Water and ion permeation in bAQP1 and GlpF channels: A kinetic Monte Carlo study

Biophysical Journal

Volumn 87, Issue 6, 2004, Pages 3690-3702

  Miloshevsky, Gennady V ^a   Jordan, Peter C ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AQUAPORIN 1; ASPARAGINE; CATION; CATION CHANNEL; GLYCEROL; ION; PROLINE; PROTEIN; PROTEIN GLPF; PROTON; UNCLASSIFIED DRUG; WATER;

AMINO ACID SEQUENCE; ARTICLE; CYTOPLASM; ENERGY; HYDROGEN BOND; HYDROPHOBICITY; ION PERMEABILITY; KINETICS; MODEL; MONTE CARLO METHOD; PROTEIN MOTIF; PROTON TRANSPORT;

EID: 10044238762     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.043315     Document Type: Article

References (60)

1. 1 ATPases? Biophys. J. 60:101-109.
2. Åqvist, J., H. Luecke, F. A. Quiocho, and A. Warshel. 1991. Dipoles localized at helix termini of proteins stabilize charges. Proc. Natl. Acad. Sci. USA. 88:2026-2030.
3. Åqvist, J., and A. Warshel. 1993. Simulation of enzyme reactions using valence bond force fields and other hybrid quantum/classical approaches. Chem. Rev. 93:2523-2544.
4. 15N NRM. Chem. Commun. 5:501-502.
5. Beckstein, O., and M. S. P. Sansom. 2004. The influence of geometry, surface character and flexibility on the permeation of ions and water through biological pores. Phys. Biol. 1:42-52.
6. Binder, K. 1992. The Monte Carlo Method in Condensed Matter Physics. Springer-Verlag, Berlin, Germany.
7. Borgnia, M., S. Nielsen, A. Engel, and P. Agre. 1999. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68:425-458.
8. Burykin, A., and A. Warshel. 2003. What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals. Biophys. J. 85:3696-3706.
9. Burykin, A., and A. Warshel. 2004. On the origin of the electrostatic barrier for proton transport in aquaporin. FEBS Lett. 570:41-46.
10. Chakrabarti, N., E. Tajkhorshid, B. Roux, and R. Pomès. 2004. Molecular basis of proton blockage in aquaporins. Structure. 12:65-74.
11. Day, T. J. F., A. V. Soudackov, M. Čuma, U. W. Schmitt, and G. A. Voth. 2002. A second generation multistate empirical valence bond model for proton transport in aqueous systems. J. Chem. Phys. 117:5839-5849.
12. Dorman, V. L., and P. C. Jordan. 2004. Ionic permeation free energy in gramicidin. A semi-microscopic perspective. Biophys. J. 86:3529-3541.
13. Dorman, V., M. B. Partenskii, and P. C. Jordan. 1996. A semi-microscopic Monte Carlo study of permeation energetics in a gramicidin-like channel: the origin of cation selectivity. Biophys. J. 70:121-134.
14. de Groot, B. L., A. Engel, and H. Grubmüller. 2001. A refined structure of human aquaporin-1. FEBS Lett. 504:206-211.
15. de Groot, B. L., T. Frigate, V. Helms, and H. Grubmüller. 2003. The mechanism of proton exclusion in aquaporin-1 water channel. J. Mol. Biol. 333:279-293.
16. de Groot, B. L., and H. Grubmüller. 2001. Water permeation through biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 294:2353-2357.
17. Gilson, M. K., and B. Honig. 1988. Energetics of charge-charge interactions in proteins. Proteins. 3:32-52.
18. Fu, D., A. Libson, L. J. W. Miercke, C. Weitzman, P. Nollert, J. Krucinski, and R. M. Stroud. 2000. Structure of a glycerol conducting channel and the basis for its selectivity. Science. 290:481-486.
19. Harms, G. S., G. Orr, M. Montai, B. D. Thrall, S. D. Colson, and H. P. Lu. 2003. Probing conformational changes of gramicidin ion channels by single-molecule patch-clamp fluorescence microscopy. Biophys. J. 85: 1826-1838.
20. Ilan, B., E. Tajkhorshid, K. Schulten, and G. A. Voth. 2004. The mechanism of proton exclusion in aquaporin channels. Proteins. 55:223-228.
21. Jackson, J. D. 1962. Classical Electrodynamics. John Wiley, New York.
22. Jensen, M. Ø., E. Tajkhorshid, and K. Schulten. 2001. The mechanism of glycerol conduction in aquaglyceroporins. Structure. 9:1083-1093.
23. Jensen, M. Ø., E. Tajkhorshid, and K. Schulten. 2003. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85:2884-2899.
24. Kong, Y., and J. Ma. 2001. Dynamic mechanisms of the membrane water channel aquaporin-1 (AQP1). Proc. Natl. Acad. Sci. USA. 98:14345-14349.
25. Kuyucak, S., O. S. Andersen, and S. H. Chung. 2001. Models of permeation in ion channels. Rep. Prog. Phys. 64:1427-1472.
26. Leach, A. R. 2001. Molecular Modelling: Principles and Applications. Prentice Hall, Harlow, England; New York, NY.
27. Lobaugh, J., and G. A. Voth. 1996. The quantum dynamics of an excess proton in water. J. Chem. Phys. 104:2056-2069.
28. Lockhart, D. J., and P. S. Kim. 1993. Electrostatic screening of charge and dipole interactions with the helix backbone. Science. 260:198-202.
