The role of tryptophan side chains in membrane protein anchoring and hydrophobic mismatch

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 2, 2013, Pages 864-876

  De Jesus, Armando J ^a   Allen, Toby W ^a,b  

^a RMIT UNIVERSITY   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Free energy; Hydrophobic mismatch; Membrane protein; Molecular Dynamics; Protein lipid interactions; Tryptophan

Indexed keywords

CARBONYL DERIVATIVE; GLYCEROL; MEMBRANE PROTEIN; PHOSPHATE; SKATOLE; TRYPTOPHAN; UNCLASSIFIED DRUG; WALP LIKE PEPTIDE;

ALPHA HELIX; ARTICLE; HYDROGEN BOND; MEMBRANE DAMAGE; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN STABILITY; THERMODYNAMICS;

BIOPHYSICS; CATIONS; CELL MEMBRANE; GLYCEROL; HYDROGEN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LEUCINE; LIPID BILAYERS; LIPIDS; MOLECULAR DYNAMICS SIMULATION; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; THERMODYNAMICS; TRYPTOPHAN; WATER;

EID: 84871752186     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.09.009     Document Type: Article

References (78)

1. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter Molecular Biology of the Cell 2002 Garland Science New York, NY
2. R. Gennis Biomembrane - Molecular Structure and Function 1989 Springer-Verlag New York
3. G. von Heijne The membrane protein universe: what's out there and why bother? J. Intern. Med. 261 2007 543 557
4. D.J. Muller, N. Wu, and K. Palczewski Vertebrate membrane proteins: structure, function, and insights from biophysical approaches Pharmacol. Rev. 60 2008 43 78
5. A.G. Lee How lipids affect the activities of integral membrane proteins Biochim. Biophys. Acta Biomembr. 1666 2004 62 87
6. C. Hunte, and S. Richers Lipids and membrane protein structures Curr. Opin. Struct. Biol. 18 2008 406 411
7. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
8. A.J. de Jesus, T.W. Allen, On the responses to hydrophobic mismatch of transmembrane helices, BBA-Biomembranes, submitted for publication.
9. J.A. Killian Hydrophobic mismatch between proteins and lipids in membranes Biochim. Biophys. Acta Rev. Biomembr. 1376 1998 401 416
10. O.S. Andersen, and R.E. Koeppe Bilayer thickness and membrane protein function: an energetic perspective Annu. Rev. Biophys. Biomol. 36 2007 107 130
11. G. von Heijne The distribution of positively charged residues in bacterial inner membrane proteins correlates with the transmembrane topology EMBO J. 5 1986 3021 3027
12. M. Schiffer, C.H. Chang, and F.J. Stevens The functions of tryptophan residues in membrane-proteins Protein Eng. 5 1992 213 214
13. J.A. Killian, and G. von Heijne How proteins adapt to a membrane-water interface Trends Biochem. Sci. 25 2000 429 434
14. W.M. Yau, W.C. Wimley, K. Gawrisch, and S.H. White The preference of tryptophan for membrane interfaces Biochemistry-Us 37 1998 14713 14718
15. M.R.R. de Planque, J.A.W. Kruijtzer, R.M.J. Liskamp, D. Marsh, D.V. Greathouse, R.E. Koeppe, B. de Kruijff, and J.A. Killian Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane alpha-helical peptides J. Biol. Chem. 274 1999 20839 20846
16. M.R.R. de Planque, B.B. Bonev, J.A.A. Demmers, D.V. Greathouse, R.E. Koeppe, F. Separovic, A. Watts, and J.A. Killian Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions Biochemistry-Us 42 2003 5341 5348
17. M.R.R. de Planque, and J.A. Killian Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring (Review) Mol. Membr. Biol. 20 2003 271 284
18. N. Bordag, and S. Keller alpha-Helical transmembrane peptides: a "divide and conquer" approach to membrane proteins Chem. Phys. Lipids 163 2010 1 26
19. A. Ridder, S. Morein, J.G. Stam, A. Kuhn, B. de Kruijff, and J.A. Killian Analysis of the role of interfacial tryptophan residues in controlling the topology of membrane proteins Biochemistry-Us 39 2000 6521 6528
20. C. Landolt-Marticorena, K.A. Williams, C.M. Deber, and R.A.F. Reithmeier Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins J. Mol. Biol. 229 1993 602 608
21. I.T. Arkin, and A.T. Brunger Statistical analysis of predicted transmembrane alpha-helices Biochim. Biophys. Acta 1429 1998 113 128
22. S.W. Cowan, T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, R.A. Pauptit, J.N. Jansonius, and J.P. Rosenbusch Crystal-structures explain functional-properties of 2 Escherichia coli porins Nature 358 1992 727 733
23. M.S. Weiss, U. Abele, J. Weckesser, W. Welte, E. Schiltz, and G.E. Schulz Molecular architecture and electrostatic properties of a bacterial porin Science 254 1991 1627 1630
24. + conduction and selectivity Science 280 1998 69 77
