Structure, energetics, and dynamics of lipid-protein interactions: A molecular dynamics study of the gramicidin A channel in a DMPC bilayer

Proteins: Structure, Function and Genetics

Volumn 24, Issue 1, 1996, Pages 92-114

  Woolf, Thomas B ^a,b   Roux, Benoît ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

antibiotics; computer simulations; permeation; phospholipid membranes; tryptophan; water

Indexed keywords

DIMYRISTOYLPHOSPHATIDYLCHOLINE; GRAMICIDIN A;

ARTICLE; COMPUTER SIMULATION; HYDROPHILICITY; LIPID BILAYER; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LIPID INTERACTION; STRUCTURE ANALYSIS;

BIOPHYSICS; DIMYRISTOYLPHOSPHATIDYLCHOLINE; GRAMICIDIN; HYDROGEN BONDING; ION CHANNELS; LIPID BILAYERS; MICROSCOPY; MODELS, CHEMICAL; MODELS, MOLECULAR; MODELS, THEORETICAL; PROTEIN CONFORMATION; WATER;

EID: 0030038849     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(199601)24:1<92::AID-PROT7>3.0.CO;2-Q     Document Type: Article

References (89)

1. Deisenhofer, J., Michel, H. The photosynthetic reaction center from the purple bacterium rhodopseudomonas viridis. Science 245:1463-1473, 1989.
2. Henderson, R., Baldwin, J.M., Ceska, T.A., Zemlin, F., Beckmann, E., Downing, K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol. Biol. 213:899-929, 1990.
3. Shon, K., Kim, Y., Colnago, L.A., Opella, S.J. Nmr studies of the structure and dynamics of membrane-bound bacteriophage pf1 coat protein. Science 252:1303-1305, 1991.
4. Eisenberg, D., Weiss, R.M., Terwilliger, T.C. The helical hydrophobic moment: A measure of the amphiphilicity of a helix. Nature (London) 299:371-374, 1982.
5. Engelman, D.M., Steitz, T.A., Goldman, A. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15:321-353, 1986.
6. Wesson, L., Eisenberg, D. Atomic solvation parameters applied to molecular dynamics of proteins in solution. Protein Sci. 1:227-235, 1992.
7. Edholm, O., Jahnig, F. The structure of a membrane-spanning polypeptide studied by molecular dynamics. Biophys. Chem. 30:279-292, 1988.
8. Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Gosh, R., Pauptit, R.A., Jansonius, J.N. Crystal structures explain functional properties of two E. coli porins. Nature (London) 358:727-733, 1992.
9. Weiss, M.S., Schulz, G.E. Structure of porin refined at 1.8 Å resolution. J. Mol. Biol. 227:493-509, 1992.
10. McDonnell, P.A., Shon, K., Kim, Y., Opella, S.J. fd coat protein structure in membrane environments. J. Mol. Biol. 233:447-463, 1993.
11. 2 synthase-1. Nature (London) 367:243-249, 1994.
12. Ketchem, R.R., Hu, W., Cross, T.A. High-resolution conformation of gramicidin A in lipid bilayer by solid-state nmr. Science 261:1457-1460, 1993.
13. White, J. Membrane fusion. Nature (London) 258:917-924, 1992.
14. Landolt-Marticorena, C., Williams, K.A., Deber, C.M., Reithmeier, R.A.F. Nonrandom distribution of amino acids in the transmembrane segments of human type i single span membrane proteins. J. Mol. Biol. 229:602-608, 1993.
15. Jacobs, R.E., White, S.H. The nature of the hydrophobic binding of small peptides at the bilayer interface: Implications for the insertion of transbilayer helices. Biochemistry 28:3421-3437, 1989.
16. Brooks, C.L., III, Karplus, M., Pettitt, B.M. Proteins. A theoretical perspective of dynamics, structure and thermodynamics. In: "Advances in Chemical Physics," Vol. LXXI. Prigogine, I., Rice, S.A. (eds.). New York: John Wiley, 1988.
17. Pastor, R.W. Molecular dynamics and Monte Carlo simulations of lipid bilayers. Curr. Opin. Struc. Biol. 4:486-492, 1994.
18. Egberts, E. Molecular dynamics simulation of multibilayer membranes. Ph.D. Thesis, Univ. Groningen, 1988.
