Ion permeation through a narrow channel: Using gramicidin to ascertain all-atom molecular dynamics potential of mean force methodology and biomolecular force fields

Biophysical Journal

Volumn 90, Issue 10, 2006, Pages 3447-3468

  Allen, Toby W ^a   Andersen, Olaf S ^b   Roux, Benoit ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRAMICIDIN; HYDROCARBON; LIPID; POTASSIUM ION;

ARTICLE; ATOM; BINDING SITE; BIOMOLECULAR ELECTRONICS; COMPARATIVE STUDY; DISSOCIATION CONSTANT; ENERGY TRANSFER; ION TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR SIZE; POLARIZATION; POTASSIUM CONDUCTANCE; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; STATISTICAL ANALYSIS; SURFACE PROPERTY; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

EID: 33646192258     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.077073     Document Type: Article

References (98)

1. Karplus, M. 2002. Molecular dynamics simulations of biomolecules. Acc. Chem. Res. 35:321-323.
2. Roux, B., T. Allen, S. Bernèche, and W. Im. 2004. Theoretical and computational models of biological ion channels. Q. Rev. Biophys. 37:15-103.
3. Allen, T. W., O. S. Andersen, and B. Roux. 2004. On the importance of flexibility in studies of ion permeation. J. Gen. Physiol. 124:679-690.
4. Lindorff-Larsen, K., R. Best, M. Depristo, C. Dobson, and M. Vendruscolo. 2005. Simultaneous determination of protein structure and dynamics. Nature. 433:128-132.
5. Karplus, M., and J. McCammon. 1981. The internal dynamics of globular proteins. CRC Crit. Rev. Biochem. 9:293-349.
6. Karplus, M., and G. Petsko. 1990. Molecular dynamics simulations in biology. Nature. 347:631-639.
7. Mamonov, A. B., R. D. Coalson, A. Nitzan, and M. G. Kurnikova. 2003. The role of the dielectric barrier in narrow biological channels: a novel composite approach to modeling single-channel currents. Biophys. J. 84:3646-3661.
8. Kurnikova, M., R. Coalson, P. Graf, and A. Nitzan. 1999. A lattice relaxation algorithm for three-dimensional Poisson-Nernst-Planck theory with application to ion transport through the gramicidin A channel. Biophys. J. 76:642-656.
9. Nadler, B., U. Hollerbach, and R. S. Eisenberg. 2003. Dielectric boundary force and its crucial role in gramicidin. Phys. Rev. E. 68:021905.
10. Edwards, S., B. Corry, S. Kuyucak, and S.-H. Chung. 2002. Continuum electrostatics fails to describe ion permeation in the gramicidin channel. Biophys. J. 83:1348-1360.
11. Mashl, R., Y. Tang, J. Schnitzer, and E. Jakobsson. 2001. Hierarchical approach to predicting permeation in ion channels. Biophys. J. 81:2473-2483.
12. Chung, S. H., T. Allen, and S. Kuyucak. 2002. Conducting state properties of the KcsA potassium channel from molecular and Brownian dynamics simulations. Biophys. J. 82:628-645.
13. Dorman, V. L., and P. C. Jordan. 2004. Ionic permeation free energy in gramicidin: a semi-microscopic perspective. Biophys. J. 86:3529-3541.
14. + channel. Proc. Natl. Acad. Sci. USA. 100:8644-8648.
15. Allen, T. W., O. S. Andersen, and B. Roux. 2004. Energetics of ion conduction through the gramicidin channel. Proc. Natl. Acad. Sci. USA. 101:117-122.
16. LD helix. Proc. Natl. Acad. Sci. USA. 68:672-676.
17. Arseniev, A. S., A. L. Lomize, I. L. Barsukov, and V. F. Bystrov. 1986. Gramicidin A transmembrane ion-channel three-dimensional structure reconstruction based on NMR spectroscopy and energy refinement. (In Russian.). Biol. Membr. 3:1077-1104.
18. Townsley, L. E., W. A. Tucker, S. Sham, and J. F. Hinton. 2001. Structures of gramicidins A, B, and C incorporated into sodium dodecyl sulfate micelles. Biochemistry. 40:11676-11686.
19. Ketchem, R. R., B. Roux, and T. A. Cross. 1997. High resolution refinement of a solid-state NMR-derived structure of gramicidin A in a lipid bilayer environment. Structure. 5:1655-1669.
