The liquid-ordered phase in sphingomyelin-cholesterol membranes as detected by the discrimination by oxygen transport (DOT) method

Cellular and Molecular Biology Letters

Volumn 13, Issue 3, 2008, Pages 430-451

  Wisniewska, Anna ^a,b   Subczynski, Witold K ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Cholesterol; EPR; Lipid bilayer; Liquid ordered phase; Raft domain; Sphingomyelin; Spin labeling

Indexed keywords

CHOLESTEROL; NITROXIDE; OXYGEN; SPHINGOMYELIN;

ARTICLE; IMMOBILIZATION; LIPID BILAYER; OXYGEN TRANSPORT; SPIN LABELING;

EID: 56349152783     PISSN: 14258153     EISSN: 16891392     Source Type: Journal    
DOI: 10.2478/s11658-008-0012-y     Document Type: Article

References (59)

1. Simons, K. and Ikonen, E. Functional rafts in cell membranes. Nature 387 (1997) 569-572.
2. Shaikh, S.R. and Edidin, M.A. Membranes are not just rafts. Chem. Phys. Lipids 144 (2006) 1-3.
3. Kusumi, A., Koyama-Honda, I. and Suzuki, K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5 (2004) 213-230.
4. Mayor, S. and Rao, M. Rafts, scale dependent, active lipid organization at the cell surface. Traffic 5 (2004) 231-240.
5. Edidin, M. The state of lipid rafts from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 257-283.
6. Munro, S. Lipid rafts: delusive or illusive. Cell 115 (2003) 377-388.
7. Brown, D.A. and London, E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275 (2000) 17221-17224.
8. Brown, D.A. and Rose, J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68 (1992) 533-544.
9. Ridgway, N.D. Interaction between metabolism and intracellular distribution of cholesterol and sphingomyelin. Biochim. Biophys. Acta 1484 (2000) 129-141.
10. Pralle, A., Keller, P., Florin, E.L., Simons, K. and Horber, J.K.H. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148 (2000) 997-1008.
11. Friedrichson, T. and Kurzchalia, T.V. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394 (1998) 802-805.
12. Heerklotz, H. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83 (2002) 2693-2701.
13. Pike, L.J. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 47 (2006) 1597-1598.
14. Kawasaki, K., Yin, J.-J., Subczynski, W.K., Hyde, J.S. and Kusumi. A. Pulse EPR detection of lipid exchange between protein-rich raft and bulk domains in the membrane: Methodology development and its application to studies of influenza viral membrane. Biophys. J. 80 (2001) 738-748.
15. Suzuki, K.G.N., Fujiwara, T.K., Sanematsu, F., Iino, R., Edidin, M. and Kusumi, A. GPI-anchored receptor clusters transiently recruit Lyn and Gα for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol. 177 (2007) 717-730.
16. +2 signaling: single-molecule tracking study 2. J. Cell Biol. 177 (2007) 731-742.
17. Kusumi, A., Subczynski, W.K., Pasenkiewicz-Gierula, M., Hyde, J.S. and Merkle H. Spin-label studies on phosphatidylcholine-cholesterol membranes: effects of alkyl chain length and unsaturation in the fluid phase. Biochim. Biophys. Acta 854 (1986) 307-317.
18. Recktenwald, D.J. and McConnell, H.M. Phase equilibria in binary mixture of phosphatidylcholine and cholesterol. Biochemistry 20 (1981) 4505-4510.
19. Shimshick, E.J. and McConnell, H.M. Lateral phase separation in phospholipid membranes. Biochemistry 12 (1973) 2351-2360.
20. Subczynski, W.K., Widomska, J., Wisniewska, A. and Kusumi, A. Saturation recovery EPR discrimination by oxygen transport (DOT) method for characterizing membrane domains. in: Methods in Molecular Biology. Vol. 398. Lipid Rafts. (McIntosh, T.J., Ed.), Humana Press Inc., Totowa, New York, 2007, 145-160.
