Glycosylation induces shifts in the lateral distribution of cholesterol from ordered towards less ordered domains

Biochimica et Biophysica Acta - Biomembranes

Volumn 1778, Issue 4, 2008, Pages 1100-1111

  Halling, Katrin K ^a   Ramstedt, Bodil ^a   Slotte, J Peter ^a  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Cell stress; Cholesteryl galactoside; Cholesteryl glucoside; Model membrane

Indexed keywords

CHOLESTEROL; CHOLESTEROL GLUCOSIDE; CHOLESTERYL GALACTOSIDE; GLYCEROPHOSPHOLIPID; MEMBRANE LIPID; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; CELL STRESS; CHOLESTEROL TRANSPORT; DIFFERENTIAL SCANNING CALORIMETRY; FLUORESCENCE; GLYCOSYLATION; LIPID BILAYER; PHASE TRANSITION; PRIORITY JOURNAL;

ANISOTROPY; CALORIMETRY, DIFFERENTIAL SCANNING; CHOLESTEROL; GLUCOSIDES; GLYCOSYLATION; LIPID BILAYERS; MEMBRANE FLUIDITY; PHOSPHATIDYLCHOLINES; PRESSURE;

EID: 40949096381     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.01.001     Document Type: Article

References (74)

1. Moreau R.A., Whitaker B.D., and Hicks K.B. Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. Prog. Lipid Res. 41 (2002) 457-500
2. Sakaki T., Zähringer U., Warnecke D.C., Fahl A., Knogge W., and Heinz E. Sterol glycosides and cerebrosides accumulate in Pichia pastoris, Rhynchosporium secalis and other fungi under normal conditions or under heat shock and ethanol stress. Yeast 18 (2001) 679-695
3. Peng L., Kawagoe Y., Hogan P., and Delmer D. Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295 (2002) 147-150
4. Lynch D.V., Criss A.K., Lehoczky J.L., and Bui V.T. Ceramide glucosylation in bean hypocotyl microsomes: evidence that steryl glucoside serves as glucose donor. Arch. Biochem. Biophys. 340 (1997) 311-316
5. Ullmann P., Ury A., Rimmele D., Benveniste P., and Bouvier-Navé P. UDP-glucose sterol β-d-glucosyltransferase, a plasma membrane-bound enzyme of plants: enzymatic properties and lipid dependence. Biochimie 75 (1993) 713-723
6. Ly P.T.T., Singh S., and Shaw C.A. Novel environmental toxins: steryl glycosides as a potential etiological factor for age-related neurodegenerative diseases. J. Neurosci. Res. 85 (2007) 231-237
7. Nazarko T.Y., Polupanov A.S., Manjithaya R.R., Subramani S., and Sibirny A.A. The requirement of sterol glucoside for pexophagy in yeast is dependent on the species and nature of peroxisome inducers. Mol. Biol. Cell 18 (2007) 106-118
8. Murakami-Murofushi K., Nishikawa K., Hirakawa E., and Murofushi H. Heat stress induces a glycosylation of membrane sterol in myxoamoebae of a true slime mold, Physarum polycephalum. J. Biol. Chem. 272 (1997) 486-489
9. Kunimoto S., Kobayashi T., Kobayashi S., and Murakami-Murofushi K. Expression of cholesteryl glucoside by heat shock in human fibroblasts. Cell Stress Chaperones 5 (2000) 3-7
10. Kunimoto S., Murofushi W., Yamatsu I., Hasegawa Y., Sasaki N., Kobayashi S., Kobayashi T., Murofushi H., and Murakami-Murofushi K. Cholesteryl glucoside-induced protection against gastric ulcer. Cell Struct. Funct. 28 (2003) 179-186
11. Mouritsen O.G., and Zuckermann M.J. What's so special about cholesterol?. Lipids 39 (2004) 1101-1113
12. Ramstedt B., and Slotte J.P. Sphingolipids and the formation of sterol-enriched ordered membrane domains. Biochim. Biophys. Acta 1758 (2006) 1945-1956
13. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
14. Jacobson K., Mouritsen O.G., and Anderson R.G.W. Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9 (2007) 7-14
