Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile

Biochimica et Biophysica Acta - Biomembranes

Volumn 1666, Issue 1-2, 2004, Pages 275-288

  Van Den Brink Van Der Laan, Els ^a   Antoinette Killian, J ^a   De Kruijff, Ben ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Curvature; Ion channel; KcsA; Leader Peptidase; Lipid polymorphism; Nonlamellar lipid; Oligomer; Phosphatidylethanolamine; Protein lipid interaction

Indexed keywords

MEMBRANE PROTEIN; SIGNAL PEPTIDASE;

BILAYER MEMBRANE; GENETIC POLYMORPHISM; HYDROPHOBICITY; LIPID MEMBRANE; MEMBRANE COMPONENT; MEMBRANE STRUCTURE; NONHUMAN; OLIGOMERIZATION; PREDICTION; PRESSURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

LIPID BILAYERS; LIPIDS; MEMBRANE PROTEINS; MICELLES; MOLECULAR CONFORMATION; PRESSURE;

EID: 7044232102     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2004.06.010     Document Type: Review

References (136)

1. P.R. Cullis, and B. de Kruijff Lipid polymorphism and the functional roles of lipids in biological membranes Biochim. Biophys. Acta 559 1979 399 420
2. W. Helfrich Elastic properties of lipid bilayers: theory and possible experiments Z. Naturforsch., C 28 1973 693 703
3. J.N. Israelachvili, S. Marcelja, and R.G. Horn Physical principles of membrane organization Q. Rev. Biophys. 13 1980 121 200
4. J.N. Israelachvili, D.J. Mitchell, and B.W. Ninham Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers J. Chem. Soc., Faraday Trans. II 72 1976 1525 1568
5. R.B. Gennis Biomembranes: Molecular Structure and Function 1989 Springer-Verlag New York
6. J.M. Seddon, and R.H. Templer Polymorphism of lipid-water systems R. Lipowski E. Sackmann Handbook of Biological Physics 1995 Elsevier Science B.V. Amsterdam 97 160
7. S. Gruner Stability of lyotropic phases with curved interfaces J. Phys. Chem. 93 1989 7562 7570
8. M.W. Tate, E.F. Eikenberry, D.C. Turner, E. Shyamsunder, and S.M. Gruner Nonbilayer phases of membrane lipids Chem. Phys. Lipids 57 1991 147 164
9. 2+ and temperature Biochim. Biophys. Acta 684 1982 282 286
10. B. de Kruijff Lipids beyond the bilayer Nature 386 1997 129 130
11. B. de Kruijff Lipid polymorphism and biomembrane function Curr. Opin. Chem. Biol. 1 1997 564 569
12. S.M. Gruner Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids Proc. Natl. Acad. Sci. U. S. A. 82 1985 3665 3669
13. S. Leikin, M.M. Kozlov, N.L. Fuller, and R.P. Rand Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes Biophys. J. 71 1996 2623 2632
14. N. Fuller, C.R. Benatti, and R.P. Rand Curvature and bending constants for phosphatidylserine-containing membranes Biophys. J. 85 2003 1667 1674
15. R.P. Rand, and N.L. Fuller Structural dimensions and their changes in a reentrant hexagonal-lamellar transition of phospholipids Biophys. J. 66 1994 2127 2138
16. S. Morein, A. Andersson, L. Rilfors, and G. Lindblom Wild-type Escherichia coli cells regulate the membrane lipid composition in a quot;window" between gel and non-lamellar structures J. Biol. Chem. 271 1996 6801 6809
17. A.G. Rietveld, J.A. Killian, W. Dowhan, and B. de Kruijff Polymorphic regulation of membrane phospholipid composition in Escherichia coli J. Biol. Chem. 268 1993 12427 12433
18. G. Lindblom, J.B. Hauksson, L. Rilfors, B. Bergenstahl, A. Wieslander, and P.O. Eriksson Membrane lipid regulation in Acholeplasma laidlawii grown with saturated fatty acids. Biosynthesis of a triacylglucolipid forming reversed micelles J. Biol. Chem. 268 1993 16198 16207
19. S. Vikstrom, L. Li, and A. Wieslander The nonbilayer/bilayer lipid balance in membranes. Regulatory enzyme in Acholeplasma laidlawii is stimulated by metabolic phosphates, activator phospholipids, and double-stranded DNA J. Biol. Chem. 275 2000 9296 92302
