Atom-scale molecular interactions in lipid raft mixtures

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 1, 2009, Pages 122-135

  Niemelä, Perttu S ^a   Hyvönen, Marja T ^b   Vattulainen, Ilpo ^a,c,d  

^a AALTO UNIVERSITY   (Finland)

^b WIHURI RESEARCH INSTITUTE   (Finland)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Bilayer; Cholesterol; Lipid; Membrane; Molecular dynamics; Phosphatidylcholine; Raft; Simulation; Sphingomyelin; Sterol

Indexed keywords

CHOLESTEROL; DESMOSTEROL; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN; STEROL;

CELL MEMBRANE; CHEMICAL REACTION; CHEMICAL STRUCTURE; HYDROGEN BOND; LIPID COMPOSITION; LIPID RAFT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRIORITY JOURNAL; REVIEW;

ANIMALS; HUMANS; HYDROGEN BONDING; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; SPHINGOMYELINS; STEROLS;

EID: 58149201160     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.08.018     Document Type: Review

References (134)

1. van Meer G. Cellular lipidomics. EMBO J. 24 (2005) 3159-3165
2. Sackmann E. Biological membranes architecture and function. In: Lipowsky R., and Sackmann E. (Eds). Structure and Dynamics of Membranes: From Cells to Vesicles (1995), Elsevier, Amsterdam 1-65
3. Singer S.J., and Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720-731
4. Oldfield E., and Chapman D. Dynamics of lipids in membranes: heterogeneity and the role of cholesterol. FEBS Lett. 23 (1972) 285-297
5. Shimshick E.J., and McConnell H.M. Lateral phase separation in phospholipid membranes. Biochemistry 12 (1973) 2351-2360
6. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
7. Edidin M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 257-283
8. Pike L.J. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378 (2004) 281-292
9. Pike L.J. Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J. Lipid Res. 47 (2006) 1597-1598
10. Hevonoja T., Pentikäinen M.O., Hyvönen M.T., Kovanen P.T., and Ala-Korpela M. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta 1488 (2000) 189-210
11. Feigenson G.W. Phase boundaries and biological membranes. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 63-77
12. Varma R., and Mayor S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394 (1998) 798-801
13. Cottingham K. Do you believe in lipid rafts?. Anal. Chem. 76 (2004) 403-406
14. Simons K., and Vaz W.L.C. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 269-295
15. Gaus K., Gratton E., Kable E.P.W., Jones A.S., Gelissen I., Kritharides L., and Jessup W. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15554-15559
16. Brown R.E. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell. Sci. 111 (1998) 1-9
17. London E. How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells. Biochim. Biophys. Acta 1746 (2005) 203-220
18. Ramstedt B., and Slotte J.P. Membrane properties of sphingomyelins. FEBS Lett. 531 (2002) 33-37
19. Holopainen J.M., Metso A.J., Mattila J.P., Jutila A., and Kinnunen P.K.J. Evidence for the lack of a specific interaction between cholesterol and sphingomyelin. Biophys. J. 86 (2004) 1510-1520
20. Ramstedt B., and Slotte J.P. Comparison of the biophysical properties of racemic and d-erythro-N-acyl sphingomyelins. Biophys. J. 77 (1999) 1498-1506
21. Barenholz Y., and Thompson T.E. Sphingomyelin: biophysical aspects. Chem. Phys. Lipids 102 (1999) 29-34
22. Ramstedt B., and Slotte J.P. Sphingolipids and the formation of sterol-enriched ordered membrane domains. Biochim. Biophys. Acta 1758 (2006) 1945-1956
