Sterol Structure and Sphingomyelin Acyl Chain Length Modulate Lateral Packing Elasticity and Detergent Solubility in Model Membranes

Biophysical Journal

Volumn 85, Issue 6, 2003, Pages 3788-3801

  Li, Xin Min ^a,b   Momsen, Maureen M ^a   Brockman, Howard L ^a   Brown, Rhoderick E ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 OXOCHOLESTANOL; ANDROST 5 EN 3BETA OL; CHOLESTANOL; CHOLESTEROL; DETERGENT; HYDROCARBON; SPHINGOMYELIN; STEROL; TRITON X 100; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL MEMBRANE; CAVEOLA; CELL MEMBRANE; ELASTICITY; LIPID MEMBRANE; MITOCHONDRIAL MEMBRANE; SOLUBILITY;

SPHINGIODEA;

EID: 0345413250     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74794-8     Document Type: Article

References (72)

1. Ahmed, S. N., D. A. Brown, and E. London. 1997. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiologic concentrations of cholesterol and sphingolipids induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry. 36:10944-10953.
2. Ali, S., J. M. Smaby, H. L. Brockman, and R. E. Brown. 1994. Cholesterol's interfacial interactions with galactosylceramides. Biochemistry. 33:2900-2906.
3. Ali, S., J. M. Smaby, M. M. Momsen, H. L. Brockman, and R. E. Brown. 1998. Acyl chain-length asymmetry alters the interfacial elastic interactions of phosphatidylcholine. Biophys. J. 74:338-348.
4. Bartlett, G. R. 1959. Phosphorus assay in column chromatography. J. Biol. Chem. 234:466-468.
5. Behroozi, F. 1996. Theory of elasticity in two dimensions and its application to Langmuir-Blodgett films. Langmuir. 12:2289-2291.
6. Bitman, J., L. Wood, N. R. Mehta, P. Hamosh, and M. Hamosh. 1984. Comparison of the phospholipid composition of breast milk from mothers of term and preterm infants during lactation. Am. J. Clin. Nutr. 40:1103-1119.
7. Bretscher, M. S., and S. Munro. 1993. Cholesterol and the Golgi apparatus. Science. 261:1280-1281.
8. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
9. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
10. Brown, R. E. 1998. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 111:1-9.
11. 2+ efflux. FEBS Lett. 379:305-308.
12. Chong, P. L.-G., and I. P. Sugár. 2002. Fluorescence studies of lipid regular distribution in membranes. Chem. Phys. Lipids. 116:153-175.
13. Cladera, J., and P. Oshea. 1998. Intramembrane molecular dipoles affect the membrane insertion and folding of a model amphiphilic peptide. Biophys. J. 74:2434-2442.
14. nd. Ed. Academic Press, New York. 265.
15. Davies, M. A., H. F. Schuster, J. W. Brauner, and R. Mendelsohn. 1990. Effects of cholesterol on conformational disorder in dipalmitoylphos-phatidylcholine bilayers. A quantitative IR study of the depth dependence. Biochemistry. 29:4368-4373.
16. Edidin, M. 2003. The state of lipid rafts: From model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
17. Estep, T. N., D. B. Mountcastle, Y. Barenholz, R. L. Biltonen, and T. E. Thompson. 1979. Thermal behavior of synthetic sphingomyelin-cholesterol dispersions. Biochemistry. 10:2112-2117.
18. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J. Phys. Chem. 91:4219-4228.
19. Franklin, J. C., and D. S. Cafiso. 1993. Internal electrostatic potentials in bilayers-measuring and controlling dipole potentials in lipid vesicles. Biophys. J. 65:289-299.
20. Guo, Z., D. H. Beach, and E. S. Kaneshiro. 1996. Fatty acid composition of the major phospholipids of Pneumocystis carinii: comparison with those in the lungs of normal and methylprednisolone-immunosuppressed rats. Infect. Immun. 64:1407-1412.
21. Huang, C. 1977. A structural model for the cholesterol-phosphatidylcholine complexes in bilayer membranes. Lipids. 12:348-356.
22. Hubbell, W. L., and H. M. McConnell. 1971. Molecular motion in spin-labeled phospholipids and membranes. J. Am. Chem. Soc. 93:314-326.
23. Ipsen, J. H., G. Karlstrom, O. G. Mouritsen, H. Wennerstrom, and M. H. Zuckermann. 1987. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta. 905:162-172.
24. Kaganer, V. M., H. Möhwald, and P. Dutta. 1999. Structure and phase transitions in Langmuir monolayers. Rev. Mod. Phys. 71:779-819.