20. B. De Kruijff, P.R. Cullis, A. Verkleij, M.J. Hope, C.J.A. Van Echteld, and T.F. Taraschi Lipid polymorphism and membrane function A.N. Martonosi Membrane structure and dynamics 1985 Plenum Press New York 131 204
21. R.M. Epand Lipid polymorphism and protein-lipid interactions Biochim. Biophys. Acta 1376 1998 353 368
22. D.P. Siegel, and R.M. Epand The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanisms Biophys. J. 73 1997 3089 3111
23. J. Wegener, and H.-J. Galla The role of non-lamellar lipid structures in the formation of tight junctions Chem. Phys. Lipids 81 1996 229 255
24. V. Luzzati Biological significance of lipid polymorphism: the cubic phases Curr. Opin. Struck. Biol. 7 1997 661 668
25. G. Senisterra, and R.M. Epand Role of membrane defects in the regulation of the activity of protein kinase C Arch. Biochem. Biophys. 300 1993 378 383
26. C.D. Stubbs, and S.J. Slater The effects of non-lamellar forming lipids on membrane protein-lipid interactions Chem. Phys. Lipids 81 1996 185 195
27. R.B. Cornell, and R.S. Arnold Modulation of the activities of enzymes of membrane lipid metabolism by non-bilayer forming lipids Chem. Phys. Lipids 81 1996 215 227
28. G.S. 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
29. L. Li, P. Storm, O.P. Karlsson, S. Berg, and A. Wieslander Irreversible binding and activity control of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii at an anionic lipid bilayer surface Biochemistry 42 2003 9677 9686
30. S. Vikstrom, L. Li, O.P. Karlsson, and A. Wieslander Key role of the diglucosyldiacylglycerol synthase for the nonbilayer-bilayer lipid balance of Acholeplasma laidlawii membranes Biochemistry 38 1999 5511 5520
31. O.P. Karlsson, M. Rytomaa, A. Dahlqvist, P.K. Kinnunen, and A. Wieslander Correlation between bilayer lipid dynamics and activity of the diglucosyldiacylglycerol synthase from Acholeplasma laidlawii membranes Biochemistry 35 1996 10094 10102
32. C. van der Does, J. Swaving, W. van Klompenburg, and A.J. Driessen Non-bilayer lipids stimulate the activity of the reconstituted bacterial protein translocase J. Biol. Chem. 275 2000 2472 2478
33. D. Schwarz, P. Kisselev, W. Pfeil, S. Pisch, U. Bornscheuer, and R.D. Schmid Evidence that nonbilayer phase propensity of the membrane is important for the side chain cleavage activity of cytochrome P450SCC Biochemistry 36 1997 14262 14270
34. A.V. Botelho, N.J. Gibson, R.L. Thurmond, Y. Wang, and M.F. Brown Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids Biochemistry 41 2002 6354 6368
35. M.S. Brown, and J.L. Goldstein The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor Cell 89 1997 331 340
36. J. Streicher-Scott, R. Lapidus, and P.M. Sokolove The reconstituted mitochondrial adenine nucleotide translocator: effects of lipid polymorphism Arch. Biochem. Biophys. 315 1994 548 554
37. T. van der Heide, and B. Poolman Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane Proc. Natl. Acad. Sci. U. S. A. 97 2000 7102 7106
38. T. van der Heide, M.C.A. Stuart, and B. Poolman On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine EMBO J. 20 2001 7022 7032
39. F.Y. Yang, and F. Hwang Effect of non-bilayer lipids on the activity of membrane enzymes Chem. Phys. Lipids 81 1996 197 202
40. H.M. Chang, R. Reitstetter, and R. Gruener Lipid-ion channel interactions: increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior J. Membr. Biol. 145 1995 13 19
41. S.L. Keller, S.M. Bezrukov, S.M. Gruner, M.W. Tate, I. Vodyanoy, and V.A. Parsegian Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids Biophys. J. 65 1993 23 27
42. J.A. Lundbaek, A.M. Maer, and O.S. Andersen Lipid bilayer electrostatic energy, curvature stress, and assembly of gramicidin channels Biochemistry 36 1997 5695 5701
43. N.M. Rao, and C.S. Sundaram Sensitivity of phospholipase C (Bacillus cereus) activity to lipid packing in sonicated lipid mixtures Biochemistry 32 1993 8547 8552
