Thermodynamics of lipid interactions in complex bilayers

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 1, 2009, Pages 72-85

  Almeida, Paulo F F ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Condensed complexes; Lipid lipid interactions; Liquid ordered phase; Phase separation; Rafts; Transbilayer coupling

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CHOLESTEROL; DIOLEOYLPHOSPHATIDYLCHOLINE; LIPID; LONG CHAIN FATTY ACID; PHOSPHATIDYLSERINE; PHOSPHOLIPID; SPHINGOMYELIN;

ENTHALPY; FLUORESCENCE MICROSCOPY; LAMELLAR BODY; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE; PHASE SEPARATION; PHASE TRANSITION; PHOSPHOLIPID MEMBRANE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; REVIEW; TEMPERATURE; THERMODYNAMICS;

ANIMALS; HUMANS; LIPID BILAYERS; LIPID METABOLISM; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; THERMODYNAMICS;

EID: 58149178875     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.08.007     Document Type: Review

References (110)

1. Schimshick E.J., and McConnell H.M. Lateral phase separation in phospholipid membranes. Biochemistry 12 (1973) 2351-2360
2. Schimshick E.J., and McConnell H.M. Lateral phase separation in binary mixtures of cholesterol and phospholipids. Biochem. Biophys. Res. Comm. 53 (1973) 446-451
3. Wu S.H., and McConnell H.M. Phase separations in phospholipid membranes. Biochemistry 14 (1975) 847-854
4. Mabrey S., and Sturtevant J. Investigation of phase transitions of lipids and lipid mixtures by high sensitivity differential scanning calorimetry. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 3862-3866
5. Ipsen J.H., Karlstroem G., Mouritsen O.G., Wennerstroem H., and Zuckermann M.J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta 905 (1987) 162-172
6. Mabrey S., Mateo P.L., and Sturtevant J.M. High-sensitivity scanning calorimetric study of mixtures of cholesterol with dimyristoyl- and dipalmitoylphosphatidylcholines. Biochemistry 17 (1978) 2464-2468
7. Ipsen J.H., Mouritsen O.G., and Zuckermann M.J. Theory of thermal anomalies in the specific heat of lipid bilayers containing cholesterol. Biophys. J. 56 (1989) 661-667
8. Vist M.R., and Davis J.H. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: deuterium nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 29 (1990) 451-464
9. 2H-Nuclear Magnetic Resonance study. Biochemistry 29 (1990) 10676-10684
10. Sankaram M.B., and Thompson T.E. Interaction of cholesterol with various glycero- phospholipids and sphingomyelin. Biochemistry 29 (1990) 10670-10675
11. Sankaram M.B., and Thompson T.E. Cholesterol-induced fluid-phase immiscibility in membranes. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 8686-8690
12. Almeida P.F.F., Vaz W.L.C., and Thompson T.E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry 31 (1992) 6739-6747
13. Almeida P.F.F., Vaz W.L.C., and Thompson T.E. Percolation and diffusion in three-component lipid bilayers: effect of cholesterol on an equimolar mixture of two phosphatidylcholines. Biophys. J. 64 (1993) 399-412
14. McMullen T.P.W., Lewis R.N.A.H., and 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
15. Collado M.I., Goñi F.M., Alonso A., and Marsh D. Domain formation in sphingomyelin/cholesterol mixed membranes studied by spin-label electron spin resonance spectroscopy. Biochemistry 44 (2005) 4911-4918
16. Radhakrishnan A., and McConnell H.M. Condensed complexes of cholesterol and phospholipids. Biophys. J. 77 (1999) 1507-1517
17. Radhakrishnan A., and McConnell H.M. Chemical activity of cholesterol in membranes. Biochemistry 39 (2000) 8119-8124
18. McConnell H.M., and Vrljic M. Liquid-liquid immiscibility in membranes. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 469-492