23. Koynova R., and Caffrey M. Phases and phase transitions of the sphingolipids. Biochim. Biophys. Acta 1255 (1995) 213-236
24. Bar L.K., Barenholz Y., and Thompson T.E. Effect of sphingomyelin composition on the phase structure of phosphatidylcholine-sphingomyelin bilayers. Biochemistry 36 (1997) 2507-2516
25. Koynova R., and Caffrey M. Phases and phase transitions of the phosphatidylcholines. Biochim. Biophys. Acta 1376 (1998) 91-145
26. Silvius J.R. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta 1610 (2003) 174-183
27. Talbott C.M., Vorobyov I., Borchman D., Taylor K.G., DuPré D.B., and Yappert M.C. Conformational studies of sphingolipids by NMR spectroscopy. II. Sphingomyelin. Biochim. Biophys. Acta 1467 (2000) 326-337
28. 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) 2614-2622
29. 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
30. Bloom M., Evans E., and Mouritsen O.G. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Q. Rev. Biophys. 24 (1991) 293-397
31. Ohvo-Rekilä H., Ramstedt B., Leppimäki P., and Slotte J.P. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41 (2002) 66-97
32. Xiang T. Translational diffusion in lipid bilayers: dynamic free-volume theory and molecular dynamics simulation. J. Phys. Chem. B 103 (1999) 385-394
33. Jedlovszky P., and Mezei M. Effect of cholesterol on the properties of phospholipid membranes. 2. Free energy profile of small molecules. J. Phys. Chem. B 107 (2003) 5322-5332
34. Hofsäss C., Lindahl E., and Edholm O. Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 84 (2003) 2192-2206
35. Falck E., Patra M., Karttunen M., Hyvönen M.T., and Vattulainen I. Lessons of slicing membranes: interplay of packing, free area, and lateral diffusion in phospholipid/cholesterol bilayers. Biophys. J. 87 (2004) 1076-1091
36. Kupiainen M., Falck E., Ollila S., Niemelä P., Gurtovenko A.A., Hyvönen M.T., Patra M., Karttunen M., and Vattulainen I. Free volume properties of sphingomyelin, DMPC, DPPC, and PLPC bilayers. J. Comput. Theor. Nanosci. 2 (2005) 401-413
37. Pandit S.A., Jakobsson E., and Scott H.L. Simulation of the early stages of nano-domain formation in mixed bilayers of sphingomyelin, cholesterol, and dioleylphosphatidylcholine. Biophys. J. 87 (2004) 3312-3322
38. Róg T., and Pasenkiewicz-Gierula M. Cholesterol effects on a mixed-chain phosphatidylcholine bilayer: a molecular dynamics simulation study. Biochimie 88 (2006) 449-460
39. Pitman M.C., Suits F., MacKerell A.D., and Feller S.E. Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol. Biochemistry 43 (2004) 15318-15328
40. Maulik P.R., and Shipley G.G. N-palmitoyl sphingomyelin bilayers: structure and interactions with cholesterol and dipalmitoylphosphatidylcholine. Biochemistry 35 (1996) 8025-8034
41. Li X.M., Smaby J.M., Momsen M.M., Brockman H.L., and Brown R.E. Sphingomyelin interfacial behavior: the impact of changing acyl chain composition. Biophys. J. 78 (2000) 1921-1931
42. Nagle J.F., and Tristram-Nagle S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469 (2000) 159-195
43. Niemelä P., Hyvönen M.T., and Vattulainen I. Structure and dynamics of sphingomyelin bilayer: insight gained through systematic comparison to phosphatidylcholine. Biophys. J. 87 (2004) 2976-2989
44. Böckmann R.A., Hac A., Heimburg T., and Grubmüller H. Effect of sodium chloride on a lipid bilayer. Biophys. J. 85 (2003) 1647-1655
45. Böckmann R.A., and Grubmüller H. Multistep binding of divalent cations to phospholipid bilayers: a molecular dynamics study. Angew. Chem., Int. Ed. 43 (2004) 1021-1024