44. J.D. Pilot, J.M. East, and A.G. Lee Effects of phospholipid headgroup and phase on the activity of diacylglycerol kinase of Escherichia coli Biochemistry 40 2001 14891 14897
45. 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 9336
46. M. Bogdanov, and W. Dowhan Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease EMBO J. 17 1998 5255 5264
47. M. Bogdanov, M. Umeda, and W. Dowhan Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone J. Biol. Chem. 274 1999 12339 12345
48. M. Wikstrom, J. Xie, M. Bogdanov, E. Mileykovskaya, P. Heacock, A. Wieslander, and W. Dowhan Monoglucosyldiacylglycerol, a foreign lipid, can substitute for phosphatidylethanolamine in essential membrane-associated functions in Escherichia coli J. Biol. Chem. 279 2004 10484 10493
49. B. de Kruijff Polymorphic regulation of membrane lipid composition Nature 329 1987 587 588
50. J.S. Hah, S.W. Hui, and C.Y. Jung Effects of physical states of phospholipids on the incorporation and cytochalasin B binding activity of human erythrocyte membrane proteins in reconstituted vesicles Biochemistry 22 1983 4763 4769
51. S.W. Hui, and A. Sen Effects of lipid packing on polymorphic phase behavior and membrane properties Proc. Natl. Acad. Sci. U. S. A. 86 1989 5825 5829
52. N. Janes Curvature stress and polymorphism in membranes Chem. Phys. Lipids 81 1996 133 150
53. R.M. Ep, and R.F. Epand Calorimetric detection of curvature strain in phospholipid bilayers Biophys. J. 66 1994 1450 1456
54. R.H. Templer, S.J. Castle, A.R. Curran, G. Rumbles, and D.R. Klug Sensing isothermal changes in the lateral pressure in model membranes using di-pyrenyl phosphatidylcholine Faraday Discuss. 1998 41 53 (discussion 69-78)
55. P.J. Booth The trials and tribulations of membrane protein folding in vitro Biochim. Biophys. Acta 1610 2003 51 56
56. S.M. Davies, R.M. Epand, R. Kraayenhof, and R.B. Cornell Regulation of CTP:phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: an important role for stored curvature strain energy Biochemistry 40 2001 10522 10531
57. J.R. Lewis, and D.S. 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
58. J.A. Lundbaek, P. Birn, J. Girshman, A.J. Hansen, and O.S. Andersen Membrane stiffness and channel function Biochemistry 35 1996 3825 3830
59. M.F. Brown Modulation of rhodopsin function by properties of the membrane bilayer Chem. Phys. Lipids 73 1994 159 180
60. C. Nielsen, M. Goulian, and O.S. Andersen Energetics of inclusion-induced bilayer deformations Biophys. J. 74 1998 1966 1983
61. A. Sen, T.V. Isac, and S.W. Hui Bilayer packing stress and defects in mixed dilinoleoylphosphatidylethanolamine and palmitoyloleoylphosphatidylcholine and their susceptibility to phospholipase A2 Biochemistry 30 1991 4516 4521
62. S.W. Hui Geometry of phase-separated domains in phospholipid bilayers by diffraction-contrast electron microscopy Biophys. J. 34 1981 383 395
63. J.L. Soulages, Z. Salamon, M.A. Wells, and G. Tollin Low concentrations of diacylglycerol promote the binding of apolipophorin III to a phospholipid bilayer: a surface plasmon resonance spectroscopy study Proc. Natl. Acad. Sci. U. S. A. 92 1995 5650 5654
64. P.K.J. Kinnunen On the molecular-level mechanisms of peripheral protein-membrane interactions induced by lipids forming inverted non-lamellar phases Chem. Phys. Lipids 81 1996 151 166
65. E.K. Tuominen, C.J. Wallace, and P.K. Kinnunen Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage J. Biol. Chem. 277 2002 8822 8826
66. H.H. de Jongh, J.A. Killian, and B. de Kruijff A water-lipid interface induces a highly dynamic folded state in apocytochrome c and cytochrome c, which may represent a common folding intermediate Biochemistry 31 1992 1636 1643
