The Affinity of Cholesterol for Different Phospholipids Affects Lateral Segregation in Bilayers

Biophysical Journal

Volumn 111, Issue 3, 2016, Pages 546-556

  Engberg, Oskar ^a   Hautala, Victor ^a   Yasuda, Tomokazu ^b,c   Dehio, Henrike ^a   Murata, Michio ^b,c   Slotte, J Peter ^a   Nyholm, Thomas K M ^a  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b OSAKA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; LIPID BILAYER; PHOSPHOLIPID;

CHEMISTRY; DOSE RESPONSE; ENZYME SPECIFICITY; LIPID BILAYER; METABOLISM; TEMPERATURE;

CHOLESTEROL; DOSE-RESPONSE RELATIONSHIP, DRUG; LIPID BILAYERS; PHOSPHOLIPIDS; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84981288236     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2016.06.036     Document Type: Article

References (60)

1. 1 Lingwood, D., Kaiser, H.J., et al., Simons, K., Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37 (2009), 955–960.
2. 2 Veatch, S.L., Keller, S.L., Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta 1746 (2005), 172–185.
3. 3 Nyholm, T.K., Lindroos, D., et al., Slotte, J.P., Construction of a DOPC/PSM/cholesterol phase diagram based on the fluorescence properties of trans-parinaric acid. Langmuir 27 (2011), 8339–8350.
4. 4 Konyakhina, T.M., Wu, J., et al., Feigenson, G.W., Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/Chol. Biochim. Biophys. Acta 1828 (2013), 2204–2214.
5. 5 Marsh, D., Cholesterol-induced fluid membrane domains: a compendium of lipid-raft ternary phase diagrams. Biochim. Biophys. Acta 1788 (2009), 2114–2123.
6. 6 Ipsen, J.H., Karlström, G., et al., Zuckermann, M.J., Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta 905 (1987), 162–172.
7. 7 Quinn, P.J., Wolf, C., The liquid-ordered phase in membranes. Biochim. Biophys. Acta 1788 (2009), 33–46.
8. 8 van Dijck, P.W.M., Negatively charged phospholipids and their position in the cholesterol affinity sequence. Biochim. Biophys. Acta 555 (1979), 89–101.
9. 9 Gawrisch, K., Soubias, O., Structure and dynamics of polyunsaturated hydrocarbon chains in lipid bilayers-significance for GPCR function. Chem. Phys. Lipids 153 (2008), 64–75.
10. 10 Stillwell, W., Wassall, S.R., Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids 126 (2003), 1–27.
11. 11 Heberle, F.A., Doktorova, M., et al., Feigenson, G.W., Hybrid and nonhybrid lipids exert common effects on membrane raft size and morphology. J. Am. Chem. Soc. 135 (2013), 14932–14935.
12. 12 van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 (2008), 112–124.
13. 13 Feller, S.E., Acyl chain conformations in phospholipid bilayers: a comparative study of docosahexaenoic acid and saturated fatty acids. Chem. Phys. Lipids 153 (2008), 76–80.
14. 14 Shaikh, S.R., Cherezov, V., et al., Wassall, S.R., Molecular organization of cholesterol in unsaturated phosphatidylethanolamines: x-ray diffraction and solid state 2H NMR reveal differences with phosphatidylcholines. J. Am. Chem. Soc. 128 (2006), 5375–5383.
15. 15 Wassall, S.R., Stillwell, W., Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. Biochim. Biophys. Acta 1788 (2009), 24–32.
16. 16 Kullberg, A., Ekholm, O.O., Slotte, J.P., Miscibility of sphingomyelins and phosphatidylcholines in unsaturated phosphatidylcholine bilayers. Biophys. J. 109 (2015), 1907–1916.
17. 17 Sklar, L.A., Hudson, B.S., Simoni, R.D., Conjugated polyene fatty acids as fluorescent probes: synthetic phospholipid membrane studies. Biochemistry 16 (1977), 819–828.