20. Allen, T. W., O. S. Andersen, and B. Roux. 2003. The structure of gramicidin A in a lipid bilayer environment determined using molecular dynamics simulations and solid-state NMR data. J. Am. Chem. Soc. 125:9868-9877.
21. Hladky, S. B., B. Urban, and D. Haydon. 1979. Ion movements in pores formed by gramicidin A. Membr. Transport Processes. 3:89-103.
22. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J. Membr. Biol. 76:197-225.
23. Andersen, O., and R. Koeppe. 1992. Molecular determinants of channel function. Physiol. Rev. 72:S89-S158.
24. Busath, D. 1993. The use of physical methods in determining gramicidin channel structure and function. Annu. Rev. Physiol. 55:473-501.
25. Andersen, O. S., R. E. Koeppe II, and B. Roux. 2005. Gramicidin channels. IEEE Trans. Nanobiosci. 4:10-20.
26. Faraldo-Gomez, J. D., L. R. Forrest, M. Baaden, P. J. Bond, C. Domene, G. Patargias, J. Cuthbertson, and M. S. P. Sansom. 2004. Conformational sampling and dynamics of membrane proteins from 10-nanosecond computer simulations. Proteins. 57:783-791.
27. Mackay, D. H. J., P. H. Berens, K. R. Wilson, and A. T. Hagler. 1984. Structure and dynamics of ion transport through gramicidin A. Biophys. J. 46:229-248.
28. Roux, B. 2002. Computational studies of the gramicidin channel. Acc. Chem. Res. 35:366-375.
29. Roux, B., and M. Karplus. 1993. Ion transport in the gramicidin channel: free energy of the solvated right-handed dimer in a model membrane. J. Am. Chem. Soc. 115:3250-3262.
30. Allen, T. W., T. Bastug, S. Kuyucak, and S. H. Chung. 2003. Gramicidin-A channel as a test ground for molecular dynamics force fields. Biophys. J. 84:2159-2168.
31. Jordan, P. C. 1987. Microscopic approach to ion transport through transmembrane channels. The model system gramicidin. J. Phys. Chem. 91:6582-6591.
32. Batug, T., and S. Kuyucak. 2005. Test of molecular dynamics force fields in gramicidin A. Eur. Biophys. J. 34:377-382.
33. Andersen, O. S. 1984. Gramicidin channels. Annu. Rev. Physiol. 46:531-548.
34. Chandler, D. 1978. Statistical mechanics of isomerization dynamics in liquids and the transition state approximation. J. Chem. Phys. 68:2959-2970.
35. Hinsen, K., and B. Roux. 1997. Potential of mean force and reaction rates for proton transfer in acetylacetone. J. Chem. Phys. 106:3567-3577.
36. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:187-217.
37. MacKerell, A. D., Jr., D. Bashford, M. Bellot, 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 III, B. Roux, B. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
38. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
39. Beglov, D., and B. Roux. 1994. Finite representation of an infinite bulk system: solvent boundary potential for computer simulations. J. Chem. Phys. 100:9050-9063.
40. Cornell, W., P. Cieplak, C. Bayly, I. Gould, K. Merz, Jr., D. Ferguson, D. Spellmeyer, T. Fox, J. Caldwell, and P. Kollman. 1995. A second generation force field for the simulation of proteins and nucleic acids. J. Am. Chem. Soc. 117:5179-5197.
41. Åqvist, J. 1990. Ion water interaction potential derived from free energy perturbation simulations. J. Phys. Chem. 94:8021-8024.
42. van Gunsteren, W., X. Daura, and A. Mark. 1999. GROMOS force field. In Encyclopaedia of Computational Chemistry, Vol. 2. E.-I.-C. P. von Ragu Schelyer, editor. John Wiley & Sons, London. 1211-1216.
43. Berendsen, H., J. Postma, W. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to proteins hydration. In Intermolecular Forces. B. Pullman, editor. Reidel, Dordrecht, The Netherlands. 331-342.
44. Straatsma, T. P., and H. J. C. Berendsen. 1988. Free energy of ionic hydration: analysis of a thermodynamic intergration technique to evaluate free energy differences by molecular dynamics simulations. J. Chem. Phys. 89:5876-5886.
45. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, Jr., D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second-generation force field for the simulation of proteins and nucleic acids. J. Am. Chem. Soc. 117:5179-5197.
46. Schlenkrich, M., J. Brickmann, A. J. MacKerell, and M. Karplus. 1996. An empirical potential energy function for phospholipids: criteria for parameters optimization and applications. In Biological Membranes. A Molecular Perspective from Computation and Experiment. K. Merz, and B. Roux, editors. Birkhauser, Boston, MA. 31-81.
47. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
48. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equation of motions of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Chem. 23:327-341.
49. Feller, S. E., Y. H. Zhang, R. W. Pastor, and B. R. Brooks. 1995. Constant pressure molecular dynamics simulation - the Langevin piston method. J. Chem. Phys. 103:4613-4621.
50. Woolf, T., and B. Roux. 1996. Structure, energetics and dynamics of lipid-protein interactions: a molecular dynamics study of the gramicidin A channel in a DMPC bilayer. Proteins Struct. Funct. Genet. 24:92-114.
51. Ketchem, R. R., W. Hu, and T. A. Cross. 1993. High-resolution conformation of gramicidin A in lipid bilayer by solid-state NMR. Science. 261:1457-1460.
52. 16. J. Phys. Chem. 67:776-779.
53. Roux, B. 1999. Statistical mechanical equilibrium theory of selective ion channels. Biophys. J. 77:139-153.
54. 13 gramicidin A currents. Biophys. J. 81:1245-1254.
55. Roux, B. 1997. The influence of the membrane potential on the free energy of an intrinsic protein. Biophys. J. 73:2980-2989.
56. Torrie, G. M., and J. P. Valleau. 1977. Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling. J. Comput. Phys. 23:187-199.
57. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13:1011-1021.
58. Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: solution to four relevant electrostatic problems. Nature. 221:844-846.
59. Tian, F., and T. Cross. 1999. Cation transport: an example of structural based selectivity. J. Mol. Biol. 285:1993-2003.
60. Olah, G. A., H. W. Huang, W. Liu, and Y. Wu. 1991. Location of ion-binding sites in the gramicidin channel by x-ray diffraction. J. Mol. Biol. 218:847-858.
61. Finkelstein, A., and O. S. Andersen. 1981. The gramicidin A channel: a review of its permeability characteristics with special reference to the single-file aspect of transport. J. Membr. Biol. 59:155-171.
62. 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.
63. Huang, W., and D. G. Levitt. 1977. Theoretical calculation of the dielectric constant of a bilayer membrane. Biophys. J. 17:111-128.
64. Simon, S. A., and T. J. McIntosh. 1986. Depth of water penetration into bilayers. Methods Enzymol. 127:511-521.
65. Lide, D. R. (Editor-in-Chief). 1992. CRC Handbook of Chemistry and Physics, 72nd Ed. CRC Press, Boston, MA.
66. Hunenberger, P. H., and J. A. McCammon. 1999. Ewald artifacts in computer simulations of ionic solvation and ion-ion interaction: a continuum electrostatics study. J. Chem. Phys. 110:1856-1872.
67. Lewis, B. A., and D. M. Engelman. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211-217.
68. Lamoureux, G., A. D. MacKerell Jr., and B. Roux. 2003. A simple polarizable model of water based on classical drude oscillators. J. Chem. Phys. 119:5185-5197.
69. + by gramicidin A. Biophys. J. 56:171-182.
70. Jordan, P. C., R. J. Bacquet, J. A. McCammon, and P. Tran. 1989. How electrolyte shielding influences the electrical potential in transmembrane ion channels. Biophys. J. 55:1041-1052.
71. 23Na-NMR. Biochim. Biophys. Acta. 1238:1-11.