19. Loof, H.D., Harvey, S.C., Segrest, J.P., Pastor, R.W. Mean field stochastic boundary molecular dynamics simulation of a phospholipid in a membrane. Biochemistry 30:2099-2113, 1991.
20. Bassolino-Klimas, D., Alper, H.E., Stouch, T.R. Solute diffusion in lipid bilayer membranes: An atomic level study by molecular dynamics simulation. Biochemistry 32: 12624-12637, 1993.
21. Merz, K.M., Damodaran, K.V. A comparison of DMPC-and DLPE-based lipid bilayers. Biophys J. 66:1076-1087, 1994.
22. Venable, R.M., Zhang, Y., Hardy, B.J., Pastor, R.W. Molecular dynamics simulations of a lipid bilayer and of hexadecane: An investigation of membrane fluidity. Science 262:223-226, 1993.
23. Pascher, I., Lundmark, M., Nyhohn, P.G., Sundell, S. Crystal structures of membrane lipids. Biochim. Biophys. Acta 1113:339-373, 1992.
24. Hauser, H., Pascher, I., Pearson, R.H., Sundell, S. Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine. Biochim. Biophys. Acta 650:21-51, 1981.
25. Engelman, D.M., Lewis, B.A. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211-217, 1983.
26. Ulrich, A.S., Volke, F., Watts, A. The dependence of phospholipid head-group mobility on hydration as studied by deuterium-nmr spin-lattice relaxation time measurements. Chem. Phys. Lipids 55:61-66, 1990.
27. 2H-nmr study. Chem. Phys. Lipids 58:1-5, 1991.
28. Woolf, T.B., Roux, B. Molecular dynamics simulations of proteins in lipid membranes: The first steps. Biophys. J. A354:1993.
29. Woolf, T.B., Roux, B. Molecular dynamics simulations of lipid:protein interactions: Gramicidin A in a dmpc bilayer. Biophys. J. A348:1994.
30. Woolf, T.B., Desharnais, J., Roux, B. Structure and dynamics of the sidechains of gramicidin in a DMPC bilayer. In "NATO ASI Series: Computational Approaches in Supramolecular Chemistry," Vol. 426. Wipff, G. (ed.). Dordrecht: Kluwer Academic Publishers, 1994:519-531.
31. Woolf, T.B., Roux, B. Molecular dynamics simulation of the gramicidin channel in a phospholipid bilayer. Proc. Natl Acad. Sci. U.S.A. 91:11631-11635, 1994.
32. Pastor, R.W., Venable, R.M., Karplus, M. Model for the structure of the lipid bilayer. Proc. Natl. Acad. Sci. U.S.A. 88:892-896, 1991.
33. Smith, R., Thomas, D.E., Separovic, F., Atkins, A.R., Cornell, B.R. Determination of the structure of a membrane-incorporated ion channel. Biophys. J. 56:307-314, 1989.
34. Prosser, R.W., Davis, J.H., Dahlquist, F.W., Lindorfer, M.A. 2h nuclear magnetic resonance of the gramicidin A backbone in a phospholipid bilayer. Biochemistry 30: 4687-4696, 1991.
35. Andersen, O.S., Koeppe, R.E., II. Molecular determinants of channel function. Physiol. Rev. 72:S89-S158, 1992.
36. Killian, J.A. Gramicidin and gramicidin-lipid interactions. Biochim. Biophys. Acta 1113:391-425, 1992.
37. Roux, B., Karplus, M. Molecular dynamics simulations of the gramicidin channel. Annu. Rev. Biomol. Struc. Dyn. 23:731-761, 1994.
38. Rice, D., Oldfield, E. Deuterium nuclear magnetic resonance studies of the interaction between dimyristoylphosphatidylcholine and gramicidin A. Biochemistry 18:3272-3279, 1979.
39. Watnick, P.I., Chan, S.I., Dea, P. Hydrophobic mismatch in gramicidin A'/lecithin systems. Biochemistry 29:6215-6221, 1990.
40. Davies, J.A., Braunder, J.W., Schuster, H.F., Mendelsohn, R. A quantitative infrared determination of acyl chain conformation in gramicidin/dipalmitoylphosphatidyleholine mixtures. Biochem. Biophys. Res. Commun. 168:85-90, 1990.
41. King, J., Scott, H.L. Monte carlo studies of lipid chains and gramicidin a in a model membrane. Biochem Biophys. Res. Commun. 165:1-6, 1989.
42. Xing, J., Scott, H.L. Monte carlo studies of a model for lipid-gramicidin A bilayers. Biocheim. Biophys. Acta 1106: 227-232, 1992.
