Membrane proteins, lipids and detergents: Not just a soap opera

Biochimica et Biophysica Acta - Biomembranes

Volumn 1666, Issue 1-2, 2004, Pages 105-117

  Seddon, Annela M ^a   Curnow, Paul ^a   Booth, Paula J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Bacteriorhodopsin; Detergent; Folding; Lipid; Membrane proteins; Reconstitution

Indexed keywords

DETERGENT; LIPID; LIPOSOME; MEMBRANE PROTEIN;

ADSORPTION; CRYSTALLIZATION; DIALYSIS; GEL CHROMATOGRAPHY; HYDROPHOBICITY; IN VITRO STUDY; ION EXCHANGE CHROMATOGRAPHY; MICELLE; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; REVIEW; SOLUBILIZATION;

EID: 7044272757     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2004.04.011     Document Type: Review

References (113)

1. E. Wallin, and G. von Heijne Genome-wide analysis of integral membrane proteins from eubacterial, archaean and eukaryotic organisms Protein Sci. 7 1998 1029 1038
2. D. Drew Assembly and overexpression of membrane proteins in Escheria coli Biochim. Biophys. Acta 1610 2003 3 10
3. M. Fukuda, Y. Eshdat, G. Tarone, and V.T. Marchesi Isolation characterisation of peptides derived from cytoplasmic segment of band-3, predominant intrinsic membrane protein of human erythrocyte J. Biol. Chem. 253 1978 2419 2428
4. M. le Maire, P. Champeil, and J.V. Møller Interaction of membrane proteins and lipids with solubilizing detergents Biochim. Biophys. Acta 1508 2000 86 111
5. R.M. Garavito, and S. Ferguson-Miller Detergents as tools in membrane biochemistry J. Biol. Chem. 276 2001 32403 32406
6. Y. Gohon, and J.-L. Popot Membrane protein-surfactant complexes Curr. Opin. Colloid Interface Sci. 8 2003 15 22
7. P.J. Booth, S.L. Flitsch, L.J. Stern, D.A. Greenhalgh, P.S. Kim, and H.G. Khorana Intermediates in the folding of the membrane protein bacteriorhodopsin Nat. Struct. Biol. 2 1995 139 143
8. P.J. Booth, and H. Paulsen Assembly of the light harvesting chloropyhyll a/b complex in vitro. Time resolved fluorescence measurements Biochemistry 35 1996 5103 5108
9. H. Paulsen, B. Finkenzeller, and N. Kühlein Pigments induce folding of light harvesting chlorophyll a/b binding protein Eur. J. Biochem. 215 1993 809 817
10. F.W. Lau, and J.U. Bowie A method for assessing the stability of a membrane protein Biochemistry 36 1997 5884 5892
11. M. Dong, L.G. Bagetto, P. Falson, M. Le Maire, and F. Penin Complete removal and exchange of sodium dodecyl sulfate bound to soluble and membrane proteins and restoration of their activities, using ceramic hydroxyapatite chromatography Anal. Biochem. 247 1997 333 341
12. D. Wessel, and U.I. Flügge A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Anal. Biochem. 138 1984 141 143
13. W.H. Konigsberg, and L. Henderson Removal of sodium dodecyl sulfate from proteins by ion pair extraction Methods Enzymol. 91 1983 254 259
14. D.K. Trask, J.A. DiDonato, and M.T. Muller Rapid detection and isolation of covalent DNA/protein complexes: application to topoisomerase I and II EMBO J. 3 1984 671 676
15. K. Suzuki, and H. Kawasaki Separation of peptides dissolved in a sodium dodecyl sulfate solution by reversed phase liquid chromatography-removal of sodium dodecyl sulfate from peptides using an ion exchange precolumn Anal. Biochem. 186 1990 292 298
16. 2+-ATPase from sarcoplasmic reticulum J. Biol. Chem. 264 1989 4907 4915
17. T. Van Aken, S. Foxall-Van Aken, S. Castleman, and S. Ferguson-Miller Alkyk glycoside detergents-synthesis and applications to the study of membrane proteins Methods Enzymol. 125 1986 27 35
18. K.G. Fleming, A.I. Ackerman, and D.M. Engelman The effect of point mutations on the free energy of transmembrane alpha-helix dimerization J. Mol. Biol. 272 1997 266 275
19. J. Deisenhofer, O. Epp, R.H. Miki, R. Huber, and H. Michel Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3-Å resolution Nature 318 1985 618 624
20. C. Sardet, A. Tardieu, and V. Luzzati Shape and size of bovine rhodopsin-small angle X-ray scattering study of a rhodopsin detergent complex J. Mol. Biol. 105 1976 383 407
21. S.M. Bhairi, A guide to the properties and uses of detergents in biological systems, 1997 Calbiochem-Novabiochem Corporation.
