What Really Prevents Proton Transport through Aquaporin? Charge Self-Energy versus Proton Wire Proposals

Biophysical Journal

Volumn 85, Issue 6, 2003, Pages 3696-3706

  Burykin, Anton ^a   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; PROTON; WATER;

ARTICLE; ENERGY; MOLECULAR DYNAMICS; PROTEIN STRUCTURE; PROTON TRANSPORT; SIMULATION; SOLVATION;

EID: 0344825877     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74786-9     Document Type: Article

References (85)

1. Agmon, N. 1995. The Grotthuss mechanism. Chem. Phys. Lett. 244:456-462.
2. Alden, R. G., W. W. Parson, Z. T. Chu, and A. Warshel. 1995. Calculations of electrostatic energies in photosynthetic reaction centers. J. Am. Chem. Soc. 117:12284-12298.
3. Alhambra, C., J. C. Corchado, M. L. Sanchez, J. Gao, and D. G. Truhlar. 2000. Quantum dynamics of hydride transfer in enzyme catalysis. J. Am. Chem. Soc. 122:8197-8203.
4. Aqvist, 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.
5. + by gramicidin A. Biophys. J. 56:171-182.
6. Aqvist, 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.
7. Berendsen, H. J. C. 2001. Reality simulation - observe while it happens. Science. 294:2304-2305.
8. Billeter, S. R., S. P. Webb, T. Iordanov, P. K. Agarwal, and S. Hammes-Schiffer. 2001. Hybrid approach for including electronic and nuclear quantum effects in molecular dynamics simulations of hydrogen transfer reactions in enzymes. J. Chem. Phys. 114:6925-6936.
9. Burykin, A., M. Kato, and A. Warshel. 2003. Exploring the origin of the ion selectivity of the KcsA potassium channel. Proteins. 52:412-426.
10. Burykin, A., C. N. Schutz, J. Villa, and A. Warshel. 2002. Simulations of ion current in realistic models of ion channels: the KcsA potassium channel. Prot. Struc. Func. Gen. 47:265-280.
11. de Groot, B. L., T. Frigate, V. Helms, and H. Grubmüller. 2003. The mechanism of proton exclusion in aquaporin-I channel. J. Mol. Biol. 333:279-293.
12. de Groot, B., and H. Grubmüller. 2001. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 294:2353-2357.
13. Decoursey, T. E. 2003. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83:475-579.
14. Dellago, C., M. Naor, and G. Hummer. 2003. Proton transport through water-filled nanotubes. Phys. Rev. Lett. 90:105902/1-105902/4.
15. Eigen, M. 1964. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Angew. Chem. Int. Ed. Engl. 3:1-72.
16. Ermler, U., G. Fritzsch, S. K. Buchanan, and H. Michel. 1994. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65-E resolution: cofactors and protein-cofactor interactions. Structure. 2:925-936.
17. Feierberg, I., V. Luzhkov, and J. Eqvist. 2000. Computer simulation of primary kinetic isotope effects in the proposed rate limiting step of the glyoxalase I catalyzed reaction. J. Biol. Chem. 275:22657-22662.
18. Fu, D., A. Libson, L. Miercke, C. Weitzmann, 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. Gennis, R. B. 1989. Biomembranes: Molecular Structure and Function. Springer-Verlag, New York.
20. Girvin, M. E., V. K. Rastogi, F. Abildgaard, J. L. Markley, and R. H. Fillingame. 1998. Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry. 37:8817-8824.
21. Hammes-Schiffer, S. 1996. Multiconfigurational molecular dynamics with quantum transitions: multiple proton transfer reactions. J. Chem. Phys. 105:2236-2246.
22. Hummer, G., J. C. Rasaiah, and J. P. Noworyta. 2001. Water conduction through the hydrophobic channel of a carbon nanotube. Nature. 414:188-190.
23. n2 reactions in aqueous solution. J. Am. Chem. Soc. 110:5297-5311.
24. Hwang, J.-K., and A. Warshel. 1996. How important are quantum mechanical nuclear motions in enzyme catalysis? J. Am. Chem. Soc. 118:11745-11751.
25. Jensen, M. Ø., E. Tajkhorshid, and K. Schulten. 2003. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85:1-16.
26. Johnson, E. T., and W. W. Parson. 2002. Electrostatic interactions in an integral membrane protein. Biochemistry. 41:6483-6494.
27. Kannt, A., R. D. Lancaster, and H. Michel. 1998. The coupling of eiectron transfer and proton translocation: electrostatic calculations on Paracoccus dentrificans cytochrome c oxidase. Biophys. J. 74:708-721.
