Indole localization in lipid membranes revealed by molecular simulation

Biophysical Journal

Volumn 91, Issue 6, 2006, Pages 2046-2054

  Norman, Kristen E ^a   Nymeyer, Hugh ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BENZENE; CARBONYL DERIVATIVE; CATION; CHOLINE; GLYCEROL; HYDROCARBON; INDOLE; NITROGEN; PHOSPHATE; WATER;

ARTICLE; CELLULAR DISTRIBUTION; DIPOLE; ELECTRIC FIELD; ELECTRICITY; ENTHALPY; HYDROGEN BOND; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE BINDING; MOLECULAR DYNAMICS; SIMULATION;

EID: 33748493587     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.080275     Document Type: Article

References (51)

1. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
2. Deisenhofer, J., O. Epp, K. Miki, R. Huber, and H. Michel. 1985. Structure of the protein subunits in the photosynthetic reaction centre of rhodopseudomonas viridis at 3 Å resolution. Nature. 318:618-624.
3. Landolt-Marticorena, C., K. A. Williams, C. M. Deber, and R. A. F. Reithmeier. 1993. Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J. Mol. Biol. 229:602-608.
4. Arkin, I. T., and A. T. Brunger. 1998. Statistical analysis of predicted transmembrane α-helices. Biochim. Biophys. Acta. 1429:113-128.
5. Ulmschneider, M. B., M. S. P. Sansom, and A. Di Nola. 2005. Properties of integral membrane protein structures: derivation of an implicit membrane potential. Proteins. 59:252-265.
6. Braun, P., and G. von Heijne. 1999. The aromatic residues Trp and Phe have different effects on the positioning of a transmembrane helix in the microsomal membrane. Biochemistry. 38:9778-9782.
7. Whiles, J. A., K. J. Glover, R. R. Vold, and E. A. Komives. 2002. Methods for studying transmembrane peptides in bicelles: consequences of hydrophobic mismatch and peptide sequence. J. Magn. Reson. 158:149-156.
8. Koeppe II, R. E., F. J. Sigworth, G. Szabo, D. W. Urry, and A. Wooley. 1999. Gramicidin channel controversy: the structure in a lipid environment. Nat. Struct. Biol. 6:609.
9. Killian, J. A., I. Salemink, M. R. R. de Planque, G. Lindbloom, R. E. Koeppe II, and D. V. Greathouse. 1996. Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane α-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry. 35:1037-1045.
10. de Planque, M. R. R., E. Goormaghtigh, D. V. Greathouse, R. E. Koeppe II, J. A. W. Kruijtzer, R. M. J. Liskamp, B. de Kruijff, and J. A. Killian. 2001. Sensitivity of single membrane-spanning α-helical peptides to hydrophobic mismatch with a lipid bilayer: effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry. 40:5000-5010.
11. de Planque, M. R. R., B. B. Bonev, J. A. A. Demmers, D. V. Greathouse, R. E. Koeppe II, F. Separovic, A. Watts, and J. A. Killian. 2003. Interfacial anchor over hydrophobic matching effects in peptide-lipid interactions. Biochemistry. 42:5341-5348.
12. 2H-NMR. Biophys. J. 75:1365-1371.
13. Yau, W.-M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry. 37:14713-14718.
14. Gaede, H. C., W.-M. Yau, and K. Gawrisch. 2005. Electrostatic contributions to indole-lipid interactions. J. Phys. Chem. B. 109:13014-13023.
15. Kachel, K., E. Asuncion-Punzalan, and E. London. 1995. Anchoring of tryptophan and tyrosine analogs at the hydrocarbon-polar boundary in model membrane vesicles: parallax analysis of fluorescence quenching induced by nitroxide-labeled phospholipids. Biochemistry. 34:15475-15479.
16. Grossfield, A., J. Sachs, and T. B. Woolf. 2000. Dipole lattice membrane model for protein calculations. Proteins. 41:211-223.
17. Tanizaki, S., and M. Feig. 2005. A generalized born formalism for heterogeneous dielectric environments: an application to the implicit modeling of biological membranes. J. Chem. Phys. 122:124706.
18. Grossfield, A., and T. B. Woolf. 2002. Interaction of tryptophan analogs with POPC lipid bilayers investigated by molecular dynamics calculations. Langmuir. 18:198-210.
19. Woolf, T. B. 1998. Molecular dynamics simulations of individual α-helices of bacteriorhodopsin in dimyristoylphosphatidylcholine. II. Interaction energy analysis. Biophys. J. 74:115-131.
20. MacCallum, J. L., and D. P. Tieleman. 2006. Molecular dynamics calculations of the distribution of amino acid side chains in a lipid bilayer. Biophys. J. 90:1026. (Abstr.).
21. Dougherty, D. A. 1996. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science. 271:163-168.
22. Ma, J. C., and D. A. Dougherty. 1997. The cation-π interaction. Chem. Rev. 97:1303-1324.
