Ligand-gated ion channels: Mechanisms underlying ion selectivity

Progress in Biophysics and Molecular Biology

Volumn 86, Issue 2, 2004, Pages 161-204

  Keramidas, Angelo ^a   Moorhouse, Andrew J ^a   Schofield, Peter R ^b   Barry, Peter H ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Electrostatics; Ligand gated ion channels; Permeation models; Pore diameter; Selectivity filter; Selectivity mutants

Indexed keywords

ION; ION CHANNEL; LIGAND;

ANIMAL; BIOLOGICAL MODEL; BRAIN; CHANNEL GATING; HUMAN; PHYSIOLOGY; REVIEW;

ANIMALS; BRAIN; HUMANS; ION CHANNEL GATING; ION CHANNELS; IONS; LIGANDS; MODELS, BIOLOGICAL;

EID: 3543062342     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2003.09.002     Document Type: Review

References (116)

1. Adams D.J., Dwyer T.M., Hille B. The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75:1980;493-510
2. Adcock C., Smith G.R., Sansom M.S.P. Electrostatics and the ion selectivity of ligand-gated channels. Biophys. J. 75:1998;1211-1222
3. Akabas M.H., Kaufmann C., Archdeacon P., Karlin A. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the α subunit. Neuron. 13:1994;919-927
4. Barry P.H., Diamond J.M. Junction potentials, electrode standard potentials, and other problems in interpreting electrical properties in membranes. J. Membr. Biol. 3:1970;93-122
5. Barry P.H., Diamond J.M. A theory of ion permeation through membranes with fixed sites. J. Membr. Biol. 4:1971;295-330
6. Barry, P.H., Gage, P.W., 1984. Ionic selectivity of channels at the end plate. In: Stein, W.D. (Ed.), Current Topics in Membranes and Transport, Vol. 21. Academic Press, London, pp. 1-51.
7. Barry P.H., Lynch J.W. Topical review. Liquid junction potentials and small cell effects in patch clamp analysis. J. Membr. Biol. 121:1991;101-117
8. Bera A.K., Chatav M., Akabas M.H. GABA(A) receptor M2-M3 loop secondary structure and changes in accessibility during channel gating. J. Biol. Chem. 277(45):2002;43002-43010
9. Bertrand D., Galzi J-L., Devillers-Thiéry A., Bertrand S., Changeux J-P. Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc. Nat. Acad. Sci. USA. 90:1993;6971-6975
10. Birnir B., Eghbali M., Everitt A.B., Gage P.W. Bicuculline, pentobarbital and diazepam modulate spontaneous GABA(A) channels in rat hippocampal neurons. Br. J. Pharmacol. 131:2000;695-704
11. A channels in outside-out patches from rat hippocampal neurons. J. Membr. Biol. 181:2001;171-183
12. Bormann J., Hamill O.P., Sakmann B. Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385:1987;243-286
13. Bormann J., Rundstrom N., Betz H., Langosch D. Residues within transmembrane segment M2 determine chloride conductance of glycine receptor homo- and hetero-oligomers. EMBO J. 12:1993;3729-3737
14. Brejc K., van Dijk W.J., Klaassen R.V., Schuurmans M., van der Oost J., Smit A.B., Sixma T.K. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature. 411:2001;269-276
15. 3A). J. Physiol. 507:1998;653-665
16. Cohen B.N., Labarca C., Davidson N., Lester H.A. Mutations in M2 alter the selectivity of the mouse nicotinic acetylcholine receptor for organic and alkali metal cations. J. Gen. Physiol. 100:1992;373-400
17. + permeability ratios of nicotinic acetylcholine receptors are reduced by mutations near the intracellular end of the M2 region. J. Gen. Physiol. 99:1992;545-572
18. Corringer J-P., Bertrand S., Galzi J-L., Devillers-Thiery A., Changeux J-P., Bertrand D. Mutational analysis of the charge selectivity filter of the α7 nicotinic acetylcholine receptor. Neuron. 22:1999;831-843
19. Corry B., Kuyucak S., Chung S-H. Test of Poisson-Nernst-Planck theory in ion channels. J. Gen. Physiol. 114:1999;597-599
