Use of cyclodextrins to manipulate plasma membrane cholesterol content: Evidence, misconceptions and control strategies

Biochimica et Biophysica Acta (BBA) - Biomembranes - Tập 1768 Số 6 - Trang 1311-1324 - 2007
Raphael Zidovetzki1, Irena Levitan2
1Department of Cell Biology and Neuroscience, University of California, Riverside, CA 90291, USA
2Department of Medicine, University of Illinois at Chicago, Chicago, IL 60304, USA

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Davis, 2004, Cyclodextrin-based pharmaceutics: past, present and future, Nat. Rev., Drug Discov., 3, 1023, 10.1038/nrd1576

Uekama, 2004, Design and evaluation of cyclodextrin-based drug formulation, Chem. Pharm. Bull. (Tokyo), 52, 900, 10.1248/cpb.52.900

Irie, 1992, Hydroxypropylcyclodextrins in parenteral use. I: lipid dissolution and effects on lipid transfers in vitro, J. Pharm. Sci., 81, 521, 10.1002/jps.2600810609

Ohtani, 1989, Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes, Eur. J. Biochem., 186, 17, 10.1111/j.1432-1033.1989.tb15171.x

Ohvo, 1996, Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate, Biochemistry, 35, 8018, 10.1021/bi9528816

Tsamaloukas, 2005, Interactions of cholesterol with lipid membranes and cyclodextrin characterized by calorimetry, Biophys. J., 89, 1109, 10.1529/biophysj.105.061846

Kilsdonk, 1995, Cellular cholesterol efflux mediated by cyclodextrins, J. Biol. Chem., 270, 17250, 10.1074/jbc.270.29.17250

Christian, 1997, Use of cyclodextrins for manipulating cellular cholesterol content, J. Lipid Res., 38, 2264, 10.1016/S0022-2275(20)34940-3

Atger, 1997, Cyclodextrins as catalysts for the removal of cholesterol from macrophage foam cells, J. Clin. Invest., 99, 773, 10.1172/JCI119223

Levitan, 2000, Membrane cholesterol content modulates activation of volume-regulated anion current (VRAC) in bovine endothelial cells, J. Gen. Physiol., 115, 405, 10.1085/jgp.115.4.405

Irie, 1982, Cyclodextrin-induced hemolysis and shape changes of human erythrocytes in vitro, J. Pharmacobio-dyn., 5, 741, 10.1248/bpb1978.5.741

Matthews, 2003, Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE), J. Biol. Chem., 278, 38829, 10.1074/jbc.M210584200

Niu, 2002, Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation, J. Biol. Chem., 277, 20139, 10.1074/jbc.M200594200

Sheets, 1999, Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes, J. Cell Biol., 145, 877, 10.1083/jcb.145.4.877

Dreja, 2002, Cholesterol depletion disrupts caveolae and differentially impairs agonist-induced arterial contraction, Arterioscler. Thromb. Vasc. Biol., 22, 1267, 10.1161/01.ATV.0000023438.32585.A1

Keller, 1998, Cholesterol is required for surface transport of influenza virus hemagglutinin, J. Cell Biol., 140, 1357, 10.1083/jcb.140.6.1357

Romanenko, 2004, Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels, Biophys. J., 87, 3850, 10.1529/biophysj.104.043273

Grimmer, 2002, Membrane ruffling and macropinocytosis in A431 cells require cholesterol, J. Cell Sci., 115, 2953, 10.1242/jcs.115.14.2953

Fulop, 2001, Cyclodextrin modulation of T lymphocyte signal transduction with aging, Mech. Ageing Dev., 122, 1413, 10.1016/S0047-6374(01)00274-3

Davis, 1987, Modulation of 3-hydroxy-3-methylglutaryl-CoA reductase by changes in microsomal cholesterol content or phospholipid composition, Proc. Natl. Acad. Sci. U. S. A., 84, 118, 10.1073/pnas.84.1.118

Slotte, 1988, Depletion of plasma-membrane sphingomyelin rapidly alters the distribution of cholesterol between plasma membranes and intracellular cholesterol pools in cultured fibroblasts, Biochem. J., 250, 653, 10.1042/bj2500653

Lange, 1991, Disposition of intracellular cholesterol in human fibroblasts, J. Lipid Res., 32, 329, 10.1016/S0022-2275(20)42093-0

Lange, 1989, Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts, J. Biol. Chem., 264, 3786, 10.1016/S0021-9258(19)84918-9