21. Ashikawa, I., Yin, J.-J., Subczynski, W.K., Kouyama, T., Hyde, J.S. and Kusumi. A. Molecular organization and dynamics in bacteriorhodopsin-rich reconstituted membranes: Discrimination of lipid environments by the oxygen transport parameter using a pulse ESR spin-labeling technique. Biochemistry 33 (1994) 4947-4952.
22. Subczynski, W.K., Wisniewska, A., Hyde, J.S. and Kusumi, A. Three-dimensional dynamic structure of the liquid-ordered domain as examined by a pulse-EPR oxygen probing. Biophys. J. 92 (2007) 1573-1584.
23. Subczynski, W.K., Pasenkiewicz-Gierula, M., McElhaney, R.N., Hyde, J.S. and Kusumi, A. Molecular dynamics of 1-palmitoyl-2-oleoylphosphatidylcholine membranes containing transmembrane α-helical peptides with alternating leucine and alanine residues. Biochemistry 42 (2003) 3939-3948.
24. Subczynski, W.K., Lewis, R.N.A.H., McElhaney, R.N., Hodges, R.S., Hyde, J.S. and Kusumi, A. Molecular organization and dynamics of 1-palmitoyl-2- oleoylphosphatidylcholine bilayers containing a transmembrane α-helical peptide. Biochemistry 37 (1998) 3156-3164.
25. Subczynski, W.K., Hopwood, L.E. and Hyde, J.S. Is the mammalian cell plasma membrane a barrier to oxygen transport? J. Gen. Physiol. 100 (1992) 69-87.
26. Subczynski, W.K., Hyde, J.S. and Kusumi, A. Effect of alkyl chain unsaturation and cholesterol intercalation on oxygen transport in membranes: a pulse ESR spin labeling study. Biochemistry 30 (1991) 8578-8590.
27. Subczynski, W.K., Hyde, J.S. and Kusumi, A. Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proc. Natl. Acad. Sci. USA 86 (1989) 4474-4478.
28. Kusumi, A., Subczynski, W.K. and Hyde, J.S. Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels. Proc. Natl. Acad. Sci. USA 79 (1982) 1854-1858.
29. Ge, M., Field, K.A., Aneja, R., Holovka, D., Baird, B. and Freed J.H. Electron spin resonance characterization of liquid ordered phase of detergent-resistant membranes from RBL-2H3 cells. Biophys. J. 77 (1999) 925-933.
30. London, E. Insights into lipid raft structure and formation from experiments in model systems. Curr. Opin. Struct. Biol. 12 (2002) 480-486.
31. Almeida, P.F.F., Vaz, W.L.C. and Thompson, T.E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol bilayers: a free volume analysis. Biochemistry 31 (1992) 6739-6747.
32. Costa-Filho, A.J., Shimoyama, Y. and Freed, J.H. A2D-ELDOR study of the liquid ordered phase in multilamellar vesicle membranes. Biophys. J. 84 (2003) 2619-2633.
33. Ge, M., Gidvani, A., Brown, H.A., Holovka, D., Baird, B. and Freed, J.H. Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells. Biophys. J. 85 (2003) 1278-1288.
34. Veiga, M.P., Arrondo, J.L.R., Goni, F.M., Alonso, A. and Marsh, D. Interaction of cholesterol with sphingomyelin in mixed membranes containing phosphatidylcholine, studied by spin-label ESR and IR spectroscopies. A possible stabilization of gel-phase sphingolipid domains by cholesterol. Biochemistry 40 (2001) 2614-1622.
35. Wolf, C. and Chachaty, C. Compared effects of cholesterol and 7-dehydrocholesterol on sphingomyelin-glycerophospholipid bilayers studied by ESR. Biophys. Chem. 84 (2000) 269-279.
36. Gaffney, B.J. and Marsh, D. High-frequency, spin-label EPR of nonaxial lipid ordering and motion in cholesterol-containing membranes. Proc. Natl. Acad. Sci. USA 95 (1998) 12490-12493.
37. Almeida, P.F.F., Pokorny, A. and Hinderliter, A. Thermodynamics of membrane domains. Biochim. Biophys. Acta 1720 (2005) 1-13.
38. Sankaram, M.B. and Thompson, T.E. Interaction of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry 29 (1990) 10670-10675.
39. 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.