20. Couturier S., Bertrand D., Matter J-M., Hernandez M-C., Bertrand S., Millar N., Valera S., Barkas T., Ballivet M. A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron. 5:1990;847-856
21. Cutting G.R., Lu L., O′Hara B.F., Kasch L.M., Montrose-Rafizadeh C., Donovan D.M., Shimada S., Antonarakis S.E., Guggino W.B., Uhl G.R., et al. Cloning of the gamma-aminobutyric acid (GABA) rho 1 cDNA. a GABA receptor subunit highly expressed in the retina Proc. Nat. Acad. Sci. USA. 88:1991;2673-2677
22. Dani J.A. Open channel structure and ion binding sites of the nicotinic acetylcholine receptor channel. J. Neurosci. 9:1989;884-892
23. 3BR subunit is a major determinant of serotonin-receptor function. Nature. 397:1999;359-363
24. 2+. J Biol. Chem. 278:2003;712-717
25. + conduction and selectivity Science. 280:1998;69-77
26. Dutzler R., Campbell E.B., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a ClC channel at 3.0. Å reveals the molecular basis of anion selectivity Nature. 415:2002;287-294
27. Dwyer T.M., Adams D.J., Hille B. The permeability of the endplate channel to organic cations in frog muscle. J. Gen. Physiol. 75:1980;469-492
28. Eghbali M., Curmi J.P., Birnir B., Gage P.W. Hippocampal GABA(A) channel conductance increased by diazepam. Nature. 388:1997;71-75
29. Eghbali M., Gage P.W., Birnir B. Pentobarbital modulates gamma-aminobutyric acid-activated single-channel conductance in rat cultured hippocampal neurons. Mol. Pharmacol. 58:2000;463-469
30. Eisenberg R.S. Computing the field in proteins and channels. J. Membr. Biol. 150:1996;1-25
31. Eisenman G., Horn R. Ionic selectivity revisited. the role of kinetic and equilibrium processes in ion permeation through channels J. Membr. Biol. 76:1983;197-225
32. Fatima-Shad K., Barry P.H. Anion permeation in GABA- and glycine-gated channels of mammalian cultured hippocampal neurons. Proc. R. Soc. London Ser. B. 253:1993;69-75
33. Fieber L.A., Adams D.J. Acetylcholine-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. J. Gen. Physiol. 434:1991;215-237
34. Franciolini F., Nonner W. Anion and cation permeability of a chloride channel in rat hippocampal neurons. J. Gen. Physiol. 90:1987;453-478
35. Franciolini F., Nonner W. Anion-cation interactions in the pore of neuronal background chloride channels. J. Gen. Physiol. 104:1994;711-723
36. Franciolini F., Nonner W. A multi-ion permeation mechanism in neuronal background chloride channels. J. Gen. Physiol. 104:1994;725-746
37. Franciolini F., Petris A. Chloride channels of biological membranes. Biochim. Biophys. Acta. 1031:1990;247-259
38. Gage P.W. Signal transduction in ligand-gated receptors. Immunol. Cell Biol. 76:1998;436-440
39. Galzi J-L., Devillers-Thiéry A., Hussey N., Bertrand S., Changeux J-P., Bertrand D. Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature. 359:1992;500-505
40. Gillespie D., Eisenberg R.S. Physical descriptions of experimental selectivity measurements in ion channels. Eur. Biophys. J. 31:2002;454-466
41. Goldman D.E. Potential, impedence and rectification in membranes. J. Gen. Physiol. 27:1943;37-60
42. Grenningloh G., Rienitz A., Schmitt B., Methfessel C., Zensen M., Beyreuther K., Gundelfinger E.D., Betz H. The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature. 328:1987;215-220
43. Grenningloh G., Pribilla I., Multhaup M., Beyreuther K., Taleb O., Betz H. Cloning and expression of the 58. kd β subunit of the inhibitory glycine receptor Neuron. 4:1990;963-970
44. Guinamard R., Akabas M.H. Arg352 is a major determinant of charge selectivity in the cystic fibrosis transmembrane conductance regulator chloride channel. Biochem. 38:1999;5528-5537
45. 3A receptor from cationic to anionic reveals a conserved feature of the ligand-gated ion channel superfamily. J. Biol. Chem. 276:2001;10977-10983