Kim, 1991, b-VLDL increases endothelial cell plasma membrane cholesterol, J. Lipid Res., 32, 1125, 10.1016/S0022-2275(20)41975-3

van Meer, 1989, Lipid traffic in animal cells, Annu. Rev. Cell Biol., 5, 247, 10.1146/annurev.cb.05.110189.001335

Hao, 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, 10.1074/jbc.M108861200

Lange, 1999, Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol, J. Lipid Res., 40, 2264, 10.1016/S0022-2275(20)32101-5

Lange, 2004, How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids, Proc. Natl. Acad. Sci. U. S. A., 101, 11664, 10.1073/pnas.0404766101

Pike, 2006, Rafts defined: a report on the Keystone symposium on lipid rafts and cell function, J. Lipid Res., 47, 1597, 10.1194/jlr.E600002-JLR200

Sowa, 2001, Distinction between signaling mechanisms in lipid rafts vs. caveolae, Proc. Natl. Acad. Sci. U. S. A., 98, 14072, 10.1073/pnas.241409998

Oh, 2001, Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default, Mol. Biol. Cell, 12, 685, 10.1091/mbc.12.3.685

Pike, 2002, Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis, Biochemistry, 41, 2075, 10.1021/bi0156557

Anderson, 2002, A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains, Science, 296, 1821, 10.1126/science.1068886

Kiyokawa, 2005, Spatial and functional heterogeneity of sphingolipid-rich membrane domains, J. Biol. Chem., 280, 24072, 10.1074/jbc.M502244200

Simons, 1997, Functional rafts in cell membranes, Nature, 387, 569, 10.1038/42408

Simons, 2000, Lipid rafts and signal transduction. Nature reviews, Mol. Cell. Biol., 1, 31

Edidin, 2001, Membrane cholesterol, protein phosphorylation and lipid rafts, Sci. STKE, 67, PE1

Edidin, 2003, The state of lipid rafts: from model membranes to cells, Annu. Rev. Biophys. Biomol. Struct., 32, 257083, 10.1146/annurev.biophys.32.110601.142439

Pike, 2003, Lipid rafts: bringing order to chaos, J. Lipid Res., 44, 655, 10.1194/jlr.R200021-JLR200

Munro, 2003, Lipid rafts: elusive or illusive?, Cell, 115, 377, 10.1016/S0092-8674(03)00882-1

McConnell, 2003, Liquid–liquid immiscibility in membranes, Annu. Rev. Biophys. Biomol. Struct., 32, 469, 10.1146/annurev.biophys.32.110601.141704

Lommerse, 2004, In vivo plasma membrane organization: results of biophysical approaches, Biochim. Biophys. Acta (BBA) — Biomembr., 1664, 119, 10.1016/j.bbamem.2004.05.005

London, 2005, How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells, Biochim. Biophys. Acta (BBA) — Mol. Cell Res., 1746, 203, 10.1016/j.bbamcr.2005.09.002

Lagerholm, 2005, Detecting microdomains in intact cell membranes, Annu. Rev. Phys. Chem., 56, 309, 10.1146/annurev.physchem.56.092503.141211

Pike, 2005, Growth factor receptors, lipid rafts and caveolae: an evolving story, Biochim. Biophys. Acta (BBA) — Mol. Cell Res., 1746, 260, 10.1016/j.bbamcr.2005.05.005

Hancock, 2006, Lipid rafts: contentious only from simplistic standpoints, Nat. Rev., Mol. Cell Biol., 7, 456, 10.1038/nrm1925

Silvius, 2005, Lipid microdomains in model and biological membranes: how strong are the connections?, Q. Rev. Biophys., 38, 373, 10.1017/S003358350600415X

Heerklotz, 2002, Triton promotes domain formation in lipid raft mixtures, Biophys. J., 83, 2693, 10.1016/S0006-3495(02)75278-8

Lichtenberg, 2005, Detergent-resistant membranes should not be identified with membrane rafts, Trends Biochem. Sci., 30, 430, 10.1016/j.tibs.2005.06.004

Schuck, 2003, Resistance of cell membranes to different detergents, Proc. Natl. Acad. Sci. U. S. A., 100, 5795, 10.1073/pnas.0631579100

Babiychuk, 2006, Biochemical characterization of detergent-resistant membranes: a systematic approach, Biochem. J., 397, 407, 10.1042/BJ20060056