67. H.H. de Jongh, T. Ritsema, and J.A. Killian Lipid specificity for membrane mediated partial unfolding of cytochrome c FEBS Lett. 360 1995 255 260
68. R.S. Cantor Lateral pressures in cell membranes: a mechanism for modulation of protein function J. Phys. Chem., B 101 1997 1723 1725
69. D. Marsh Components of the lateral pressure in lipid bilayers deduced from HII phase dimensions Biochim. Biophys. Acta 1279 1996 119 123
70. D. Marsh Lateral pressure in membranes Biochim. Biophys. Acta 1286 1996 183 223
71. K. Gawrisch, and L.L. Holte NMR investigations of non-lamellar phase promoters in the lamellar phase state Chem. Phys. Lipids 81 1996 105 116
72. E. van den Brink-van der Laan, R.E. Dalbey, R.A. Demel, J.A. Killian, and B. de Kruijff Effect of nonbilayer lipids on membrane binding and insertion of the catalytic domain of leader peptidase Biochemistry 40 2001 9677 9684
73. R.S. Cantor The lateral pressure profile in membranes: a physical mechanism of general anesthesia Biochemistry 36 1997 2339 2344
74. R.S. Cantor The lateral pressure profile in membranes: a physical mechanism of general anesthesia Toxicol. Lett. 100 1998 451 458
75. R.S. Cantor The influence of membrane lateral pressures on simple geometric models of protein conformational equilibria Chem. Phys. Lipids 101 1999 45 56
76. R.S. Cantor Lipid composition and the lateral pressure profile in bilayers Biophys. J. 76 1999 2625 2639
77. R.S. Cantor Size distribution of barrel-stave aggregates of membrane peptides: influence of the bilayer lateral pressure profile Biophys. J. 82 2002 2520 2525
78. I.I. Szleifer, A. Ben-Shaul, and W.M. Gelbart Chain packing statistics and thermodynamics of amphiphile monolayers J. Phys. Chem. 94 1990 5081 5089
79. I.I. Szleifer, D. Kramer, A. Ben-Shaul, W.M. Gelbart, and S.A. Safran Molecular theory of curvature elacticity in surfactant films J. Chem. Phys. 92 1990 6800 6817
80. I.I. Szleifer, D. Kramer, A. Ben-Shaul, D. Roux, and W.M. Gelbart Curvature elasticity of pure and mixed surfactant films Phys. Rev. Lett. 60 1988 1966 1969
81. D. Harries, and A. Ben-Shaul Conformational chain statistics in a model lipid bilayer: comparison between mean field and Monte Carlo calculations J. Chem. Phys. 106 1997 1609 1619
82. T.X. Xiang, and B.D. Anderson Molecular distributions in interphases: statistical mechanical theory combined with molecular dynamics simulation of a model lipid bilayer Biophys. J. 66 1994 561 573
83. M. Venturoli, and B. Smit Simulating the self-assembly of model membranes Phys. Chem. Comm. 10 1999
84. E. Lindahl, and O. Edholm Spatial and energetic-entropic decomposition of surface tension in a lipid bilayer by molecular dynamics simulations J. Chem. Phys. 113 2000 3882 3893
85. J. Gullingsrud, and K. Schulten Gating of MscL studied by steered molecular dynamics Biophys. J. 85 2003 2087 2099
86. R.S. Cantor Breaking the Meyer-Overton rule: predicted effects of varying stiffness and interfacial activity on the intrinsic potency of anesthetics Biophys. J. 80 2001 2284 2297
87. S.M. Bezrukov Functional consequences of lipid packing stress Curr. Opin. Colloid Interface Sci. 5 2000 237 243
88. P.R. Cullis, M.J. Hope, and C.P. Tilcock Lipid polymorphism and the roles of lipids in membranes Chem. Phys. Lipids 40 1986 127 144
89. D. Marsh, A. Watts, and I.C. Smith Dynamic structure and phase behavior of dimyristoylphosphatidylethanolamine bilayers studied by deuterium nuclear magnetic resonance Biochemistry 22 1983 3023 3026
90. B. Perly, I.C. Smith, and H.C. Jarrell Effects of replacement of a double bond by a cyclopropane ring in phosphatidylethanolamines: a 2H NMR study of phase transitions and molecular organization Biochemistry 24 1985 1055 1063
91. R.S. Cantor Solute modulation of conformational equilibria in intrinsic membrane proteins: apparent "cooperativity" without binding Biophys. J. 77 1999 2643 2647