15. Csont T., Balogh G., Csonka C., Boros I., Horváth I., Vigh L., and Ferdinandy P. Hyperlipidemia induced by high cholesterol diet inhibits heat shock response in rat hearts. Biochem. Biophys. Res. Commun. 290 (2002) 1535-1538
16. Balogh G., Horváth I., Nagy E., Hoyk Z., Benko S., Bensaude O., and Vigh L. The hyperfluidization of mammalian cell membranes acts as a signal to initiate the heat shock protein response. FEBS J. 272 (2005) 6077-6086
17. Nagy E., Balogi Z., Gombos I., Åkerfelt M., Björkbom A., Balogh G., Török Z., Maslyanko A., Fiszer-Kierzkowska A., Lisowska K., Slotte P.J., Sistonen L., Horváth I., and Vigh L. Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 7945-7950
18. Vigh L., Horváth I., Maresca B., and Harwood J.L. Can the stress protein response be controlled by 'membrane-lipid therapy'?. TRENDS Biochem. Sci. 32 (2007) 357-363
19. Nagarajan S., Rao L.J.M., and Gurudutt K.N. A convenient preparative method for the glucosides of fatty alcohols and sterols. Ind. J. Chem. 37B (1998) 132-134
20. Iga D.P., Iga S., Schmidt R.R., and Buzas M.-C. Chemical synthesis of cholesteryl β-d-galactofuranoside and -pyranoside. Carbohydr. Res. 340 (2005) 2052-2054
21. Cohen R., Barenholz Y., Gatt S., and Dagan A. Preparation and characterization of well defined d-erythro sphingomyelins. Chem. Phys. Lipids 35 (1984) 371-384
22. Szolderits G., Daum G., Paltauf F., and Hermetter A. Protein-catalyzed transport of ether phospholipids. Biochim. Biophys. Acta 1063 (1991) 197-202
23. Rouser G., Fleischer S., and Yamamoto A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5 (1970) 494-496
24. Kuklev D.V., and Smith W.L. Synthesis of four isomers of parinaric acid. Chem. Phys. Lipids 131 (2004) 215-222
25. Sklar L.A., Hudson B.S., Petersen M., and Diamond J. Conjugated polyene fatty acids on fluorescent probes: spectroscopic characterization. Biochemistry 16 (1977) 813-819
26. Björkqvist Y.J.E., Nyholm T.K.M., Slotte J.P., and Ramstedt B. Domain formation and stability in complex lipid bilayers as reported by cholestatrienol. Biophys. J. 88 (2005) 4054-4063
27. Alanko S.M.K., Halling K.K., Maunula S., Slotte J.P., and Ramstedt B. Displacement of sterols from sterol/sphingomyelin domains in fluid bilayer membranes by competing molecules. Biochim. Biophys. Acta 1715 (2005) 111-121
28. Ahmed S.N., Brown D.A., and 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 36 (1997) 10944-10953
29. Davies M.A., Schuster H.F., Brauner J.W., and Mendelsohn R. Effects of cholesterol on conformational disorder in dipalmitoylphosphatidylcholine bilayers. A quantitative IR study of the depth dependence. Biochemistry 29 (1990) 4368-4373
30. Pebay-Peyroula E., Dufourc E.J., and Szabo A.G. Location of diphenyl-hexatriene and trimethylammonium-diphenyl-hexatriene in dipalmitoylphosphatidylcholine bilayers by neutron diffraction. Biophys. Chem. 53 (1994) 45-56
31. Kawato S., Kinosita K., and Ikegami A. Effect of cholesterol on the molecular motion in the hydrocarbon region of lecithin bilayers studied by nanosecond fluorescence techniques. Biochemistry 17 (1978) 5026-5031
32. Kuikka M., Ramstedt B., Ohvo-Rekilä H., Tuuf J., and Slotte J.P. Membrane properties of d-erythro-N-acyl sphingomyelins and their corresponding dihydro species. Biophys. J. 80 (2001) 2327-2337
33. Térová B., Heczko R., and Slotte J.P. On the importance of the phosphocholine methyl groups for sphingomyelin/cholesterol interactions in membranes: a study with ceramide phosphoethanolamine. Biophys. J. 88 (2005) 2661-2669
34. Koynova R., and Caffrey M. Phases and phase transitions of the phosphatidylcholines. Biochim. Biophys. Acta 1376 (1998) 91-145