25. Karlsson, A. Å., P. Michélsen, and G. Odham. 1998. Molecular species of sphingomyelin: determination by high-performance liquid chromatography/mass spectrometry with electrospray and high-performance liquid chromatography/tandem mass spectrometry with atmospheric pressure chemical ionization. J. Mass Spectrom. 33:1192-1198.
26. Li, X. M., J. M. Smaby, M. M. Momsen, H. L. Brockman, and R. E. Brown. 2000. Sphingomyelin interfacial behavior: The impact of changing acyl chain composition. Biophys. J. 78:1921-1931.
27. Li, X. M., M. M. Momsen, J. M. Smaby, H. L. Brockman, and R. E. Brown. 2001. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins. Biochemistry. 40:5954-5963.
28. Li, X. M., M. Ramakrishnan, H. L. Brockman, R. E. Brown, and M. J. Swamy. 2002. N-myristoylated phosphatidylethanolamine: Interfacial behavior and interaction with cholesterol. Langmuir. 18:231-238.
29. London, E., and D. A. Brown. 2000. Insolubility of lipids in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta. 1508:182-195.
30. Lundbæk, J. A., O. S. Andersen, T. Werge, and C. Nielsen. 2003. Cholesterol-induced protein sorting: An analysis of energetic feasibility. Biophys. J. 84:2080-2089.
31. Luria, A., V. Vegelyte-Avery, B. Stith, N. M. Tsvetkova, W. F. Wolkers, J. H. Crowe, F. Tablin, and R. Nuccitelli. 2002. Detergent-free domain isolated from Xenopus egg plasma membrane with properties similar to those of detergent-resistant membranes. Biochemistry. 41:13189-13197.
32. MacDonald, R. C. 1996. The relationship and interactions between lipid bilayer vesicles and lipid monolayers at the air/water interface. In Vesicles. M. Rosoff, editor. Marcel Dekker, New York, NY. 3-48.
33. Marsh, D. 1996. Lateral pressure in membranes. Biochim. Biophys. Acta. 1286:183-223.
34. Mattjus, P., J. G. Molotkovsky, J. M. Smaby, and R. E. Brown. 1999. A fluorescence resonance energy transfer approach for monitoring protein-mediated glycolipid transfer between vesicle membranes. Anal. Biochem. 268:297-304.
35. Maulik, P. R., and G. G. Shipley. 1996. Interactions of N-stearoyl-sphingomyelin with cholesterol and dipalmitoylphosphatidylcholine in bilayer membranes. Biophys. J. 70:2256-2265.
36. McConnell, H. M., and A. Radhakrishnan. 2003. Condensed complexes of cholesterol and phospholipid. Biochim. Biophys. Acta. 1610:159-173.
37. McIntosh, T. J., S. A. Simon, D. Needham, and C. Huang. 1992. Structure and cohesive properties of sphingomyelin/cholesterol bilayers. Biochemistry. 31:2012-2020.
38. McMullen, T. P. W., R. N. A. H. Lewis, and R. N. McElhaney. 1993. Differential scanning calorimetric study of the effect of cholesterol on the thermotropic phase behavior of a homologous series of linear saturated phosphatidylcholines. Biochemistry. 32:516-522.
39. Merkel, R., and E. Sackmann. 1994. Nonstationary dynamics of excimer formation in two-dimensional fluids. J. Phys. Chem. 98:4428-4442.
40. Möhwald, H. 1995. Phospholipid monolayers. In Handbook of Biological Physics. R. Lipowsky and E. Sackmann, Eds. vol. 1, Elsevier Science, Amsterdam. 161-211.
41. Momsen, W. E., J. M. Smaby, and H. L. Brockman. 1990. The suitability of nichrome for measurement of gas-liquid interfacial tension by the Wilhelmy method. J. Colloid Interface Sci. 135:547-552.
42. Needham, D. 1995. Cohesion and permeability of lipid bilayer vesicles. In Permeability and Stability of Lipid Bilayers. E. A. Disalvo and S. Simon, Eds. CRC Press, Boca Raton, FL. 49-76.
43. Needham, D., and R. S. Nunn. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997-1009.
44. Ohvo-Rekilä, H., P. Mattjus, and J. P. Slotte. 1998. The influence of] hydrophobic mismatch on androsterol/phosphatidylcholine interactions in model membranes. Biochim. Biophys. Acta. 1372:331-338.
45. Ohvo-Rekilä, H., B. Ramstedt, P. Leppimaki, and J. P. Slotte. 2002. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41:66-97.
46. Rokitskaya, T. I., Y. N. Antonenko, and E. A. Kotova. 1997. Effect of dipole potential of a bilayer lipid membrane on gramicidin channel dissociation kinetics. Biophys. J. 73:850-854.
47. Rokitskaya, T. I., E. A. Kotova, and Y. N. Antonenko. 2002. Membrane dipole potential modulates proton conductance through gramicidin channel: Movement of negative ionic defects inside the channel. Biophys. J. 82:865-873.
