Cholesterol-sphingomyelin interactions: A molecular dynamics simulation study

Biophysical Journal

Volumn 91, Issue 10, 2006, Pages 3756-3767

  Róg, Tomasz ^a,b   Pasenkiewicz Gierula, Marta ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b AALTO UNIVERSITY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; SPHINGOMYELIN; STEAROYLSPHINGOMYELIN; UNCLASSIFIED DRUG; WATER;

ARTICLE; HYDROGEN BOND; LIPID BILAYER; MOLECULAR DYNAMICS; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; TEMPERATURE SENSITIVITY;

EID: 33751237380     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.080887     Document Type: Article

References (60)

1. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
2. Pandit, S. A., S. Vasudevan, S. W. Chiu, R. J. Mashl, E. Jacobsson, and H. L. Scott. 2004. Sphingomyelin-cholesterol domains in phospholipid membranes: atomistic simulation. Biophys. J. 87:1092-1100.
3. Pandit, S. A., E. Jacobsson, and H. L. Scott. 2004. Simulation of the early stages of nano-domain formation in mixed bilayers of sphingomyelin, cholesterol, and dioleoylphosphatidylcholine. Biophys. J. 87:3312-3322.
4. Ramstedt, B., and P. Slotte. 2002. Membrane properties of sphingomyelins. FEBS Lett. 531:33-37.
5. Koynova, R., and M. Caffrey. 1995. Phases and phase transitions of the sphingolipids. Biochim. Biophys. Acta. 1255:213-236.
6. Robinson, A. J., W. G. Richards, P. J. Thomas, and M. M. Hann. 1995. Behavior of cholesterol and its effect on head group and chain conformations in lipid bilayers: a molecular dynamics study. Biophys. J. 68:164-170.
7. Tu, K., M. L. Klein, and D. J. Tobias. 1998. Constant-pressure molecular dynamics investigation of cholesterol effects in a dipalmitoylphosphatidylcholine bilayer. Biophys. J. 75:2147-2156.
8. Pasenkiewicz-Gierula, M., T. Róg, K. Kitamura, and A. Kusumi. 2000. Cholesterol effects on the phosphatidylcholine bilayer polar region: a molecular simulation study. Biophys. J. 78:1376-1389.
9. Veiga, M. P., J. L. R. Arrondo, F. M. Goni, A. Alonso, and D. Marsh. 2001. 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. 40:2614-2622.
10. Kan, C. C., Z. S. Ruan, and R. Bittman. 1991. Interaction of cholesterol with sphingomyelin in bilayer membranes: evidence that hydroxyl group of sphingomyelin does not modulate the rate of cholesterol exchange between vesicles. Biochemistry. 30:7759-7766.
11. Mombelli, E., R. Morris, W. Taylor, and F. Fraternali. 2003. Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophys. J. 84:1507-1517.
12. Chiu, S. W., S. Vasudevan, E. Jakobsson, R. J. Mashl, and H. L. Scott. 2003. Structure of sphingomyelin bilayers: a simulation study. Biophys. J. 85:3624-3635.
13. Niemelä, P., M. T. Hyvönen, and I. Vattulainen. 2004. Structure and dynamics of sphingomyelin bilayer: insight gained through systematic comparison to phosphatidylcholine. Biophys. J. 87:2976-2989.
14. Talbott, C. M., I. Vorobyov, D. Borchman, K. G. Taylor, D. B. DuPré, and M. C. Yappert. 2000. Conformational studies of sphingolipids by NMR spectroscopy. II. Sphingomyelin. Biochim. Biophys. Acta. 1467:326-337.
15. Holopainen, J. M., A. J. Metso, J. Mattila, A. Jutila, and P. K. J. Kinnunen. 2004. Evidence for the lack of a specific interaction between cholesterol and sphingomyelin. Biophys. J. 86:1510-1520.
16. Urbina, J. A., B. Moreno, W. Arnold, C. H. Taron, P. Orlean, and E. Oldfield. 1998. A carbon-13 nuclear magnetic resonance spectroscopic study of inter-proton pair order parameters: a new approach to study order and dynamics in phospholipid membrane systems. Biophys. J. 75:1372-1383.