Scheiffele, 1997, Interaction of influenza virus haemagglutinin with sphingolipid–cholesterol membrane domains via its transmembrane domain, EMBO J., 16, 5501, 10.1093/emboj/16.18.5501

Cheng, 1999, A role for lipid rafts in B cell antigen receptor signaling and antigen targeting, J. Exp. Med., 190, 1549, 10.1084/jem.190.11.1549

Kabouridis, 2000, Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes, Eur. J. Immunol., 30, 954, 10.1002/1521-4141(200003)30:3<954::AID-IMMU954>3.0.CO;2-Y

Predescu, 2005, Cholesterol-dependent syntaxin-4 and SNAP-23 clustering regulates caveolar fusion with the endothelial plasma membrane, J. Biol. Chem., 280, 37130, 10.1074/jbc.M505659200

Harder, 1998, Lipid domain structure of the plasma membrane revealed by patching of membrane components, J. Cell Biol., 141, 929, 10.1083/jcb.141.4.929

Pralle, 2000, Sphingolipid–cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells, J. Cell Biol., 148, 997, 10.1083/jcb.148.5.997

Gidwani, 2001, Fluorescence anisotropy measurements of lipid order in plasma membranes and lipid rafts from rbl-2h3 mast cells, Biochemistry, 40, 12422, 10.1021/bi010496c

Gaus, 2003, Visualizing lipid structure and raft domains in living cells with two-photon microscopy, Proc. Natl. Acad. Sci. U. S. A., 100, 15554, 10.1073/pnas.2534386100

Ushio-Fukai, 2001, Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells, J. Biol. Chem., 276, 48269, 10.1074/jbc.M105901200

Brown, 1992, Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface, Cell, 68, 533, 10.1016/0092-8674(92)90189-J

Rouquette-Jazdanian, 2006, Revaluation of the role of cholesterol in stabilizing rafts implicated in T cell receptor signaling, Cell. Signal., 18, 105, 10.1016/j.cellsig.2005.03.024

Larbi, 2004, Effects of methyl-beta-cyclodextrin on T lymphocytes lipid rafts with aging, Exp. Gerontol., 39, 551, 10.1016/j.exger.2003.10.031

Gaus, 2004, Apolipoprotein A-1 interaction with plasma membrane lipid rafts controls cholesterol export from macrophages, FASEB J., 18, 574, 10.1096/fj.03-0486fje

Gaus, 2005, Domain-specific lipid distribution in macrophage plasma membranes, J. Lipid Res., 46, 1526, 10.1194/jlr.M500103-JLR200

Smart, 1995, A detergent-free method for purifying caveolae membrane from tissue culture cells, Proc. Natl. Acad. Sci., 92, 10104, 10.1073/pnas.92.22.10104

Sampson, 2004, Caveolae localize protein kinase A signaling to arterial ATP-sensitive potassium channels, Circ. Res., 95, 1012, 10.1161/01.RES.0000148634.47095.ab

Giurisato, 2003, T cell receptor can be recruited to a subset of plasma membrane rafts, independently of cell signaling and attendantly to raft clustering, J. Biol. Chem., 278, 6771, 10.1074/jbc.M210758200

Schutz, 2000, Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy, EMBO J., 19, 892, 10.1093/emboj/19.5.892

Swamy, 2006, Coexisting domains in the plasma membranes of live cells characterized by spin-label ESR spectroscopy, Biophys. J., 90, 4452, 10.1529/biophysj.105.070839

Almeida, 2005, Thermodynamics of membrane domains, Biochim. Biophys. Acta (BBA)—Biomembr., 1720, 1, 10.1016/j.bbamem.2005.12.004

Ottico, 2003, Dynamics of membrane lipid domains in neuronal cells differentiated in culture, J. Lipid Res., 44, 2142, 10.1194/jlr.M300247-JLR200

Klein, 1995, Alteration of the myometrial plasma membrane cholesterol with b-cyclodextrin modulates the binding affinity of the oxytocin receptor, Biochemistry, 34, 13784, 10.1021/bi00042a009

Romanenko, 2002, Modulation of endothelial inward rectifier K+ current by optical isomers of cholesterol, Biophys. J., 83, 3211, 10.1016/S0006-3495(02)75323-X

Gimpl, 1995, Expression of the human oxytocin receptor in baculovirus-infected insect cells: high-affinity binding is induced by a cholesterol–cyclodextrin complex, Biochemistry, 34, 13794, 10.1021/bi00042a010

