Agonist-activated ion channels

British Journal of Pharmacology

Volumn 147, Issue SUPPL. 1, 2006, Pages

  Colquhoun, David ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Acetylcholine; Glycine receptor; History; Ion channel; Receptor; Single channel

Indexed keywords

ACETYLCHOLINE; ANTIBIOTIC AGENT; GRAMICIDIN; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NICOTINIC RECEPTOR;

AGONIST; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; MEDICAL RESEARCH; MOLECULAR MECHANICS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; ION CHANNEL GATING; ION CHANNELS; LIGANDS;

EID: 30444448205     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706502     Document Type: Review

References (109)

1. ANDERSON, C.R. & STEVENS, C.F. (1973). Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction. J. Physiol. (London), 235, 655-691.
2. ARIENS, E.J. (1954). Affinity and intrinsic activity in the theory of competitive inhibition. Part I. Problems and theory. Arch. Int. Pharmacodyn., 99, 33-49.
3. AUERBACH, A. (2005). Gating of acetylcholine receptor channels: brownian motion across a broad transition state. Proc. Natl. Acad. Sci. U.S.A., 102, 1408-1412.
4. BANKE, T.G. & TRAYNELIS, S.F. (2003). Activation of NR1/NR2B NMDA receptors. Nat. Neurosci., 6, 144-152.
5. BEATO, M., GROOT-KORMELINK, P.J., COLQUHOUN, D. & SIVILOTTI, L.G. (2004). The activation mechanism of α1 homomeric glycine receptors. J. Neurosci., 24, 895-906.
6. BLATZ, A.L. & MAGLEBY, K.L. (1989). Adjacent interval analysis distinguishes among gating mechanisms for the fast chloride channel from rat skeletal muscle. J. Physiol. (London). 410, 561-585.
7. BODENREIDER, C. & KIEFHABER, T. (2005). Interpretation of protein folding psi values. J. Mol. Biol., 351, 393-401.
8. BREJC, K., VAN DIJK, W.J., KLAASSEN, R.V., SCHUURMANS, M., VAN DER, O.J., SMIT, A.B. & SIXMA, T.K. (2001). Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature, 411, 269-276.
9. BREJC, K., VAN DIJK, W.J., SMIT, A.B. & SIXMA, T.K. (2002). The 2.7 A structure of AChBP, homologue of the ligand-binding domain of the nicotinic acetylcholine receptor. Novartis. Found. Symp., 245, 22-29.
10. BURZOMATO, V., BEATO, M., GROOT-KORMELINK, P.J., COLQUHOUN, D. & SIVILOTTI, L.G. (2004). Single-Channel Behavior of Heteromeric {alpha}1{beta} Glycine Receptors: An Attempt to Detect a Conformational Change before the Channel Opens. J. Neurosci., 24, 10924-10940.
11. CELIE, P.H., ROSSUM-FIKKERT, S.E., VAN DIJK, W.J., BREJC, K., SMIT, A.B. & SIXMA, T.K. (2004). Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron, 41, 907-914.
12. CHAKRAPANI, S. & AUERBACH, A. (2005). A speed limit for conformational change of an allosteric membrane protein. Proc. Natl. Acad. Sci. U.S.A., 102, 87-92.
13. CHAKRAPANI, S., BAILEY, T.D. & AUERBACH, A. (2003). The role of loop 5 in acetylcholine receptor channel gating. J. Gen. Physiol., 122, 521-539.
14. CHAKRAPANI, S., BAILEY, T.D. & AUERBACH, A. (2004). Gating dynamics of the acetylcholine receptor extracellular domain. J. Gen. Physiol., 123, 341-356.
15. CLARK, A.J. (1933). The Mode of Action of Drugs on Cells. London: Edward Arnold & Co., pp 1-298.
16. COLQUHOUN, D. (1973). The relation between classical and cooperative models for drug action. In: Drug Receptors. ed. RANG, H.P., pp. 149-182. London: Macmillan Press.
