Amino-acid solvation structure in transmembrane helices from molecular dynamics simulations

Biophysical Journal

Volumn 91, Issue 12, 2006, Pages 4450-4463

  Johansson, Anna C V ^a   Lindahl, Erik ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; ASPARTIC ACID; GLUTAMIC ACID; LYSINE; MEMBRANE PROTEIN; SERINE; THREONINE; TRYPTOPHAN; TYROSINE; WATER;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HYDROPHOBICITY; MOLECULAR DYNAMICS; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 33845424528     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.092767     Document Type: Article

References (62)

1. Wallin, E., and G. von Heijne. 1998. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7:1029-1038.
2. Terstappen, G., and A. Reggiani. 2001. In silico research in drug discovery. Trends Pharmacol. Sci. 22:23-26.
3. Popot, J. L., and D. M. Engelman. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry. 29:4031-4037.
4. White, S. H., and G. von Heijne. 2005. Transmembrane helices before, during, and after insertion. Curr. Opin. Struct. Biol. 15:378-386.
5. White, S. 2006. Membrane proteins of known structure. Http://blanco.biomol.uci.edu/Membrane_Proteins_xtal.html.
6. Dempsey, C. 1990. The actions of melittin on membranes. Biochim. Biophys. Acta. 1031:143-161.
7. Blobel, G., and B. Dobberstein. 1975. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67:835-851.
8. Engelman, D., Y. Chen, C.-N. Chi, A. Curran, A. Dixon, A. Dupuy, A. Lee, U. Lehnert, E. Matthews, Y. Reshetnyak, A. Senes, and J.-L. Popot. 2003. Membrane protein folding: beyond the two-stage model. FEBS Lett. 555:122-125.
9. Tourasse, N. J., and W. H. Li. 2000. Selective constraints, amino acid composition, and the rate of protein evolution. Mol.Biol. Evol. 17:656-664.
10. Arkin, I. T., and A. T. Brunger. 1998. Statistical analysis of predicted transmembrane α-helices. Biochim. Biophys. Acta. 1429:113-128.
11. Henderson, R., J. M. Baldwin, T. A. Ceska, F. Zemlin, E. Beckmann, and K. H. Downing. 1990. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213:899-929.
12. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structural changes in bacteriorhodopsin during ion transport at 2 Ångström resolution. Science. 286:255-261.
13. Iwata, S., C. Ostermeier, B. Ludwig, and H. Michel. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 376:660-669.
14. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87.
15. Gumbart, J., and K. Schulten. 2006. Molecular dynamics studies of the archaeal translocon. Biophys. J. 90:2356-2367.
16. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
17. Hristova, K., C. E. Dempsey, and S. H. White. 2001. Structure, location, and lipid perturbations of melittin at the membrane interface. Biophys. J. 80:801-811.
18. Aliste, M., and D. P. Tieleman. 2005. Computer simulation of partitioning of 10 pentapeptides ACE-WLXLL at the cyclohexane/water and phospholipid/water interfaces. BMC Biochem. 6:30.
19. Bond, P. J., and M. S. P. Sansom. 2006. Insertion and assembly of membrane proteins via simulation. J. Am. Chem. Soc. 128:2697-2704.
20. Johnston, J. M., G. A. Cook, J. M. Tomich, and M. S. P. Sansom. 2006. Conformation and environment of channel-forming peptides: a simulation study. Biophys. J. 90:1855-1864.
21. Monticelli, L., K. M. Robertson, J. L. MacCallum, and D. P. Tieleman. 2004. Computer simulation of the KVaP voltage-gated potassium channel: steered molecular dynamics of the voltage sensor. FEBS Lett. 564:325-332.
22. Freites, J. A., D. J. Tobias, G. von Heijne, and S. H. White. 2005. Interface connections of a transmembrane voltage sensor. Proc. Natl. Acad. Sci. USA. 102:15059-15064.
23. Fleming, K. G., and D. M. Engelman. 2001. Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants. Proc. Natl. Acad. Sci. USA. 98:14340-14344.
24. Gratkowski, L., J. D. Lear, and W. F. DeGrado. 2001. Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. USA. 98:880-885.
25. Zhou, R., B. J. Berne, and R. Germain. 2001. The free energy landscape for β hairpin folding in explicit water. Proc. Natl. Acad. Sci. USA. 98:14931-14936.
26. Hénin, J., A. Pohorille, and C. Chipot. 2005. Insights into the recognition and association of transmembrane α-helices. The free energy of α-helix dimerization in glycophorin A. J. Am. Chem. Soc. 127:8478-8484.
27. Mottamal, M., J. Zhang, and T. Lazaridis. 2006. Energetics of the native and non-native states of the glycophorin transmembrane helix dimer. Proteins Struct. Funct. Gen. 62:996-1009.
28. Chamberlain, A. K., Y. Lee, S. Kim, and J. U. Bowie. 2004. Snorkeling preferences foster an amino acid composition bias in transmembrane helices. J. Mol. Biol. 339:471-479.
29. Chamberlain, A. K., and J. U. Bowie. 2004. Analysis of side-chain rotamers in transmembrane proteins. Biophys. J. 87:3460-3469.