18. 18 Williams, J.A., Wassall, C.D., et al., Wassall, S.R., An electron paramagnetic resonance method for measuring the affinity of a spin-labeled analog of cholesterol for phospholipids. J. Membr. Biol. 246 (2013), 689–696.
19. 19 Halling, K.K., Ramstedt, B., et al., Nyholm, T.K., Cholesterol interactions with fluid-phase phospholipids: effect on the lateral organization of the bilayer. Biophys. J. 95 (2008), 3861–3871.
20. 20 Mason, J.T., Broccoli, A.V., Huang, C., A method for the synthesis of isomerically pure saturated mixed-chain phosphatidylcholines. Anal. Biochem. 113 (1981), 96–101.
21. 21 Rouser, G., Fleischer, S., 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.
22. 22 Jungner, M., Ohvo, H., Slotte, J.P., Interfacial regulation of bacterial sphingomyelinase activity. Biochim. Biophys. Acta 1344 (1997), 230–240.
23. 23 Fischer, R.T., Stephenson, F.A., et al., Schroeder, F., δ5,7,9(11)-Cholestatrien-3 β-ol: a fluorescent cholesterol analogue. Chem. Phys. Lipids 36 (1984), 1–14.
24. 24 Kuklev, D.V., Smith, W.L., Synthesis of four isomers of parinaric acid. Chem. Phys. Lipids 131 (2004), 215–222.
25. 25 Lakowicz, J.R., Principles of Fluorescence Spectroscopy. 1999, Kluwer Academic/Plenum Publishers, New York.
26. 26 Nyström, J.H., Lönnfors, M., Nyholm, T.K., Transmembrane peptides influence the affinity of sterols for phospholipid bilayers. Biophys. J. 99 (2010), 526–533.
27. 27 Björkqvist, Y.J., Nybond, S., et al., Ramstedt, B., N-palmitoyl-sulfatide participates in lateral domain formation in complex lipid bilayers. Biochim. Biophys. Acta 1778 (2008), 954–962.
28. 28 Petruzielo, R.S., Heberle, F.A., et al., Feigenson, G.W., Phase behavior and domain size in sphingomyelin-containing lipid bilayers. Biochim. Biophys. Acta 1828 (2013), 1302–1313.
29. 29 Ramstedt, B., Slotte, J.P., Membrane properties of sphingomyelins. FEBS Lett. 531 (2002), 33–37.
30. 30 Lönnfors, M., Doux, J.P., et al., Slotte, J.P., Sterols have higher affinity for sphingomyelin than for phosphatidylcholine bilayers even at equal acyl-chain order. Biophys. J. 100 (2011), 2633–2641.
31. 31 Scheidt, H.A., Muller, P., et al., Huster, D., The potential of fluorescent and spin-labeled steroid analogs to mimic natural cholesterol. J. Biol. Chem. 278 (2003), 45563–45569.
32. 32 Milles, S., Meyer, T., et al., Müller, P., Organization of fluorescent cholesterol analogs in lipid bilayers—lessons from cyclodextrin extraction. Biochim. Biophys. Acta 1828 (2013), 1822–1828.
33. 33 Niu, S.L., Litman, B.J., Determination of membrane cholesterol partition coefficient using a lipid vesicle-cyclodextrin binary system: effect of phospholipid acyl chain unsaturation and headgroup composition. Biophys. J. 83 (2002), 3408–3415.
34. 34 Tsamaloukas, A., Szadkowska, H., Heerklotz, H., Thermodynamic comparison of the interactions of cholesterol with unsaturated phospholipid and sphingomyelins. Biophys. J. 90 (2006), 4479–4487.
35. 35 Tsamaloukas, A., Szadkowska, H., et al., Heerklotz, H., Interactions of cholesterol with lipid membranes and cyclodextrin characterized by calorimetry. Biophys. J. 89 (2005), 1109–1119.
36. 36 Estep, T.N., Mountcastle, D.B., et al., Thompson, T.E., Thermal behavior of synthetic sphingomyelin-cholesterol dispersions. Biochemistry 18 (1979), 2112–2117.
37. 37 Yasuda, T., Tsuchikawa, H., et al., Matsumori, N., Deuterium NMR of raft model membranes reveals domain-specific order profiles and compositional distribution. Biophys. J. 108 (2015), 2502–2506.
38. 2H NMR spectroscopy. J. Am. Chem. Soc. 130 (2008), 14521–14532.
39. 39 Davis, J.H., Clair, J.J., Juhasz, J., Phase equilibria in DOPC/DPPC-d62/cholesterol mixtures. Biophys. J. 96 (2009), 521–539.
