Charge delocalization in proton channels, I: The aquaporin channels and proton blockage

Biophysical Journal

Volumn 92, Issue 1, 2007, Pages 46-60

  Chen, Hanning ^a   Ilan, Boaz ^a,c   Wu, Yujie ^a   Zhu, Fangqiang ^b   Schulten, Klaus ^b   Voth, Gregory A ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQUAPORIN 1; PROTEIN GLYCEROL FACILITATOR; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; DIPOLE; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; PROTON TRANSPORT;

EID: 33846021582     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.091934     Document Type: Article

References (65)

1. Agmon, N. 1995. The Grotthuss mechanism. Chem. Phys. Lett. 244:456-462.
2. Decoursey, T. E. 2003. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83:475-579.
3. Agre, P., and D. Kozono. 2003. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 555:72-78.
4. Wu, Y., B. Ilan, and G. A. Voth. 2005. Electrostatics and proton delocalization in proton channels. II. The minimalist synthetic LS2 channel and proton selectivity. Biophys. J. 92:61-69.
5. Brewer, M. L., U. W. Schmitt, and G. A. Voth. 2001. The formation and dynamics of proton wires in channel environments. Biophys. J. 80:1691-1702.
6. 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.
7. Tajkhorshid, E., P. Nollert, M. Ø. Jensen, L. J. W. Miercke, J. O'Connell, R. M. Stroud, and K. Shulten. 2002. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science. 296:525-530.
8. Jensen, M. Ø., U. Röthlisberger, and C. Rovira. 2005. Hydroxide and proton migration in aquaporins. Biophys. J. 89:1744-1759.
9. Nollert, P., W. E. C. Harries, D. Fu, L. J. W. Miercke, and R. M. Stroud. 2001. Atomic structure of a glycerol channel and implications for substrated permeation in aqua(glycerol)porins. FEBS Lett. 504:112-117.
10. Yarnell, A. 2004. Blockage in the cell's waterway. Chem. Eng. News. 82:42-44.
11. de Groot, B. L., T. Frigato, V. Helms, and H. Grubmueller. 2003. The mechanism of proton exclusion in aquaporin-1 water channel. J. Mol. Biol. 333:279-293.
12. 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.
13. Burykin, A., and A. Warshel. 2004. On the origin of the electrostatic barrier for proton transport in aquaporin. FEBS Lett. 570:41-46.
14. Chakrabarti, N., E. Tajkhorshid, B. Roux, and R. Pomes. 2004. Molecular basis of proton blockage in aquaporins. Structure. 12:1-20.
15. Chakrabarti, N., B. Roux, and R. Pomes. 2004. Structural determinants of proton blockage in aquaporins. J. Mol. Biol. 343:493-510.
16. Ilan, B., E. Tajkhorshid, K. Shulten, and G. A. Voth. 2004. The mechanism of proton exclusion in aquaporin channels. Proteins Struct. Funct. Bioinform. 55:223-228.
17. Chen, H., Y. Wu, and G. A. Voth. 2006. Origins of proton transport behavior from selectivity domain mutations of the aquaporin-1 channel. Biophys. J. 90:L73-L75.
18. Beitz, E., B. Wu, L. M. Holm, J. E. Schultz, and T. Zeuthen. 2006. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc. Natl. Acad. Sci. USA. 103:269-274.
19. Chernyshev, A., and S. Cukierman. 2002. Thermodynamic view of activation energies or proton transfer in various gramicidin A channels. Biophys. J. 82:182-192.
20. Berry, R. S., S. A. Rice, and J. Ross. 2000. Physical Chemistry. Oxford University Press, New York.
21. 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.
22. Day, T. J. F., A. V. Soudackov, M. Cuma, 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.
23. Voth, G. A. 2006. Computer simulation of proton solvation and transport in aqueous and biomolecular systems. Acc. Chem. Res. 39:143-150.
24. Cuma, M., U. W. Schmitt, and G. A. Voth. 2001. Multi-state empirical valence bond model for weak acid dissociation in aqueous solution. J. Phys. Chem. A. 105:187-199.
25. Schmitt, U. W., and G. A. Voth. 1999. The computer simulation of proton transport in water. J. Chem. Phys. 111:9361-9381.
26. Schmitt, U. W., and G. A. Voth. 1998. A multi-state empirical valence bond model for proton transport in water. J. Phys. Chem. B. 102:5547-5551.
27. Lobaugh, J., and G. A. Voth. 1996. The quantum dynamics of an excess proton in water. J. Chem. Phys. 104:2056-2069.
28. Schmitt, U. W., and G. A. Voth. 1999. Quantum properties of the excess proton in liquid water. Israel J. Chem. 39:483-492.
29. Cuma, M., U. W. Schmitt, and G. A. Voth. 2000. A multi-state empirical valence bond model for acid-base chemistry in aqueous solution. Chem. Phys. 258:187.
30. Schmitt, U. W., and G. A. Voth. 2000. The isotope substitution effect on the hydrated proton. Chem. Phys. Lett. 329:36-41.
31. Day, T. J. F., U. W. Schmitt, and G. A. Voth. 2000. The mechanism of hydrated proton transport in water. J. Am. Chem. Soc. 122:12027-12028.
