Properties of integral membrane protein structures: Derivation of an implicit membrane potential

Proteins: Structure, Function and Genetics

Volumn 59, Issue 2, 2005, Pages 252-265

  Ulmschneider, Martin B ^a   Sansom, Mark S P ^b   Di Nola, Alfredo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

helices; Amino acid distribution; Implicit membrane; Membrane protein; Potential of mean force

Indexed keywords

ALANINE; ARGININE; GLYCINE; LYSINE; MEMBRANE PROTEIN; SERINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CALCULATION; ENERGY; HYDROPHOBICITY; MEMBRANE POTENTIAL; NORMAL DISTRIBUTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACIDS; MEMBRANE LIPIDS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; PROTEIN STRUCTURE, SECONDARY; SOLVENTS;

EID: 16344390562     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20334     Document Type: Article

References (116)

1. Jones DT. Do transmembrane protein superfolds exist? FEBS Lett 1998;423:281-285.
2. Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 1998;7:1029-1038.
3. von Heijne G. Recent advances in the understanding of membrane protein assembly and structure. Q Rev Biophys 1999;32:285-307.
4. Terstappen GC, Reggiani A. In silico research in drug discovery. Trends Pharm Sci 2001;22:23-26.
5. Grisshammer R, Tate CG. Overexpression of integral membrane-proteins for structural studies. Q Rev Biophys 1995;28:315-422.
6. Chiu ML, Nollert P, Loewen MC, Belrhali H, Pebay-Peyroula E, Rosenbusch JP, Landau EM. Crystallization in cubo: general applicability to membrane proteins. Acta Crystallogr 2000;56:781-784.
7. Fernández C, Hilty C, Wider G, Güntert P, Wuthrich K. NMR structure of the integral membrane protein OmpX. J Mol Biol 2004;336:1211-1221.
8. Fernández C, Wüthrich K. NMR solution structure determination of membrane proteins reconstituted in detergent micelles. FEBS Lett 2003;555:144-150.
9. Tamm LK, Abildgaard F, Arora A, Blad H, Bushweller JH. Structure, dynamics and function of the outer membrane protein A (OmpA) and influenza hemagglutinin fusion domain in detergent micelles by solution NMR. FEBS Lett 2003;555:139-143.
10. Lazaridis T, Karplus M. Effective energy functions for protein structure prediction. Curr Opin Struct Biol 2000;10:139-145.
11. Rost B, Casadio R, Fariselli P, Sander C. Transmembrane helices predicted at 95% accuracy. Protein Sci 1995;4:521-533.
12. Rost B, Fariselli P, Casadio R. Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci 1996;5:1704-1718.
13. Jayasinghe S, Hristova K, White SH. Energetics, stability, and prediction of transmembrane helices. J Mol Biol 2001;312:927-934.
14. Zhou H, Zhou Y. Stability scale and atomic solvation parameters extracted from 1023 mutation experiments. Proteins 2002;49:483-492.
15. Engelman DM, Steitz TA, Goldman A. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem 1986;15:321-353.
16. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982;157:105-132.
17. von Heijne G. Membrane-protein structure prediction-hydrophobicity analysis and the positive-inside rule. J Mol Biol 1992;225:487-494.
18. Czerzo M, Wallin E, Simon I, von Heijne G, Elofsson A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 1997;10:673-676.
19. Zhou H, Zhou Y. Predicting the topology of transmembrane helical proteins using mean burial propensity and a hidden-Markov-model-based method. Protein Sci 2003;12:1547-1555.
20. Punta M, Maritan A. A knowledge-based scale for amino acid membrane propensity. Proteins 2003;50:114-121.
21. Persson B, Argos P. Prediction of transmembrane segments utilising multiple sequence alignments. J Mol Biol 1994;237:182-192.
22. Persson B, Argos P. Prediction of membrane protein topology utilizing multiple sequence alignments. J Protein Chem 1997;16:453-457.
23. Casadio R, Fariselli P, Taroni C, Compiani M. A predictor of transmembrane alpha-helix domains of proteins based on neural networks. Eur Biophys J 1996;24:165-178.
24. Jones DT, Taylor WE, Thornton JM. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 1994;33:3038-3049.
25. Hofinann K, Stoffel W, TMbase-a database of membrane spanning protein segments. Biol Chem Hoppe-Seyler 1993;374:166.
26. Sonnhammer ELL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998;6:175-182.