22. J.-L. Rigaud, G. Mosser, J.-J. Lacapere, A. Olofsson, D. Levy, and J.-L. Ranck Bio-Beads: an efficient strategy for two-dimensional crystallization of membrane proteins J. Struct. Biol. 118 1997 226 235
23. S.M. Yu, D.T. McQuade, M.A. Quinn, C.P. Hackenberger, M.P. Krebs, A.S. Polans, and S.H. Gellman An improved tripod amphiphile for membrane protein solubilization Protein Sci. 9 2000 2518 2527
24. D.T. McQuade, M.A. Quinn, S.M. Yu, A.S. Polans, M.P. Krebs, and Samuel H. Gellman Rigid amphiphiles for membrane protein manipulation Angew. Chem., Int. Ed. Engl. 39 2000 758 761
25. C. Tribet, R. Audebert, and J. Popot Amphipols: polymers that keep membrane proteins in aqueous solution Proc. Natl. Acad. Sci. U. S. A. 93 1996 15047 15050
26. P.J. Reeves, J. Hwa, and H.G. Khorana Structure and function in rhodopsin: kinetic studies of retinal binding to purified opsin mutants in defined phospholipid detergent mixtures serve as probes of the retinal binding pocket Proc. Natl. Acad. Sci. U. S. A. 96 1999 1927 1931
27. E. London, and H.G. Khorana Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures J. Biol. Chem. 257 1982 7003 7011
28. M.L. Riley, B.A. Wallace, S.L. Flitsch, and P.J. Booth Slow α helical formation during folding of a membrane protein Biochemistry 36 1997 192 196
29. P.J. Booth, S.L. Flitsch, L.J. Stern, D.A. Greenhalgh, P.S. Kim, and H.G. Khorana Intermediates in the folding of the membrane protein bacteriorhodopsin Nat. Struct. Biol. 2 1995 139 143
30. P.J. Booth, and A. Farooq Transient intermediates in the regeneration of bacteriorhodopsin investigated by time-resolved absorption spectroscopy Eur. J. Biochem. 246 1997 674 680
31. G.Q. Chen, and E. Gouaux Probing the folding and unfolding of wild-type and mutant forms of bacteriorhodopsin in micellar solutions: evaluation of reversible unfolding conditions Biochemistry 38 1999 15380 15387
32. D. Riensberg, P.J. Booth, B.J. Khoo, C. Jegerschold, and H. Paulsen Folding, assembly and stability of the major light harvesting complex of higher plants, LCHII, in the presence of native lipids Biochemistry 39 2000 14305 14313
33. C.R. Sanders, and R.S. Prosser Bicelles: a model membrane system for all seasons? Structure 6 1998 1227 1234
34. L. Czerski, and C.R. Sanders Functionality of a membrane protein in bicelles Anal. Biochem. 284 2000 327 333
35. C.R. Sanders, and G.C. Landis Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies Biochemistry 34 1995 4030 4040
36. J.-L. Rigaud, A. Bluzat, and S. Büschlen Incorporation of bacteriorhodpsin into large unilamellar liposomes by reverse phase evaporation Biochem. Biophys. Res. Commun. 111 1983 373 382
37. T. Gulik-Krzywiki, M. Seigneuret, and J.-L. Rigaud Monomer-oligomer equilibrium of bacteriorhodopsin in reconstituted proteoliposomes-a freeze fracture electron microscope study J. Biol. Chem. 262 1987 15580 15588
38. M. Seigneuret, and J.-L. Rigaud Analysis of passive and light-driven ion movements in large bacteriorhodopsin liposomes reconstituted by reverse-phase evaporation. 2. Influence of passive permeability and back-pressure effects upon light-induced proton uptake Biochemistry 25 1986 6723 6730