43. Wang, J., Pullman, A. The intrinsic molecular potential of glyceryl monooleate layers and its effect on the conformation and orientation of an inserted molecule: Example of gramicidin A. Biochim. Biophys. Acta 1024:10-18, 1990.
44. Owicki, J.C., Springgate, M.W., McConnell, H.M. Theoretical study of protein-lipid interactions in bilayer membranes. Proc. Natl. Acad. Sci. U.S.A. 75:1616-1619, 1978.
45. Mouritsen, O G , Bloom, M Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153, 1984.
46. Zuckermann, M.J., Pink, D.A. The correlation length and lateral compressibility of phospholipid bilayers in the presence of thermodynamic density fluctuations. J. Chem. Phys. 73:2919-2926, 1980.
47. Zhang, Z., Sperotto, M.M., Zuckermann, M.J., Mouritsen, O.G. A microscopic model for lipid/protein bilayers with critical mixing. Biochim. Biophys. Acta 1147:154-160, 1993.
48. 1H-NMR study of gramicidin-A transmembrane ion channel. Head-to-head right-handed, single stranded helices. FEBS 186:168-174, 1985.
49. Roux, B., Karplus, M. Ion transport in the gramicidin channel: Free energy profile along the right-handed dimer. J. Am. Chem. Soc. 115:3250-3260, 1993.
50. Mackerell, A.D., Jr., Bashford, D., Bellot, M., Dunbrack, R.L., Field, M.J., Fischer, S., Gao, J., Guo, H., Joseph, D., Ha, S., Kuchnir, L., Kuczera, K., Lau, F.T.K., Mattos, C., Michnick, S., Nguyen, D.T., Ngo, T., Prodhom, B., Roux, B., Schlenkrich, B., Smith, J., Stote, R., Straub, J., Wiorkiewicz-Kuczera, J., Karplus, M. Self-consistent parametrization of biomolecules for molecular modelling and condensed phase simulations. Biophys. J. 61:A143, 1992.
51. Jorgensen, W.L., Impey, R.W., Chandrasekhar, J., Madura, J D., Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79: 926-935, 1983.
52. Davis, J.H. Personal communication, 1993.
53. Gunsteren, W F., Berendsen, H J.C. Algorithms for macromolecular dynamics and constraint dynamics. Mol. Phys 34:1311-1327, 1977.
54. Woolf, T.B., Roux, B. The conformation flexibility of o-phosphorylcholine and o-phosphorylethanolamine: A molecular dynamics study of solvation effects. J. Am. Chem. Soc. 116:5916-5926, 1994.
55. Pastor, R.W., Venable, R.M., Karplus, M. Brownian dynamics simulation of a lipid chain in a membrane bilayer. J. Chem. Phys. 89:1112-1127, 1988.
56. Hardy, B.J., Pastor, R.W. Conformation sampling of hydrocarbon and lipid chains in an orienting potential. J. Comput. Chem. 15:208-226, 1994.
57. Takeuchi, H., Nemoto, H , Harada, I. Environments and conformations of tryptophan side chains of gramicidin A in phospholipid bilayers studied by raman spectroscopy. Biochemistry 29:1572-1579, 1990.
58. Bouchard, M., Auger, M. Solvent history dependence of gramicidin-lipid interactions: A Raman and infrared spectroscopic study. Biophys. J. 65:2484-2492, 1993.
59. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., Karplus, M. CHARMM: A program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:187-217, 1983.
60. Heller, H., Schaefer, M., Schulten, K. Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid-crystal phases. J. Phys. Chem. 97:8343-8360, 1993.
61. Pastor, R.W. Personal communication, 1993.
62. Pace, R.J., Chan, S.I. Molecular motions in lipid bilayers i. Statistical mechanical model of acyl chain motion. J. Chem. Phys. 76:4217-4227, 1982.
63. Nagle, J.F., Wiener, M.C. Structure of fully hydrated bilayer dispersions. Biochim. Biophys. Acta 942:1-10, 1988.
64. Schindler, H., Seelig, J. Deuterium order parameters in relation to thermodynamic properties of a phospholiped bilayer: A statistical mechanical interpretation. Biochemistry 14:2283-2287, 1975.
65. Nagle, J.F. Area/lipid of bilayers from nmr. Biophys. J. 64:1476-1481, 1993.
66. De Young, L.R., Dill, K.A. Solute partitioning into lipid bilayer membranes. Biochemistry 27:5281-5289, 1988.