48. Rothman, J. E., and D. M. Engelman. 1972. Molecular mechanism for the interaction of phospholipid with cholesterol. Nature (London). New Biol. 237:42-44.
49. Sankaram, M. B., and T. E. Thompson. 1990. Interactions of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry. 29:10670-10675.
50. Schroeder, R., E. London, and D. A. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GP1)-anchored proteins. Proc. Natl. Acad. Sci. USA. 91:12130-12134.
51. Schroeder, R. J., S. N. Ahmed, Y. Z. Zhu, E. London, and D. A. Brown. 1998. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273:1150-1157.
52. Seddon, J. M., G. Cevc, R. D. Kaye, and D. Marsh. 1984. X-ray diffraction study of the polymorphism of hydrated diacyl- and dialkylphosphatidyl-ethanolamines. Biochemistry. 23:2634-2644.
53. Silvius, J. R. 2003. Roles of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta. 1610:174-183.
54. Simon, S. A., T. J. McIntosh, A. D. Magid, and D. A. Needham. 1992. Modulation of the interbilayer hydration pressure by the addition of dipoles at the hydrocarbon/water interface. Biophys. J. 61:786-799.
55. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
56. Simons, K., and E. Ikonen. 2000. How cells handle cholesterol. Science. 290:1721-1726.
57. Smaby, J. M., and H. L. Brockman. 1991. A simple method for estimating surfactant impurities in solvents and subphases used for monolayer studies. Chem. Phys. Lipids. 58:249-252.
58. Smaby, J. M., H. L. Brockman, and R. E. Brown. 1994. Cholesterol's interfacial interactions with sphingomyelins and phosphatidylcholines: hydrocarbon chain structure determines the magnitude of condensation. Biochemistry., 33:9135-9142.
59. Smaby, J. M., M. Momsen, V. S. Kulkarni, and R. E. Brown. 1996a. Cholesterol-induced interfacial area condensations of galactosylceramides and sphingomyelins with identical acyl chains. Biochemistry. 35:5696-5704.
60. Smaby, J. M., V. S. Kulkarni, M. Momsen, and R. E. Brown. 1996b. The interfacial elastic packing interactions of galactosylceramides, sphingomyelins and phosphatidylcholines. Biophys. J. 70:868-877.
61. Smaby, J. M., M. Momsen, H. L. Brockman, and R. E. Brown. 1997. Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol. Biophys. J. 73:1492-1505.
62. Smondyrev, A. M., and M. L. Berkowitz. 2001. Effects of oxygenated sterols on phospholipid bilayer properties: a molecular dynamics simulation. Chem. Phys. Lipids. 112:31-39.
63. Sot, J., M. I. Collado, J. L. R. Arrondo, A. Alonso, and F. M. Goni. 2002. Triton X-100-resistant bilayers: effect of lipid composition and relevance to the raft phenomenon. Langmuir. 18:2828-2835.
64. Snyder, B., and E. Freire. 1980. Compositional domain structure in phosphatidylcholine-cholesterol and sphingomyelin-cholesterol bilayers. Proc. Natl. Acad. Sci. USA. 77:4055-4059.
65. Starkov, A. A., V. I. Dedukhova, and V. P. Skulachev. 1994. 6-ketocholestanol abolishes the effect of the most potent uncouplers of oxidative phosphorylation in mitochondria. FEBS Lett. 355:305-308.
66. Starkov, A. A., D. A. Bloch, B. V. Chemyak, V. I. Dedukhova, S. E. Mansurova, I. I. Serverina, R. A. Simonyan, T. V. Vygodina, and V. P. Skulachev. 1997. 6-ketocholestanol is a recoupler for mitochondria, chromatophores and cytochrome oxidase proteoliposomes. Biochim. Biophys. Acta. 1318:159-172.
67. 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 29:451-464.
68. Voglino, L., T. J. McIntosh, and S. A. Simon. 1998. Modulation of the binding of signal peptides to lipid bilayers by dipoles near the hydrocarbon-water interface. Biochemistry. 37:12241-12252.
69. Wilson, R., and J. R. Sargent. 1993. Lipid and fatty acid composition of brain tissue from adrenoleukodystrophy patients. J. Neurochem. 61:290-297.
70. Wu, W.-G., and L.-M. Chi. 1991. Conformational change of cholesterol side chain in lipid bilayers. J. Am. Chem. Soc. 113:4683-4685.
71. Xu, X., and E. London. 2000. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry. 39:843-849.
72. Xu, X. L., R. Bittman, G. Duportail, D. Heissler, C. Vilcheze, and E. London. 2001. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). J. Biol. Chem. 276:33540-33546.