Transmembrane helices can induce domain formation in crowded model membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 984-994

  Domański, Jan ^a   Marrink, Siewert J ^a   Schäfer, Lars V ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Coarse grained; Crowding; Lipid raft; Membrane protein; Molecular dynamics

Indexed keywords

BACTERIORHODOPSIN; CHOLESTEROL; DIPALMITOYLPHOSPHATIDYLCHOLINE; GLYCEROPHOSPHOLIPID; MEMBRANE PROTEIN; PALMITOYLLINOLEOYLPHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIFFUSION; HYDROPHOBICITY; LIPID ANALYSIS; LIPID COMPOSITION; MEMBRANE COMPONENT; MEMBRANE FORMATION; MEMBRANE MODEL; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL;

BACTERIORHODOPSINS; CELL MEMBRANE; CHOLESTEROL; DIFFUSION; DIMYRISTOYLPHOSPHATIDYLCHOLINE; FATTY ACIDS, UNSATURATED; LIPID BILAYERS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; PHASE TRANSITION; PHOSPHATIDYLCHOLINES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84857648415     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.08.021     Document Type: Article

References (105)

1. S.J. Singer, and G.L. Nicholson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
2. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
3. J.U. Bowie Solving the membrane protein folding problem Nature 438 2005 581 589
4. D.M. Engelman Membranes are more mosaic than fluid Nature 438 2005 578 580
5. L.H. Chamberlain, R.D. Burgoyne, and G.W. Gould SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis Proc. Natl. Acad. Sci. U. S. A. 98 2001 5619 5624
6. T. Lang, D. Bruns, D. Wenzel, D. Riedel, P. Holroyd, C. Thiele, and R. Jahn SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis EMBO J. 20 2001 2202 2213
7. M.S. Bretscher, and S. Munro Cholesterol and the Golgi apparatus Science 261 1993 1280 1281
8. M. Kawabuchi, Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases Nature 404 2000 999 1003
9. S. Moffett, D.A. Brown, and M.E. Linder Lipid-dependent targeting of G proteins into rafts J. Biol. Chem. 275 2000 2191 2198
10. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
11. C. Eggeling, C. Ringemann, R. Medda, G. Schwarzmann, K. Sandhoff, S. Polyakova, V.N. Belov, B. Hein, C. von Middendorff, A. Schonle, and S.W. Hell Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 2009 1159 1162
12. J.F. Hancock Lipid rafts: contentious only from simplistic standpoints Nat. Rev. Mol. Cell Biol. 7 2006 456 462
13. M. Edidin The state of lipid rafts: from model membranes to cells Annu. Rev. Biophys. Biomol. Struct. 32 2003 257 283
14. K. Jacobson, O.G. Mouritsen, and R.G.W. Anderson Lipid rafts: at a crossroad between cell biology and physics Nat. Cell Biol. 9 2007 7 14
15. A.V. Samsonov, I. Mihalyov, and F.S. Cohen Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes Biophys. J. 81 2001 1486 1500
16. S.L. Veatch, and S.L. Keller Organization in lipid membranes containing cholesterol Phys. Rev. Lett. 89 2002 268101
17. T. Baumgart, S.T. Hess, and W.W. Webb Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 425 2003 821 824
18. N. Kahya, D. Scherfeld, K. Bacia, B. Poolman, and P. Schwille Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy J. Biol. Chem. 278 2003 28109 28115
19. S.L. Veatch, and S.L. Keller Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophys. J. 85 2003 3074 3083
20. H.-J. Kaiser, D. Lingwood, I. Levental, J.L. Sampaio, L. Kalvodova, L. Rajendran, and K. Simons Order of lipid phases in model and plasma membranes Proc. Natl. Acad. Sci. U. S. A. 106 2009 16645 16650
