Protonation of lysine residues inverts cation/anion selectivity in a model channel

Biophysical Journal

Volumn 78, Issue 3, 2000, Pages 1335-1348

  Borisenko, Vitali ^a   Sansom, Mark S P ^b   Woolley, G Andrew ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALAMETHICIN DERIVATIVE; ANION; ANION CHANNEL; LYSINE;

AMINO ACID SUBSTITUTION; ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; ELECTRIC ACTIVITY; MODEL; PH; PKA; PROTON TRANSPORT; REACTION ANALYSIS;

EID: 0034090665     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76688-4     Document Type: Article

References (77)

1. Adcock, C., G. R. Smith, and M. S. P. Sansom. 1998. Electrostatics and the ion selectivity of ligand-gated channels. Biophys. J. 75:1211-1222.
2. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1994. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:415-436.
3. a's of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry. 29: 10219-10225.
4. Bell, R. P. 1971 The Proton in Chemistry. Cornell University Press, Ithaca, New York.
5. Bell, T. W. 1998. Carriers and channels: current progress and future prospects. Curr. Opin. Chem. Biol. 2:711-716.
6. Boerrigter, H., L. Grave, J. Nissink, L. Chrisstoffels, J. van der Maas, W. Verboom, F. de Jong, and D. Reinhoudt. 1998. (Thio)urea resorcinarene cavitands. Complexation and membrane transport of halide anions. J. Org. Chem. 63:4174-4180.
7. Borisova, M. P., R. A. Brutyan, and L. N. Ermishkin. 1986. Mechanism of anion-cation selectivity of amphotericin B channels. J. Membr. Biol. 90:13-20.
8. Bowen, K. A., K. Tam, and M. Colombini. 1985. Evidence for titratable gating charges controlling the voltage dependence of the outer mitochondrial membrane channel, VDAC. J. Membr. Biol. 86:51-9.
9. Breed, J. 1996. Molecular Modelling of Ion Channels. Oxford University.
10. Breed, J., P. C. Biggin, I. D. Kerr, O. S. Smart, and M. S. P. Sansom. 1997. Alamethicin channels: modeling via restrained molecular dynamics simulations. Biochim. Biophys. Ada. 1325:235-249.
11. 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. Comp. Chem. 4:187-217.
12. Brunger, A. T. 1992. X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. Yale University Press, New Haven. CT.
13. Cafiso, D. S. 1994. Alamethicin: a peptide model for voltage gating and protein-membrane interactions. Annu. Rev. Biophys. Biomol. Struct. 23:141-165.
14. Cantor, C. R., and P. R. Schimmel. 1980. Biophysical Chemistry, Part III: The Behavior of Biological Macromolecules. W. H. Freeman, San Francisco.
15. Cescatti, L., C. Pederzolli, and G. Menestrina. 1991. Modification of lysine residues of Staphylococcus aureus alpha-toxin: effects on its channel-forming properties. J. Membr. Biol. 119:53-64.
16. Cherry, R. J., D. Chapman, and D. E. Graham. 1972. Studies of the conductance changes induced in bimolecular iipid membranes by alamethicin. J. Membr. Biol. 7:325-344.
17. Corringer, P. J., S. Bertrand, J. L. Galzi, A. Devillers-Thiery, J. P. Changeux, and D. Bertrand. 1999. Mutational analysis of the charge selectivity filter of the alpha7 nicotinic acetylcholine receptor. Neuron. 22: 831-843.
18. Cox, B., G. Hedwig, A. Parker, and D. 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.
19. Darveau, R. P., R. E. Hancock, and R. Benz. 1984. Chemical modification of the anion selectivity of the PhoE porin from the Escherichia coli outer membrane. Biochim. Biophys. Acta. 774:67-74.
20. Davis, M. E., J. D. Madura, B. A. Luty, and J. A. McCammon. 1991. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian dynamics program. Comput. Phys. Comm. 62:187-197.
21. Dieckmann. G. R., J. D. Lear, Q. Zhong, M. Klein, M. L. DeGrado, and K. A. Sharp. 1999. Exploration of the structural features defining the conduction properties of a synthetic channel. Biophys. J. 76:618-630.
22. Dietrich, B., M. W. Hosseini, J. M. Lehn, and R. B. Sessions. 1981. Anion receptor molecules. Synthesis and anion-binding properties of polyammonium macrocycles. J. Am. Chem. Soc. 103:1282-1283.
23. 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.