25. F. Kovacs, J. Quine, and T.A. Cross Validation of the single-stranded channel conformation of gramicidin A by solid-state NMR Proc. Natl. Acad. Sci. U.S.A. 96 1999 7910 7915
26. T.A. Cross, A. Arseniev, B.A. Cornell, J.H. Davis, J.A. Killian, R.E. Koeppe, L.K. Nicholson, F. Separovic, and B.A. Wallace Gramicidin channel controversy - revisited Nat. Struct. Biol. 6 1999 610 611
27. E. Wallin, T. Tsukihara, S. Yoshikawa, G. VonHeijne, and A. Elofsson Architecture of helix bundle membrane proteins: an analysis of cytochrome c oxidase from bovine mitochondria Protein Sci. 6 1997 808 815
28. S. Fiedler, J. Broecker, and S. Keller Protein folding in membranes Cell. Mol. Life Sci. 67 2010 1779 1798
29. K.M. Sanchez, J.E. Gable, D.E. Schlamadinger, and J.E. Kim Effects of tryptophan microenvironment, soluble domain, and vesicle size on the thermodynamics of membrane protein folding: lessons from the transmembrane protein OmpA † Biochemistry-Us 47 2008 12844 12852
30. H. Sun, D.V. Greathouse, O.S. Andersen, and R.E. Koeppe The preference of tryptophan for membrane interfaces - insights from n-methylation of tryptophans in gramicidin channels J. Biol. Chem. 283 2008 22233 22243
31. W. Hu, K.C. Lee, and T.A. Cross Tryptophans in membrane-proteins - indole ring orientations and functional implications in the gramicidin channel Biochemistry-Us 32 1993 7035 7047
32. A. Chattopadhyay, S.S. Rawat, D.V. Greathouse, D.A. Kelkar, and R.E. Koeppe Role of tryptophan residues in gramicidin channel organization and function Biophys. J. 95 2008 166 175
33. J.C. Garcia, M. Strube, K. Leingang, K. Keller, and M.M. Mueckler Amino-acid substitutions at tryptophan-388 and tryptophan-412 of the Hepg2 (Glut1) glucose transporter inhibit transport activity and targeting to the plasma-membrane in Xenopus oocytes J. Biol. Chem. 267 1992 7770 7776
34. D.A. Dougherty Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp Science 271 1996 163 168
35. M. Navedo, M. Nieves, L. Rojas, and J.A. Lasalde-Dominicci Tryptophan substitutions reveal the role of nicotinic acetylcholine receptor alpha-TM3 domain in channel gating: differences between torpedo and muscle-type AChR Biochemistry-Us 43 2004 78 84
36. H.D. Hong, S. Park, R.H.F. Jimenez, D. Rinehart, and L.K. Tamm Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins J. Am. Chem. Soc. 129 2007 8320 8327
37. H.Y. Xu, L.K. Song, M. Kim, M.A. Holmes, Z. Kraft, G. Sellhorn, E.L. Reinherz, L. Stamatatos, and R.K. Strong Interactions between lipids and human anti-HIV antibody 4E10 can be reduced without ablating neutralizing activity J. Virol. 84 2010 1076 1088
38. A.G. Lee Lipid-protein interactions in biological membranes: a structural perspective Biochim. Biophys. Acta Biomembr. 1612 2003 1 40
39. J.A. Killian, and T.K.M. Nyholm Peptides in lipid bilayers: the power of simple models Curr. Opin. Struct. Biol. 16 2006 473 479
40. A. Holt, and J.A. Killian Orientation and dynamics of transmembrane peptides: the power of simple models Eur. Biophys. J. Biophys. 39 2010 609 621
41. M.R.R. de Planque, D.V. Greathouse, R.E. Koeppe, H. Schafer, D. Marsh, and J.A. Killian Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A H-2 NMR and ESR study using designed transmembrane alpha-helical peptides and gramicidin A Biochemistry-Us 37 1998 9333 9345
42. S.O. Nielsen, B. Ensing, V. Ortiz, P.B. Moore, and M.L. Klein Lipid bilayer perturbations around a transmembrane nanotube: a coarse grain molecular dynamics study Biophys. J. 88 2005 3822 3828
43. T.M. Weiss, P.C.A. van der Wel, J.A. Killian, R.E. Koeppe, and H.W. Huang Hydrophobic mismatch between helices and lipid bilayers Biophys. J. 84 2003 379 385
44. J.A. Killian, I. Salemink, M.R. de Planque, G. Lindblom, R.E. Koeppe II, and D.V. Greathouse Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane alpha-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans Biochemistry-Us 35 1996 1037 1045
45. J.A.A. Demmers, E. van Duijn, J. Haverkamp, D.V. Greathouse, R.E. Koeppe, A.J.R. Heck, and J.A. Killian Interfacial positioning and stability of transmembrane peptides in lipid bilayers studied by combining hydrogen/deuterium exchange and mass spectrometry J. Biol. Chem. 276 2001 34501 34508
46. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848
47. H.C. Gaede, W.M. Yau, and K. Gawrisch Electrostatic contributions to indole-lipid interactions J. Phys. Chem. B 109 2005 13014 13023
48. K.E. Norman, and H. Nymeyer Indole localization in lipid membranes revealed by molecular simulation Biophys. J. 91 2006 2046 2054