29. MacKerell, A. D., Jr., D. Bashford, M. Bellott, R. L. Jr. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
30. Marx, D., M. E. Tuckerman, J. Hutter, and M. Parrinello. 1999. The nature of the hydrated excess proton in water. Nature. 397:601-604.
31. Mehrotra, P. K., M. Mezei, and D. L. Beveridge. 1983. Convergence acceleration in Monte Carlo computer simulation on water and aqueous solutions. J. Chem. Phys. 78:3156-3166.
32. Metropolis, N., A. Rosenbluth, M. Rosenbluth, A. Teller, and E. Teller. 1953. Equations of state calculations by fast computing machines. J. Chem. Phys. 21:1087-1091.
33. Miloshevsky, G. V., and P. C. Jordan. 2004a. Details of water and ion permeation in AQP1 and GlpF water channels studied by Monte Carlo simulations. Biophys. J. 86:466a (Abstr.).
34. Miloshevsky, G. V., and P. C. Jordan. 2004b. Gating gramicidin channels in lipid bilayers: reaction coordinates and the mechanism of dissociation. Biophys. J. 86:92-104.
35. - pores: electrostatic effects of charged residues. Biophys. J. 86:825-835.
36. Murata, K., K. Mitsuoka, T. Hirai, T. Walz, P. Agre, J. B. Heymann, A. Engel, and Y. Fujiyoshi. 2000. Structural determinants of water permeation through aquaporin-1. Nature. 407:599-605.
37. Owicki, J. C., and H. A. Scheraga. 1977. Preferential sampling near solutes in Monte Carlo calculations on dilute solutions. Chem. Phys. Lett. 47: 600-602.
38. Pearlman, D. A., and P. A. Kollman. 1989. A new method for carrying out free energy perturbation calculations: dynamically modified windows. J. Chem. Phys. 90:2460-2470.
39. + translocation along the single-file water chain in the gramicidin A channel. Biophys. J. 71:19-39.
40. + conduction in the single-file chain of the gramicidin channel. Biophys. J. 82:2304-2316.
41. Preston, G. M., T. P. Carroll, W. B. Guggino, and P. Agre. 1992. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 256:385-387.
42. Ren, G., V. S. Reddy, A. Cheng, P. Melnyk, and A. K. Mitra. 2001. Visualization of a water-selective pore by electron crystallography in vitreous ice. Proc. Natl. Acad. Sci. USA. 98:1398-1403.
43. Sagnella, D. E., and M. E. Tuckerman. 1998. An empirical valence bond model for proton transfer in water. J. Chem. Phys. 108:2073-2083.
44. Savage, D. F., P. F. Egea, Y. Robles-Colmenares, J. D. O'Connell III, and R. M. Stroud. 2003. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. Plos. Biol. 1:334-340.
45. Schmitt, U. W., and G. A. Voth. 1998. Multistate empirical valence bond model for proton transport in water. J. Phys. Chem. B. 102:5547-5551.
46. Schmitt, U. W., and G. A. Voth. 1999. The computer simulation of proton transfer in water. J. Chem. Phys. 111:9361-9381.
47. Schutz, C. N., and A. Warshel. 2001. What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins. 44:400-417.
48. 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.
49. Tajkhorshid, E., P. Nollert, M. O. Jensen, L. J. W. Miercke, J. O'Connell, R. M. Stroud, and K. Schulten. 2002. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science. 296:525-530.
50. Taraphder, S., and G. Hummer. 2003. Dynamic proton transfer pathways in proteins: role of sidechain conformational fluctuations. Physica A. 318: 293-301.
51. Tuckerman, M., K. Laasonen, M. Sprik, and M. Parrinello. 1995. Ab initio molecular dynamics simulation of the solvation and transport of hydronium and hydroxyl ions in water. J. Chem. Phys. 103:150-161.
52. Vuilleumier, R., and D. Borgis. 1997. Molecular dynamics of an excess proton in water using a non-additive valence bond force field. J. Mol. Struct. 436-437:555-565.
53. Vuilleumier, R., and D. Borgis. 1999. Transport and spectroscopy of the hydrated proton: a molecular dynamics study. J. Chem. Phys. 111:4251-4266.
54. + dimer solvated in liquid water. J. Mol. Struct. 552:117-136.
55. Warshel, A. 1991. Computer Modeling of Chemical Reactions in Enzymes and Solutions. Wiley, New York.
56. Warshel, A., and R. M. Weiss. 1980. An empirical valence bond approach for comparing reactions in solutions and in enzymes. J. Am. Chem. Soc. 102:6218-6226.
57. Wei, D., and D. R. Salahub. 1994. Hydrated proton clusters and solvent effects on the proton transfer barrier: a density functional study. J. Chem. Phys. 101:7633-7642.
58. Zhu, F., E. Tajkhorshid, and K. Schulten. 2001. Molecular dynamics study of aquaporin-1 water channel in a lipid bilayer. FEES Lett. 504:212-218.
59. Zhu, F., E. Tajkhorshid, and K. Schulten. 2002. Pressure-induced water transport in membrane channels studied by molecular dynamics. Biophys. J. 83:154-160.
60. Zhu, F., E. Tajkhorshid, and K. Schulten. 2004. Theory and simulation of water permeation in aquaporin-1. Biophys. J. 86:50-57.