24. + conduction and selectivity. Science. 280:69-77.
25. Dutzler, R., G. Rummel, S. Alberti, S. Hernandez-Alles, P. Phale, J. Rosenbusch, V. Benedi, and T. Schirmer. 1999. Crystal structure and functional characterization of ompK36, the osmoporin of Klebsiella pnewnoniae. Structure. 7:425-434.
26. Eigen, M. 1964. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Angew. Chem. Intl. Ed. 3:1-72.
27. Fahlke, C., H. T. Yu, C. L. Beck, T. H. Rhodes, and A. L. George, Jr. 1997. Pore-forming segments in voltage-gated chloride channels. Nature. 390: 529-532.
28. Franciolini, F., and W. Nonner. 1987. Anion and cation permeability of a chloride channel in rat hippocampal neurons. J. Gen. Physiol. 90: 453-478.
29. Guinamard, R., and M. H. Akabas. 1999. Arg352 is a major determinant of charge selectivity in the cystic fibrosis transmembrane conductance regulator chloride channel. Biochemistry. 38:5528-5537.
30. Hall, J. E., I. Vodyanoy, T. M. Balasubramanian, and G. R. Marshall. 1984. Alamethicin: a rich model for channel behavior. Biophys. J. 45:233-248.
31. Hancock, R. E., and R. Benz. 1986. Demonstration and chemical modification of a specific phosphate binding site in the phosphate-starvation-inducihle outer membrane porin protein P of Pseudonumas aeruginosa. Biochim. Biophys. Acta. 860:699-707.
32. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
33. Honig, B., K. Sharp, and A. Yang. 1993. Macroscopic models of aqueous solutions: biological and chemical applications. J. Phys. Chem. 97: 1101-1109.
34. Huyghues-Despointes, B. M., J. M. Scholtz, and R. L. Baldwin. 1993. Effect of a single aspartate on helix stability at different positions in a neutral alanine-based peptide. Protein Sci. 2:1604-1611.
35. 7 mutation. Biochemistry: 36:13873-13881.
36. Karshikoff, A., V. Spassov, S. W. Cowan, R. Ladenstein, and T. Schirmer. 1994. Electrostatic properties of two porin channels from Escherichia coli. J. Mol. Biol. 240:372-384.
37. Kasianowicz, J. J., and S. M. Bezrukov. 1995. Protonation dynamics of the alpha-toxin ion channel from spectral analysis of pH-dependent current fluctuations. Biophys. J. 69:94-105.
38. Lanyi, J. K., A. Duschl, G. Varo, and L. Zimanyi. 1990. Anion binding to the chloride pump, halorhodopsin, and its implications for the transport mechanism. FEBS Lett. 265:1-6.
39. Latorre, R., and O. Alvarez. 1981. Voltage-dependent channels in planar lipid bilayer membranes. Physiol. Rev. 61:77-150.
40. Lear, J. D., J. P. Schneider, P. K. Kienker, and W. F. DeGrado. 1997. Electrostatic effects on ion selectivity and rectification in designed ion channel peptides. J. Am. Chem. Soc: 119:3212-3217.
41. Levitt, D. G. 1991a. General continuum theory for multiion channel I. Theory. Biophys. J. 59:271-277.
42. Levitt, D. G. 1991b. General continuum theory for multiion channel II. Application to acetylcholine channel. Biophys. J. 59:278-288.
43. Malashkevich, V. N., R. A. Kammerer. V. P. Efimov, T. Schulthess, and J. Engel. 1996. The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel? Science. 274:761-765.
44. Marcus, Y. 1997. Ion Properties. Marcel Dekker, Inc., New York.
45. Marshall, G. R., and D. D. Beusen. 1994. The structural basis of peptide channel formation. In Biomembrane Electrochemistry. American Chemical Society, Washington, DC. 259-314.
46. Moczydlowski, E. 1998. Chemical basis for alkali cation selectivity in potassium-channel proteins. Chem. Biol. 5:R291-R301.
47. Nicholls. A., K. A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11:281-296.
48. Nilges, M., and A. T. Brunger. 1993. Successful prediction of the coiled coil geometry of the GCN4 leucine zipper domain by simulated annealing: comparison to the x-ray structure. Proteins: Struct., Funct., Genet. 15:133-146.
49. O'Keeffe, F., S. A. Shamsi, R. Darcy, P. Schwinte, and I. M. Warner. 1997. A persubstituted catiunic β-cyclodextrin for chiral separations. Anal. Chem. 69:4773-4782.
50. Perutz, M. F., D. T. Shih, and D. Williamson. 1994. The chloride effect in human haemoglobin. A new kind of allosteric mechanism. J. Mol. Biol. 239:555-560.