28. King, G., and A. Warshel. 1989. A surface-constrained all-atom solvent model for effective simulations of polar solutions. J. Chem. Phys. 91: 3647-3661.
29. Kitzing, E., and D. M. Soumpasis. 1996. Electrostatics of a simple membrane model using Green's functions formalism. Biophys. J. 71: 795-810.
30. Kong, Y., and G. Ma. 2001. Dynamic mechanisms of the membrane water channel aquaporin-I (AQP1). Proc. Natl. Acad. Sci. USA. 98:14345-14349.
31. + analogs in solutions. J. Am. Chem. Soc. 117:6234-6242.
32. Lancaster, C. R. D., H. Michel, and B. Honig. 1996. Calculated coupling electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys. J. 70:2469-2492.
33. Law, R. J., and M. S. P. Sansom. 2002. Water transporters: how so fast yet so selective? Curr. Biol. 12:R250-R252.
34. Lee, F. S., Z. T. Chu, and A. Warshel. 1993. Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the POLARIS and ENZYMIX programs. J. Comp. Chem. 14:161-185.
35. Lee, F. S., and A. Warshel. 1992. A local reaction field method for fast evaluation of long-range electrostatic interactions in molecular simulations. J. Chem. Phys. 97:3100-3107.
36. Luecke, H. 2000. Atomic resolution structures of bacteriorhodopsin photocycle intermediates: the role of discrete water molecules in the function of this light-driven ion pump. Biochim. Biophys. Acta. 1460:133-156.
37. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
38. Marcus, R. A. 1964. Chemical and electrochemical electron transfer theory. Annu. Rev. Phys. Chem. 15:155-196.
39. Marrink, S. J., F. Jahnig, and H. J. Berendsen. 1996. Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations. Biophys. J. 71:632-647.
40. Mitchell, P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 191:144-148.
41. Murata, K., K. Mitsuoka, T. Hiral, T. Waltz, P. Agrel, J. B. Heymann, A. Engel, and Y. Fujlyoshi. 2000. Structural determinants of water permeation through aquaporin-1. Nature. 407: 599-605.
42. Nagle, J. F., and M. Mille. 1981. Molecular models of proton pumps. J. Chem. Phys. 74:1367-1372.
43. Nagle, J. F., and H. J. Morowitz. 1978. Theory of hydrogen-bonded chains in bioenergetics. Proc. Natl. Acad. Sci. USA. 75:298-302.
44. Okamura, M. Y., and G. Feher. 1992. Proton transfer in reaction centers from photosynthetic bacteria. Annu. Rev. Biochem. 61:861-896.
45. Ostermeier, C., A. Harrenga, U. Ermler, and H. Michel. 1997. Structure at 2.7 A resolution of the Paracoccus dentrificans two-subunit cytochromec oxidase complexed with an antibody FV fragment. Proc. Natl. Acad. Sci. USA. 94:10547-10553.
46. Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature. 221:844-846.
47. Pomès, R., and B. Roux. 1998. Free energy profiles for H+ conduction along hydrogen-bonded chains of water molecules. Biophys. J. 75:33-40.
48. + conduction in the single-file chain of the gramicidin channel. Biophys. J. 82:2304-2316.
49. Royant, A., K. Edman, T. Ursby, E. Pebay-Peyroula, E. M. Landau, and R. Neutze. 2000. Helix deformation is coupled to vectorial proton transport in the photocycle of bacteriorhodopsin. Nature. 406:645-648.
50. Sansom, M. S. P., and R. J. Law. 2001. Aquaporins - channels without ions. Curr. Biol. 11:R71-R73.
51. Sass, H. J., G. Buldt, R. Gessenich, D. Hehn, D. Neff, R. Schlesinger, J. Berendzen, and P. Ormos. 2000. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature. 406:649-653.
52. Scheiner, S. 1981. Proton transfers in hydrogen-bonded systems. Cationic oligomers of water. J. Am. Chem. Soc. 103:315-320.
53. 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.
54. Schutz, C. N., and A. Warshel. 2001. What are the dielectric "constants" of proteins and how to validate electrostatic models. Prot. Struc. Func. Gen. 44:400-417.
55. Schweins, T., and A. Warshel. 1996. Mechanistic analysis of the observed linear free energy relationships in p21 ras and related systems. Biochemistry. 35:14232-14243.
56. Sham, Y., I. Muegge, and A. Warshel. 1999. Simulating proton translocations in proteins: probing proton transfer pathways in the Rhodobacter sphaeroides reaction center. Proteins. 36:484-500.
57. as of ionizable residues in proteins: semi-microscopic and macroscopic approaches. J. Phys. Chem. B. 101:4458-4472.