92. M. Buck Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins Q. Rev. Biophys. 31 1998 297 355
93. D. Hamada, F. Chiti, J.I. Guijarro, M. Kataoka, N. Taddei, and C.M. Dobson Evidence concerning rate-limiting steps in protein folding from the effects of trifluoroethanol Nat. Struct. Biol. 7 2000 58 61
94. C.P. Yiu, M.G. Mateu, and A.R. Fersht Protein folding transition states: elicitation of Hammond effects by 2,2,2-trifluoroethanol Chembiochemistry 1 2000 49 55
95. R.E. Dalbey Leader peptidase Mol. Microbiol. 5 1991 2855 2860
96. N. Bilgin, J.I. Lee, H.Y. Zhu, R. Dalbey, and G. von Heijne Mapping of catalytically important domains in Escherichia coli leader peptidase EMBO J. 9 1990 2717 2722
97. D.W. Kuo, H.K. Chan, C.J. Wilson, P.R. Griffin, H. Williams, and W.B. Knight Escherichia coli Leader Peptidase: production of an active form lacking a requirement for detergent and development of peptide substrates Arch. Biochem. Biophys. 303 1993 274 280
98. W.R. Tschantz, M. Paetzel, G. Cao, D. Suciu, M. Inouye, and R.E. Dalbey Characterization of a soluble, catalytically active form of Escherichia coli leader peptidase: requirement of detergent or phospholipid for optimal activity Biochemistry 34 1995 3935 3941
99. M. Paetzel, R.E. Dalbey, and N.C. Strynadka Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor Nature 396 1998 186 190
100. W. van Klompenburg, M. Paetzel, J.M. de Jong, R.E. Dalbey, R.A. Demel, G. von Heijne, and B. de Kruijff Phosphatidylethanolamine mediates insertion of the catalytic domain of leader peptidase in membranes FEBS Lett. 431 1998 75 79
101. E. van den Brink-van der Laan, V. Chupin, J.A. Killian, and B. De Kruijff Stability of KcsA tetramer depends on membrane lateral pressure Biochemistry 43 2004 4240 4250
102. E. van den Brink-van der Laan, V. Chupin, J.A. Killian, and B. De Kruijff Small alcohols destabilize the KcsA tetramer via their effect on the membrane lateral pressure Biochemistry 43 2004 5939 5942
103. M. Langner, and S.W. Hui Merocyanine 540 as a fluorescence indicator for molecular packing stress at the onset of lamellar-hexagonal transition of phosphatidylethanolamine bilayers Biochim. Biophys. Acta 1415 1999 323 330
104. D.A. Doyle, J. Morais Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon The structure of the potassium channel: molecular basis of K+ conduction and selectivity Science 280 1998 69 77
105. D.M. Cortes, L.G. Cuello, and E. Perozo Molecular architecture of full-length KcsA: role of cytoplasmic domains in ion permeation and activation gating J. Gen. Physiol. 117 2001 165 180
106. S.N. Irizarry, E. Kutluay, G. Drews, S.J. Hart, and L. Heginbotham Opening the KcsA K+ channel: tryptophan scanning and complementation analysis lead to mutants with altered gating Biochemistry 41 2002 13653 13662
107. M.S. Sansom, I.H. Shrivastava, J.N. Bright, J. Tate, C.E. Capener, and P.C. Biggin Potassium channels: structures, models, simulations Biochim. Biophys. Acta 1565 2002 294 307
108. B.L. Kelly, and A. Gross Potassium channel gating observed with site-directed mass tagging Nat. Struct. Biol. 10 2003 280 284
109. C.M. Nimigean, J.S. Chappie, and C. Miller Electrostatic tuning of ion conductance in potassium channels Biochemistry 42 2003 9263 9268
110. N.V. Shen, X. Chen, M.M. Boyer, and P.J. Pfaffinger Deletion analysis of K+ channel assembly Neuron 11 1993 67 76
111. H. Splitt, D. Meuser, I. Borovok, M. Betzler, and H. Schrempf Pore mutations affecting tetrameric assembly and functioning of the potassium channel KcsA from Streptomyces lividans FEBS Lett. 472 2000 83 87
112. A. van Dalen, H. Schrempf, J.A. Killian, and B. de Kruijff Efficient membrane assembly of the KcsA potassium channel in Escherichia coli requires the protonmotive force EMBO Rep. 1 2000 340 346