21. D. Lingwood, J. Ries, P. Schwille, and K. Simons Plasma membranes are poised for activation of raft phase coalescence at physiological temperature Proc. Natl. Acad. Sci. U. S. A. 105 2008 10005 10010
22. T. Baumgart, A.T. Hammond, P. Sengupta, S.T. Hess, D.A. Holowka, B.A. Baird, and W.W. Webb Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles Proc. Natl. Acad. Sci. U. S. A. 104 2007 3165 3170
23. S. Munro Lipid rafts: elusive or illusive? Cell 115 2003 377 388
24. G.W. Feigenson Phase boundaries and biological membranes Annu. Rev. Biophys. Biomol. Struct. 36 2007 63 77
25. E. London How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells Biochim. Biophys. Acta 1746 2005 203 220
26. S.L. Veatch, P. Cicuta, P. Sengupta, A. Honerkamp-Smith, D. Holowka, and B. Baird Critical fluctuations in plasma membrane vesicles ACS Chem. Biol. 3 2008 287 293
27. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
28. T.A. Ryan, J. Myers, D. Holowka, B. Baird, and W.W. Webb Molecular crowding on the cell surface Science 239 1988 61 64
29. G. Guidotti Membrane proteins Annu. Rev. Biochem. 41 1972 731 752
30. R.G.W. Anderson, and K. Jacobson Cell biology - a role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains Science 296 2002 1821 1825
31. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
32. W. Helfrich Elastic properties of lipid bilayers-theory and possible experiments Z. Naturforsch. C 28 1973 693 703
33. O.G. Mouritsen, and M. Bloom Mattress model of lipid-protein interactions in membranes Biophys. J. 46 1984 141 153
34. S.J. Marrink, A.H. de Vries, and D.P. Tieleman Lipids on the move: simulations of membrane pores, domains, stalks and curves BBA Biomembr. 1788 2009 149 168
35. G.A. Voth Coarse-Graining of Condensed Phase and Biomolecular Systems 2009 CRC Press/ Taylor and Francis Boca Raton, FL
36. E. Psachoulia, D.P. Marshall, and M.S.P. Sansom Molecular dynamics simulations of the dimerization of transmembrane alpha-helices Acc. Chem. Res. 43 2010 388 396
37. X. Periole, T. Huber, S.J. Marrink, and T.P. Sakmar G protein-coupled receptors self-assemble in dynamics simulations of model bilayers J. Am. Chem. Soc. 129 2007 10126 10132
38. U. Schmidt, G. Guigas, and M. Weiss Cluster formation of transmembrane proteins due to hydrophobic mismatching Phys. Rev. Lett. 101 2008 128104
39. B.J. Reynwar, and M. Deserno Membrane composition-mediated protein-protein interactions Biointerphases 3 2008 FA117 FA124
40. F.J.-M. de Meyer, M. Venturoli, and B. Smit Molecular simulations of lipid-mediated protein-protein interactions Biophys. J. 95 2008 1851 1865
41. D. Sengupta, and S.J. Marrink Lipid-mediated interactions tune the association of glycophorin A helix and its disruptive mutants in membranes Phys. Chem. Chem. Phys. 12 2010 12987 12996
42. D. Morozova, G. Guigas, and M. Weiss Dynamic structure formation of peripheral membrane proteins PLoS Comput. Biol. 7 2011 e1002067
43. B. West, F.L.H. Brown, and F. Schmid Membrane-protein interactions in a generic coarse-grained model for lipid bilayers Biophys. J. 96 2009 101 115
44. H.J. Risselada, and S.J. Marrink The molecular face of lipid rafts in model membranes Proc. Natl. Acad. Sci. U. S. A. 105 2008 17367 17372
45. S.J. Marrink, H.J. Risselada, S. Yefimov, D.P. Tieleman, and A.H. de Vries The MARTINI force field: coarse grained model for biomolecular simulations J. Phys. Chem. B 111 2007 7812 7824