17. Chiu, S. W., E. Jakobsson, and H. L. Scott. 2001. Combined Monte Carlo and molecular dynamics simulation of hydrated dipalmitoyl-phosphatidylcholine- cholesterol lipid bilayers. J. Chem. Phys. 114:5435-5443.
18. Chiu, S. W., E. Jakobsson, and H. L. Scott. 2001. Combined Monte Carlo and molecular dynamics simulation of hydrated lipid-cholesterol lipid bilayers at low cholesterol concentration. Biophys. J. 80:1104-1114.
19. 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.
20. Róg, T., and M. Pasenkiewicz-Gierula. 2006. Cholesterol effects on a mixed-chain phosphatidylcholine bilayer: a molecular dynamics simulation study. Biochimie. 88:449-460.
21. Ramstedt, B., and J. P. Slotte. 1999. Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length. Biophys. J. 76:908-915.
22. Sankaram, M. B., and T. E. Thompson. 1990. Interaction of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry. 29:10670-10675.
23. 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.
24. Chiu, S. W., E. Jakobsson, R. J. Mashl, and H. L. Scott. 2002. Cholesterol-induced modifications in lipid bilayers: a simulation study. Biophys. J. 83:1842-1853.
25. Smondyrev, A. M., and M. L. Berkowitz. 1999. Structure of dipalmitoylphosphatidyl-choline/cholesterol bilayer at low and high cholesterol concentrations: a molecular dynamics simulation. Biophys. J. 77:2075-2089.
26. Smondyrev, A. M., and M. L. Berkowitz. 2001. Effects of oxygenated sterol on phospholipid bilayer properties: a molecular dynamics simulation. Chem. Phys. Lipids. 112:31-39.
27. Hofsäß, C., E. Lindahl, and O. Edholm. 2003. Molecular dynamics simulation of phospholipid bilayer with cholesterol. Biophys. J. 84:2192-2206.
28. Falck, E., M. Patra, M. Karttunen, M. T. Hyvönen, and I. Vattulainen. 2004. Lessons of slicing membranes: interplay of packing, free area, and lateral diffusion in phospholipid/cholesterol bilayers. Biophys. J. 87:1076-1091.
29. Falck, E., M. Patra, M. Karttunen, M. T. Hyvönen, and I. Vattulainen. 2004. Impact of cholesterol on voids in phospholipid membranes. J. Chem. Phys. 121:12676-12680.
30. Róg, T., and M. Pasenkiewicz-Gierula. 2001. Cholesterol effects on the phosphatidylcholine bilayer nonpolar region: a molecular simulation study. Biophys. J. 81:2190-2202.
31. Róg, T., and M. Pasenkiewicz-Gierula. 2001. Cholesterol effects on the membrane packing and condensation: a molecular simulation study. FEBS Lett. 502:68-71.
32. Róg, T., and M. Pasenkiewicz-Gierula. 2003. Effects of epicholesterol on the phosphatidylcholine bilayer: a molecular simulation study. Biophys. J. 84:1818-1826.
33. Hyvönen, M. T., and P. T. Kovanen. 2003. Molecular dynamics simulation of sphingomyelin bilayer. J. Phys. Chem. B. 107:9102-9108.
34. Khelashvili, G. A., and H. L. Scott. 2004. Combined Monte Carlo and molecular dynamics simulation of hydrated 18:0 sphingomyelincholesterol lipid bilayers. J. Chem. Phys. 120:9841-9847.
35. Nyholm, P., I. Pascher, and S. Sundell. 1990. The effect of hydrogen bonds on the conformation of glycosphingolipids. methylated and unmethylated cerebroside studied by X-ray single crystal analysis and model calculations. Chem. Phys. Lipids. 52:1-10.
36. Case, D. A., D. A. Pearlman, J. W. Caldwell, T. E. Cheatham III, W. S. Ross, C. Simmerling, T. A. Darden, K. M. Merz, R. V. Stanton, A. L. Cheng, J. J. Vincent, M. Crowley, et al. 1997. AMBER 5.0. University of California, San Francisco, CA.
37. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential functions for proteins. Energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
38. Pasenkiewicz-Gierula, M., Y. Takaoka, H. Miyagawa, K. Kitamura, and A. Kusumi. 1999. Charge pairing of headgroups in phosphatidylcholine membranes: a molecular dynamics simulation study. Biophys. J. 76:1228-1240.
39. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
40. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comp. Phys. 23:327-341.
41. Egberts, E., S.-J. Marrink, and H. J. C. Berendsen. 1994. Molecular dynamics simulation of a phospholipid membrane. Eur. Biophys. J. 22:423-436.
42. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
43. Maulik, P., P. Spirada, and G. Shipley. 1991. Structure and thermotropic properties of hydrated N-stearoyl sphingomyelin bilayer membranes. Biochim. Biophys. Acta. 1062:211-219.
44. Huang, C. H., and S. S. Li. 1999. Calorimetric and molecular mechanics studies of the thermotropic phase behavior of membrane phospholipids. Biochim. Biophys. Acta. 1422:273-307.
45. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
46. Tristram-Nagle, S., R. Zhang, R. M. Suter, C. R. Worthington, W.-J. Sun, and J. Nagle. 1993. Measurement of chain tilt angle in fully hydrated bilayers of gel phase lecithins. Biophys. J. 64:1097-1109.
47. Tu, K., D. J. Tobias, J. K. Blasie, and M. L. Klein. 1996. Molecular dynamics investigation of the structure of a fully hydrated gel-phase dipalmitoylphosphatidylcholine bilayer. Biophys. J. 70:595-608.
48. Maulik, P., and G. Shipley. 1996. Structure and thermotropic properties of hydrated N-stearoyl sphingomyelin bilayer membranes. Biophys. J. 70:2256-2265.
49. Murzyn, K., T. Róg, G. Jezierski, Y. Takaoka, and M. Pasenkiewicz-Gierula. 2001. Effects of phospholipid unsaturation on the membrane/water interface: a molecular simulation study. Biophys. J. 81:170-183.
50. Vainio, S., M. Jansen, M. Koivusalo, T. Róg, M. Karttunen, I. Vattulainen, and E. Ikonen. 2006. Significance of sterol structural specificity. J. Biol. Chem. 281:348-355.
51. Pasenkiewicz-Gierula, M., Y. Takaoka, H. Miyagawa, K. Kitamura, and A. Kusumi. 1997. Hydrogen bonding of water to phosphatidylcholine in the membrane as studied by a molecular dynamics simulation: location, geometry and lipid-lipid bridging via hydrogen bonded water. J. Chem. Phys. 101:3677-3691.
52. Róg, T., K. Murzyn, R. Gurbiel, K. Kitamura, A. Kusumi, and M. Pasenkiewicz-Gierula. 2004. Effects of phospholipid unsaturation on the structure and dynamics of the hydrocarbon core of the membrane. A molecular simulation study. J. Lip. Res. 45:326-336.
53. Ramstedt, B., and J. P. Slotte. 1999. Comparison of the biophysical properties of racemic and d-erythro-N-acyl sphingomyelins. Biophys. J. 77:1498-1506.
54. Karolis, C., H. G. Coster, T. C. Chilcott, and K. D. Barrow. 1998. Differential effects of cholesterol and oxidised-cholesterol in egg lecithin bilayers. Biochim. Biophys. Acta. 1368:247-255.
55. Smondyrev, A. M., and M. L. Berkowitz. 2001. Molecular dynamics simulation of the structure of dimyristoylphosphatidylcholine bilayers with cholesterol, ergosterol, and lanosterol. Biophys. J. 80:1649-1658.
56. Smondyrev, A. M., and M. L. Berkowitz. 2000. Molecular dynamics simulation of dipalmitoylphosphatidylcholine membrane with cholesterol sulfate. Biophys. J. 78:1672-1680.
57. Faure, C., J. F. Tranchant, and E. J. Dufourc. 1996. Comparative effects of cholesterol and cholesterol sulfate on hydration and ordering of dimyristoylphosphatidylcholine membranes. Biophys. J. 70:1380-1390.
58. Huang, C., and J. T. Mason. 1986. Structure and properties of mixedchain phospholipid assemblies. Biochim. Biophys. Acta. 864:423-470.
59. Marsh, D. 1993. Analysis of the bilayer phase transition temperatures of phosphatidylcholines with mixed chains. Biophys. J. 61:1036-1040.
60. Chong, P. L.-G., and D. Choate. 1989. Calorimetric studies of the effect of cholesterol on the phase transition of C(18):C(10) phosphatidylcholine. Biophys. J. 55:551-556.