27. Landolt-Marticorena C, Williams KA, Deber CM, Reithmeier AF, Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J Mol Biol 1993;229:602-608.
28. Arkin IT, Brunger AT. Statistical analysis of predicted transmembrane alpha-helices. Biochim Biophys Acta 1998;1429:113-128.
29. Ulmschneider MB, Sansom MSP. Amino acid distributions in integral membrane protein structures. Biochim Biophys Acta 2001;1512:1-14.
30. Stevens TJ, Arkin IT. Are membrane proteins "inside-out" proteins? Proteins 1999;36:135-143.
31. Bowie JU. Helix packing in membrane proteins. J Mol Biol 1997;272:780-789.
32. Cordes FS, Bright JN, Sansom MSP. Proline-induced distortions of transmembrane helices. J Mol Biol 2002;323:951-960.
33. Javadpour MM, Eilers M, Groesbeek M, Smith SO. Helix packing in polytopic membrane proteins: Role of glycine in transmembrane helix association. Biophys J 1999;77:1609-1618.
34. Senes A, Gerstein M, Engelman DM. Statistical analysis of amino acid patterns in transmembrane helices: The GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J Mol Biol 2000;296:921-936.
35. Eilers M, Srinivasan CS, Shieh T, Smith SO, Fleming PJ. Internal packing of helical membrane proteins. PNAS 2000;97:5796-5801.
36. Eilers M, Patel AB, Liu W, Smith SO. Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophys J 2002;82:2720-2736.
37. Pilpel Y, Ben-Tal N, Lancet D. kPROT: a knowledge-based scale for the propensity of residue orientation in transmembrane segments. Application to membrane protein structure prediction. J Mol Biol 1999;294:921-935.
38. Pellegrini-Calace M, Carotti A, Jones DT. Folding in lipid membranes (FILM): a novel method for the prediction of small membrane protein 3D structures. Proteins 2003;50:537-545.
39. Sippl MJ. Calculation of conformational ensembles from potentials of mean force-an approach to the knowledge-based prediction of local structures in globular-proteins. J Mol Biol 1990;213:859-883.
40. Sippl MJ. Knowledge-based potentials for proteins. Curr Opin Struct Biol 1995;5:229-235.
41. Biggin PC, Sansom MSP. Interactions of alpha-helices with lipid bilayers: a review of simulation studies. Biophys Chem 1999;76:161-183.
42. Forrest LR, Sansom MSP. Membrane simulations: bigger and better? Curr Opin Struct Biol 2000;10:174-181.
43. Domene C, Bond P, Sansom MSP. Membrane protein simulation: ion channels and bacterial outer membrane proteins. Adv Prot Chem 2003;66:159-193.
44. Lazaridis T. Effective energy function for proteins in lipid membranes. Proteins 2003;52:176-192.
45. Maddox MW, Longo ML. A Monte Carlo study of peptide insertion into lipid bilayers: equilibrium conformations and insertion mechanisms. Biophys J 2002;82:244-263.
46. Born. Volumen und Hydratationswärme der Ionen. Z Phys 1920;1:45-48.
47. Still WC, Tempczyk A, Hawley RC, Hendrickson T. Semianalytical treatment of solvation for molecular mechanics and dynamics. J Am Chem Soc 1990;112:6127-6129.
48. Ulmschneider JP, Jorgensen WL. Polypeptide folding using Monte Carlo sampling, concerted rotation, and continuum solvation. J Am Chem Soc 2004;126:1849-1857.
49. Spassov VZ, Yan L, Szalma S. Introducing an implicit membrane in generalized Born/solvent accessibility continuum solvent models. J Phys Chem B 2002;106:8726-8738.
50. Im W, Feig M, Brooks III CL. An implicit membrane generalized born theory for the study of structure, stability, and interactions of membrane proteins. Biophys J 2003;85:2900-2918.
51. Popot JL, Engelman DM. Helical membrane protein folding, stability, and evolution. Annu Rev Biochem 2000;69:881-922.
52. Engelman DM, Chen Y, Chin CN, Curran AR, Dixon AM, Dupuy AD, Lee AS, Lehnert U, Matthews EE, Reshetnyak YK, Senes A, Popot JL. Membrane protein folding: beyond the two stage model. FEES Lett 2003;555:122-125.
53. Kabsch W, Sander C. Dictionary of protein secondary structure-pattern- recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
54. Killian JA. Synthetic peptides as models for intrinsic membrane proteins. FEES Lett 2003;555:134-138.
55. de Planque MR, Killian JA. Protein-lipid interactions studied with designed transmembrane peptides: role of Hydrophobic matching and interfacial anchoring. Mol Membr Biol 2003;20:271-284.
56. Wiener MC, White SH. Fluid bilayer structure determination by the combined use of x-ray and neutron diffraction. I. Fluid bilayer models and the limits of resolution. Biophys J 1991;59:162-173.