46. L. Monticelli, S.K. Kandasamy, X. Periole, R.G. Larson, D.P. Tieleman, and S.J. Marrink The MARTINI coarse-grained force field: extension to proteins J. Chem. Theory Comput. 4 2008 819 834
47. S.L. Veatch, I.V. Polozov, K. Gawrisch, and S.L. Keller Liquid domains in vesicles investigated by NMR and fluorescence microscopy Biophys. J. 86 2004 2910 2922
48. L.V. Schäfer, D.H. de Jong, A. Holt, A.J. Rzepiela, A.H. de Vries, B. Poolman, J.A. Killian, and S.J. Marrink Lipid packing drives the segregation of transmembrane helices into disordered lipid domains in model membranes Proc. Natl. Acad. Sci. U. S. A. 108 2011 1343 1348
49. L.V. Schäfer, and S.J. Marrink Partitioning of lipids at domain boundaries in model membranes Biophys. J. 99 2010 L91 L93
50. A. Tian, C. Johnson, W. Wang, and T. Baumgart Line tension at fluid membrane domain boundaries measured by micropipette aspiration Phys. Rev. Lett. 98 2007 208102
51. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
52. S.J. Marrink, H.J. Risselada, and A.E. Mark Simulation of gel phase formation and melting in lipid bilayers using a coarse grained model Chem. Phys. Lipids 135 2005 223 244
53. T. Schneider, and E. Stoll Molecular-dynamics study of a three-dimensional one-component model for distortive phase transitions Phys. Rev. B 17 1978 1302 1322
54. G. Bussi, and M. Parrinello Stochastic thermostats: comparison of local and global schemes Comput. Phys. Commun. 179 2008 26 29
55. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through stochastic velocity-rescaling J. Chem. Phys. 126 2007 014101
56. S.E. Feller, K. Gawrisch, and A.D. MacKerell Polyunsaturated fatty acids in lipid bilayers: intrinsic and environmental contributions to their unique physical properties J. Am. Chem. Soc. 124 2002 318 326
57. S.J. Marrink, A.H. de Vries, T.A. Harroun, J. Katsaras, and S.R. Wassall Cholesterol shows preference for the interior of polyunsaturated lipid membranes J. Am. Chem. Soc. 130 2008 10 11
58. N. Kucerka, D. Marquardt, T.A. Harroun, M.-P. Nieh, S.R. Wassall, D.H.d. Jong, L.V. Schäfer, S.J. Marrink, and J. Katsaras Cholesterol in bilayers with PUFA chains: doping with DMPC or POPC results in sterol reorientation and membrane-domain formation Biochemistry 49 2010 7485 7493
59. T. Apajalahti, P. Niemelä, P.N. Govindan, M. Miettinen, E.E. Salonen, S.J. Marrink, and I. Vattulainen Concerted diffusion of lipids in raft-like membranes Faraday Discuss. 144 2010 411 430
60. J.D. Perlmutter, and J.N. Sachs Interleaflet interaction and asymmetry in phase separated lipid bilayers: molecular dynamics simulations J. Am. Chem. Soc. 133 2011 6563 6577
61. H. Luecke, B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi Structure of bacteriorhodopsin at 1.55 A resolution J. Mol. Biol. 291 1999 899 911
62. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
63. X. Periole, M. Cavalli, S.J. Marrink, and M. Ceruso Combining an elastic network with a coarse-grained molecular force field: structure, dynamics and intermolecular recognition J. Chem. Theory Comput. 5 2009 2531 2543
64. B. Hess Determining the shear viscosity of model liquids from molecular dynamics simulations J. Chem. Phys. 116 2002 209 217
65. J.G. Kirkwood, and F.P. Buff The statistical mechanical theory of solutions J. Chem. Phys. 19 1951 774 779
66. S. Ramadurai, A. Holt, L.V. Schäfer, V.V. Krasnikov, D.T.S. Rijkers, S.J. Marrink, J.A. Killian, and B. Poolman Influence of hydrophobic mismatch and amino acid composition on the lateral diffusion of transmembrane peptides Biophys. J. 99 2010 1447 1454