39. M. Seigneuret, and J.-L. Rigaud Analysis of passive and light-driven ion movements in large bacteriorhodopsin liposomes reconstituted by reverse-phase evaporation: 1. Factors governing the passive proton permeability of the membrane Biochemistry 25 1986 6716 6722
40. M. Seigneuret, and J.-L. Rigaud Use of the fluorescent pH probe pyranine to detect heterogeneous directions of proton movement in bacteriorhodopsin reconstituted large liposomes FEBS Lett. 188 1985 101 106
41. J.-L. Rigaud, B. Pitard, and D. Levy Reconstitution of membrane proteins into liposomes: application to energy transducing membrane proteins Biochim. Biophys. Acta 1231 1995 223 246
42. M.-T. Paternostre, M. Roux, and J.L. Rigaud Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents: 1. Solubilization of large unilamellar liposomes (prepared by reverse phase evaporation) by Triton X-100, octyl glucoside and sodium cholate Biochemistry 27 1988 2668 2677
43. D. Levy, A. Gulik, M. Seigneuret, and J.L. Rigaud Phospholipid vesicle solubilization and reconstitution by detergents-symmetrical analysis of the 2 processes using octlyethylene glycol mono-n-dodecyl ether Biochemistry 29 1990 9480 9488
44. S. Almog, B.J. Litman, W. Wimley, J. Cohen, E.J. Wachtel, Y. Barenholz, A. Ben-shaul, and D. Lichtenberg States of aggregation and phase-transformations in mixtures of phosphatidylcholine and octyl glucoside Biochemistry 29 1990 4582 4592
45. M.L. Jackson, C.F. Schmidt, B. Lichtenberg, B.J. Litman, and A.D. Albert Solubilization of phosphatidylcholine bilayers by octyl glucoside Biochemistry 21 1982 4576 4582
46. M. Ollivon, O. Eidelman, R. Blumethal, and A. Walter Micelle vesicle transition of egg phosphatidylcholine and octyl glucoside Biochemistry 27 1988 1695 1703
47. O. Eidelman, R. Blumethal, and A. Walter Composition of octyl glucoside phosphatidylcholine mixed micelles Biochemistry 27 1988 2839 2848
48. 2+-ATPase-mechanisms of membrane protein insertion into liposome during reconstitution procedures involving the use of detergents Biochim. Biophys. Acta 1107 1992 283 298
49. E. London, and G.W. Feigenson Phosphorous NMR analysis of phospholipids in detergents J. Lipid Res. 20 1979 406 418
50. F.M. Goni, M.A. Urbaneja, J.L.R. Arrondo, A. Alsonso, A.A. Durrani, and D. Chapman The interaction of phosphatidylcholine bilayers with Triton-X100 Eur. J. Biochem. 160 1986 1315 1325
51. S. Almog, T. Kushnir, S. Nir, and D. Lichtenberg Kinetic and structural aspects of reconstitution of phosphatidylcholine vesicles by dilution of phosphatidylcholine sodium cholate mixed micelles Biochemistry 25 1986 2597 2605
52. N.A. Mazer, G.B. Benedek, and M.C. Carey Quasi-electric light scattering studies of aqueous binary lipid systems-mixed micelle formation in bile salt lecithin solutions Biochemistry 19 1980 601 606
53. P.K. Vinson, Y. Talmon, and A. Walter Vesicle-micelle transition of phosphatidylcholine and octyl glucoside elucidated by cryo-transmission electron microscopy Biophys. J. 56 1989 669 679
54. A. Walter, P.K. Vinson, A. Kaplan, and Y. Talmon Viewing emulsion with freeze fracture transmission electron microscopy Biophys. J. 60 1991 1315 1325
55. T. Inoue Interaction of surfactants with phospholipid vesicles M. Roscoff Surfactant Science Series: Vesicles vol. 62 1996 Marcel Dekker Inc. New York 151 195
