A generalized born implicit-membrane representation compared to experimental insertion free energies

Biophysical Journal

Volumn 92, Issue 7, 2007, Pages 2338-2349

  Ulmschneider, Martin B ^a,c   Ulmschneider, Jakob P ^b   Sansom, Mark S P ^a   Di Nolay, Alfredo ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; CHLORIDE CHANNEL; CYCLOHEXANE; CYCLOOXYGENASE 2; GLYCOPHORIN A; MEMBRANE PROTEIN; POLYPEPTIDE; PROSTAGLANDIN SYNTHASE; SENSORY RHODOPSIN; TRANSLOCON; WATER;

ALPHA HELIX; ARTICLE; CORRELATION ANALYSIS; ENERGY; HUMAN; HYDROPHOBICITY; INFLUENZA VIRUS A; MATHEMATICAL COMPUTING; MEMBRANE MODEL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SIMULATION; SOLVATION; STATISTICAL ANALYSIS;

EID: 34047240165     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.081810     Document Type: Article

References (88)

1. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
2. 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.
3. Jones, D. T. 1998. Do transmembrane protein superfolds exist? FEBS Lett. 423:281-285.
4. Terstappen, G. C., and A. Reggiani. 2001. In silico research in drug discovery. Trends Pharmacol. Sci. 22:23-26.
5. Grisshammer, R., and C. G. Tate. 1995. Overexpression of integral membrane-proteins for structural studies. Q. Rev. Biophys. 28:315-422.
6. Biggin, P. C., and M. S. P. Sansom. 1999. Interactions of α-helices with lipid bilayers: a review of simulation studies. Biophys. Chem. 76:161-183.
7. Forrest, L. R., and M. S. P. Sansom. 2000. Membrane simulations: bigger and better? Curr. Opin. Struct. Biol. 10:174-181.
8. Domene, C., P. Bond, and M. S. P. Sansom. 2003. Membrane protein simulation: ion channels and bacterial outer membrane proteins. Adv. Prot. Chem. 66:159-193.
9. Nymeyer, H., T. B. Woolf, and A. E. Garcia. 2005. Folding is not required for bilayer insertion: replica exchange simulations of an α-helical peptide with an explicit lipid bilayer. Proteins. 59:783-790.
10. Pellegrini-Calace, M., A. Carotti, and D. T. Jones. 2003. Folding in lipid membranes (FILM): a novel method for the prediction of small membrane protein 3D structures. Proteins. 50:537-545.
11. Zhang, Y., M. E. Devries, and J. Skolnick. 2006. Structure modeling of all identified G protein-coupled receptors in the human genome. PLoS Comput. Biol. 2:e13.
12. Ulmschneider, M. B., M. S. Sansom, and A. Di Nola. 2005. Properties of integral membrane protein structures: derivation of an implicit membrane potential. Proteins. 59:252-265.
13. Hurwitz, N., M. Pellegrini-Calace, and D. T. Jones. 2006. Towards genome-scale structure prediction for transmembrane proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:465-475.
14. Milik, M., and J. Skolnick. 1995. A Monte Carlo model of fd and Pf1 coat proteins in lipid membranes. Biophys. J. 69:1382-1386.
15. Maddox, M. W., and M. L. Longo. 2002. A Monte Carlo study of peptide insertion into lipid bilayers: equilibrium conformations and insertion mechanisms. Biophys. J. 82:244-263.
16. Milik, M., and J. Skolnick. 1993. Insertion of peptide chains into lipid membranes: an off-lattice Monte Carlo dynamics model. Proteins. 15:10-25.
17. Grossfield, A., J. Sachs, and T. B. Woolf. 2000. Dipole lattice membrane model for protein calculations. Proteins. 41:211-223.
18. Lazaridis, T. 2003. Effective energy function for proteins in lipid membranes. Proteins. 52:176-192.
19. Efremov, R. G., D. E. Nolde, G. Vergoten, and A. S. Arseniev. 1999. A solvent model for simulations of peptides in bilayers. I. Membrane-promoting α-helix formation. Biophys. J. 76:2448-2459.
20. Efremov, R. G., D. E. Nolde, G. Vergoten, and A. S. Arseniev. 1999. A solvent model for simulations of peptides in bilayers. II. Membrane-spanning α-helices. Biophys. J. 76:2460-2471.