67. D. Fritz, K. Koschke, V.A. Harmandaris, N.F.A. van der Vegt, and K. Kremer Multiscale modeling of soft matter: scaling of dynamics Phys. Chem. Chem. Phys. 13 2011 10412 10420
68. T.P.W. McMullen, and R.N. McElhaney Physical studies of cholesterol-phospholipid interactions Curr. Opin. Colloid Interface Sci. 1 1996 83 90
69. S.A. Akimov, P.I. Kuzmin, J. Zimmerberg, F.S. Cohen, and Y.A. Chizmadzhev An elastic theory for line tension at a boundary separating two lipid monolayer regions of different thickness J. Electroanal. Chem. 564 2004 13 18
70. C. Rosetti, and C. Pastorino Polyunsaturated and saturated phospholipids in mixed bilayers: a study from the molecular scale to the lateral lipid organization J. Phys. Chem. B 115 2010 1002 1013
71. T.K.M. Nyholm, S. Özdirekcan, and J.A. Killian How protein transmembrane segments sense the lipid environment Biochemistry 46 2007 1457 1465
72. D.H. de Jong, L.V. Schäfer, A.H. de Vries, S.J. Marrink, H.J.C. Berendsen, and H. Grubmüller Determining equilibrium constants for dimerization reactions from molecular dynamics simulations J. Comput. Chem. 32 2011 1919 1928
73. Y. Yano, and K. Matsuzaki Measurement of thermodynamic parameters for hydrophobic mismatch 1: self-association of a transmembrane helix Biochemistry 45 2006 3370 3378
74. M.J. Saxton, and K. Jacobson Single-particle tracking: applications to membrane dynamics Annu. Rev. Biophys. Biomol. Struct. 26 1997 373 399
75. A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R.S. Kasai, J. Kondo, and T. Fujiwara Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules Annu. Rev. Biophys. Biomol. Struct. 34 2005 351 378
76. M. Frick, K. Schmidt, and B.J. Nichols Modulation of lateral diffusion in the plasma membrane by protein density Curr. Biol. 17 2007 462 467
77. D.F. Kucik, E.L. Elson, and M.P. Sheetz Weak dependence of mobility of membrane protein aggregates on aggregate size supports a viscous model of retardation of diffusion Biophys. J. 76 1999 314 322
78. P.S. Niemelä, M.S. Miettinen, L. Monticelli, H. Hammaren, P. Bjelkmar, T. Murtola, E. Lindahl, and I. Vattulainen Membrane proteins diffuse as dynamic complexes with lipids J. Am. Chem. Soc. 132 2010 7574 7575
79. M.P. Sheetz Glycoprotein motility and dynamic domains in fluid plasma membranes Annu. Rev. Biophys. Biomol. Struct. 22 1993 417 431
80. M. Weiss, H. Hashimoto, and T. Nilsson Anomalous protein diffusion in living cells as seen by fluorescence correlation spectroscopy Biophys. J. 84 2003 4043 4052
81. K. Ritchie, X.Y. Shan, J. Kondo, K. Iwasawa, T. Fujiwara, and A. Kusumi Detection of non-Brownian diffusion in the cell membrane in single molecule tracking Biophys. J. 88 2005 2266 2277
82. M.J. Saxton Anomalous diffusion due to obstacles: a Monte Carlo study Biophys. J. 66 1994 394 401
83. T.J. Feder, I. Brust-Mascher, J.P. Slattery, B. Baird, and W.W. Webb Constrained diffusion or immobile fraction on cell surfaces: a new interpretation Biophys. J. 70 1996 2767 2773
84. M.J. Saxton Anomalous subdiffusion in fluorescence photobleaching recovery: a Monte Carlo study Biophys. J. 81 2001 2226 2240
85. R. Metzler, and J. Klafter The random walk's guide to anomalous diffusion: a fractional dynamics approach Phys. Rep. 339 2000 1 77
86. J. Szymanski, and M. Weiss Elucidating the origin of anomalous diffusion in crowded fluids Phys. Rev. Lett. 103 2009 038102