46. Gurtovenko A.A., Miettinen M., Karttunen M., and Vattulainen I. Effect of monovalent salt on cationic lipid membranes as revealed by molecular dynamics simulations. J. Phys. Chem. B 109 (2005) 21126-21134
47. Gurtovenko A.A., and Vattulainen I. Membrane potential and electrostatics of phospholipid bilayers with asymmetric transmembrane distribution of anionic lipids. J. Phys. Chem. B 112 (2008) 4629-4634
48. Anézo C., de Vries A.H., Höltje H.D., Tieleman D.P., and Marrink S.J. Methodological issues in lipid bilayer simulations. J. Phys. Chem. B 107 (2003) 9424-9433
49. Mombelli E., Morris R., Taylor W., and Fraternali F. Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophys. J. 84 (2003) 1507-1517
50. Hyvönen M.T., and Kovanen P.T. Molecular dynamics simulation of sphingomyelin bilayer. J. Phys. Chem. B 107 (2003) 9102-9108
51. Chiu S.W., Vasudevan S., Jakobsson E., Mashl R.J., and Scott H.L. Structure of sphingomyelin bilayers: a simulation study. Biophys. J. 85 (2003) 3624-3635
52. Róg T., and Pasenkiewicz-Gierula M. Cholesterol-sphingomyelin interactions: a molecular dynamics simulation study. Biophys. J. 91 (2006) 3756-3767
53. Sciortino F., Poole P.H., Stanley H.E., and Havlin S. Lifetime of the bond network and gel-like anomalies in supercooled water. Phys. Rev. Lett. 64 (1990) 1686-1689
54. Hammerich A.D., and Buch V. An alternative near-neighbor definition of hydrogen bonding in water. J. Chem. Phys. 128 (2008) 111101
55. Bruzik K.S., Sobon B., and Salamonczyk G.M. Nuclear magnetic resonance study of sphingomyelin bilayers. Biochemistry 29 (1990) 4017-4021
56. Schmidt C.F., Barenholz Y., and Thompson T.E. A nuclear magnetic resonance study of sphingomyelin in bilayer systems. Biochemistry 16 (1977) 2649-2656
57. Neuringer L.J., Sears B., Jungalwala F.B., and Shriver E.K. Difference in orientational order in phospholipid and sphingomyelin bilayers. FEBS Lett. 104 (1979) 173-175
58. Mehnert T., Jacob K., Bittman R., and Beyer K. Structure and lipid interaction of N-palmitoylsphingomyelin in bilayer membranes as revealed by 2H-NMR spectroscopy. Biophys. J. 90 (2006) 939-946
59. 14N-NMR study. Biochim. Biophys. Acta 645 (1981) 270-278
60. 2H-NMR study. Biophys. J. 85 (2003) 1013-1024
61. Lindahl E., and Edholm O. Molecular dynamics simulation of NMR relaxation rates and slow dynamics in lipid bilayers. J. Chem. Phys. 115 (2001) 4938-4950
62. Mashl R.J., Scott H.L., Subramaniam S., and Jakobsson E. Molecular simulation of dioleoylphosphatidylcholine lipid bilayers at differing levels of hydration. Biophys. J. 81 (2001) 3005-3015
63. Niemelä P.S., Hyvönen M.T., and Vattulainen I. Influence of chain length and unsaturation on sphingomyelin bilayers. Biophys. J. 90 (2006) 851-863
64. Jensen M.O., and Mouritsen O.G. Lipids do influence protein function - the hydrophobic matching hypothesis revisited. Biochim. Biophys. Acta 1666 (2004) 205-226
65. Andersen O.S., and Koeppe R.E. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 107-130
66. Ollila S., Hyvönen M.T., and Vattulainen I. Polyunsaturation in lipid membranes: dynamic properties and lateral pressure profiles. J. Phys. Chem. B 111 (2007) 3139-3150
67. Schmidt C.F., Barenholz Y., Huang C., and Thompson T.E. Monolayer coupling in sphingomyelin bilayer systems. Nature 271 (1978) 775-777
68. Slater J.L., and Huang C.H. Interdigitated bilayer membranes. Prog. Lipid Res. 27 (1988) 325-359
69. Kiessling V., Crane J.M., and Tamm L.K. Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91 (2006) 3313-3326
