signal transduction. Nature Reviews Molecular Cell Biology 2000, 1(1):31-39.
112. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry 1988, 27(17):6197-6202.
113. Simons K., Vaz W.L. Model systems, lipid rafts, and cell membranes. Annual Review of Biophysics and Biomolecular Structure 2004, 33:269-295.
114. Suzuki K.G. Lipid rafts generate digital-like signal transduction in cell plasma membranes. Biotechnology Journal 2012, 7(6):753-761.
115. Tank D.W., Wu E.S., Webb W.W. Enhanced molecular diffusibility in muscle membrane blebs: release of lateral constraints. Journal of Cell Biology 1982, 92(1):207-212.
116. Toulmay A., Prinz W.A. Direct imaging reveals stable, micrometer-scale lipid domains that segregate proteins in live cells. Journal of Cell Biology 2013, 202(1):35-44.
117. Veatch S.L., Cicuta P., Sengupta P., Honerkamp-Smith A., Holowka D., Baird B. Critical fluctuations in plasma membrane vesicles. ACS Chemical Biology 2008, 3(5):287-293.
118. Veatch S.L., Keller S.L. Organization in lipid membranes containing cholesterol. Physical Review Letters 2002, 89(26):268101.
119. Veatch S.L., Keller S.L. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophysical Journal 2003, 85(5):3074-3083.
120. Veatch S.L., Soubias O., Keller S.L., Gawrisch K. Critical fluctuations in domain-forming lipid mixtures. PNAS 2007, 104(45):17650-17655.
121. Zhang W., Trible R.P., Samelson L.E. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 1998, 9(2):239-246.
122. Zhao J., Wu J., Veatch S.L. Adhesion stabilizes robust lipid heterogeneity in supercritical membranes at physiological temperature. Biophysical Journal 2013, 104(4):825-834.
123. Zhou Y., Maxwell K.N., Sezgin E., Lu M., Liang H., Hancock J.F., et al. Bile acids modulate signaling by functional perturbation of plasma membrane domains. Journal of Biological Chemistry 2013, 288(50):35660-35670.
124. Zidovetzki R., Levitan I. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochimica et Biophysica Acta 2007, 1768(6):1311-1324.