19. Anderson T.G., and McConnell H.M. Condensed complexes and the calorimetry of cholesterol-phospholipid bilayers. Biophys. J. 81 (2001) 2774-2785
20. McConnell H.M., and Radhakrishnan A. Condensed complexes of cholesterol and phospholipids. Biochim. Biophys. Acta 1610 (2003) 159-173
21. Chong P.L.-G. Evidence for regular distribution of sterols in liquid crystalline phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10069-10073
22. Liu F., Sugar I.P., and Chong P.L.-G. Cholesterol and ergosterol supperlattices in three- component liquid crystalline lipid bilayers as revealed by dehyroergosterol fluorescence. Biophys. J. 72 (1997) 2243-2254
23. Huang J., and Feigenson G.W. A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys. J. 76 (1999) 2142-2157
24. Alecio M.R., Golan D.E., Veatch W.R., and Rando R.R. Use of a fluorescent cholesterol derivative to measure lateral mobility of cholesterol in membranes. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 5171-5174
25. Shin Y.-K., and Freed J.H. Dynamic imaging of lateral diffusion by electron spin resonance and study of rotational dynamics in model membranes: effect of cholesterol. Biophys. J. 55 (1989) 537-550
26. Orädd G., Lindblom G., and Westerman P.W. Lateral diffusion of cholesterol and dimyristoylphosphatidylcholine in a lipid bilayer measured by pulsed field gradient NMR spectroscopy. Biophys. J. 83 (2002) 2702-2704
27. Turner M.S., Sens P., and Socci N.D. Noneequilibrium raftlike domains under continuous recycling. Phys. Rev. Lett. 95 (2005) 168301
28. Gómez J., Sagués F., and Reigada R. Actively maintained lipid nanodomains in biomembranes. Phys. Rev. E 77 (2008) 021907
29. Almeida P.F.F., Pokorny A., and Hinderliter A. Thermodynamics of membrane domains. Biochim. Biophys. Acta 1720 (2005) 1-13
30. Jerala R., Almeida P.F.F., and Biltonen R.L. Simulation of the gel-fluid transition in a membrane composed of lipids with two connected acyl chains: application of a dimer-move step. Biophys. J. 71 (1996) 609-615
31. Hill T.L. An Introduction to Statistical Thermodynamics (1985), Dover, New York
32. Sugar I.P., Thompson T.E., and Biltonen R.L. Monte Carlo simulation of two-component bilayers: DMPC/DSPC mixtures. Biophys. J. 76 (1999) 2099-2100
33. Hinderliter A., Almeida P.F.F., Creutz C.E., and Biltonen R.L. Domain formation in a fluid mixed lipid bilayer modulated through binding of the C2 protein motif. Biochemistry 40 (2001) 4181-4191
34. Hinderliter A., Biltonen R.L., and Almeida P.F.F. Lipid modulation of protein-induced membranes domains as a mechanism for controlling signal transduction. Biochemistry 43 (2004) 7102-7110
35. Sugar I.P., Biltonen R.L., and Mitchard N. Monte Carlo simulation of membranes: phase transition of small unilamellar dipalmitoylphosphatidylcholine vesicles. Meth. Enzymol. 240 (1994) 569-593
36. Vigmond S.J., Dewa T., and Regen S.L. Nearest-neighbor recognition within a mixed phospholipid membrane: evidence for lateral heterogeneity. J. Amer. Chem. Soc. 117 (1995) 7838-7839
37. Dewa T., Vigmond S.J., and Regen S.L. Lateral heterogeneity in fluid bilayers composed of saturated and unsaturated phospholipids. J. Amer. Chem. Soc. 118 (1996) 3435-3440
38. Zhang J., Jing B., Tokutake N., and Regen S.L. Transbilayer complementarity of phospholipids. A look beyond the fluid mosaic model. J. Am. Chem. Soc. 126 (2004) 10856-10857
39. Sugahara M., Uragami M., and Regen S.L. Selective sterol-phospholipid associations in fluid bilayers. J. Am. Chem. Soc. 124 (2002) 4253-4256
40. Sugahara M., Uragami M., and Regen S.L. Selective association of cholesterol with long-chain phospholipids in liquid-ordered bilayers: support for the existence of lipid rafts. J. Am. Chem. Soc. 125 (2003) 13040-13041