67. Thurmond, R.L., Dodd, S.W., Brown, M.F. Molecular areas of phospholipids as determined by 2h nmr spectroscopy: Comparison of phosphatidylethanolamines and phosphatidylcholines. Biophys. J. 59:108-113, 1991.
68. Kemp, G., Jacobson, K.A., Wenner, C. Solution and interfacial properties of gramicidin pertinent to its effect on membranes. Biochim. Biophys. Acta 255:493-501, 1972.
69. Kemp, G., Wenner, C. Solution, interfacial, and membrane properties of gramicidin A. Arch. Biochem. Biophys. 176: 547-555, 1976.
70. Ries, H.E., Swift, H. Monolayers of two transmembrane channel formers and an ionophore. J. Colloid Interface Sci. 117:584-588, 1987.
71. Dhathathreyan, A., Baumann, U., Muller, A., Mobius, D. Characterization of complex gramicidin monolayers by light reflection and fourier transform infrared spectroscopy. Biochim. Biophys. Acta 944:265-272, 1988.
72. Mau, N.D.-V., Daumas, P., Lelievre, D., Trudelle, Y., Heitz, F. Linear gramicidins at the air-water interface. Biophys. J. 51:843-845, 1987.
73. Tournois, H., Gieles, P., Demel, R., de Gier, J., de Kruijff, B. Interfacial properties of gramicidin and gramicidin-lipid mixtures measured with static and dynamic monolayer techniques. Biophys. J. 55:557-569, 1989.
74. Buldt, G., Gally, H.U., Seelig, J., Zaccai, G. Neutron diffraction studies on phosphatidylcholine model membranes. I. head group conformation. J. Mol. Biol. 134:673-691, 1979.
75. Zaccai, G., Buldt, G., Seelig, A., Seelig, J. Neutron diffraction studies on phosphatidylcholine model membranes. II. chain conformation and segmental disorder. J. Mol. Biol. 134:693-706, 1979.
76. Seelig, J. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta 515:105-140, 1978.
77. Seelig, J., Macdonald, P.M., Scherer, P.G. Phospholipid head groups as sensors of electric charge in membranes. Biochemistry 26:7535-7541, 1987.
78. Moll, F., III, Cross, T.A. Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D. Biophys. J. 57:351-362, 1990.
79. Pink, D.A., Georgallas, A., Chapman, D. Intrinsic proteins and their effect upon lipid hydrocarbon chain order. Biochemistry 20:7152-7157, 1981.
80. Seelig, J., Seelig, A. Lipid conformation in model membranes and biological membranes. Q. Rev. Biophys. 13:19-61, 1980.
81. Ho, C. Hydration at the membrane protein-lipid interface. Biophys. J. 63:897-902, 1992.
82. Hladky, S.B., and Haydon, D.A. Ion transfer across lipid membranes in the presence of gramicidin A. I. studies of the unit conductance channel. Biochim. Biophys. Acta 274: 294-312, 1972.
83. Urry, D.W. The gramicidin A transmembrane channel: A proposed pi(l,d) helix. Proc. Natl. Acad. Sci. U.S.A. 68:672-676, 1971.
84. Becker, M.D., Greathouae, D.V., Koeppe, R.E., II, Andersen, O.S. Amino acid sequence modulation of gramicidin channel function: Effects of tryptophane-to-phenylalanine substitutions on the single-channel conductance and duration. Biochemistry 30:8830-8839, 1991.
85. Mukherjee, S., Chattopadhyay, A. Motionall restricted tryptophan environments at the peptide-lipid interface of gramicidin channels. Biochem. 33:5089-5097, 1994.
86. Yeagle, P.L., Kelsey, D. Phosphorus nuclear magnetic resonance studies of lipid-protein interactions: Human erythrocyte glycophorin and phospholipids. Biochemistry 28: 2210-2215, 1989.
87. Mouritsen, O.G., Bloom, M. Models of lipid-protein interactions in membranes. Annu. Rev. Biophys. Biomol. Struct. 22:145-171, 1993.
88. Nezil, F.N., Bloom, M. Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes. Biophys. J. 61:1176-1183, 1992.
89. He, K., Ludtke, SJ., Wu, Y., Huang, H.W. X-ray scattering with momentum transfer in the plane of membrane. Application to gramicidin organization. Biophys. J. 64:157-162, 1993.