21. Sengupta, D., L. Meinhold, D. Langosch, G. M. Ullmann, and J. C. Smith. 2005. Understanding the energetics of helical peptide orientation in membranes. Proteins. 58:913-922.
22. Ben-Tal, N., B. Honig, C. K. Bagdassarian, and A. Ben-Shaul. 2000. Association entropy in adsorption processes. Biophys. J. 79:1180-1187.
23. Woolf, T. B., D. M. Zuckerman, N. D. Lu, and H. B. Jang. 2004. Tools for channels: moving towards molecular calculations of gating and permeation in ion channel biophysics. J. Mol. Graph. 22:359-368.
24. Efremov, R. G., D. E. Nolde, A. G. Konshina, N. P. Syrtcev, and A. S. Arseniev. 2004. Peptides and proteins in membranes: What can we learn via computer simulations? Curr. Med. Chem. 11:2421-2442.
25. Born. 1920. Volumen und Hydratationswärme der Ionen. Z. Phys. 1:45-48.
26. Still, W. C., A. Tempczyk, R. C. Hawley, and T. Hendrickson. 1990. Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112:6127-6129.α
27. Ulmschneider, J. P., and W. L. Jorgensen. 2004. Polypeptide folding using Monte Carlo sampling, concerted rotation, and continuum solvation. J. Am. Chem. Soc. 126:1849-1857.
28. Chowdhury, S., W. Zhang, C. Wu, G. M. Xiong, and Y. Duan. 2003. Breaking non-native hydrophobic clusters is the rate-limiting step in the folding of an alanine-based peptide. Biopolymers. 68:63-75.
29. Jang, S., S. Shin, and Y. Pak. 2002. Molecular dynamics study of peptides in implicit water: ab initio folding of β-hairpin, β-sheet, and ββα-motif. J. Am. Chem. Soc. 124:4976-4977.
30. Simmerling, C., B. Strockbine, and A. E. Roitberg. 2002. All-atom structure prediction and folding simulations of a stable protein. J. Am. Chem. Soc. 124:11258-11259.
31. Snow, C. D., N. Nguyen, V. S. Pande, and M. Gruebele. 2002. Absolute comparison of simulated and experimental protein-folding dynamics. Nature. 420:102-106.
32. Tanizaki, S., and M. Feig. 2005. A generalized Born formalism for heterogeneous dielectric environments: application to the implicit modeling of biological membranes. J. Chem. Phys. 122:124706.
33. Spassov, V. Z., L. Yan, and S. Szalma. 2002. Introducing an implicit membrane in generalized Born/solvent accessibility continuum solvent models. J. Phys. Chem. B. 106:8726-8738.
34. Im, W., M. Feig, and C. L. Brooks III. 2003. An implicit membrane generalized Born theory for the study of structure, stability, and interactions of membrane proteins. Biophys. J. 85:2900-2918.
35. Im, W., and C. L. Brooks III. 2004. De novo folding of membrane proteins: an exploration of the structure and NMR properties of the fd coat protein. J. Mol. Biol. 337:513-519.
36. 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.
37. Hessa, T., S. H. White, and G. von Heijne. 2005. Membrane insertion of a potassium-channel voltage sensor. Science. 307:1427.
38. Totrov, M. 2004. Accurate and efficient generalized Born model based on solvent accessibility: derivation and application for LogP octanol/water prediction and flexible peptide docking. J. Comput. Chem. 25:609-619.
39. Radzicka, A., and R. Wolfenden. 1988. Comparing the polarities of the amino-acids - side-chain distribution coefficients between the vaporphase, cyclohexane, 1-octanol, and neutral aqueous-solution. Biochemistry. 27:1664-1670.
40. Wimley, W. C., T. P. Creamer, and S. H. White. 1996. Solvation energies of amino acid side chains and backbone in a family of hostguest pentapeptides. Biochemistry. 35:5109-5124.
41. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848.
42. Opella, S. J., and F. M. Marassi. 2004. Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104:3587-3606.
43. Bashford, D., and D. A. Case. 2000. Generalized Born models of macromolecular solvation effects. Annu. Rev. Phys. Chem. 51:129-152.
44. Qiu, D., P. S. Shenkin, F. P. Hollinger, and W. C. Still. 1997. The GB/SA continuum model for solvation. A fast analytical method for the calculation of approximate Born radii. J. Phys. Chem. A. 101:3005-3014.
