Structure and dynamics of sphingomyelin bilayer: Insight gained through systematic comparison to phosphatidylcholine

Biophysical Journal

Volumn 87, Issue 5, 2004, Pages 2976-2989

  Niemelä, Perttu ^a   Hyvönen, Marja T ^a,b   Vattulainen, Ilpo ^a  

^a HELSINKI INSTITUTE OF PHYSICS   (Finland)

^b WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; DIPALMITOYLPHOSPHATIDYLCHOLINE; LIPID; PALMITOYLSPHINGOMYELIN; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN; SPHINGOSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DIFFUSION; HUMAN; HYDROGEN BOND; LIPID BILAYER; MEMBRANE BIOLOGY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHASE TRANSITION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SIMULATION; STRUCTURE ANALYSIS; TRANSITION TEMPERATURE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; EVALUATION; KINETICS; MACROMOLECULE; MEMBRANE FLUIDITY; MOTION;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; KINETICS; LIPID BILAYERS; MACROMOLECULAR SUBSTANCES; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOTION; PHOSPHATIDYLCHOLINES; SPHINGOMYELINS;

EID: 16344363286     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.048702     Document Type: Article

References (88)

1. Andersen, R. G. W., and K. Jacobson. 2002. A role for lipid shells in targeting proteins to caveolae, rafts and other lipid domains. Science. 296:1821-1825.
2. Anézo, C., A. H. de Vries, H.-D. Höltje, D. P. Tieleman, and S.-J. Marrink. 2003. Methodological issues in lipid bilayer simulations. J. Phys. Chem. B. 107:9424-9433.
3. Armen, R. S., O. D. Uitto, and S. E. Feller. 1998. Phospholipid component volumes: determination and application to bilayer structure calculations. Biophys. J. 74:734-744.
4. Bar, L. K., Y. Barenholz, and T. E. Thompson. 1997. Effect of sphingomyelin composition on the phase structure of phosphatidylcholine- sphingomyelin bilayers. Biochemistry. 1997:2507-2516.
5. Barenholz, Y., and T. E. Thompson. 1999. Sphingomyelin: biophysical aspects. Chem. Phys. Lipids. 102:29-34.
6. 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.
7. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. Reidel, Dordrecht, The Netherlands. 331-342.
8. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. Gromacs: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91:43-56.
9. Berger, O., O. Edholm, and F. Jähnïg. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
10. Brown, M. F. 1984a. Theory of spin-lattice relaxation in lipid bilayers and biological membranes: dipolar relaxation. J. Chem. Phys. 80:2808-2831.
11. Brown, M. F. 1984b. Unified picture for spin-lattice relaxation of lipid bilayers and biomembranes. J. Chem. Phys. 80:2832-2836.
12. Brown, R. E. 1998. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 111:1-9.
13. Bloom, M., E. Evans, and O. G. Mouritsen. 1991. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Q. Rev. Biophys. 24:293-397.
14. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
15. Brown, M. F., J. Seelig, and U. Häberlen. 1979. Structural dynamics in phospholipid bilayers from deuterium spin-lattice relaxation time measurements. J. Chem. Phys. 70:5045-5053.
16. Bruzik, K. S., B. Sobon, and G. M. Salamonczyk. 1990. Nuclear magnetic resonance study of sphingomyelin bilayers. Biochemistry. 29:4017-4021.
17. Chiu, S.-W., M. Clark, V. Balaji, S. Subramaniam, H. L. Scott, and E. Jakobsson. 1995. Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69:1230-1245.
18. 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.
19. Douliez, J.-P., A. Léonard, and E. J. Dufourc. 1995. Restatement of order parameters in biomembranes: calculation of C-C bond order parameters from C-D quadrupolar splittings. Biophys. J. 68:1727-1739.
20. Essmann, U., L. Perera, and M. L. Berkowitz. 1995a. The origin of the hydration interaction of lipid bilayers from MD simulation of dipalmitoylphosphatidylcholine membranes in gel and crystalline phases. Langmuir. 11:4519-4531.
21. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995b. A smooth particle mesh Ewald potential. J. Chem. Phys. 103:8577-8592.
22. 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.
23. Feller, S. E. 2000. Molecular dynamics simulations of lipid bilayers. Curr. Opin. Coll. Interface Sci. 5:217-223.
24. Filippov, A., G. Orädd, and G. Lindblom. 2003. The effect of cholesterol on the lateral diffusion of phospholipids in oriented bilayers. Biophys. J. 84:3079-3086.
25. Flewelling, R. F., and W. L. Hubbel. 1986. The membrane dipole potential in a total membrane potential model. Biophys. J. 49:541-552.