57. Wiener MC, White SH. Fluid bilayer structure determination by the combined use of x-ray and neutron diffraction. II. "Composition-space" refinement method. Biophys J 1991;59:174-185.
58. Wiener MC, White SH. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys J 1992;61:437-447.
59. Yau WM, Wimley WC, Gawrisch K, White SH. The preference of tryptophan for membrane interfaces. Biochemistry 1998;37:14713-14718.
60. Jacobs RE, White SH. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry 1989;28:3421-3437.
61. Domene C, Bond PJ, Deol SS, Sansom MS. Lipid/protein interactions and the membrane/water interfacial region. J Am Chem Soc 2003;125:14966-14967.
62. White SH, King GI, Cain JI. Location of hexane in lipid bilayers determined by neutron diffraction. Nature 1981;290:161-163.
63. White SH, Wimley WC. Membrane protein folding and stability: Physical principles. Annu Rev Biophys Biomol Struct 1999;28:319-365.
64. de Planque MR, Boots JW, Rijkers DT, Liskamp RM, Greathouse DV, Killian JA. The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane alpha-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 2002;41:8396-8404.
65. Strandberg E, Morein S, Rijkers DT, Liskamp RM, van der Wel PC, Killian JA. Lipid dependence of membrane anchoring properties and snorkeling behavior of aromatic and charged residues in transmembrane peptides. Biochemistry 2002;41:7190-7198.
66. Connolly ML. Analytical molecular surface calculation. J Appl Cryst 1983;16:548-558.
67. Connolly ML. Computation of molecular volume. J Am Chem Soc 1985;107:1118-1124.
68. Byrne B, Iwata S. Membrane protein complexes. Curr Opin Struct Biol 2002;12:239-243.
69. Deisenhofer J, Michel H. The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 1989;245:1463-1473.
70. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 2000;289:739-745.
71. Van den Berg B, Clemons WM, Jr., Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA. X-ray structure of a protein-conducting channel. Nature 2004;427:36-44.
72. von Heijne G, Gavel Y. Topogenic signals in integral membrane-proteins. Eur J Biochem 1988;174:671-678.
73. Eilers M, Shekar SC, Shieh T, Smith SO, Fleming PJ. Internal packing of helical membrane proteins. Proc Natl Acad Sci USA 2000;97:5796-5801.
74. Lemmon MA, Treutlein HR, Adams PD, Brunger AT, Engelman DM. A dimerization motif for transmembrane alpha-helices. Nat Struct Biol 1994;1:157-163.
75. Brosig B, Langosch D. The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci 1998;7:1052-1056.
76. Russ WP, Engelman DM. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 2000;296:911-919.
77. Russ WP, Engelman DM. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc Natl Acad Sci USA 1999;96:863-868.
78. Rees DC, DeAntonio L, Eisenberg D. Hydrophobic organization of membrane proteins. Science 1989;245:510-513.
79. Rees DC, Eisenberg D. Turning a reference inside-out: commentary on an article by Stevens and Arkin entitled: "Are membrane proteins 'inside-out' proteins?" (Proteins 1999;36:135-143). Proteins 2000;38:121-122.
80. Casari G, Sippl MJ. Structure-derived hydrophobic potential. Hydrophobic potential derived from X-ray structures of globular proteins is able to identify native folds. J Mol Biol 1992;224:725-732.
81. Hopp TP, Woods KR. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci USA 1981;78:3824-3828.
82. Roseman MA. Hydrophilicity of polar amino acid side-chains is markedly reduced by flanking peptide bonds. J Mol Biol 1988;200:513-522.
83. Wimley WC, White SH. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 1996;3:842-848.
84. Killian JA, von Heijne G. How proteins adapt to a membrane-water interface. Trends Biochem Sci 2000;25:429-434.
85. Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP. Crystal-structures explain functional-properties of 2 Escherichia coli porins. Nature 1992;358:727-733.
86. Persson S, Killian JA, Lindblom G. Molecular ordering of interfacially localized tryptophan analogs in ester- and ether-lipid bilayers studied by 2H-NMR. Biophys J 1998;75:1365-1371.
87. de Planque MR, Bonev BB, Demmers JA, Greathouse DV, Koeppe RE, 2nd, Separovic F, Watts A, Killian JA. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 2003;42:5341-5348.