58. Sham, Y. Y., I. Muegge, and A. Warshel. 1998. The effect of protein relaxation on charge-charge interactions and dielectric constants of proteins. Biophys. J. 74:1744-1753.
59. Strajbl, M., G. Hong, and A. Warshel. 2002. Ab-initio QM/MM simulation with proper sampling: "first principle" calculations of the free energy of the auto-dissociation of water in aqueous solution. J. Phys. Chem. B. 106:13333-13343.
60. Sui, H., B.-G. Han, J. K. Lee, P. Walian, and B. K. Jap. 2001. Structural basis of water-specific transport through the AQPI water channel. Nature. 414:872-878.
61. Tajkhorshid, E., P. Nollert, M. Jensen, L. Miercke, R. M. Stroud, and K. Schulten. 2002. Control of the selectivity of the aquaporin water channel by global orientational tuning. Science. 296:525-530.
62. Villa, J., and A. Warshel. 2001. Energetics and dynamics of enzymatic reactions. J. Phys. Chem. B. 105:7887-7907.
63. n clusters and liquid water. Chem. Phys. Lett. 284:71-77.
64. Vuilleumier, R., and D. Borgis. 1999. Transport and spectroscopy of the hydrated proton: a molecular dynamics study. J. Chem. Phys. 111: 4251-4266.
65. Warshel, A. 1979. Conversion of light energy to electrostatic energy in the proton pump of Halobacterium' halobium. Photochem. Photobiol. 30:285-290.
66. Warshel, A. 1981. Energetics of light-induced charge separation across membranes. Isr. J. Chem. 21:341-347.
67. Warshel, A. 1982. Dynamics of reactions in polar solvents. semiclassical trajectory studies of electron-transfer and proton-transfer reactions. J. Phys. Chem. 86:2218-2224.
68. Warshel, A. 1984a. Dynamics of enzymatic reactions. Proc. Natl. Acad. Sci. USA. 81:444-448.
69. Warshel, A. 1984b. Simulating the energetics and dynamics of enzymatic reactions. Pontificiae Academiae Scientiarum Scripta Varia. 55(Specif. Biol. Interact.):59-81.
70. Warshel, A. 1986. Correlation between structure and efficiency of light-induced proton pumps. In Methods in Enzymology. L. Packer, editor. Academic Press, London, UK. 578-587.
71. Warshel, A. 1991. Computer Modeling of Chemical Reactions in Enzymes and Solutions. John Wiley & Sons, New York.
72. Warshel, A. 2002. Molecular dynamics simulations of biological reactions. Acc. Chem. Res. 35:385-395.
73. Warshel, A. 2003. Computer simulations of enzyme catalysis: methods, progress, and insights. Annu. Rev. Biophys. Biomol. Struct. 32:425-443.
74. Warshel, A., J. Aqvist, and S. Creighton. 1989. Enzymes work by solvation substitution rather than by desolvation. Proc. Natl. Acad. Sci. USA. 86:5820-5824.
75. Warshel, A., and M. Levitt. 1976. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J. Mol. Biol. 103:227-249.
76. Warshel, A., and S. T. Russell. 1984. Calculations of electrostatic interactions in biological systems and in solutions. Q. Rev. Biophys. 17: 283-421.
77. Warshel, A., S. T. Russell, and A. K. Churg. 1984. Macroscopic models for studies of electrostatic interactions in proteins: limitations and applicability. Proc. Natl. Acad. Sci. USA. 81:4785-4789.
78. Warshel, A., and D. W. Schlosser. 1981. Electrostatic control of the efficiency of light-induced electron transfer across membranes. Proc. Natl. Acad. Sci. USA. 78:5564-5568.
79. Warshel, A., T. Schweins, and M. Fothergill. 1994. Linear free energy relationships in enzymes. theoretical analysis of the reaction of tyrosyl-tRNA synthetase. J. Am. Chem. Soc. 116:8437-8442.
80. Warshel, A., and R. M. Weiss. 1980. An empirical valence bond approach for comparing reactions insolutions and in enzymes. J. Am. Chem. Soc. 102:6218-6226.
81. Wikstrom, M. 1998. Proton translocation by bacteriorhodopsin and heme-copper oxidases. Curr. Op. Struct. Biol. 8:480-488.
82. 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.
83. Yoshikawa, S., K. Shinzawa-Itoh, R. Nakashima, R. Yaono, E. Yamashita, N. Inoue, M. Yao, M. J. Fei, C. P. Libeu, T. Mizushima, H. Yamaguchi, T. Tomizaki, and T. Tsukihara. 1998. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science. 280:1723-1729.
84. Zeuthen, T. 2001. How water molecules pass through aquaporins. Trends Biochem. Sci. 26:77-78.
85. Zundel, G., and J. Frish. 1986. Chapter 2. In The Chemical Physics of Solvation, Vol. 2. Elsevier, Amsterdam, The Netherlands.