30. Granseth, E., G. von Heijne, and A. Elofsson. 2005. A study of the membrane-water interface region of membrane proteins. J. Mol. Biol. 346:377-385.
31. Strandberg, E., S. Morein, D. T. S. Rijkers, R. M. J. Liskamp, P. r. C. A. van der Wel, and J. A. Killian. 2002. Lipid dependence of membrane anchoring properties and snorkeling behavior of aromatic and charged residues in transmembrane peptides. Biochemistry. 41:7190-8.
32. Strandberg, E., and J. A. Killian. 2003. Snorkeling of lysine side chains in transmembrane helices: how easy can it get? FEBS Lett. 544:69-73.
33. Deol, S. S., P. J. Bond, C. Domene, and M. S. P. Sansom. 2004. Lipid-protein interactions of integral membrane proteins: a comparative simulation study. Biophys. J. 87:3737-3749.
34. Kandasamy, S. K., and R. G. Larson. 2005. Molecular dynamics study of the lung surfactant peptide SP-B1-25 with DPPC monolayers: insights into interactions and peptide position and orientation. Biophys. J. 88:1577-1592.
35. Stockner, T., W. L. Ash, J. L. MacCallum, and D. P. Tieleman. 2004. Direct simulation of transmembrane helix association: role of asparagines. Biophys. J. 87:1650-1656.
36. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848.
37. Hessa, T., S. H. White, and G. von Heijne. 2005. Membrane insertion of a potassium-channel voltage sensor. Science. 307:1427.
38. Hessa, T., H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, H. Andersson, I. Nilsson, S. H. White, and G. von Heijne. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature. 433:377-381.
39. Heinrich, S., W. Mothes, J. Brunner, and T. Rapoport. 2000. The SEC61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell. 102:233-244.
40. Lindahl, E., and O. Edholm. 2000. Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecules dynamics simulations. Biophys. J. 79:426-433.
41. Berger, O., O. Edholm, and F. Jähnig. 1997. Molecular dynamics simulation of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure and constant temperature. Biophys. J. 72:2002-2013.
42. Ryckaert, J., and A. Bellemans. 1975. Molecular dynamics of liquid n-butane near its boiling point. Chem. Phys. Lett. 30:123-125.
43. Lindahl, E., and O. Edholm. 2001. Molecular dynamics simulation of NMR relaxation rates and slow dynamics in lipid bilayers. J. Chem. Phys. 115:4938-4950.
44. Benz, R., F. Castro-Roman, D. Tobias, and S. White. 2005. Experimental validation of molecular dynamics simulations of lipid bilayers: a new approach. Biophys. J. 88:805-817.
45. Schuler, L. D., X. Daura, and W. F. van Gunsteren. 2001. An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase. J. Comput. Chem. 22:1205-1218.
46. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. D. Reidel Publishing Company, Dordrecht, The Netherlands. 331-342.
47. Lindahl, E., B. A. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7:306-317.
48. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
49. Miyamoto, S., and P. A. Kollman. 1992. SETTLE: An analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comput. Chem. 13:952-962.
50. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8592.
51. Wohlert, J., and O. Edholm. 2004. The range and shielding of dipoledipole interactions in phospholipid bilayers. Biophys. J. 87:2433-2445.
52. Berendsen, H. J. C., J. P. M. Postma, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
53. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
54. Adamian, L., V. Nanda, W. F. DeGrado, and J. Liang. 2005. Empirical lipid propensities of amino acid residues in multispan alpha-helical membrane proteins. Proteins Struct. Funct. Gen. 59:496-509.
55. α-H. . .O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc. Natl. Acad. Sci. USA. 98:9056-9061.
56. de Planque, M. R., B. B. Bonev, J. A. Demmers, D. V. Greathouse, R. E. Koeppe, F. Separovic, A. Watts, and J. A. Killian. 2003. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry. 42:5341-5348.
57. Lear, J. D., H. Gratkowski, L. Adamian, J. Liang, and W. F. DeGrado. 2003. Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry. 42:6400-6407.
58. Hofsäss, C., E. Lindahl, and O. Edholm. 2003. Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 84:2192-2206.
59. Repáková, J., J. M. Holopainen, M. Karttunen, and I. Vattulainen. 2006. Influence of pyrene-labeling on fluid lipid membranes. J. Phys. Chem. B. 110:15403-15410.
60. Sum, A. K., R. Faller, and J. J. de Pablo. 2003. Molecular simulation study of phospholipid bilayers and insights of the interactions with disaccharides. Biophys. J. 85:2830-2844.
61. Woolfson, D. N., R. J. Mortishire-Smith, and D. H. Williams. 1991. Conserved positioning of proline residues in membrane-spanning helices of ion-channel proteins. Biochim. Biophys. Acta. 175:733-737.
62. Varma, S., S.-W. Chiu, and E. Jakobsson. 2006. The influence of amino acid protonation states on molecular dynamics simulations of the bacterial porin OmpF. Biophys. J. 90:112-123.