32. Kim, J., U. W. Schmitt, J. A. Grüetzmacher, G. A. Voth, and N. F. Scherer. 2002. The vibrational spectrum of the hydrated proton: comparison of experiment, simulation, and normal mode analysis. J. Chem. Phys. 116:737-746.
33. Petersen, M. K., S. S. Iyengar, T. J. F. Day, and G. A. Voth. 2004. The hydrated proton at the water liquid/vapor interface. J. Phys. Chem. B. 108:14804-14806.
34. Lapid, H., N. Agmon, M. K. Petersen, and G. A. Voth. 2004. A bond-order analysis of the mechanism for hydrated proton mobility in liquid water. J. Chem. Phys. 122:014506.
35. Wang, F., and G. A. Voth. 2005. A linear-scaling self-consistent generalization of the multi-state empirical valence bond model for multiple excess protons in aqueous systems. J. Chem. Phys. 122:144105.
36. + conduction in the D-pathway of cytochrome c oxidase: a study of the wildtype and N98D mutant enzymes. Biochim. Biophys. Acta. 1757:852-859.
37. Xu, J., and G. A. Voth. 2005. Computer simulation of explicit proton translocation in cytochrome c oxidase: the D-pathway. Proc. Natl. Acad. Sci. USA. 102:6795-6800.
38. Smondyrev, M., and G. A. Voth. 2002. Molecular dynamics simulation of proton transport near the surface of a phospholipid membrane. Biophys. J. 82:1460-1468.
39. Smondyrev, M., and G. A. Voth. 2002. Molecular dynamics simulation of proton transport through the influenza A virus M2 channel. Biophys. J. 83:1987-1996.
40. Wu, Y., and G. A. Voth. 2003. A computer simulation study of the hydrated proton in a synthetic proton channel. Biophys. J. 85:864-875.
41. Wu, Y., and G. A. Voth. 2003. Computational studies of proton transport through the M2 channel. FEBS Lett. 552:23-27.
42. Voth, G. A. 2003. The computer simulation of proton transport in biomolecular systems. Front. Biosci. 8:1384-1397.
43. Tepper, H. L., and G. A. Voth. 2005. Protons may leak through pure lipid bilayers via a concerted mechanism. Biophys. J. 88:3095-3108.
44. Beckstein, O., K. Tai, and M. S. Sansom. 2004. Not ions alone: barriers to ion permeation in nanopores and channels. J. Am. Chem. Soc. 126:14694-14695.
45. 2+ regulation of aquaporin water permeability. J. Gen. Physiol. 123:573-580.
46. Lear, J. D., Z. R. Wasserman, and W. F. DeGrado. 1998. Synthetic amphiphilic peptide models for protein ion channels. Science. 240:1177-1181.
47. Jensen, M. Ø., E. Tajkhorshid, and K. Schulten. 2003. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85:2884-2899.
48. Kramers, H. A. 1940. Computational studies of membrane channels. Phys. 7:284-304.
49. Levitt, D. 1991. General continuum theory for multiion channel. I. Theory. Biophys. J. 59:271-277.
50. Berne, B. J., M. Borkovec, and J. E. Straub. 1988. Classical and modern methods in reaction rate theory. J. Phys. Chem. 92:3711-3725.
51. Woolf, T. B., and B. Roux. 1994. Conformational flexibility of O-phosphorylcholine and O-phosphorylethanolamine: a molecular dynamics study of solvation effects. J. Am. Chem. Soc. 116:5916-5926.
52. Smart, O., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460.
53. Finkelstein, A. 1987. Water Movement Through Lipid Bilayers, Pores and Plasma Membranes. Wiley, New York.
54. Pohl, P., S. M. Saparov, M. J. Borgnia, and P. Agre. 2001. Highly selective water channel activity measured by voltage clamp: analysis of planar lipid bilayers reconstituted with purified AqpZ. Proc. Natl. Acad. Sci. USA. 98:9624-9629.
55. Fangqiang, Z., E. Tajkhorshid, and K. Schulten. 2004. Theory and simulation of water permeation in aquaporin-1. Biophys. J. 86:50-57.
56. 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.
57. Smith, W., and T. R. Forester. The DL-POLY Molecular Simulation Package. In CCLRC. Daresbury Laboratory, Daresbury, Warrington, England.
58. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulation liquid water. J. Chem. Phys. 79:926-935.
59. Soper, A. K. 2000. The radial distribution functions of water and ice from 220 to 673 K and at pressures up to 400 MPa. Chem. Phys. 258:121-137.
60. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for freeenergy calculations. J. Comput. Chem. 13:1011-1021.
61. Park, S., F. Khalili-Araghi, E. Tajkhorshid, and K. Schulten. 2003. Free energy calculation from steered molecular dynamics simulations using Jarzynski's equality. J. Chem. Phys. 199:3559-3566.
62. Hummer, G. 2001. Fast-growth thermodynamic integration: error and efficiency analysis J. Chem. Phys. 114:7330-7337.
63. Hummer, G. 2005. Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular systems. N. J. Phys. 7:34-47.
64. Manly, B. F. J. 1998. Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman and Hall, London.
65. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.