41. Tokutake N., Jing B., and Regen S.L. Detection of unusual lipid mixing in cholesterol-rich phospholipid bilayers: the long and the short of it. J. Am. Chem. Soc. 125 (2003) 8994-8995
42. Krisovitch S.M., and Regen S.L. Nearest-neighbor recognition in phospholipid membranes: a molecular-level approach to the study of membrane suprastructure. J. Am. Chem. Soc. 114 (1992) 9828-9835
43. Davidson S.M.K., and Regen S.L. Nearest-neighbor recognition in phospholipid membranes. Chem. Rev. 97 (1997) 1269-1279
44. Huang J., Swanson J.E., Dibble A.R.G., Hinderliter A.K., and Feigenson G.W. Nonideal mixing of phosphatidylserine and phosphatidylcholine in the fluid lamellar phase. Biophys. J. 64 (1993) 413-425
45. Parsegian V.A. The cows or the fence?. Mol. Membr. Biol. 12 (1995) 5-7
46. Frazier M.L., Wright J.R., Pokorny A., and Almeida P.F.F. Investigation of domain formation in sphingomyelin/cholesterol/POPC mixtures by fluorescence resonance energy transfer and Monte Carlo simulations. Biophys. J. 92 (2007) 2422-2433
47. Zhang J., Cao H., Jing B., Almeida P.F., and Regen S.L. Cholesterol-phospholipid association in fluid bilayers: a thermodynamic analysis from nearest-neighbor recognition measurements. Biophys. J. 91 (2006) 1402-1406
48. Tsamaloukas A., Szadkowska H., and Heerklotz H. Nonideal mixing in multicomponent lipid/detergent systems. J. Phys. Condens. Matter 18 (2006) S1125-S1138
49. von Dreele P.H. Estimation of lateral species separation from phase transitions in nonideal two-dimensional. Biochemistry 19 (1980) 88-94
50. Brumbaugh E.E., Johnson M.L., and Huang C. Non-linear least squares analysis of phase diagrams fro non-ideal binary mixtures of phospholipids. Chem. Phys. Lipids 52 (1990) 69-78
51. Freire E., and Snyder B. Estimation of the lateral distribution of molecules in two-component lipid bilayers, lipid mixtures. Biochemistry 17 (1978) 3939-3934
52. Johann C., Garidel P., Mennicke L., and Blume A. New approaches to the simulation of heat capacity curves and phase diagrams of pseudobinary phospholipid mixtures. Biophys. J. 71 (1996) 3215-3228
53. Garidel P., Johann C., and Blume A. Nonideal mixing and phase separation in phosphatidylcholine-phosphatidic acid mixtures as a function of acyl chain length and pH. Biophys. J. 72 (1997) 2196-2210
54. Garidel P., Johann C., Mennicke L., and Blume A. The mixing behavior of pseudobinary phosphatidylcholine mixtures as a function of pH and chain length. Eur. Biophys. J. 26 (1997) 447-459
55. Garidel P., and Blume A. Miscibility of phospholipids with identical headgroups and acyl chain lengths differing by two methylene units: effects of headgroup structure and headgroup charge. Biochim. Biophys. Acta 1371 (1998) 83-95
56. Garidel P., and Blume A. Miscibility of phosphatidylethanolamine-phosphatidylglycerol mixtures as a function of pH and acyl chain length. Eur. Biophys. J. 28 (2000) 629-638
57. Heimburg T., and Biltonen R.L. A Monte Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. Biophys. J. 70 (1996) 84-96
58. Knoll W., Ibel K., and Sackmann E. Small-angle neutron scattering study of lipid phase diagrams by the contrast variation method. Biochemistry 20 (1981) 6379-6383
59. Risbo J., Sperotto M.M., and Mouritsen O.G. Theory of phase equilibria and critical mixing points in binary lipid bilayers. J. Chem. Phys. 103 (1995) 3643-3656
60. Lehtonen J.Y., Holopainen J.M., and Kinnunen P.K. Evidence for the formation of microdomains in liquid crystalline large unilamellar vesicles caused by hydrophobic mismatch of the constituent phospholipids. Biophys. J. 70 (1996) 1753-1760