35. Prendergast F.G., Haugland R.P., and Callahan P.J. 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers. Biochemistry 20 (1981) 7333-7338
36. Maunula S., Björkqvist Y.J.E., Slotte J.P., and Ramstedt B. Differences in the domain forming properties of N-palmitoylated neutral glycosphingolipids in bilayer. Biochim. Biophys. Acta 1768 (2007) 336-345
37. Baglioni P., Cestelli G., Dei L., and Gabrielli G. Monolayers of cholesterol at water-air interface: mechanism of collapse. J. Colloid Interface Sci. 104 (1985) 143-150
38. Ohvo-Rekilä H., Åkerlund B., and Slotte J.P. Cyclodextrin-catalyzed extraction of fluorescent sterols from monolayer membranes and small unilamellar vesicles. Chem. Phys. Lipids 105 (2000) 167-178
39. Hinz H.J., Kuttenreich H., Meyer R., Renner M., Fründ R., Koynova R., Boyanov A.I., and Tenchov B.G. Stereochemistry and size of sugar head groups determine structure and phase behavior of glycolipid membranes: densitometric, calorimetric, and X-ray studies. Biochemistry 30 (1991) 5125-5138
40. Mannock D.A., Harper P.E., Gruner S.M., and McElhaney R.N. The physical properties of glycosyl diacylglycerols. Calorimetric, X-ray diffraction and Fourier transform spectroscopic studies of a homologous series of 1,2-di-O-acyl-3-O-(β-d-galactopyranosyl)-sn-glycerols. Chem. Phys. Lipids 111 (2001) 139-161
41. Murari R., Murari M.P., and Baumann W.J. Sterol orientations in phosphatidylcholine liposomes as determined by deuterium NMR. Biochemistry 25 (1986) 1062-1067
42. 2H NMR investigation. FEBS Lett. 451 (1999) 197-202
43. Villalaín J. Location of cholesterol in model membranes by magic-angle-sample-spinning NMR. Eur. J. Biochem. 241 (1996) 586-593
44. Kessel A., Ben-Tal N., and May S. Interactions of cholesterol with lipid bilayers: the preferred configuration and fluctuations. Biophys. J. 81 (2001) 643-658
45. Bach D., Sela B., and Miller I.R. Compositional aspects of lipid hydration. Chem. Phys. Lipids 31 (1982) 381-394
46. 2H-NMR dynamical parameters on water environment depending on their lipid composition. Mol. Membr. Biol. 20 (2003) 319-327
47. Mouritsen O.G., and Bloom M. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46 (1984) 141-153
48. McMullen T.P.W., Lewis R.N.A.H., and McElhaney R.N. Differential scanning calorimetric study of the effect of cholesterol on the thermotropic phase behavior of a homologous series of linear saturated phosphatidylcholines. Biochemistry 32 (1993) 516-522
49. Aittoniemi J., Róg T., Niemelä P., Pasenkiewicz-Gierula M., Karttunen M., and Vattulainen I. Tilt: major factor in sterols' ordering capability in membranes. J. Phys. Chem. Lett. B 110 (2006) 25562-25564
50. Muramatsu K., Masumizu T., Maitani Y., Hwang S.H., Kohno M., Takayama K., and Nagai T. Electron spin resonance studies of dipalmitoylphosphatidylcholine liposomes containing soybean-derived sterylglucoside. Chem. Pharmaceut. Bull. 48 (2000) 610-613
51. Schofield M., Jenski L.J., Dumaual A.C., and Stillwell W. Cholesterol versus cholesterol sulfate: effects on properties of phospholipid bilayers containing docosahexaenoic acid. Chem. Phys. Lipids 95 (1998) 23-36
52. Langlais J., Zollinger M., Plante L., Chapdelaine A., Bleau G., and Roberts K.D. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation. Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 7266-7270
53. Lampe M.A., Burlingame A.L., Whitney J., Williams M.L., Brown B.E., Roitman E., and Elias P.M. Human stratum corneum lipids: characterization and regional variations. J. Lipid Res. 24 (1983) 120-130