40. 40 Yasuda, T., Kinoshita, M., et al., Matsumori, N., Detailed comparison of deuterium quadrupole profiles between sphingomyelin and phosphatidylcholine bilayers. Biophys. J. 106 (2014), 631–638.
41. 41 Darke, A., Finer, E.G., et al., Phillips, M.C., Nuclear magnetic resonance study of lecithin-cholesterol interactions. J. Mol. Biol. 63 (1972), 265–279.
42. 42 Engberg, O., Nurmi, H., et al., Slotte, J.P., Effects of cholesterol and saturated sphingolipids on acyl chain order in 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine bilayers—a comparative study with phase-selective fluorophores. Langmuir 31 (2015), 4255–4263.
43. 43 Bezlyepkina, N., Gracià, R.S., et al., Dimova, R., Phase diagram and tie-line determination for the ternary mixture DOPC/eSM/cholesterol. Biophys. J. 104 (2013), 1456–1464.
44. 44 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 36 (1997), 10944–10953.
45. 45 Filippov, A., Orädd, G., Lindblom, G., Domain formation in model membranes studied by pulsed-field gradient-NMR: the role of lipid polyunsaturation. Biophys. J. 93 (2007), 3182–3190.
46. 46 Konyakhina, T.M., Feigenson, G.W., Phase diagram of a polyunsaturated lipid mixture: brain sphingomyelin/1-stearoyl-2-docosahexaenoyl-sn-glycero-3-phosphocholine/cholesterol. Biochim. Biophys. Acta 1858 (2016), 153–161.
47. 47 Lindblom, G., Orädd, G., Filippov, A., Lipid lateral diffusion in bilayers with phosphatidylcholine, sphingomyelin and cholesterol. An NMR study of dynamics and lateral phase separation. Chem. Phys. Lipids 141 (2006), 179–184.
48. 48 Brzustowicz, M.R., Cherezov, V., et al., Wassall, S.R., Molecular organization of cholesterol in polyunsaturated membranes: microdomain formation. Biophys. J. 82 (2002), 285–298.
49. 49 Nyholm, T.K.M., Nylund, M., Slotte, J.P., A calorimetric study of binary mixtures of dihydrosphingomyelin and sterols, sphingomyelin, or phosphatidylcholine. Biophys. J. 84 (2003), 3138–3146.
50. 50 McMullen, T.P., Lewis, R.N., 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.
51. 51 Staneva, G., Seigneuret, M., et al., Angelova, M.I., Detergents induce raft-like domains budding and fission from giant unilamellar heterogeneous vesicles: a direct microscopy observation. Chem. Phys. Lipids 136 (2005), 55–66.
52. 2H NMR spectra. Langmuir 31 (2015), 13783–13792.
53. 53 Sodt, A.J., Pastor, R.W., Lyman, E., Hexagonal substructure and hydrogen bonding in liquid-ordered phases containing palmitoyl sphingomyelin. Biophys. J. 109 (2015), 948–955.
54. 54 Engberg, O., Yasuda, T., et al., Slotte, J.P., Lipid interactions and organization in complex bilayer membranes. Biophys. J. 110 (2016), 1563–1573.
55. 55 Heberle, F.A., Petruzielo, R.S., et al., Katsaras, J., Bilayer thickness mismatch controls domain size in model membranes. J. Am. Chem. Soc. 135 (2013), 6853–6859.
56. 56 Georgieva, R., Chachaty, C., et al., Staneva, G., Docosahexaenoic acid promotes micron scale liquid-ordered domains. A comparison study of docosahexaenoic versus oleic acid containing phosphatidylcholine in raft-like mixtures. Biochim. Biophys. Acta 1848 (2015), 1424–1435.
57. 57 van Duyl, B.Y., Ganchev, D., et al., 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.
58. 58 Slotte, J.P., The importance of hydrogen bonding in sphingomyelin's membrane interactions with co-lipids. Biochim. Biophys. Acta 1858 (2016), 304–310.
59. 14N-NMR study. Biochim. Biophys. Acta 645 (1981), 270–278.
60. 60 Ackerman, D.G., Feigenson, G.W., Lipid bilayers: clusters, domains and phases. Essays Biochem. 57 (2015), 33–42.