61. Rodŕi{dotless}guez Y., Mezei M., and Osman R. Association free energy of dipalmitoylphosphatidylserines in a mixed dipalmitoylphosphatidylcholine membrane. Biophys. J. 92 (2007) 3071-3080
62. Mouritsen O.G., and Bloom M. Mattress model of lipid protein interactions in membranes. Biophys. J. 46 (1984) 141-153
63. Fattal D.R., and Ben-Shaul A. A molecular model for lipid-protein interaction in membranes: The role of hydrophobic mismatch. Biophys. J. 65 (1993) 1795-1809
64. 1H-NMR study of the effects of metal ions, cholesterol and n-alkanes on phase transitions in the inner and outer monolayers of phospholipid vesicular membranes. Biochim. Biophys. Acta 507 (1978) 242-261
65. Schmidt C.F., Barenholz Y., Huang C., and Thompson T.E. Monolayer coupling in sphingomyelin bilayer systems. Nature 271 (1978) 775-777
66. Sillerud L.O., and Barnett R.E. Lack of transbilayer copling in phase transitions of phosphatidylcholine vesicles. Biochemistry 21 (1982) 1756-1760
67. Almeida P.F.F., Vaz W.L.C., and Thompson T.E. Lateral diffusion and percolation in two-phase, two-component lipid bilayers. Topology of the solid phase domains in-plane and across the lipid bilayer. Biochemistry 31 (1992) 7198-7210
68. Vaz W.L.C., Hallmann D., Clegg R.M., Gambacorta A., and De Rosa M. A comparison of the translational diffusion of a normal and a membrane-spanning lipid in L alpha phase 1-palmitoyl-2-oleoylphosphatidylcholine bilayers. Eur. Biophys. J. 12 (1985) 19-24
69. Korlach J., Schwille P., Webb W.W., and Feigenson G.W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 8461-8466
70. Zhang J., Jing B., Janout V., and Regen S.L. Detecting cross talk between two halves of a phospholipid bilayer. Langmuir 23 (2007) 8709-8712
71. Stevens M.J. Complementary matching in domain formation within lipid bilayers. J. Amer. Chem. Soc. 127 (2005) 15330-15331
72. Zhang J., Jing B., Tokutake N., and Regen S.L. Transbilayer complementarity of phospholipids in cholesterol-rich membranes. Biochemistry 44 (2005) 3598-3603
73. Collins M.C., and Keller S.L. Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 124-128
74. Collins M.C. Interleaflet coupling mechanisms in bilayers of lipid and cholesterol. Biophys. J. 94 (2008) L32-L34
75. 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
76. Putzel G.G., and Schick M. Phase behavior of a model bilayer membrane with coupled leaves. Biophys. J. 94 (2008) 869-877
77. 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
78. McMullen T.P.W., and McElhaney R.N. New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry. Biochim. Biophys. Acta 1234 (1995) 90-98
79. Veatch S.L., and Keller S.L. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta 1746 (2005) 172-185
80. Veatch S.L., and Keller S.L. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85 (2003) 3074-3083
81. Feigenson G.W., and Buboltz J.T. Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/ cholesterol: nanoscopic domain formation driven by cholesterol. Biophys. J. 80 (2001) 2775-2788
82. Findlay A. The Phase Rule. 9th ed. (1951), Dover, New York 8
83. Hill T.L. Thermodynamics of small systems (Parts I and II) (1994), Dover, New York
84. Mateo R.C., Acuña A.U., and Brochon J.-C. Liquid-crystalline phases of cholesterol/lipid bilayers as revealed by the fluorescence of trans-parinaric acid. Biophys. J. 68 (1995) 978-987
85. de Almeida R.F.M., Fedorov A., and Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85 (2003) 2406-2416
86. de Almeida R.F.M., Loura L.M.S., Fedorov A., and Prieto M. Lipid rafts have different sizes depending on membrane composition: a time-resolved fluorescence resonance energy transfer study. J. Mol. Biol. 346 (2005) 1109-1120
87. Veatch S.L., and Keller S.L. Miscibility phase diagrams of giant vesicles containing sphingomyelin. Phys. Rev. Lett. 94 (2005) 148101