54. Higashi Y., Fuda H., Yanai H., Lee Y., Fukushige T., Kanzaki T., and Strott C.A. Expression of cholesterol sulfotransferase (SULT2B1b) in human skin and primary cultures of human epidermal keratinocytes. J. Invest. Dermatol. 122 (2004) 1207-1213
55. Faure C., Tranchant J.F., and Dufourc E.J. Comparative effects of cholesterol and cholesterol sulfate on hydration and ordering of dimyristoylphosphatidylcholine membranes. Biophys. J. 70 (1996) 1380-1390
56. Mudd J.B., and McManus T.T. Effect of steryl glycosides on the phase transition of dipalmitoyl lecithin. Plant Physiol. 65 (1980) 78-80
57. Vilchèze C., McMullen T.P.W., McElhaney R.N., and Bittman R. The effect of side-chain analogues of cholesterol on the thermotropic phase behavior of 1-stearoyl-2-oleoylphosphatidylcholine bilayers: a differential scanning calorimetric study. Biochim. Biophys. Acta 1279 (1996) 235-242
58. Zeyda M., and Stulnig T.M. Lipid Rafts & Co.: an integrated model of membrane organization in T cell activation. Prog. Lipid Res. 45 (2006) 187-202
59. Hanzal-Bayer M.F., and Hancock J.F. Lipid rafts and membrane traffic. FEBS Lett. 581 (2007) 2098-2104
60. Laloi M., Perret A.M., Chatre L., Melser S., Cantrel C., Vaultier M.N., Zachowski A., Bathany K., Schmitter J.M., Vallet M., Lessire R., Hartmann M.A., and Moreau P. Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol. 143 (2007) 461-472
61. Lefebvre B., Furt F., Hartmann M.A., Michaelson L.V., Carde J.P., Sargueil-Boiron F., Rossignol M., Napier J.A., Cullimore J., Bessoule J.J., and Mongrand S. Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol. 144 (2007) 402-418
62. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83 (2002) 2693-2701
63. Shogomori H., and Brown D.A. Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol. Chem. 384 (2003) 1259-1263
64. Lichtenberg D., Goni F.M., and Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. TRENDS Biochem. Sci. 30 (2005) 430-436
65. de Almeida R.F.M., Fedorov A., and Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85 (2003) 2406-2416
66. Demel R.A., Jansen J.W.C.M., van Dijck P.W.M., and van Deenen L.L.M. Preferential Interaction of cholesterol with different classes of phospholipids. Biochim. Biophys. Acta 465 (1977) 1-10
67. van Duyl B.Y., Ganchev D., Chupin V., de Kruijff B., and Killian J.A. Sphingomyelin is much more effective than saturated phosphatidylcholine in excluding unsaturated phosphatidylcholine from domains formed with cholesterol. FEBS Lett. 547 (2003) 101-106
68. Xu X., and London E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39 (2000) 843-849
69. Wang J.W., Megha, and London E. Relationship between sterol/steroid structure and participation in ordered lipid domains (lipid rafts): implications for lipid raft structure and function. Biochemistry 43 (2004) 1010-1018
70. Bacia K., Schwille P., and Kurzchalia T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3272-3277
71. Maggio B., Fanani M.L., Rosetti C.M., and Wilke N. Biophysics of sphingolipids II. Glycosphingolipids: an assortment of multiple structural information transducers at the membrane surface. Biochim. Biophys. Acta 1758 (2006) 1922-1944
72. Ali S., Smaby J.M., and Brown R.E. Acyl structure regulates galactosylceramide's interfacial interactions. Biochemistry 32 (1993) 11696-11703
73. Maggio B. The surface behavior of glycosphingolipids in biomembranes: a new frontier of molecular ecology. Prog. Biophys. Mol. Biol. 62 (1994) 55-117
74. Li X.M., Momsen M.M., Brockman H.L., and Brown R.E. Lactosylceramide: effect of acyl chain structure on phase behavior and molecular packing. Biophys. J. 83 (2002) 1535-1546