70. Wan C., Kiessling V., and Tamm L.K. Coupling of cholesterol-rich lipid phases in asymmetric bilayers. Biochemistry 47 (2008) 2190-2198
71. Allender D.W., and Schick M. Phase separation in bilayer lipid membranes: effects on the inner leaf due to coupling to the outer leaf. Biophys. J. 91 (2006) 2928-2935
72. Wagner A.J., Loew S., and May S. Influence of monolayer-monolayer coupling on the phase behavior of a fluid lipid bilayer. Biophys. J. 93 (2007) 4268-4277
73. Levin I.W., Thompson T.E., Barenholz Y., and Huang C. Two types of hydrocarbon chain interdigitation in sphingomyelin bilayers. Biochemistry 24 (1985) 6282-6286
74. Huang C., and Mason J.T. Structure and properties of mixed-chain phospholipid assemblies. Biochim. Biophys. Acta 864 (1986) 423-470
75. Maulik P.R., Atkinson D., and Shipley G.G. X-ray scattering of vesicles of N-acyl sphingomyelins: determination of bilayer thickness. Biophys. J. 50 (1986) 1071-1077
76. Shkulipa S.A., den Otter W.K., and Briels W.J. Surface viscosity, diffusion, and intermonolayer friction: simulating sheared amphiphilic bilayers. Biophys. J. 89 (2005) 823-829
77. Huster D., Scheidt H.A., Arnold K., Herrmann A., and Müller P. Desmosterol may replace cholesterol in lipid membranes. Biophys. J. 88 (2005) 1838-1844
78. 31P-NMR spectroscopy. Biochim. Biophys. Acta 1238 (1995) 163-176
79. Hsueh Y.W., Chen M.T., Patty P.J., Code C., Cheng J., Frisken B.J., Zuckermann M., and Thewalt J. Ergosterol in POPC membranes: physical proerties and comparison with structurally similar sterols. Biophys. J. 92 (2007) 1606-1615
80. Schuler I., Milon A., Nakatani Y., Ourisson G., Albrecht A.M., Benveniste P., and Hartmann M.A. Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 6926-6930
81. Halling K.K., and Slotte J.P. Membrane properties of plant sterols in phospholipid bilayers as determined by differential scanning calorimetry, resonance energy transfer and detergent-induced solubilization. Biochim. Biophys. Acta 1664 (2004) 161-171
82. Smondyrev A.M., and Berkowitz M. Molecular dynamics simulation of the structure of dimyristoylphosphatidylcholine bilayers with cholesterol, ergosterol, and lanosterol. Biophys. J. 80 (2001) 1649-1658
83. Cournia Z., Ullmann G.M., and Smith J.C. Differential effects of cholesterol, ergosterol and lanosterol on dipalmitoyl phosphatidylcholine membrane: a molecular dynamics simulation study. J. Phys. Chem. B 111 (2007) 1786-1801
84. Vainio S., Jansen M., Koivusalo M., Róg T., Karttunen M., Vattulainen I., and Ikonen E. Significance of sterol structural specifity. Desmosterol cannot replace cholesterol in lipid rafts. J. Biol. Chem. 281 (2006) 348-355
85. T. Róg, I. Vattulainen, M. Jansen, E. Ikonen, M. Karttunen, Comparison of cholesterol and its direct precursors along the biosynthetic pathway: effects of cholesterol, desmosterol and 7-dehydrocholesterol on saturated and unsaturated lipid bilayers, J. Chem. Phys. (in press).
86. Czub J., and Baginski M. Comparative molecular dynamics study of lipid memranes containing cholesterol and ergosterol. Biophys. J. 90 (2006) 2368-2382
87. Róg T., Pasenkiewicz-Gierula M., Vattulainen I., and Karttunen M. What happens if cholesterol is made smoother: importance of methyl substituents in cholesterol ring structure on phosphatidylcholine-sterol interaction. Biophys. J. 92 (2007) 3346-3357
88. Pöyry S., Róg T., Karttunen M., and Vattulainen I. Significance of cholesterol methyl groups. J. Phys. Chem. B 112 (2008) 2922-2929
89. Aittoniemi J., Niemelä P.S., Hyvönen M.T., Karttunen M., and Vattulainen I. Insight into the putative specific interactions between cholesterol, sphingomyelin and palmitoyl-oleoyl phosphatidylcholine. Biophys. J. 92 (2007) 1125-1137