Yancey, 1996, Cellular cholesterol efflux mediated by cyclodextrins. Demonstration Of kinetic pools and mechanism of efflux, J. Biol. Chem., 271, 16026, 10.1074/jbc.271.27.16026

Breusegem, 2005, Acute and chronic changes in cholesterol modulate Na–Pi cotransport activity in OK cells, Am. J. Physiol., Renal Physiol., 289, F154, 10.1152/ajprenal.00331.2004

Romanenko, 2004, Sensitivity of volume-regulated anion current to cholesterol structural analogues, J. Gen. Physiol., 123, 77, 10.1085/jgp.200308882

Sponne, 2004, Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of amyloid-beta peptide, FASEB J., 18, 836, 10.1096/fj.03-0372fje

Lange, 1983, Analysis of the distribution of cholesterol in the intact cell, J. Biol. Chem., 258, 15130, 10.1016/S0021-9258(17)43782-3

Bar, 1986, Fraction of cholesterol undergoing spontaneous exchange between small unilamellar phosphatidylcholine vesicles, Biochemistry, 25, 6701, 10.1021/bi00369a056

Haynes, 2000, Efflux of cholesterol from different cellular pools, Biochemistry, 39, 4508, 10.1021/bi992125q

Steck, 2002, Probing red cell membrane cholesterol movement with cyclodextrin, Biophys. J., 83, 2118, 10.1016/S0006-3495(02)73972-6

Jones, 1989, Spontaneous phosphatidylcholine transfer by collision between vesicles at high lipid concentration, Biochemistry, 28, 129, 10.1021/bi00427a019

Wimley, 1991, Phosphatidylethanolamine enhances the concentration-dependent exchange of phospholipids between bilayers, Biochemistry, 30, 4200, 10.1021/bi00231a014

Thurnhofer, 1990, Uptake of cholesterol by small intestinal brush border membrane is protein-mediated, Biochemistry, 29, 2142, 10.1021/bi00460a026

Nichols, 1981, Kinetics of soluble lipid monomer diffusion between vesicles, Biochemistry, 20, 2783, 10.1021/bi00513a012

Steck, 1988, An activation-collision mechanism for cholesterol transfer between membranes, J. Biol. Chem., 263, 13023, 10.1016/S0021-9258(18)37666-X

Phillips, 1987, Mechanisms and consequences of cellular cholesterol exchange and transfer, Biochim. Biophys. Acta, 906, 223, 10.1016/0304-4157(87)90013-X

Backer, 1981, Mechanism of cholesterol exchange between phospholipid vesicles, Biochemistry, 20, 3805, 10.1021/bi00516a021

Butko, 1990, Acidic phospholipids strikingly potentiate sterol carrier protein 2 mediated intermembrane sterol transfer, Biochemistry, 29, 4070, 10.1021/bi00469a007

Rodrigueza, 1995, Transbilayer movement and net flux of cholesterol and cholesterol sulfate between liposomal membranes, Biochemistry, 34, 6208, 10.1021/bi00018a025

Bojesen, 1996, Oleic acid binding and transport capacity of human red cell membrane, Acta Physiol. Scand., 156, 501, 10.1046/j.1365-201X.1996.456173000.x

Jonas, 1979, Kinetics and mechanism of phosphatidylcholine and cholesterol exchange between single bilayer vesicles and bovine serum high-density lipoprotein, Biochemistry, 18, 1722, 10.1021/bi00576a014

Poznansky, 1979, Cholesterol exchange as a function of cholesterol/phospholipid mole ratios, Biochem. J., 177, 989, 10.1042/bj1770989

Gottlieb, 1980, Rates of cholesterol exchange between human erythrocytes and plasma lipoproteins, Biochim. Biophys. Acta, 600, 530, 10.1016/0005-2736(80)90454-X

McLean, 1982, Cholesterol desorption from clusters of phosphatidylcholine and cholesterol in unilamellar vesicle bilayers during lipid transfer or exchange, Biochemistry, 21, 4053, 10.1021/bi00260a022

McLean, 1981, Mechanism of cholesterol and phosphatidylcholine exchange or transfer between unilamellar vesicles, Biochemistry, 20, 2893, 10.1021/bi00513a028