40. Kusumi, A., Subczynski, W.K. and Hyde, J.S. Effects of pH on ESR spectra of stearic acid spin labels in membranes: probing the membrane surface. Fed. Proc. 41 (1982) 1394.
41. Papahadjopoulos, D. Surface properties of acidic phospholipids: Interaction of monolayers and hydrated liquid crystals with uni- and bi-valent metal ions. Biochim. Biophys. Acta 163 (1968) 240-254.
42. Hyde, J.S. and Subczynski, W.K. Spin-label oximetry. in: Biological Magnetic Resonance. Vol. 8. Spin labeling: theory and applications. (Berliner, L.J. and Reuben, J. Eds.), Plenum, New York, 1989, 399-425.
43. Subczynski, W.K., Felix, C.C., Klug, C.S. and Hyde, J.S. Concentration by centrifugation for gas exchange EPR oximetry measurements with loop-gap resonators. J. Magn. Reson. 176 (2005) 244-248.
44. Yin, J.J. and Subczynski, W.K. Effect of lutein and cholesterol on alkyl chain bending in lipid bilayers: a pulse electron paramagnetic resonance spin labeling study. Biophys. J. 71 (1996) 832-839.
45. Yin, J.J., Pasenkiewicz-Gierula, M. and Hyde, J.S. Lateral diffusion of lipids in membranes by pulse saturation recovery electron spin resonance. Proc. Natl. Acad. Sci. USA 84 (1987) 964-968.
46. Windrem, D.A. and Plachy, W.Z. The diffusion-solubility of oxygen in lipid bilayers. Biochim. Biophys. Acta 600 (1980) 655-665.
47. Robinson, B.H., Hass, D.A. and Mailer, C. Molecular dynamics in liquid: spin lattice relaxation of nitroxide spin labels. Science 263 (1994) 490-493.
48. Loura, L.M.S., Fedorov, A. and Prieto, M. Fluid-fluid membrane microheterogenity: a fluorescence resonance energy transfer study. Biophys. J. 80 (2001) 778-788.
49. Subczynski, W.K. and Kusumi, A. Effects of very small amounts of cholesterol on gel-phase phosphatidylcholine membranes. Biochim. Biophys. Acta 854 (1986) 318-320.
50. Widomska, J., Raguz, M., Dillon, J., Gaillard, E.R. and Subczynski, W.K. Physical properties of the lipid bilayer membrane made of calf lens lipids: EPR spin labeling studies. Biochim. Biophys. Acta 1768 (2007) 1454-1465.
51. Widomska, J., Raguz, M. and Subczynski, W.K. Oxygen permeability of the lipid bilayer membrane made of calf lens lipids. Biochim. Biophys. Acta 1768 (2007) 2635-2645.
52. Collado, M.I., Goni, F.M., Alonso, A. and Marsh, D. Domain formation in sphingomyelin/cholesterol mixed membranes studied by spin-label electron spin resonance spectroscopy. Biochemistry 44 (2005) 4911-4918.
53. Hubbell, W.L. and McConnell, H.M. Molecular motion in spin-labeled phospholipids and membranes. J. Am. Chem. Soc. 93 (1971) 314-326.
54. Gaffney, B.J. Principal considerations for the calculation of order parameters for fatty acid or phospholipid spin labels in membranes. in: Spin labeling: theory and applications. (Berliner, L.J. Ed.), Academic Press, New York, 1976, 567-571.
55. Koynova, R. and Caffrey, M. Phases and phase transitions of the sphingolipids. Biochim. Biophys. Acta 1255 (1995) 213-236.
56. Ramstedt, B. and Slotte, J.P. Sphingolipids and the formation of sterol-enriched ordered membrane domains. Biochim. Biophys. Acta 1758 (2006) 1945-1956.
57. Guo, W., Kurze, V., Huber, T., Afdhal, N.H., Beyer, K. and Hamilton, J.A. A solid-state NMR study of phospholipid-cholesterol interactions: sphingomyelin-cholesterol binary systems. Biophys. J. 83 (2002) 1465-1478.
58. Ohvo, H. and Slotte, J.P. Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate. Biochemistry 35 (1996) 8018-8024.
59. Slotte, J.P. Enzyme-catalyzed oxidation of cholesterol in mixed phospholipid monolayers reveals stoichiometry at which free cholesterol clusters disappear. Biochemistry 31 (1992) 5472-5477.