90. Zhang Z., Bhide S.Y., and Berkowitz M.L. Molecular dynamics simulations of bilayers containing mixtures of sphingomyelin with cholesterol and phosphatidylcholine with cholesterol. J. Phys. Chem. B 111 (2007) 12888-12897
91. Khelashvili G.A., and Scott H.L. Combined Monte Carlo and molecular dynamics simulation of hydrated 18:0 sphingomyelin-cholesterol lipid bilayers. J. Chem. Phys. 120 (2004) 9841-9847
92. Bhide S.Y., Zhang Z., and Berkowitz M.L. Molecular dynamics simulations of SOPS and sphingomyelin bilayers containing cholesterol. Biophys. J. 92 (2007) 1284-1295
93. Niemelä P.S., Ollila S., Hyvönen M.T., Karttunen M., and Vattulainen I. Assessing the nature of lipid rafts. PLoS Comput. Biol. 3 (2007) 304-312
94. Bachar M., Brunelle P., Tieleman D.P., and Rauk A. Molecular dynamics simulation of a polyunsaturated lipid bilayer susceptible to lipid peroxidation. J. Phys. Chem. B 108 (2004) 7170-7179
95. Aittoniemi J., Róg T., Niemelä P., Pasenkiewicz-Gierula M., Karttunen M., and Vattulainen I. Tilt: major factor in sterols' ordering capability in membranes. J. Phys. Chem. B 110 (2006) 25562-25564
96. Pandit S.A., Vasudevan S., Chiu S.W., Mashl R.J., Jakobsson E., and Scott H.L. Sphingomyelin-cholesterol domains in phospholipid membranes: atomistic simulation. Biophys. J. 87 (2004) 1092-1100
97. Huang J., and Feigenson G.W. A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys. J. 76 (1999) 2142-2157
98. Zhang Z., Lu L., and Berkowitz M.L. Energetics of cholesterol transfer between lipid bilayers. J. Phys. Chem. B 112 (2008) 3807-3811
99. Rinia H.A., Snel M.M.E., van der Eerden J.P.J.M., and de Kruijff B. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501 (2001) 92-96
100. McIntosh T.J. X-ray diffraction to determine the thickness of raft and nonraft bilayers. Methods Mol. Biol. 398 (2007) 221-230
101. Filippov A., Orädd G., and Lindblom G. Sphingomyelin structure influences the lateral diffusion and raft formation in lipid bilayers. Biophys. J. 90 (2006) 2086-2092
102. Kučerka N., Tristram-Nagle S., and Nagle J.F. Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J. Membr. Biol. 208 (2005) 193-202
103. Patra M., Salonen E., Terama E., Vattulainen I., Faller R., Lee B.W., Holopainen J., and Karttunen M. Under the influence of alcohol: The effect of ethanol and methanol on lipid bilayers. Biophys. J. 90 (2006) 1121-1135
104. Lindahl E., and Edholm O. Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophys. J. 79 (2000) 426-433
105. Evans E., and Rawicz W. Entropy driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64 (1990) 2094-2097
106. Rawicz W., Olbrich K.C., McIntosh T., Needham D., and Evans E. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79 (2000) 328-339
107. Needham D., McIntosh T.J., and Evans E. Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers. Biochemistry 27 (1988) 4668-4673
108. Needham D., and Nunn R.S. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58 (1990) 997-1009
109. Murtola T., Róg T., Falck E., Karttunen M., and Vattulainen I. Transient ordered domains in single-component phospholipid bilayers. Phys. Rev. Lett. 97 (2006) 238102
110. Cantor R.S. The influence of membrane lateral pressures on simple geometric models of protein conformational equilibria. Chem. Phys. Lipids 101 (1999) 45-56
111. Gullingsrud J., and Schulten K. Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys. J. 86 (2004) 3496-3509