45. Jorgensen, W. L., J. P. Ulmschneider, and J. Tirado-Rives. 2004. Free energies of hydration from a generalized Born model and an ALL-atom force field. J. Phys. Chem. B. 108:16264-16270.
46. Schaefer, M., C. Bartels, and M. Karplus. 1998. Solution conformations and thermodynamics of structured peptides: molecular dynamics simulation with an implicit solvation model. J. Mol. Biol. 284:835-848.
47. Killian, J. A. 2003. Synthetic peptides as models for intrinsic membrane proteins. FEBS Lett. 555:134-138.
48. de Planque, M. R., and J. A. Killian. 2003. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 20:271-284.
49. Wiener, M. C., and S. H. White. 1991. 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. 59:162-173.
50. Wiener, M. C., and S. H. White. 1991. Fluid bilayer structure determination by the combined use of x-ray and neutron diffraction. II. "Composition-space" refinement method. Biophys. J. 59:174-185.
51. Wiener, M. C., and S. H. White. 1992. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61:437-447.
52. White, S. H., G. I. King, and J. I. Cain. 1981. Location of hexane in lipid bilayers determined by neutron diffraction. Nature. 290:161-163.
53. Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature. 221:844-846.
54. Saaf, A., E. Wallin, and G. von Heijne. 1998. Stop-transfer function of pseudo-random amino acid segments during translocation across prokaryotic and eukaryotic membranes. Eur. J. Biochem. 251:821-829.
55. Opella, S. J., F. M. Marassi, J. J. Gesell, A. P. Valente, Y. Kim, M. Oblatt-Montal, and M. Montal. 1999. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol. 6:374-379.
56. Wang, J., S. Kim, F. Kovacs, and T. A. Cross. 2001. Structure of the transmembrane region of the M2 protein H(+) channel. Protein Sci. 10:2241-2250.
57. Marassi, F. M., and S. J. Opella. 2003. Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci. 12:403-411.
58. Bechinger, B., M. Zasloff, and S. J. Opella. 1993. Structure and orientation of the antibiotic peptide magainin in membranes by solidstate nuclear magnetic resonance spectroscopy. Protein Sci. 2:2077-2084.
59. Sawai, M. V., A. J. Waring, W. R. Kearney, P. B. McCray, Jr., W. R. Forsyth, R. I. Lehrer, and B. F. Tack. 2002. Impact of single-residue mutations on the structure and function of ovispirin/novispirin antimicrobial peptides. Protein Eng. 15:225-232.
60. Oh, D., S. Y. Shin, S. Lee, J. H. Kang, S. D. Kim, P. D. Ryu, K. S. Hahm, and Y. Kim. 2000. Role of the hinge region and the tryptophan residue in the synthetic antimicrobial peptides, cecropin A(1-8)-magainin 2(1-12) and its analogues, on their antibiotic activities and structures. Biochemistry. 39:11855-11864.
61. Steiner, H., D. Andreu, and R. B. Merrifield. 1988. Binding and action of cecropin and cecropin analogues: antibacterial peptides from insects. Biochim. Biophys. Acta. 939:260-266.
62. Ramamoorthy, A., F. M. Marassi, M. Zasloff, and S. J. Opella. 1995. Three-dimensional solid-state NMR spectroscopy of a peptide oriented in membrane bilayers. J. Biomol. NMR. 6:329-334.
63. Gazit, E., I. R. Miller, P. C. Biggin, M. S. P. Sansom, and Y. Shai. 1996. Structure and orientation of the mammalian antibacterial peptide cecropin P1 within phospholipid membranes. J. Mol. Biol. 258:860-870.
64. Yamaguchi, S., D. Huster, A. Waring, R. I. Lehrer, W. Kearney, B. F. Tack, and M. Hong. 2001. Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR spectroscopy. Biophys. J. 81:2203-2214.
65. MacKenzie, K. R., J. H. Prestegard, and D. M. Engelman. 1997. A transmembrane helix dimer: structure and implications. Science. 276:131-133.
66. Sass, H. J., G. Buldt, R. Gessenich, D. Hehn, D. Neff, R. Schlesinger, J. Berendzen, and P. Ormos. 2000. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature. 406:649-653.