49. S. Persson, J.A. Killian, and G. Lindblom Molecular ordering of interfacially localized tryptophan analogs in ester- and ether-lipid bilayers studied by H-2 NMR Biophys. J. 75 1998 1365 1371
50. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Distribution of amino acids in a lipid bilayer from computer simulations Biophys. J. 94 2008 3393 3404
51. F.N.R. Petersen, M.O. Jensen, and C.H. Nielsen Interfacial tryptophan residues: a role for the cation-pi effect? Biophys. J. 89 2005 3985 3996
52. J.T. Durkin, L.L. Providence, R.E. Koeppe, and O.S. Andersen Formation of non-beta-6.3-helical gramicidin channels between sequence-substituted gramicidin analogs Biophys. J. 62 1992 145 159
53. D. Salom, E. Perez-Paya, J. Pascal, and C. Abad Environment- and sequence-dependent modulation of the double-stranded to single-stranded conformational transition of gramicidin A in membranes Biochemistry-Us 37 1998 14279 14291
54. J.C. Ma, and D.A. Dougherty The cation-pi interaction Chem. Rev. 97 1997 1303 1324
55. T.B. Woolf, A. Grossfield, and J.G. Pearson Indoles at interfaces: calculations of electrostatic effects with density functional and molecular dynamics methods Int. J. Quantum Chem. 75 1999 197 206
56. A. Grossfield, and T.B. Woolf Interaction of tryptophan analogs with POPC lipid bilayers investigated by molecular dynamics calculations Langmuir 18 2002 198 210
57. G.M. Torrie, and J.P. Valleau Non-physical sampling distributions in Monte-Carlo free-energy estimation - Umbrella Sampling J. Comput. Phys. 23 1977 187 199
58. S. Dorairaj, and T.W. Allen On the thermodynamic stability of a charged arginine side chain in a transmembrane helix Proc. Natl. Acad. Sci. U.S.A. 104 2007 4943 4948
59. L.B. Li, I. Vorobyov, and T.W. Allen Potential of mean force and pK(a) profile calculation for a lipid membrane-exposed arginine side chain J. Phys. Chem. B 112 2008 9574 9587
60. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
61. S.E. Feller, and A.D. MacKerell An improved empirical potential energy function for molecular simulations of phospholipids J. Phys. Chem. B 104 2000 7510 7515
62. A.D. MacKerell, D. Bashford, M. Bellott, R.L. Dunbrack, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F.T.K. Lau, C. Mattos, S. Michnick, T. Ngo, D.T. Nguyen, B. Prodhom, W.E. Reiher, B. Roux, M. Schlenkrich, J.C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
63. D. Yin, and A.D. MacKerell Combined ab initio/empirical approach for optimization of Lennard-Jones parameters J. Comput. Chem. 19 1998 334 348
64. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
65. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
66. J.-P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
67. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N [center-dot] log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
68. S. Nose A molecular-dynamics method for simulations in the canonical ensemble Mol. Phys. 52 1984 255 268
69. W.G. Hoover Canonical dynamics - equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
70. S.E. Feller, Y.H. Zhang, R.W. Pastor, and B.R. Brooks Constant-pressure molecular-dynamics simulation - the Langevin piston method J. Chem. Phys. 103 1995 4613 4621
71. L. Li, I. Vorobyov, A.D. MacKerell, and T.W. Allen Is arginine charged in a membrane? Biophys. J. 94 2008 L11 L13
72. J.F. Nagle Area/lipid of bilayers from NMR Biophys. J. 64 1993 1476 1481
73. S. Kumar, D. Bouzida, R.H. Swendsen, P.A. Kollman, and J.M. Rosenberg The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method J. Comput. Chem. 13 1992 1011 1021
74. L.B. Li, I. Vorobyov, S. Dorairaj, and T.W. Allen Charged protein side chain movement in lipid bilayers explored with free energy simulation Curr. Top. Membr. 60 2008 405 459
75. H.I. Petrache, S.E. Feller, and J.F. Nagle Determination of component volumes of lipid bilayers from simulations Biophys. J. 72 1997 2237 2242
76. M.P. Aliste, J.L. MacCallum, and D.P. Tieleman Molecular dynamics simulations of pentapeptides at interfaces: salt bridge and cation-pi interactions Biochemistry-Us 42 2003 8976 8987
77. A. Radzicka, and R. Wolfenden Comparing the polarities of the amino-acids - side-chain distribution coefficients between the vapor-phase, cyclohexane, 1-octanol, and neutral aqueous-solution Biochemistry-Us 27 1988 1664 1670
78. V.V. Vostrikov, B.A. Hall, D.V. Greathouse, R.E. Koeppe, and M.S.P. Sansom Changes in transmembrane helix alignment by arginine residues revealed by solid-state NMR experiments and coarse-grained MD simulations J. Am. Chem. Soc. 132 2010 5803 5811