23. Caldwell, J. W., and P. A. Kollman. 1995. Cation-π interactions: nonadditive effects are critical in their accurate representation. J. Am. Chem. Soc. 117:4177-4178.
24. Cubero, E., F. J. Luque, and M. Orozco. 1998. Is polarization important in cation-π interactions? Proc. Natl. Acad. Sci. USA. 95:5976-5980.
25. Minoux, H., and C. Chipot. 1999. Cation-π interactions in proteins: can simple models provide an accurate description? J. Am. Chem. Soc. 121:10366-10372.
26. Woolf, T. B., A. Grossfield, and J. G. Pearson. 1999. Indoles at interfaces: calculations of electrostatic effects with density functional and molecular dynamics methods. Int. J. Quantum. Chem. 75:197-206.
27. Haydon, D. A., and V. B. Meyers. 1973. Surface charge, surface dipoles, and membrane conductance. Biochim. Biophys. Acta. 307:429-443.
28. Davis, M. E., and J. A. McCammon. 1990. Electrostatics in biomolecular structure and dynamics. Chem. Rev. 90:509-521.
29. Gawrisch, K., D. Ruston, J. Zimmerberg, V. A. Parsegian, R. P. Rand, and N. Fuller. 1992. Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. Biophys. J. 61:1213-1223.
30. Zhou, F., and K. Schulten. 1995. Molecular dynamics study of a membrane-water interface. J. Phys. Chem. 99:2194-2207.
31. Im, W., S. Berneche, and B. Roux. 2001. Generalized solvent boundary potential for computer simulations. J. Chem. Phys. 114:2924-2937.
32. Ladokhin, A. S., and S. H. White. 2001. Protein chemistry at membrane interfaces: non-additivity of electrostatic and hydrophobic interactions. J. Mol. Biol. 309:543-552.
33. Lin, J.-H., N. A. Baker, and J. A. McCammon. 2002. Bridging implicit and explicit solvent approaches for membrane electrostatics. Biophys. J. 83:1374-1379.
34. Stern, H. A., and S. E. Feller. 2003. Calculation of the dielectric permittivity profile for a nonuniform system: application to a lipid bilayer simulation. J. Chem. Phys. 118:3401-3412.
35. Marrink, S. J., and H. J. C. Berendsen. 1996. Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations. J. Phys. Chem. 100:16729-16738.
36. Jacobs, R. E., and S. H. White. 1989. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry. 28:3421-3437.
37. Sitkoff, D., K. A. Sharp, and B. Honig. 1994. Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
38. Peterson, F. N. R., M. Ø. Jensen, and C. H. Nielsen. 2005. Interfacial tryptophan residues: a role for the cation-π effect? Biophys. J. 89:3985-3996.
39. Aliste, M. P., J. L. MacCallum, and D. P. Tieleman. 2003. Molecular dynamics simulations of pentapeptides at interfaces: salt bridge and cation-π interactions. Biochemistry. 42:8976-8987.
40. Huang, C., and J. P. Charlton. 1972. Interactions of phosphatidylcholine vesicles with 2-p-toluidinylnaphthalene-6-sulfonate. Biochemistry. 11:735-740.
41. Seelig, J., and P. Ganz. 1991. Nonclassical hydrophobic effect in membrane binding equilibria. Biochemistry. 30:934-959.
42. DeVido, D. R., J. G. Dorsey, H. S. Chan, and K. A. Dill. 1998. Oil/water partitioning has a different thermodynamic signature when the oil solvent chains are aligned than when they are amorphous. J. Phys. Chem. 102:7272-7279.
43. MacCallum, J. L., and D. P. Tieleman. 2006. Computer simulation of the distribution of hexane in a lipid bilayer: spatially resolved free energy, entropy, and enthalpy profiles. J. Am. Chem. Soc. 128:125-130.
44. Tieleman, D. P., H. J. C. Berendsen, and M. S. P. Sansom. 1999. An alamethicin channel in a lipid bilayer: molecular dynamics simulations. Biophys. J. 76:1757-1769.
45. van der Spoel, D., B. Hess, and E. Lindahl. 2004. GROMACS user manual version 3.2. www.gromacs.org. [Online].
46. Chandrasekhar, I., M. Kastenholz, R. D. Lins, C. Oostenbrink, L. Schuler, D. P. Tieleman, and W. F. van Gunsteren. 2003. A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 force field. Eur. Biophys. J. 32:67-77.
47. Chiu, S.-W., M. Clark, V. Balaji, S. Subramanian, H. L. Scott, and E. Jakobsson. 1995. Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69:1230-1245.
48. Schuler, L. D., X. Daura, and W. F. van Gunsteren. 2001. An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase. J. Comp. Chem. 22:1205-1218.
49. 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, Dordrecht, The Netherlands. 331-342.
50. 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.
51. York, D., T. A. Darden, and L. Pedersen. 1993. The effect of long-range electrostatic interactions in simulations of macromolecular crystals: a comparison of the Ewald and truncated list methods. J. Chem. Phys. 99:8345-8348.