67. Royant, A., P. Nollert, K. Edman, R. Neutze, E. M. Landau, E. Pebay-Peyroula, and J. Navarro. 2001. X-ray structure of sensory rhodopsin II at 2.1-A resolution. Proc. Natl. Acad. Sci. USA. 98:10131-10136.
68. Sui, H., B. G. Han, J. K. Lee, P. Walian, and B. K. Jap. 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature. 414:872-878.
69. Savage, D. F., P. F. Egea, Y. Robles-Colmenares, J. D. O'Connell 3rd, and R. M. Stroud. 2003. Architecture and selectivity in aquaporins: 2.5 a X-ray structure of aquaporin Z. PLoS Biol. 1:E72.
70. Dutzler, R., E. B. Campbell, M. Cadene, B. T. Chait, and R. MacKinnon. 2002. X-ray structure of a CIC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature. 415:287-294.
71. Kurumbail, R. G., A. M. Stevens, J. K. Gierse, J. J. McDonald, R. A. Stegeman, J. Y. Pak, D. Gildehaus, J. M. Miyashiro, T. D. Penning, K. Seibert, P. C. Isakson, and W. C. Stallings. 1996. Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature. 384:644-648.
72. Ulmschneider, J. P., and W. L. Jorgensen. 2003. Monte Carlo backbone sampling for polypeptides with variable bond angles and dihedral angles using concerted rotations and a Gaussian bias. J. Chem. Phys. 118:4261-4271.
73. Ulmschneider, J. P., M. B. Ulmschneider, and A. Di Nola. 2006. Monte Carlo vs molecular dynamics for all-atom polypeptide folding simulations. J. Phys. Chem. B. 110:16733-16742.
74. Jorgensen, W. L., D. S. Maxwell, and J. Tirado-Rives. 1996. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118:11225-11236.
75. Ulmschneider, J. P., and W. L. Jorgensen. 2004. Monte Carlo backbone sampling for nucleic acids using concerted rotations including variable bond angles. J. Phys. Chem. B. 108:16883-16892.
76. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Comm. 95:43-56.
77. Hess, B., J. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: A linear constraint solver for molecular simulations. J. Comp. Chem. 18:1463-1472.
78. Yau, W. M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry. 37:14713-14718.
79. Marassi, F. M., S. J. Opella, P. Juvvadi, and R. B. Merrifield. 1999. Orientation of cecropin A helices in phospholipid bilayers determined by solid-state NMR spectroscopy. Biophys. J. 77:3152-3155.
80. Ulmschneider, M. B., M. S. P. Sansom, and A. Di Nola. 2006. Evaluating tilt angles of membrane-associated helices: comparison of computational and NMR techniques. Biophys. J. 90:1650-1660.
81. von Heijne, G. 1992. Membrane-protein structure prediction: hydrophobicity analysis and the Positive-inside Rule. J. Mol. Biol. 225:487-494.
82. Biggin, P. C., and M. S. Sansom. 1999. Interactions of α-helices with lipid bilayers: a review of simulation studies. Biophys. Chem. 76:161-183.
83. Popot, J. L., and D. M. Engelman. 1990. Membrane-protein folding and oligomerization: the 2-stage model. Biochemistry. 29:4031-4037.
84. Engelman, D. M., Y. Chen, C. N. Chin, A. R. Curran, A. M. Dixon, A. D. Dupuy, A. S. Lee, U. Lehnert, E. E. Matthews, Y. K. Reshetnyak, A. Senes, and J. L. Popot. 2003. Membrane protein folding: beyond the two stage model. FEBS Lett. 555:122-125.
85. Kessel, A., D. Shental-Bechor, T. Haliloglu, and N. Ben-Tal. 2003. Interactions of hydrophobic peptides with lipid bilayers: Monte Carlo simulations with M2δ. Biophys. J. 85:3431-3444.
86. Kessel, A., T. Haliloglu, and N. Ben-Tal. 2003. Interactions of the M2d segment of the acetylcholine receptor with lipid bilayers: a continuum-solvent model study. Biophys. J. 85:3687-3695.
87. Ben-Tal, N., A. Ben-Shaul, A. Nicholls, and B. Honig. 1996. Free-energy determinants of α-helix insertion into lipid bilayers. Biophys. J. 70:1803-1812.
88. Kessel, A., D. P. Tieleman, and N. Ben-Tal. 2004. Implicit solvent model estimates of the stability of model structures of the alamethicin channel. Eur. Biophys. J. 33:16-28.