88. Henriksen J., Rowat J.A.C., Brief E., Hsueh Y.W., Thewalt J.L., Zuckermann M.J., and Ipsen J.H. Universal behavior of membranes with sterols. Biophys. J. 90 (2006) 1639-1649
89. Pokorny A., Yandek L.E., Elegbede A.I., Hinderliter A., and Almeida P.F.F. Temperature and composition dependence of the interaction of δ-lysin with ternary mixtures of sphingomyelin/cholesterol/POPC. Biophys. J. 91 (2006) 2184-2197
90. Heerklotz H., and Tsamaloukas A. Gradual change or phase transition: characterizing fluid lipid-cholesterol membranes on the basis of thermal volume changes. Biophys. J. 91 (2006) 600-607
91. Zhao J., Wu J., Heberle F.A., Mills T.T., Klawitter P., Huang G., Costanza G., and Feigenson G.W. Phase studies of model biomembranes: complex behavior of DSPC/DOPC/cholesterol. Biochim. Biophys. Acta 1768 (2007) 2764-2776
92. Zhao J., Wu J., Shao H., Kong F., Jain N., Hunt G., and Feigenson G. Phase studies of model biomembranes: macroscopic coexistence of Lα+Lβ, with light-induced coexistence of Lα+Lo phases. Biochim. Biophys. Acta 1768 (2007) 2777-2786
93. Silvius J.R. Fluorescence energy transfer reveals microdomain formation at physiological temperatures in lipid mixtures modeling the outer leaflet of the plasma membrane. Biophys. J. 85 (2003) 1034-1045
94. McConnell H. Complexes in ternary cholesterol-phospholipid mixtures. Biophys. J. 88 (2005) L23-L25
95. Elliott R., Szleifer I., and Schick M. Phase diagram of a ternary mixture of cholesterol and saturated and unsaturated lipids calculated from a microscopic model. Phys. Rev. Lett. 96 (2006) 098101
96. Silvius J.R. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta 1610 (2003) 174-183
97. Harroun T.A., Katsaras J., and Wassall S.R. Cholesterol hydroxyl group is found to reside in the center of a polyunsaturated lipid membrane. Biochemistry 45 (2006) 1227-1233
98. Feller S.E., and Gawrisch K. Properties of docosahexanoic-acid-containing lipids and their influence on the function of rhodopsin. Curr. Opin. Struct. Biol. 15 (2005) 416-422
99. Zhang Z., Lu L., and Berkowitz M.L. Energetics of cholesterol transfer between lipid bilayers. J. Phys. Chem. B. 112 (2008) 3807-3811
100. Ohvo-Rekilä H., Ramstedt B., Leppimäki P., and Slotte J.P. Cholesterol interaction with phospholipids in membranes. Prog. Lipid Res. 41 (2002) 66-97
101. McMullen T.P.W., Lewis R.N.A.H., and McElhaney R.N. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Curr. Opin. Colloid Interface Sci. 8 (2004) 459-468
102. Niu S.-L., and 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
103. Tsamaloukas A., Szadkowska H., and Heerklotz H. Thermodynamic comparison of the interactions of cholesterol with unsaturated phospholipid and sphingomyelins. Biophys. J. 90 (2006) 4479-4487
104. 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
105. 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
106. Veatch S.L., Polozov I.V., Gawrisch K., and Keller S.L. Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 86 (2004) 2910-2922
107. Radhakrishnan A., and McConnell H. Condensed complexes in vesicles containing cholesterol and phospholipids. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 12662-12666
108. McConnell H., and Radhakrishnan A. Theory of the deuterium NMR of sterol-phospholipid membranes. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1184-1189
109. Barenholz Y., and Thompson T.E. Sphingomyelins in bilayers and biological membranes. Biochim. Biophys. Acta 604 (1980) 129-158
110. Reigada R., Buceta J., Gómez J., Sagués F., and Lindenberg K. Phase separation in three-component lipid membranes: from Monte Carlo simulations to Ginzburg-Landau equations. J. Chem. Phys. 128 (2008) 025102