56. J.-L. Rigaud, M.-T. Paternostre, and A. Bluzat Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 2. Incorporation of the light-driven proton pump bacteriorhodopsin Biochemistry 27 1988 2677 2688
57. M. Putman, H.W. van Veen, B. Poolman, and W.N. Konings Restrictive use of detergents in the functional reconstitution of the secondary multidrug transporter LmrP Biochemistry 38 1999 1002 1008
58. J. Knol, K. Sjollema, and B. Poolman Detergent-mediated reconstitution of membrane proteins Biochemistry 37 1998 16410 16415
59. S. Batzri, and E.D. Korn Single bilayer liposome prepared without sonication Biochim. Biophys. Acta 298 1973 1015 1019
60. D. Deamer, and A.D. Bangham Large volume liposomes by an ether vaporization method Biochim. Biophys. Acta 443 1976 629 634
61. F. Szoka, and D. Papahadjopoulos Procedure for the preparation of liposomes with large internal aqueous space and high capture by reverse phase evaporation Proc. Natl. Acad. Sci. U. S. A. 75 1978 4194 4198
62. A. Darszon, C.A. Vandeberg, M. Schšnfeld, M.H. Ellison, N.C. Spitzer, and M. Montal Reassembly of protein-lipid complexes into large bilayer vesicles-perspectives for membrane reconstitution Proc. Natl. Acad. Sci. U. S. A. 77 1980 239 243
63. A. Darszon, C.A. Vandeberg, M.H. Ellison, and M. Montal Incorporation of membrane proteins into large single bilayer vesicles-application to rhodopsin J. Cell Biol. 81 1979 446 452
64. J.-L. Rigaud, A. Bluzat, and S. Büschlen Incorporation of bacteriorhodopsin into large unilamellar liposomes by reverse phase evaporation Biochem. Biophys. Res. Commun. 111 1983 373 382
65. M. Kashara, and P.C. Hinkle Reconstitution and purification of d-glucose transporter from human erythrocytes J. Biol. Chem. 252 1977 7384 7390
66. H. Pain Mechanisms of Protein Folding 2000 Oxford University Press Oxford
67. K.S. Huang, H. Bayley, M.J. Liao, E. London, and H.G. Khorana Refolding of an integral membrane protein. Denaturation, renaturation and reconstitution of proteolytic fragments J. Biol. Chem. 256 1981 3802 3809
68. B.M. Gorzelle, J.K. Nagy, K. Oxenoid, W.L. Lonzer, D.S. Cafiso, and C.R. Sanders Reconstitutive refolding of diacylglycerol kinase, an intergral membrane protein Biochemistry 38 1999 16373 16382
69. T. Surrey, and F. Jahnig Refolding and oriented insertion of a membrane protein into a lipid bilayer Proc. Natl. Acad. Sci. U. S. A. 89 1992 7457 7461
70. T. Surrey, A. Schmid, and F. Jahnig Folding and membrane insertion of the trimeric β-barrel protein OmpF Biochemistry 35 1996 2283 2288
71. H. Lilie, E. Schwarz, and R. Rudolph Advances in refolding of proteins produced in E Coli Curr. Opin. Biotech. 9 1998 497 501
72. M. Bloom, E. Evans, and O.G. Mouritsen Physical properties of the fluid lipid bilayer component of cell membranes: a perspective Quart. Rev. Biophys. 24 1997 293 397
73. J.M. Seddon Structure of the inverted hexagonal (HII) phase and non-lamellar phase transitions of lipids Biochim. Biophys. Acta 1031 1990 1 69
74. P.J. Booth, M.L. Riley, S.L. Flitsch, R.H. Templer, A. Farooq, A.R. Curran, N. Chadborn, and P. Wright Evidence that bilayer bending rigidity affects membrane protein folding Biochemistry 36 1997 197 203
75. A.R. Curran, R.H. Templer, and P.J. Booth Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer Biochemistry 38 1999 9328 9936