72. + 205 nuclear magnetic resonance spectroscopy. Biophys. J. 50:539-544.
73. Roux, B., B. Prod'hom, and M. Karplus. 1995. Ion transport in the gramicidin channel: molecular dynamics study of single and double occupancy. Biophys. J. 68:876-892.
74. Woolf, T., and B. Roux. 1997. The binding site of sodium in the gramicidin A channel: a comparison of molecular dynamics simulations with solid state NMR data. Biophys. J. 72:1930-1945.
75. Levitt, D. 1986. Interpretation of biological channel flux data - reactionrate theory versus continuum theory. Annu. Rev. Biophys. Chem. 15:29-57.
76. Corry, B., and S. H. Chung. 2005. Influence of protein flexibility on the electrostatic energy landscape in gramicidin a. Eur. Biophys. J. 34:208-216.
77. Becker, M. D., R. E. Koeppe, and O. S. Andersen. 1992. Amino acid substitutions and ion channel function. Model-dependent conclusions. Biophys. J. 62:25-27.
78. Roux, B., and M. Karplus. 1991. Ion transport in a gramicidin-like channel: dynamics and mobility. J. Phys. Chem. 95:4856-4868.
79. Andersen, O. S. 1983. Ion movement through gramicidin A channels. Studies on the diffusion-controlled association step. Biophys. J. 41:147-165.
80. Berne, B. J., M. Borkovec, and J. E. Straub. 1988. Classical and modern methods in reaction rate theory. J. Phys. Chem. 92:3711-3725.
81. Crouzy, S., T. Woolf, and B. Roux. 1994. A molecular dynamics study of gating in dioxolane-linked gramicidin A channels. Biophys. J. 67:1370-1386.
82. Busath, D. D., C. D. Thulin, R. W. Hendershot, L. R. Phillips, P. Maughan, C. D. Cole, N. C. Bingham, S. Morrison, L. C. Baird, R. J. Hendershot, M. Cotten, and T. A. Cross. 2003. Noncontact dipole. Biophys. J. 75:2830-2844.
83. + channel. Nature. 414:73-77.
84. Allen, T. W., S. Kuyucak, and S. H. Chung. 1999. Molecular dynamics study of the KcsA potassium channel. Biophys. J. 77:2502-2516.
85. Allen, T., A. Bliznyuk, A. Rendell, S. Kuyucak, and S. Chung. 2000. The potassium channel: structure, selectivity and diffusion. J. Chem. Phys. 112:8191-8204.
86. + channel. Biochemistry. 38:8599-8604.
87. + channel. FEBS Lett. 477:37-42.
88. Shrivastava, I., and M. Sansom. 2000. Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophys. J. 78:557-570.
89. Biggin, P., G. Smith, I. Shrivastava, S. Choe, and M. Sansom. 2001. Potassium and sodium ions in a potassium channel studied by molecular dynamics simulations. Biochim. Biophys. Acta. 1510:1-9.
90. Åqvist, J., and V. Luzhkov. 2000. Ion permeation mechanism of the potassium channel. Nature. 404:881-884.
91. Oostenbrink, C., A. Villa, A. E. Mark, and W. F. van Gunsteren. 2004. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force field parameter sets 53a5 and 53a6. J. Comput. Chem. 25:1656-1676.
92. Cox, B. G., G. R. Hedwig, A. J. Parker, and D. W. Watts. 1974. Solvation of ions. XIX. Thermodynamic properties for transfer of single ions between protic and dipolar aprotic solvents. Aust. J. Chem. 27:477-501.
93. Nathan, W. I., R. M. Meighan, and R. H. Cole. 1964. Dielectric properties of alkyl amides. II. Liquid dielectric constant and loss. J. Phys. Chem. 68:509-515.
94. Roux, B., and S. Bernèche. 2002. On the potential functions used in molecular dynamics simulations of ion channels. Biophys. J. 82:1681-1684.
95. + in the gramicidin channel. Chem. Phys. Lett. 212:231-240.
96. Finkelstein, A., and P. A. Rosenberg. 1979. Membrane Transport Processes, Vol. 3. C.F. Stevens and R.W. Tsien, editors. Raven Press, New York. 73-88.
97. Mackerell, A. D., Jr. 2004. Empirical force fields for biological macromolecules: overview and issues. J. Comput. Chem. 25:1584-1604.
98. Roux, B., and S. Bernèche. 2002. On the potential functions used in molecular dynamics simulations of ion channels. Biophys. J. 82:1681-1684.