46. A receptors in dopaminergic neurons of the rat substantia nigra pars compacta. J. Physiol. 516:1999;719-737
47. Henderson D. Recent progress in the theory of the electric double layer. Prog. Surf. Sci. 13:1983;197-224
48. Henderson D. Fundamentals of Inhomogeneous Fluids. 1992;Marcel Dekker, New York, USA
49. Hodgkin A.L., Katz B. The effects of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. 108:1949;37-77
50. Imoto K., Busch C., Sakmann B., Mishina M., Konno T., Nakai J., Bujo H., Mori Y., Fukuda K., Numa S. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature. 335:1988;645-648
51. Imoto K., Konno T., Nakai J., Wang F., Mishina M., Numa S. A ring of uncharged polar amino acids as a component of channel constriction in the nicotinic acetylcholine receptor. FEBS Lett. 289:1991;193-200
52. A receptor. J. Biol. Chem. 277:2002;41438-41447
53. Karlin A., Akabas M.H. Towards a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron. 15:1995;1231-1244
54. 3 receptors. Nature. 424:2003;321-324
55. Keramidas A., Moorhouse A.J., French C.R., Schofield P.R., Barry P.H. M2 pore mutations convert the glycine receptor channel from being anion- to cation-selective. Biophys. J. 78:2000;247-259
56. Keramidas A., Moorhouse A.J., Pierce K.D., Schofield P.R., Barry P.H. Cation-selective mutations of the inhibitory glycine receptor channel reveal determinants of ion-charge selectivity. J. Gen. Physiol. 119:2002;393-410
57. Kienker P., Tomaselli G., Jurman M., Yellen G. Conductance mutations of the nicotinic acetylcholine receptor do not act by a simple electrostatic mechanism. Biophys. J. 66:1994;325-334
58. Kneussel M., Betz H. Receptors, gephyrin and gephyrin-associated proteins. novel insights into the assembly of inhibitory postsynaptic membrane specializations J. Physiol. 525:2000;1-9
59. Konno T., Busch C., Von Kitzing E., Imoto K., Wang F., Nakai J., Mishina M., Numa S., Sakmann B. Rings of anionic amino acids as structural determinants of ion selectivity in the acetylcholine receptor channel. Proc. R. Soc. London Ser. B. 244:1991;69-79
60. Kosolapov A.V., Filatov G.N., White M.M. Acetylcholine receptor gating is influenced by the polarity of amino acids at position 9′ in the M2 domain. J. Membr. Biol. 174:2000;191-197
61. Kuyucak S., Hoyles M., Chung S-H. Analytical solutions of Poisson's equations for realistic geometrical shapes of membrane ion channels. Biophys. J. 74:1998;22-36
62. Langosch D., Herbold A., Schmieden V., Bormann J., Kirsch J. Importance of Arg-219 for correct biogenesis of α1 homoligomeric glycine receptors. FEBS Lett. 336:1993;540-544
63. Langosch D., Laube B., Rundstrom N., Schmieden V., Bormann J., Betz H. Decreased agonist affinity and chloride conductance of mutant glycine receptors associated with human hereditary hyperekplexia. EMBO J. 13:1994;4223-4228
64. Lee, D.J-S, Keramidas, A., Moorhouse, A.J., Schofield, P.R., Barry, P.H., 2003. The contribution of proline 250 (P-2′) to pore diameter and ion selectivity in the human glycine receptor channel. Neurosci. Lett., in press.
65. Le Novére N., Changeux J-P. Molecular evolution of the nicotinic acetylcholine receptor. an example of multigene family in excitable cells J. Mol. Evol. 40:1995;155-172
66. Lester H.A. The permeation pathway of neurotransmitter-gated ion channels. Annu. Rev. Biophys. Biomol. Struct. 21:1992;267-292
67. Li S.C., Hoyles M., Kuyucak S., Chung S-H. Brownian dynamics study of ion transport in the vestibule of membrane channels. Biophys. J. 74:1998;37-47
68. Lynch J.W., Han R.N-L., Haddrill J., Pierce K.D., Schofield P.R. The surface accessibility of the glycine receptor M2-M3 loop is increased in the channel open state. J. Neurosci. 21:2001;2589-2599
69. 3 receptor, a serotonin-gated ion channel. Science. 254:1991;432-437