Slotte, 1983, Transfer of [3H]cholesterol between lipid vesicles and rat arterial smooth muscle cells in vitro, Biochim. Biophys. Acta, 750, 434, 10.1016/0005-2760(83)90182-0

McLean, 1984, Kinetics of phosphatidylcholine and lysophosphatidylcholine exchange between unilamellar vesicles, Biochemistry, 23, 24, 10.1021/bi00315a017

Nichols, 1985, Thermodynamics and kinetics of phospholipid monomer-vesicle interaction, Biochemistry, 24, 6390, 10.1021/bi00344a011

Puglisi, 1996, Interaction of natural and modified β-cyclodextrins with a biological membrane model of dipalmitoylphosphatidylcholine, J. Colloid Interface Sci., 180, 542, 10.1006/jcis.1996.0335

Leventis, 2001, Use of cyclodextrins to monitor transbilayer movement and differential lipid affinities of cholesterol, Biophys. J., 81, 2257, 10.1016/S0006-3495(01)75873-0

Giocondi, 2004, Use of cyclodextrin for AFM monitoring of model raft formation, Biophys. J., 86, 861, 10.1016/S0006-3495(04)74161-2

Fukasawa, 2000, Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-beta-cyclodextrin, J. Biol. Chem., 275, 34028, 10.1074/jbc.M005151200

Hansen, 2001, Lipid rafts exist as stable cholesterol-independent microdomains in the brush border membrane of enterocytes, J. Biol. Chem., 276, 32338, 10.1074/jbc.M102667200

Liu, 2003, Cyclodextrins differentially mobilize free and esterified cholesterol from primary human foam cell macrophages, J. Lipid Res., 44, 1156, 10.1194/jlr.M200464-JLR200

Nakanishi, 1992, Effect of cyclodextrins on biological membrane. II. Mechanism of enhancement on the intestinal absorption of non-absorbable drug by cyclodextrins, Chem. Pharm. Bull. (Tokyo), 40, 1252, 10.1248/cpb.40.1252

Singh, 1983, Effect of cyclodextrins on the solubilization of lignoceric acid, ceramide, and cerebroside, and on the enzymatic reactions involving these compounds, J. Lipid Res., 24, 662, 10.1016/S0022-2275(20)37973-6

Casu, 1990, Interaction of cyclodextrinscyclomalto-oligosaccharides with glycolipids: N.M.R. studies of aqueous system of cyclomaltohexaose and alkyl glycosides, Carbohydr. Res., 200, 101, 10.1016/0008-6215(90)84185-W

Shiraishi, 1993, Effects of cyclodextrins on the hydrolysis of ganglioside GM1 by acid beta-galactosidases, Glycoconj. J., 170, 10.1007/BF00737714

Ahmed, 1994, Disruption of micellar aggregates of ganglioside GM-1 by complexation with -cyclodextrin, Int. J. Pharm., 109, 99, 10.1016/0378-5173(94)90137-6

Monnaert, 2004, Behavior of alpha-, beta-, and gamma-cyclodextrins and their derivatives on an in vitro model of blood–brain barrier, J. Pharmacol. Exp. Ther., 310, 745, 10.1124/jpet.104.067512

Rawyler, 1996, Cyclodextrins: a new tool for the controlled lipid depletion of thylakoid membranes, Biochim. Biophys. Acta, 1278, 89, 10.1016/0005-2736(95)00190-5

Anderson, 2004, Calorimetric measurement of phospholipid interaction with methyl-beta-cyclodextrin, Biochemistry, 43, 2251, 10.1021/bi0358869

Cooper, 1992, Effect of cyclodextrins on the thermal stability of globular proteins, J. Am. Chem. Soc., 114, 9208, 10.1021/ja00049a074

Horský, 1994, Inclusion complexes of proteins: interaction of cyclodextrins with peptides containing aromatic amino acids studied by competitive spectrophotometry, J. Incl. Phenom. Mol. Recognit. Chem., 18, 291, 10.1007/BF00708735

Breslow, 1998, Sequence selective binding of peptides by artificial receptors in aqueous solution, J. Am. Chem. Soc., 120, 3536, 10.1021/ja973991y

Uekama, 1999, Cyclodextrins in drug delivery system, Adv. Drug Deliv. Rev., 36, 1

Pitha, 1988, Drug solubilizers to aid pharmacologists: amorphous cyclodextrin derivatives, Life Sci., 43, 493, 10.1016/0024-3205(88)90150-6