88. de Planque MR, Kruijtzer JA, Liskamp RM, Marsh D, Greathouse DV, Koeppe RE, 2nd, de Kruijff B, Killian JA. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane alpha-helical peptides. J Biol Chem 1999;274:20839-20846.
89. Gray TM, Matthews BM. Intrahelical hydrogen bonding of serine, threonine and cysteine residues within α-helices and its relevance to membrane-bound proteins. J Mol Biol 1984;175:75-81.
90. Brandi CJ, Deber CM. Hypothesis about the function of membrane-buried proline residues in transport proteins. Proc Natl Acad Sci USA 1986;83:917-921.
91. von Heijne G. Proline kinks in transmembrane α-helices. J Mol Biol 1991;218:499-503.
92. Woolfson DN, Mortishire-Smith RJ, Williams DH. Conserved positioning of proline residues in membrane-spanning helices of ion-channel proteins. Biochem Biophys Res Comm 1991;175:733-737.
93. Sansom MSP, Weinstein H. Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha helices. TIPS 2000;21:445-451.
94. Subramaniam S, Henderson R. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 2000;406:653-657.
95. Sass HJ, Buldt G, Gessenich R, Hehn D, Neff D, Schlesinger R, Berendzen J, Ormos P. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature 2000;406:649-653.
96. Royant A, Nollert P, Edman K, Neutze R, Landau EM, Pebay-Peyroula E, Navarro J. X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc Natl Acad Sci USA 2001;98:10131-10136.
97. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 Å resolution. Nature 2001;414:43-48.
98. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 2003;301:616-620.
99. MacKenzie KR, Prestegard JH, Engelman DM. A transmembrane helix dimer: structure and implications. Science 1997;276:131-133.
100. Sui H, Han BG, Lee JK, Walian P, Jap BK. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001;414:872-878.
101. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R. X-ray structure of a CIC chloride channel at 3.0 angstrom reveals the molecular basis of anion selectivity. Nature 2002;415:287-294.
102. Hunt JF, Earnest TN, Bousche O, Kalghatgi K, Reilly K, Horvath C, Rothschild KJ, Engelman DM. A biophysical study of integral membrane protein folding. Biochemistry 1997;36:15156-15176.
103. Hunt JF, Rath P, Rothschild KJ, Engelman DM. Spontaneous, pH-dependent membrane insertion of a transbilayer alpha-helix. Biochemistry 1997;36:15177-15192.
104. Bechinger B. Towards membrane protein design: pH-sensitive topology of histidine-containing polypeptides. J Mol Biol 1996;263:768-775.
105. Moll TS, Thompson TE. Semisynthetic proteins: model systems for the study of the insertion of hydrophobic peptides into preformed lipid bilayers. Biochemistry 1994;33:15469-15482.
106. Soekarjo M, Eisenhawer M, Kuhn A, Vogel H. Thermodynamics of the membrane insertion process of the M13 procoat protein, a lipid bilayer traversing protein containing a leader sequence. Biochemistry 1996;35:1232-1241.
107. White SH, Wimley WC. Hydrophobic interactions of peptides with membrane interfaces. Biochim Biophys Acta 1998;1376:339-352
108. Opella SJ, Marassi FM, Gesell JJ, Valente AP, Kim Y, Oblatt-Montal M, Montai M. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat Struct Biol 1999;6:374-379.
109. Kessel A, Shental-Bechor D, Haliloglu T, Ben-Tal N. Interactions of hydrophobic peptides with lipid bilayers: Monte Carlo simulations with M2delta. Biophys J 2003;85:3431-3444.
110. Kessel A, Haliloglu T, Ben-Tal N. Interactions of the M2delta segment of the acetylcholine receptor with lipid bilayers: a continuum-solvent model study. Biophys J 2003;85:3687-3695.
111. Ben-Tal N, Ben-Shaul A, Nicholls A, Honig B. Free-energy determinants of alpha-helix insertion into lipid bilayers. Biophys J 1996;70:1803-1812.
112. Kessel A, Tieleman DP, Ben-Tal N. Implicit solvent model estimates of the stability of model structures of the alamethicin channel. Eur Biophys J 2004;33:16-28.
113. Popot JL, Engelman DM. Membrane-protein folding and oligomerization-the 2-stage model. Biochemistry 1990;29:4031-4037.
114. Liao MJ, Huang KS, Khorana HG. Regeneration of native bacteriorhodopsin structure from fragments. J Biol Chem 1984;259:4200-4204.
115. Liao MJ, London E, Khorana HG. Regeneration of the native bacteriorhodopsin structure from 2 chymotryptic fragments. J Biol Chem 1983;258:9949-9955.
116. von Heijne G. Principles of membrane protein assembly and structure. Prog Biophys Mol Biol 1997;66:113-139.