76. J. Lewis, and D. Cafiso Correlation between the free energy of a channel forming voltage gated peptide and the spontaneous curvature of bilayer lipids Biochemistry 38 1999 5932 5938
77. A.V. Botelho, N.J. Gibson, R.L. Thurmond, Y. Wang, and M.F. Brown Conformational energetics of rhodopsin modulated by non-lamellar forming lipids Biochemistry 41 2002 6354 6368
78. G. Attard, R.H. Templer, W.S. Smith, A.N. Hunt, and S. Jackowski Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress Proc. Natl. Acad. Sci. U. S. A. 97 2000 9032 9036
79. W. Meijberg, and P.J. Booth The activation energy for insertion of transmembrane alpha-helices is dependent on membrane composition J. Mol. Biol. 319 2002 839 853
80. J. Lundbaek, A. Maer, and O. Andersen Lipid bilayer electrostatic energy, curvature stress and assembly of gramicidin channels Biochemistry 36 1997 5695 5701
81. M. Goulian, O.N. Mesquita, D.K. Fygenson, C. Nielsen, O.S. Andersen, and A. Libchaber Gramicidin channel kinetics under tension Biophys. J. 74 1998 328 337
82. J.K. Nagy, W.L. Lonzer, and C.R. Sanders Kinetic study of folding and misfolding of diacylglycerol kinase in model membranes Biochemistry 40 2001 8971 8980
83. P.K. Fyfe, K.E. McAuley, A.W. Roszak, N.W. Isaacs, R.J. Cogdell, and M.R. Jones Probing the interface between membrane proteins and membrane lipids by X-ray crystallography TIBS 26 2001 106 112
84. A.G. Lee Lipid-protein interactions in biological membranes: a structural perspective Biochim. Biophys. Acta 1612 2003 1 40
85. K.E. McAuley, P.K. Fyfe, J.P. Ridge, N.W. Isaacs, R.J. Cogdell, and M.R. Jones Structural details of an interaction between cardiolipin and an integral membrane protein Proc. Natl. Acad. Sci. U. S. A. 96 1999 14706 14711
86. A. Camara-Artigas, C.L. Magee, J.C. Williams, and J.P. Allen Individual interactions influence the crystalline order for membrane proteins Acta Crystallogr., D 57 2001 1281 1285
87. G.B. Birrell, W.R. Sistrom, and O.H. Griffith Lipid-protein associations in chromatophores from photosynthetic bacterium Rhodopseudomonas sphaeroides Biochemistry 17 1978 3768 3773
88. W. Welte, and W. Kreutz Formation, structure and composition of a planar hexagonal lattice composed of specific protein-lipid complexes in the thylakoid membranes of Rhodopseudomonas viridis Biochim. Biophys. Acta 692 1982 479 488
89. M.C. Wakeham, R.B. Sessions, M.R. Jones, and P.K. Fyfe Is there a conserved interaction between cardiolipin and the type II bacterial reaction center? Biophys. J. 80 2001 1395 1405
90. T. Mizushima, M. Yao, N. Inoue, H. Aoyama, E. Yamashita, H. Yamaguchi, T. Tsukihara, R. Nakashima, K. Shinzawa-Itoh, R. Yaono, and S. Yoshikawa Structure of phospholipids in a membrane protein complex, bovine heart cytochrome c oxidase Acta Crystallogr., A 55 1999 (supplement) Abstr. P06.04.069
91. Y.C. Awasthi, T.F. Chuang, T.W. Keenan, and F.L. Crane Tightly bound cardiolipin in cytochrome oxidase Biochim. Biophys. Acta 26 1971 42 52
92. P. Nollert, J. Navarro, and E.M. Landau Crystallization of membrane proteins in cubo Method Enzymol. 343 2002 183 199
93. M. Caffery Membrane protein crystallization J. Struct. Biol. 142 2003 108 132
94. C. Hunte, and H. Michel Crystallization of membrane proteins mediated by antibody fragments Curr, Opin. Struct. Biol. 12 2002 503 508