51. + ions on simulated structure and dynamics of βARK1 PH domain. Proteins: Struct., Funct., Genet. 35:206-217.
52. 2+ channel. Nature. 329:243-246.
53. Rink, T., H. Bartel, G. Jung, W. Bannwarth, and G. Boheim. 1994. Effects of polycations on ion channels formed by neutral and negatively charged alamethicins. Eur. Biophys. J. 23:155-165.
54. Robinson, R. A., and R. H. Stokes. 1968. Electrolyte Solutions. Butterworths, London.
55. Root, M. J., and R. MacKinnon. 1994. Two identical noninteracting sites in an ion channel revealed by proton transfer. Science. 265:1852-1856.
56. Sansom, M. S. P. 1991. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 55:139-235.
57. Sansom, M. S. P. 1993a. Alamethicin and related peptaibols - model ion channels. Eur. Biophys. J. 22:105-124.
58. Sansom, M. S. P. 1993b. Structure and function of channel-forming peptaibols. Q. Rev. Biophys. 26:365-421.
59. Sansom, M. S. P. 1998. Models and simulations of ion channels and related membrane proteins. Curr. Opin. Struct. Biol. 8:237-244.
60. Schmid, B., L. Maveyraud, M. Kromer, and G. E. Schulz. 1998. Porin mutants with new channel properties. Protein Sci. 7:1603-1611.
61. Schmidtchen, F., and M. Berger. 1997. Artificial organic host molecules for anions. Chem. Rev. 97:1609-1646.
62. Sitkoff. D., D. J. Lockhart, K. A. Sharp, and B. Honig. 1994. Calculation of electrostatic effects at the amino terminus of an alpha helix. Biophys. J. 67:2251-2260.
63. Smart, O. S., J. Breed, G. R. Smith, and M. S. P. Sansom. 1997. A novel method for structure-based prediction of ion channel conductance properties. Biophys. J. 72:1109-1126.
64. Smart, O. S., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460.
65. Starostin, A. V., R. Butan, V. Borisenko, D. A. James, H. Wenschuh, M. S. P. Sansom, and G. A. Woolley. 1999. An anion-selective analogue of the channel-forming peptide alamethicin. Biochemistry. 38: 6144-6150.
66. Tabcharani, J. A., P. Linsdell, and J. W. Hanrahan. 1997. Halide permeation in wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride channels. J. Gen. Physiol. 110:341-54.
67. Tieleman, D. P., H. J. Berendsen, and M. S. P. Sansom. 1999a. An alamethicin channel in a lipid bilayer: molecular dynamics simulations. Biophys. J. 76:1757-1769.
68. Tieleman, D. P., M. S. P. Sansom, and H. J. C. Berendsen. 1999b. Alamethicin helices in a bilayer and in solution: molecular dynamics simulations. Biophys. J. 76:40-49.
69. Van Gelder, P., N. Saint, R. van Boxtel, J. P. Rosenbusch, and J. Tommassen. 1997. Pore functioning of outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng. 10:699-706.
70. a calculations: conformational averaging versus the average structure. Proteins: Struct., Funct., Genet. 33:145-158.
71. Wang, C. T., H. G. Zhang, T. A. Rocheleau, R. H. ffrench-Constant, and M. B. Jackson. 1999. Cation permeability and cation-anion interactions in a mutant GABA-gated chloride channel from Drosophila. Biophys. J. 77:691-700.
72. Warshel, A., and A. Papazyan. 1998. Electrostatic effects in macromolecules: fundamental concepts and practical modeling. Curr. Opin. Struct. Biol. 8:211-217.
73. Weast, R. C., and M. J. Astle. 1981. CRC Handbook of Chemistry and Physics. CRC Press Inc., Boca Raton, FL.
74. Weetman, P., S. Goldman, and C. G. Gray. 1997. Use of the Poisson-Boltzmann equation to estimate the electrostatic free energy barrier for dielectric models of biological ion channels. J. Phys. Chem. B. 101: 6073-6078.
75. Woolley, G. A., P. C. Biggin, A. Schultz, L. Lien, D. C. J. Jaikaran, J. Breed, K. Crowhurst, and M. S. P. Sansom. 1997. Intrinsic rectification of ion flux in alamethicin channels: studies with an alamethicin dimer. Biophys. J. 73:770-778.
76. Woolley, G. A., and B. A. Wallace. 1992. Model ion channels: gramicidin and alamethicin. J. Membr. Biol. 129:109-136.
77. You, S., S. Peng, L. Lien, J. Breed, M. S. P. Sansom, and G. A. Woolley. 1996. Engineering stabilized ion channels: covalent dimers of alamethicin. Biochemistry. 35:6225-6232.