Aachmann, 2003, Structural background of cyclodextrin–protein interactions, Protein Eng., 16, 905, 10.1093/protein/gzg137

Williamson, 1997, Function of conserved tryptophans in the Aspergillus niger glucoamylase 1 starch binding domain, Biochemistry, 36, 7535, 10.1021/bi9702896

Schmidt, 1998, Structure of cyclodextrin glycosyltransferase complexed with a derivative of its main product beta-cyclodextrin, Biochemistry, 37, 5909, 10.1021/bi9729918

Evenas, 2001, Ligand-induced structural changes to maltodextrin-binding protein as studied by solution NMR spectroscopy, J. Mol. Biol., 309, 961, 10.1006/jmbi.2001.4695

Duan, 2001, Crystal structures of the maltodextrin/maltose-binding protein complexed with reduced oligosaccharides: flexibility of tertiary structure and ligand binding, J. Mol. Biol., 306, 1115, 10.1006/jmbi.2001.4456

Larson, 1994, Refined molecular structure of pig pancreatic alpha-amylase at 2.1 A resolution, J. Mol. Biol., 235, 1560, 10.1006/jmbi.1994.1107

Mikami, 1993, The 2.0-A resolution structure of soybean beta-amylase complexed with alpha-cyclodextrin, Biochemistry, 32, 6836, 10.1021/bi00078a006

Ilangumaran, 1998, Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane, Biochem. J., 335, 433, 10.1042/bj3350433

Locke, 2004, Reversible pore block of connexin channels by cyclodextrins, J. Biol. Chem., 279, 22883, 10.1074/jbc.M401980200

Gu, 1999, Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter, Nature, 398, 686, 10.1038/19491

Rozema, 1996, Artificial chaperone-assisted refolding of carbonic anhydrase B, J. Biol. Chem., 271, 3478, 10.1074/jbc.271.7.3478

Kwik, 2003, Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin, Proc. Natl. Acad. Sci. U. S. A., 100, 13964, 10.1073/pnas.2336102100

Gimpl, 1997, Cholesterol as modulator of receptor function, Biochemistry, 36, 10959, 10.1021/bi963138w

Ferraro, 2004, Depletion of plasma membrane cholesterol dampens hydrostatic pressure and shear stress-induced mechanotransduction pathways in osteoblast cultures, Am. J. Physiol., Cell Physiol., 286, C831, 10.1152/ajpcell.00224.2003

Byfield, 2004, Cholesterol depletion increases membrane stiffness of aortic endothelial cells, Biophys. J., 87, 3336, 10.1529/biophysj.104.040634

Slotte, 1994, Effect of sterol side-chain structure on sterol–phosphatidylcholine interactions in monolayers and small unilamellar vesicles, Biochim. Biophys. Acta, 1190, 435, 10.1016/0005-2736(94)90105-8

Mattjus, 1995, Lateral domain formation in cholesterol/phospholipid monolayers as affected by the sterol side chain conformation, Biochim. Biophys. Acta, 1240, 237, 10.1016/0005-2736(95)00179-4

Slotte, 1995, Effect of sterol structure on molecular interactions and lateral domain formation in monolayers containing dipalmitoyl phosphatidylcholine, Biochim. Biophys. Acta, 1237, 127, 10.1016/0005-2736(95)00096-L

Bittman, 1972, The phospholipid–cholesterol interaction. Kinetics of water permeability in liposomes, Biochemistry, 11, 4821, 10.1021/bi00775a029

Demel, 1972, The effect of sterol structure on the permeability of liposomes to glucose, glycerol and Rb+, Biochim. Biophys Acta, 255, 321, 10.1016/0005-2736(72)90031-4

De Kruyff, 1972, The effects of cholesterol and epicholesterol incorporation on the permeability and the phase transition of intact Acholeplasma Laidlawii cell membranes and derived liposomes, Biochim. Biophys Acta, 255, 331, 10.1016/0005-2736(72)90032-6

Halling, 2004, Membrane properties of plant sterols in phospholipid bilayers as determined by differential scanning calorimetry, resonance energy transfer and detergent-induced solubilization, Biochim. Biophys. Acta, 1664, 161, 10.1016/j.bbamem.2004.05.006

Xu, 2000, The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation, Biochemistry, 39, 843, 10.1021/bi992543v

Sooksawate, 2001, Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones, Neuropharmacology, 40, 178, 10.1016/S0028-3908(00)00159-3