112. Cantor R.S. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 36 (1997) 2339-2344
113. Eckenhoff R.G. Promiscuous ligands and attractive cavities. How do the inhaled anesthetics work?. Mol. Interv. 1 (2001) 258-268
114. Lindahl E., and Edholm O. Spatial and energetic-entropic decomposition of surface tension in lipid bilayers from molecular dynamics simulations. J. Chem. Phys. 113 (2000) 3882-3893
115. Patra M. Lateral pressure profiles in cholesterol-DPPC bilayers. Eur. Biophys. J. 35 (2005) 79-88
116. Sonne J., Hansen F.Y., and Peters G.H. Methodological problems in pressure profile calculations for lipid bilayers. J. Chem. Phys. 122 (2005) 124903
117. S. Ollila, Lateral pressure profile calculations of lipid membranes from atomic scale molecular dynamics simulations, Master's thesis, Helsinki Univ. Tech. (2006).
118. Sukharev S., Durell S.R., and Guy H.R. Structural models of the MscL gating mechanism. Biophys. J. 81 (2001) 917-936
119. Sukharev S.I., Sigurdson W.J., Kung C., and Sachs F. Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J. Gen. Physiol. 113 (1999) 525-540
120. Lewis J.R., and Cafiso D.S. Correlation of the free energy of a channel-forming voltage-gated peptide and the spontaneous curvature of bilayer lipids. Biochemistry 38 (1999) 5932-5938
121. Allende D., Simon S.A., and McIntosh T.J. Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 88 (2005) 1828-1837
122. Safran S. Statistical Thermodynamics of Surfaces, Interfaces and Membranes (1994), Addison-Wesley, New York
123. Murtola T., Falck E., Patra M., Karttunen M., and Vattulainen I. Coarse-grained model for phospholipid/cholesterol bilayer. J. Chem. Phys. 121 (2004) 9156-9165
124. Murtola T., Falck E., Karttunen M., and Vattulainen I. Coarse-grained model for phospholipid/cholesterol bilayer employing inverse Monte Carlo with thermodynamic constraints. J. Chem. Phys. 126 (2007) 075101
125. Khelashvili G.A., Pandit S.A., and Scott H.L. Self-consistent mean field model based on molecular dynamics: application to lipid-cholesterol bilayers. J. Chem. Phys. 123 (2005) 34910
126. Pandit S.A., Chiu S.W., Jakobsson E., Grama A., and Scott H.L. Cholesterol surrogates: a comparison of cholesterol and 16:0 ceramide in POPC bilayers. Biophys. J. 92 (2007) 920-927
127. Marrink S.J., de Vries A.H., and Mark A.E. Coarse grained model for semiquantitative lipid simulations. J. Phys. Chem. B 108 (2004) 750-760
128. Marrink S.J., de Vries A.H., Harroun T.A., Katsaras J., and Wassall S.R. Cholesterol shows preference for the interior of polyunsaturated lipid membranes. J. Am. Chem. Soc. 130 (2007) 10-11
129. Faller R., and Marrink S.J. Simulation of domain formation in DLPC-DSPC bilayers. Langmuir 20 (2004) 7686-7693
130. Marrink S.J., Risselada J., and Mark A.E. Simulation of gel phase formation and melting in lipid bilayers using a coarse grained model. Chem. Phys. Lipids 135 (2005) 223-244
131. Baoukina S., Monticelli L., Marrink S.J., and Tieleman D.P. Pressure-area isotherm of a lipid monolayer from molecular dynamics simulations. Langmuir 23 (2007) 12617-12623
132. Gurtovenko A.A., and Vattulainen I. Lipid transmembrane asymmetry and intrinsic membrane potential: two sides of the same coin. J. Am. Chem. Soc. 129 (2007) 5358
133. Róg T., Vattulainen I., and Karttunen M. Modelling glycolipids: take one. Cell. Mol. Biol. Lett. 10 (2005) 625-630
134. Róg T., Vattulainen I., Bunker A., and Karttunen M. Glycolipid membranes through atomistic simulations: effect of glucose and galactose head groups on lipid bilayer properties. J. Phys. Chem. B 111 (2007) 10146-10154