70. Mascia M.P., Trudell J.R., Harris R.A. Specific binding sites for alcohols and anesthetics on ligand-gated ion channels. Proc. Nat. Acad. Sci. USA. 97:2000;9305-9310
71. Miller C. Ion hopping defended. J. Gen. Physiol. 113:1999;783-787
72. Miller C. Ion channels. doing hard chemistry with hard ions Curr. Opin. Chem. Biol. 4:2000;148-151
73. Miyazawa A., Fujiyoshi Y., Stowell M., Unwin N. Nicotinic acetylcholine receptor at 4.6. Å resolution transverse tunnels in the channel wall J. Mol. Biol. 288:1999;765-786
74. Miyazawa A., Fujiyoshi Y., Unwin N. Structure and gating mechanism of the acetylcholine receptor pore. Nature. 424:2003;949-955
75. Moorhouse A.J., Keramidas A., Zaykin A., Schofield P.R., Barry P.H. Single channel analysis of conductance and rectification in cation-selective, mutant glycine receptor channels. J. Gen. Physiol. 119:2002;411-425
76. Noda M., Takahashi H., Tanabe T., Toyosato M., Furutani Y., Hirose T., Asai M., Inayama S., Miyata T., Numa S. Primary structure of α-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature. 299:1982;793-797
77. Nonner W., Chen D.P., Eisenberg B. Anomalous mole fraction, electrostatics, and binding in ionic channels. Biophys. J. 74:1998;2327-2334
78. Nonner W., Chen D.P., Eisenberg B. Progress and prospects in permeation. J. Gen. Physiol. 113:1999;773-782
79. Nonner W., Eisenberg B. Ion permeation and glutamate residues linked by Poisson-Nernst-Planck theory in L-type calcium channels. Biophys. J. 75:1998;1287-1305
80. - channels can pass cations. Biophys. J. 57:1990;124a
81. O'Mara M., Barry P.H., Chung S.H. A model of the glycine receptor deduced from Brownian dynamics studies. Proc. Nat. Acad. Sci. USA. 100(7):2003;4310- 4315
82. Ortells M.O., Lunt G.G. Evolutionary history of the ligand-gated ion-channel superfamily of receptors. TINS. 18:1995;121-127
83. Palma E., Maggi L., Eusebi F., Miledi R. Neuronal nicotinic threonine-for-leucine 247 α7 mutant receptors show different gating kinetics when activated by acetylcholine or by the noncompetitive agonist 5-hydroxytryptamine. Proc. Nat. Acad. Sci. USA. 94:1997;9915-9919
84. Panicker S., Cruz H., Arrabit C., Slesinger P.A. Evidence of a centrally located gate in the pore of a serotonin-gated ion channel. J. Neurosci. 22(5):2002;1629-1639
85. Parsegian A. Energy of an ion crossing a low dielectric membrane. solutions to four relevant electrostatic problems Nature. 221:1969;844-846
86. Pascual J.M., Karlin A. State-dependent accessibility and electrostatic potential in the channel of the acetylcholine receptor. J. Gen. Physiol. 111:1998;171-739
87. Qu Z., Apel E.D., Doherty C.A., Hoffman C.A., Huganir R.L. The synapse-associated protein rapsyn regulates tyrosine phosphorylation of proteins colocalized at nicotinic acetylcholine receptor clusters. Mol. Cell. Neurosci. 8:1996;171-184
88. Rajendra, S., 1995. Molecular determinants of ligand binding and channel activation in the human glycine receptor. Ph.D. Thesis. The University of New South Wales, Sydney, Australia.
89. Rajendra S., Lynch J.W., Pierce K.D., French C.R., Barry P.H., Schofield P.R. Mutations of an arginine residue in the human glycine receptor transforms β-alanine and taurine from agonists to competitive antagonists. Neuron. 14:1995;169-175
90. 3 receptor pore revealed by substituted cysteine accessibility mutagenesis. J. Biol. Chem. 276:2001;42035-42042
91. Revah F., Bertrand D., Galzi J.L., Devillers-Thiéry A., Mulle C., Hussy N., Bertrand S., Balliret M., Changeux J-P. Mutations in the channel domain after desensitization of a neuronal nicotinic receptor. Nature. 353:1991;846-849
92. Rundström N., Schmieden V., Betz H., Bormann J., Langosch D. Cyanotriphenylborate. subtype-specific blocker of glycine receptor chloride channels Proc. Nat. Acad. Sci. USA. 91:1994;8950-8954