113. A. van Dalen, S. Hegger, J.A. Killian, and B. de Kruijff Influence of lipids on membrane assembly and stability of the potassium channel KcsA FEBS Lett. 525 2002 33 38
114. A. van Dalen, M. van der Laan, A.J. Driessen, J.A. Killian, and B. de Kruijff Components required for membrane assembly of newly synthesized K+ channel KcsA FEBS Lett. 511 2002 51 58
115. N. Umigai, Y. Sato, A. Mizutani, T. Utsumi, M. Sakaguchi, and N. Uozumi Topogenesis of two transmembrane type K+ channels, Kir 2.1 and KcsA J. Biol. Chem. 278 2003 40373 40384
116. D.M. Cortes, and E. Perozo Structural dynamics of the Streptomyces lividans K+ channel (SKC1): oligomeric stoichiometry and stability Biochemistry 36 1997 10343 10352
117. L. Heginbotham, E. Odessey, and C. Miller Tetrameric stoichiometry of a prokaryotic K+ channel Biochemistry 36 1997 10335 10342
118. J.A. Demmers, A. van Dalen, B. de Kruijff, A.J. Heck, and J.A. Killian Interaction of the K+ channel KcsA with membrane phospholipids as studied by ESI mass spectrometry FEBS Lett. 541 2003 28 32
119. F.I. Valiyaveetil, Y. Zhou, and R. MacKinnon Lipids in the structure, folding, and function of the KcsA K+ channel Biochemistry 41 2002 10771 10777
120. S.J. Alvis, I.M. Williamson, J.M. East, and A.G. Lee Interactions of anionic phospholipids and phosphatidylethanolamine with the potassium channel KcsA Biophys. J. 85 2003 3828 3838
121. R.F. Zwaal, B. Roelofsen, and C.M. Colley Localization of red cell membrane constituents Biochim. Biophys. Acta 300 1973 159 182
122. A.J. Verkleij, R.F. Zwaal, B. Roelofsen, P. Comfurius, D. Kastelijn, and L.L. van Deenen The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy Biochim. Biophys. Acta 323 1973 178 193
123. A. van Dalen, Protein insertion and assembly in the Escherichia coli inner membrane, thesis, Utrecht University, 2002.
124. A. Kuhn Bacteriophage M13 procoat protein inserts into the plasma membrane as a loop structure Science 238 1987 1413 1415
125. A.S. Shaw, P.J. Rottier, and J.K. Rose Evidence for the loop model of signal-sequence insertion into the endoplasmic reticulum Proc. Natl. Acad. Sci. U. S. A. 85 1988 7592 7596
126. Y. Wang, R. Bruckner, and R.L. Stein Regulation of signal peptidase by phospholipids in membrane: characterization of phospholipid bilayer incorporated Escherichia coli signal peptidase Biochemistry 43 2004 265 270
127. A. van Dalen and B. De Kruijff, The role of lipids in membrane insertion and translocation of bacterial proteins, (2003).
128. Y. Jiang, A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon The open pore conformation of potassium channels Nature 417 2002 523 526
129. P.C. Biggin, and M.S. Sansom Open-state models of a potassium channel Biophys. J. 83 2002 1867 1876
130. E. Perozo, and D.C. Rees Structure and mechanism in prokaryotic mechanosensitive channels Curr. Opin. Struck. Biol. 13 2003 432 442
131. E. Perozo, A. Kloda, D.M. Cortes, and B. Martinac Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating Nat. Struct. Biol. 9 2002 696 703
132. Y. Jiang, V. Ruta, J. Chen, A. Lee, and R. MacKinnon The principle of gating charge movement in a voltage-dependent K+ channel Nature 423 2003 42 48
133. G.E. Breitwieser G protein-coupled receptor oligomerization: implications for G protein activation and cell signaling Circ. Res. 94 2004 17 27
134. L.M. Veenhoff, E.H. Heuberger, and B. Poolman Quaternary structure and function of transport proteins Trends Biochem. Sci. 27 2002 242 249
135. K.Y. Hostetler Effect of thyroxine on the activity of mitochondrial cardiolipin synthase in rat liver Biochim. Biophys. Acta 1086 1991 139 140
136. R.S. Cantor Receptor desensitization by neurotransmitters in membranes: are neurotransmitters the endogenous anesthetics? Biochemistry 42 2003 11891 11897