26. Gawrisch, K., D. Ruston, J. Zimmerberg, V. A. Parsegian, R. P. Rand, and N. Fuller. 1992. Membrane dipole potentials, hydration forces, and the ordering of water at membrane surface. Biophys. J. 61:1213-1223.
27. Guo, W., V. Kurze, T. Huber, N. H. Afdhal, K. Beyer, and J. A. Hamilton. 2002. A solid-state NMR study of phospholipid-cholesterol interactions: sphingomyelin-cholesterol binary systems. Biophys. J. 83:1465-1478.
28. Helms, J. B., and C. Zurzolo. 2004. Lipids as targeting signals: lipid rafts and intracellular traffiking. Traffic. 5:247-254.
29. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
30. Hevonoja, T., M. O. Pentikäinen, M. T. Hyvönen, P. T. Kovanen, and M. Ala-Korpela. 2000. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta. 1488:189-210.
31. Hill, W. G., and M. L. Zeidel. 2000. Reconstructing the barrier properties of a water-tight membrane by design of leaflet-specific liposomes. J. Biol. Chem. 275:30176-30185.
32. Holopainen, J. M., A. J. Metso, J.-P. 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.
33. Hoover, W. G. 1985. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
34. Hyvönen, M. T., and P. T. Kovanen. 2003. Molecular dynamics simulation of sphingomyelin bilayer. J. Phys. Chem. B. 107:9102-9108.
35. Hyvönen, M. T., T. T. Rantala, and M. Ala-Korpela. 1997. Structure and dynamic properties of diunsaturated 1-palmitoyl-2-linoleoyl-in-glycero-3- phosphatidylcholine lipid bilayer from molecular dynamics simulation. Biophys. J. 73:2907-2923.
36. Katsaras, J., and T. Gutberiet, editors, 2001. Lipid Bilayers: Structure and Interactions. Springer-Verlag, Berlin, Germany.
37. Khelashvili, G. A., and H. L. Scott. 2004. Combined Monte Carlo and molecular dynamics simulation of hydrated 18:0 sphingomyelin-cholesterol lipid bilayers. J. Chem. Phys. 120:9841-9847.
38. König, S., W. Pfeiffer, T. Bayerl, D. Richter, and E. Sackmann. 1992. Molecular dynamics of lipid bilayers studied by incoherent quasi-elastic neutron scattering. J. Phys. II France. 2:1589-1615.
39. Koynova, R., and M. Caffrey. 1995. Phases and phase transitions of the sphingolipids. Biochim. Biophys. Acta. 1255:213-236.
40. Ladanyi, B. M., and M. S. Skaf. 1993. Computer simulation of hydrogen-bonding liquids. Annu. Rev. Phys. Chem. 44:335-368.
41. 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.
42. Lindahl, E., and O. Edholm. 2001. Molecular dynamics simulation of NMR relaxation rates and slow dynamics in lipid bilayers. J. Chem. Phys. 115:4938-4950.
43. Lindahl, E., B. Hess, and D. van der Spoel. 2001. Gromacs 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7:306-317.
44. Luzar, A., and D. Chandler. 1996. Effect of environment on hydrogen bond dynamics in liquid water. Phys. Rev. Lett. 76:928-931.
45. Mashl, R. J., H. L. Scott, S. Subramaniam, and E. Jakobsson. 2001. Molecular simulation of dioleoylphosphatidylcholine lipid bilayers at differing levels of hydration. Biophys. J. 81:3005-3015.
46. Maulik, P. R., and G. G. Shipley. 1996. N-palmitoyl sphingomyelin bilayers: structure and interactions with cholesterol and dipalmitoylphosphatidylcholine. Biochemistry. 35:8025-8034.
47. Maulik, P. R., P. K. Sripada, and G. G. Shipley. 1991. Structure and thermotropic properties of hydrated N-stearoyl sphingomyelin bilayer membranes. Biochim. Biophys. Acta. 1062:211-219.
48. Maxfield, F. R. 2002. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14:483-487.
49. Mayor, S., and M. Rao. 2004. Rafts: scale-dependent, active lipid organization at the cell surface. Traffic. 5:231-240.
50. McIntosh, T. J., S. A. Simon, D. Needham, and C.-H. Huang. 1992. Interbilayer interactions between sphingomyelin and sphingomyelin/cholesterol bilayers. Biochemistry. 31:2020-2024.
51. Miyamoto, S., and P. A. Kollman. 1992. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comput. Chem. 13:952-962.
52. 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.
53. Nagle, J. F., and S. Tristram-Nagle. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta. 1469:159-195.
54. Neuringer, L. J., B. Sears, F. B. Jungalwala, and E. K. Shriver. 1979. Difference in orientational order in phospholipid and sphingomyelin bilayers. FEBS Lett. 104:173-175.
55. 13C nuclear magnetic resonance relaxation data as a function of frequency and temperature. J. Chem. Phys. 107:10288-10310.
56. Nose, S. 1984. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52:255-268.
57. Nose, S., and M. L. Klein. 1983. Constant pressure molecular dynamics for molecular systems. Mol. Phys. 50:1055-1076.