87. M. Magdziarz, A. Weron, K. Burnecki, and J. Klafter Fractional Brownian motion versus the continuous-time random walk: a simple test for subdiffusive dynamics Phys. Rev. Lett. 103 2009 180602
88. V. Tejedor, O. Bénichou, R. Voituriez, R. Jungmann, F. Simmel, C. Selhuber-Unkel, L.B. Oddershede, and R. Metzler Quantitative analysis of single particle trajectories: mean maximal excursion method Biophys. J. 98 2010 1364 1372
89. G. Guigas, and M. Weiss Sampling the cell with anomalous diffusion - the discovery of slowness Biophys. J. 94 2008 90 94
90. I. Golding, and E.C. Cox Physical nature of bacterial cytoplasm Phys. Rev. Lett. 96 2006 098102
91. E. Flenner, J. Das, M.C. Rheinstädter, and I. Kosztin Subdiffusion and lateral diffusion coefficient of lipid atoms and molecules in phospholipid bilayers Phys. Rev. E 79 2009 011907
92. U. Schmidt, and M. Weiss Anomalous diffusion of oligomerized transmembrane proteins J. Chem. Phys. 134 2011 165101
93. N. Kahya, D.A. Brown, and P. Schwille Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles Biochemistry 44 2005 7479 7489
94. B.A. Lewis, and D.M. Engelman Bacteriorhodopsin remains dispersed in fluid phospholipid bilayers over a wide range of bilayer thicknesses J. Mol. Biol. 166 1983 203 210
95. H. Shogomori, A.T. Hammond, A.G. Ostermeyer-Fay, D.J. Barr, G.W. Feigenson, E. London, and D.A. Brown Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells J. Biol. Chem. 280 2005 18931 18942
96. T.J. McIntosh, A. Vidal, and S.A. Simon Sorting of lipids and transmembrane peptides between detergent-soluble bilayers and detergent-resistant rafts Biophys. J. 85 2003 1656 1666
97. J. Nikolaus, S. Scolari, E. Bayraktarov, N. Jungnick, S. Engel, A.P. Plazzo, M. Stöckl, R. Volkmer, M. Veit, and A. Herrmann Hemagglutinin of influenza virus partitions into the nonraft domain of model membranes Biophys. J. 99 2010 489 498
98. M.E. Fastenberg, H. Shogomori, X. Xu, D.A. Brown, and E. London Exclusion of a transmembrane-type peptide from ordered-lipid domains (rafts) detected by fluorescence quenching: extension of quenching analysis to account for the effects of domain size and domain boundaries Biochemistry 42 2003 12376 12390
99. A. Vidal, and T.J. McIntosh Transbilayer peptide sorting between raft and nonraft bilayers: comparisons of detergent extraction and confocal microscopy Biophys. J. 89 2005 1102 1108
100. K. Bacia, C.G. Schuette, N. Kahya, R. Jahn, and P. Schwille SNAREs prefer liquid-disordered over "raft" (liquid-ordered) domains when reconstituted into giant unilamellar vesicles J. Biol. Chem. 279 2004 37951 37955
101. A.T. Hammond, F.A. Heberle, T. Baumgart, D. Holowka, B. Baird, and G.W. Feigenson Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes Proc. Natl. Acad. Sci. U. S. A. 102 2005 6320 6325
102. L. Kalvodova, N. Kahya, P. Schwille, R. Ehehalt, P. Verkade, D. Drechsel, and K. Simons Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids, and anionic phospholipids in vitro J. Biol. Chem. 280 2005 36815 36823
103. I. Levental, M. Grzybek, and K. Simons Greasing their way: lipid modifications determine protein association with membrane rafts Biochemistry 49 2010 6305 6316
104. I. Levental, D. Lingwood, M. Grzybek, U. Coskun, and K. Simons Palmitoylation regulates raft affinity for the majority of integral raft proteins Proc. Natl. Acad. Sci. U. S. A. 107 2010 22050 22054
105. D.L. Parton, J.W. Klingelhoefer, and M.S.P. Sansom Aggregation of model membrane proteins, modulated by hydrophobic mismatch, membrane curvature, and protein class Biophys. J. 101 2011 691 699