95. C. Hunte, and H. Michel Membrane protein crystallization C. Hunte G. von Jagow H. Schagger Membrane Protein Purification and Crystallization: A Practical Guide 2003 Academic Press San Diego 143 160
96. H. Michel Crystallization of membrane proteins TIBS 8 1983 56 59
97. E.M. Landau, and J.P. Rosenbusch Lipidic cubic phases: a novel concept for the crystallization of membrane proteins Proc. Natl. Acad. Sci. U. S. A. 93 1996 14532 14535
98. G. Rummel, A. Hardmeyer, C. Widmer, M.L. Chiu, P. Nollert, K.P. Locher, I. Pedruzzi, E.M. Landau, and J.P. Rosenbusch Lipidic cubic phases: new matrices for the three-dimensional crystallization of membrane proteins J. Struct Biol. 121 1998 82 91
99. E. Pebay-Peyroula, G. Rummel, J.P. Rosenbusch, and E.M. Landau X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases Science 277 1997 1676 1681
100. H. Luecke, H.T. Richter, and J.K. Lanyi Proton transfer pathways in bacteriorhodopsin at 2.3 Angstrom resolution Science 280 1998 1934 1937
101. H. Belrhali, P. Nollert, A. Royant, C. Menzel, J.P. Rosenbusch, E.M. Landau, and E. Pebay-Peyroula Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 angstrom resolution Structure 7 1999 909 917
102. H. Luecke, B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi Structural changes in bacteriorhodopsin during ion transport at 2 Angstrom resolution Science 286 1999 255 260
103. K. Edman, P. Nollert, A. Royant, H. Belrhali, E. Pebay-Peyroula, J. Hajdu, R. Neutze, and E.M. Landau High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle Nature 401 1999 822 826
104. H. Luecke, B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi Structural changes in bacteriorhodopsin during ion transport at 2 Angstrom resolution Science 286 1999 255 260
105. A. Royant, K. Edman, T. Ursby, E. Pebay-Peyroula, E.M. Landau, and R. Neutze Helix deformation is coupled to vectorial proton transport in the photocycle of bacteriorhodopsin Nature 406 2000 645 648
106. P. Nollert, A. Royant, E. Pebay-Peyroula, and E.M. Landau Detergent-free membrane protein crystallization FEBS Lett. 457 1999 205 208
107. M.L. Chiu, P. Nollert, M.C. Loewen, H. Belrhali, E. Pebay-Peyroula, J.P. Rosenbusch, and E.M. Landau Crystallization in cubo: general applicability to membrane proteins Acta Crystallogr., D 56 2000 781 784
108. R.P. Haugland, Handbook of Fluorescent Probes and Research Chemicals 6th Ed. http://www.probes.com/.
109. L. Kallal, and J.L. Benovic Using green fluorescent proteins to study G-protein-coupled receptor localization and trafficking TIPS 21 2000 175 180
110. G.S. Baird, D.A. Zacharias, and R.Y. Tsien Circular permutation and receptor insertion within green fluorescent proteins Proc. Natl. Acad. Sci. U. S. A. 96 1999 11241 11246
111. G.G. Prive, and H.R. Kaback Engineering the lac permease for purification and crystallization J. Bioenerg. Biomembranes 28 1996 29 34 (FEB)
112. C. Sennoga, A. Heron, J.M. Seddon, R.H. Templer, and B. Hankamer Membrane-protein crystallization in cubo: temperature-dependent phase behaviour of monoolein-detergent mixtures Acta Crystallog., D 59 2003 239 246
113. S. Fahem, and J.U. Bowie Bicelle Crystallization; A new method for crystallizing membrane proteins yields a monomeric bacteriorhodsopin structure J. Mol. Biol. 316 2002 1 6