58. Pandit, S. A., D. Bostick, and M. L. Berkowitz. 2004. Complexation of phosphatidylcholine lipids with cholesterol. Biophys. J. 86:1345-1356.
59. Parrinello, M., and A. Rahman. 1981. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52:7182-7190.
60. Pastor, R. W., and S. E. Feller. 1996. Time scales of lipid dynamics and molecular dynamics. In Biological Membranes: A Molecular Perspective from Computation and Experiment. K. M. Merz and B. Roux, editors. Birkhauser, Boston, MA. 3-30.
61. Pastor, R. W., R. M. Venable, and S. E. Feller. 2002. Lipid bilayers, NMR relaxation and computer simulations. Acc. Chem. Res. 35:438-446.
62. Patra, M., M. Karttunen, M. T. Hyvönen, E. Falck, P. Lindqvist, and I. Vattulainen. 2003. Molecular dynamics simulations of lipid bilayers: major artifacts due to truncating electrostatic interactions. Biophys. J. 84:3636-3645.
63. Patra, M., M. Karttunen, M. T. Hyvönen, E. Falck, and I. Vattulainen. 2004. Lipid bilayers driven to a wrong lane in molecular dynamics simulations by subtle changes in long-range electrostatic interactions. J. Phys. Chem. B. 108:4485-4494.
64. 2H NMR spectroscopy. Biophys. J. 79:3172-3192.
65. Pike, L. J. 2004. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378:281-292.
66. Ramstedt, B., P. Leppiäki, M. Axberg, and J. P. Slotte. 1999. Analysis of natural and synthetic sphingomyelins using high-performance thin-layer chromatography. Eur. J. Biochem. 266:997-1002.
67. Ramstedt, B., and P. Slotte. 2002. Membrane properties of sphingomyelin. FEBS Lett. 531:33-37.
68. Sackmann, E. 1995. Physical basis of self-organization and function of membranes: physics of vesicles. In Structure and Dynamics of Membranes: From Cells to Vesicles. R. Lipowsky and E. Sackmann, editors. Elsevier, Amsterdam, The Netherlands. 213-304.
69. Saiz, L., and M. L. Klein. 2002. Computer simulation studies of model biological membranes. Acc. Chem. Res. 35:482-489.
70. Schmidt, C. F., Y. Barenholz, and T. E. Thompson. 1977. A nuclear magnetic resonance study of sphingomyelin in bilayer systems. Biochemistry. 16:2649-2656.
71. Sciortino, F., P. H. Poole, H. E. Stanley, and S. Havlin. 1990. Lifetime of the bond network and gel-like anomalies in supercooled water. Phys. Rev. Lett. 64:1686-1689.
72. Scott, H. L. 2002. Modeling the lipid component of membranes. Curr. Opin. Struct. Biol. 12:495-502.
73. Seelig, A., and J. Seelig. 1974. The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry. 13:4839-4845.
74. Seelig, J., and N. Waespe-Sarcevic. 1978. Molecular order in cis and trans unsaturated phospholipid bilayers. Biochemistry. 17:3310-3315.
75. Shinoda, W., and S. Okazaki. 1998. A Voronoi analysis of lipid area fluctuation in a bilayer. J. Chem. Phys. 109:1517-1521.
76. Simon, S. A., and T. J. McIntosh. 1989. Magnitude of the solvation pressure depends on dipole potential. Proc. Natl. Acad. Sci. USA. 86:9263-9267.
77. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-571.
78. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-41.
79. 2H-NMR study. Biophys. J. 85:1013-1024.
80. Sun, F. 2002. Constant normal pressure, constant surface tension, and constant temperature molecular dynamics simulation of hydrated 1,2-dilignoceroylphosphatidylcholine monolayer. Biophys. J. 82:2511-2519.
81. 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.
82. Tieleman, D. P., and H. J. C. Berendsen. 1996. Molecular dynamics simulations of a fully hydrated dipalmitoylphosphatidylcholine bilayer with different macroscopic boundary conditions and parameters. J. Chem. Phys. 105:4871-4880.
83. Tieleman, D. P., and H. J. C. Berendsen. 1998. A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer. Biophys. J. 74:2786-2801.
84. Tieleman, D. P., S. J. Marrink, and H. J. C. Berendsen. 1997. A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim. Biophys. Acta. 1331:235-270.
85. Tu, K., D. J. Tobias, 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.
86. van Gunsteren, W. F., P. Krüger, S. R. Billeter, A. E. Mark, A. A. Eising, W. R. P. Scott, P. H. Hüneberg, and I. G. Tironi. 1996. Biomolecular simulation: the GROMOS96 manual and user guide. Biomos, Groningen and Hochsuchulverlag AG, Germany and er ETH Zürich, Zurich, Switzerland.
87. Vaz, W. L. C., R. M. Clegg, and D. Hallmann. 1985. Translational diffusion of lipids in liquid crystalline phase phosphatidylcholine multibilayers: a comparison of experiment with theory. Biochemistry. 24:781-786.
88. Zachowski, A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294:1-14.