93. Sansom M.S.P., Adcock C., Smith G.R. Modelling and simulation of ion channels. applications to the nicotinic acetylcholine receptor J. Struct. Biol. 121:1998;246-262
94. Sansom M.S.P., Shrivastava I.H., Ranatunga K.M., Smith G.R. Simulations of ion channels - watching ions and water move. TIBS. 25:2000;368-374
95. Saul B., Kuner T., Sobetzko D., Brune W., Hanefeld F., Meinck H.M., Becker C.M. Novel GLRA1 missense mutation (P250T) in dominant hyperekplexia defines an intracellular determinant of glycine receptor channel gating. J. Neurosci. 19:1999;869-877
96. Schlesinger P.H., Ferdani R., Liu J., Pajewska J., Pajewski R., Saito M., Shabany H., Gokel G.W. SCMTR. a chloride-selective, membrane-anchored peptide channel that exhibits voltage gating J. Am. Chem. Soc. 124:2002;1848-1849
97. A receptor shows a ligand-gated receptor super-family. Nature. 328:1987;221-227
98. + ions in models of ion channels. a molecular dynamics study Biophys. J. 75:1998;2767-2782
99. - ions in ion channel models. Biophys. Chem. 79:1999;129-151
100. Unwin N. Nicotinic acetylcholine receptor at 9. Å resolution J. Mol. Biol. 299:1993;1101-1124
101. Unwin N. Acetylcholine receptor channel imaged in the open state. Nature. 373:1995;37-43
102. Unwin N. The Croonian Lecture 2000. Nicotinic acetylcholine receptor and the structural basis of fast synaptic transmission. Philos. Trans. R. Soc. London Ser. B. 355:2000;1813-1829
103. Vassilatis D.K., Elliston K.O., Paress P.S., Hamelin M., Arena J.P., Schaeffer J.M., Van der Ploeg L.H.T., Cully D.F. Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate-gated chloride channels. J. Mol. Evol. 44:1997;501-508
104. Villarroel A., Herlitze S., Koenen M., Sakmann B. Location of a threonine residue in the α-subunit M2 transmembrane segment that determines the ion flow through the acetylcholine receptor channel. Proc. R. Soc. London Ser. B. 243:1991;69-74
105. Villarroel A., Herlitze S., Witzemann V., Koenen M., Sakmann B. Asymmetry of the rat acetylcholine receptor subunits in the narrow region of the pore. Proc. R. Soc. London Ser. B. 249:1992;317-324
106. Wang F., Imoto K. Pore size and negative charge as structural determinants of permeability in the Torpedo nicotinic acetylcholine receptor channel. Proc. R. Soc. London Ser. B. 250:1992;11-17
107. Wang C-T., Zhang H-G., Rocheleau T.A., ffrench-Constant R.H., Jackson M.B. Cation permeability and cation-anion interactions in a mutant GABA-gated chloride channel from Drosophila. Biophys. J. 77:1999;691-700
108. Wilson G.G., Karlin A. The location of the gate in the acetylcholine receptor channel. Neuron. 20:1998;1269-1281
109. Wilson G.G., Karlin A. Acetylcholine receptor channel structure in the resting, open, and desensitized states probed with the substituted-cysteine- accessibility method. Proc. Nat. Acad. Sci. USA. 98:2001;1241-1248
110. Wilson G.G., Pascual J.M., Broomijmans N., Murray D., Karlin A. The intrinsic electrostatic potential and the intermediate ring of charge in the acetylcholine receptor channel. J. Gen. Physiol. 115:2000;93-106
111. C receptors. J. Physiol. 521:1999;327-336
112. Wotring V.E., Miller T.S., Weiss D.S. Mutations at the GABA receptor selectivity filter. a possible role for effective charges J. Physiol. 548(2):2003;527-540
113. Wu J. Microscopic model for selectivity permeation in ion channels. Biophys. J. 60:1991;238-251
114. A receptor α1 subunit. J. Gen. Physiol. 107:1996;195-205
115. A receptor channel-lining residues probed in cysteine mutants. Biophys. J. 69:1995;1858-1867
116. Yang J. Ion permeation through 5-Hydroxytryptamine-gated channels in neuroblastoma N18 Cells. J. Gen. Physiol. 96:1990;1177-1198