17. COLQUHOUN, D. (1987). Affinity, efficacy and receptor classification: is the classical theory still useful?. In: Perspectives on Hormone Receptor Classification. ed. Black, J.W., pp. 103-114. New York: Alan R. Liss Inc.
18. COLQUHOUN, D. (1998). Binding, gating, affinity and efficacy. The interpretation of structure- activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol., 125, 923-948.
19. COLQUHOUN, D. (2003a). Professor Sir Bernard Katz. Biophysicist who arrived in England with £4 and went on to win a Nobel Prize. (Obituary) The Independent, 26 April 2003.
20. COLQUHOUN, D. (2003b). Bernard Katz. pp. 34-38 Physiology News (The Physiological Society), Number 52, 34-38.
21. COLQUHOUN, D. (2005). From shut to open: what can we learn from linear free energy relationships? Biophys. J., 89, 3673-3675.
22. COLQUHOUN, D. (2006). The quantitative analysis of drug receptor interactions: a short history. Trends Pharmacol. Sci., (in press).
23. COLQUHOUN, D., CULL-CANDY, S.G. & MATHIE, A. (1989). The inward rectification of whole-cell current responses elicited by nicotinic agonists in dissociated rat sympathetic ganglion cells. J. Physiol. (London), 410, 28P.
24. COLQUHOUN, D., DIONNE, V.E., STEINBACH, J.H. & STEVENS, C.F. (1975). Conductance of channels opened by acetylcholine-like drugs in muscle end- plate. Nature, 253, 204-206.
25. COLQUHOUN, D. & HAWKES, A.G. (1977). Relaxation and fluctuations of membrane currents that flow through drug- operated channels. Proc. R. Soc. Lond. B, 199, 231-262.
26. COLQUHOUN, D. & HAWKES, A.G. (1982). On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Philos. Trans. R. Soc. Lond. B Biol. Sci., 300, 1-59.
27. COLQUHOUN, D. & HAWKES, A.G. (1987). A note on correlations in single ion channel records. Proc. R. Soc. Lond. B, 230, 15-52.
28. COLQUHOUN, D. & HAWKES, A.G. (1995a). A Q-matrix cookbook. In: Single Channel Recording. ed. SAKMANN, B. & NEHER, E., pp. 589-633. New York: Plenum Press.
29. COLQUHOUN, D. & HAWKES, A.G. (1995b). The principles of the stochastic interpretation of ion channel mechanisms. In: Single Channel Recording. ed. Sakmann, B. & Neher, E., pp. 397-482. New York: Plenum Press.
30. COLQUHOUN, D., HAWKES, A.G., MERLUSHKIN, A. & EDMONDS, B. (1997). Properties of single ion channel currents elicited by a pulse of agonist concentration or voltage. Philos. Trans. R. Soc. Lond. A, 355, 1743-1786.
31. COLQUHOUN, D., HAWKES, A.G. & SRODZINSKI, K. (1996). Joint distributions of apparent open times and shut times of single ion channels and the maximum likelihood fitting of mechanisms. Philos. Trans. R. Soc. Lond. A, 354, 2555-2590.
32. COLQUHOUN, D. & OGDEN, D.C. (1988). Activation of ion channels in the frog end-plate by high concentrations of acetylcholine. J. Physiol. (London), 395, 131-159.
33. COLQUHOUN, D. & SAKMANN, B. (1981). Fluctuations in the microsecond time range of the current through single acetylcholine receptor ion channels. Nature, 294, 464-466.
34. COLQUHOUN, D. & SAKMANN, B. (1985). Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. J. Physiol. (London), 369, 501-557.
35. COLQUHOUN, D. & SAKMANN, B. (1998). From muscle endplate to brain synapses: A short history of synapses and agonist-activated ion channels. Neuron, 20, 381-387.
36. COLQUHOUN, D., UNWIN, N., SHELLEY, C., HATTON, C. & SIVILOTTI, L.G. (2003). Nicotinic acetylcholine receptors. In: Drug Discovery and Drug Development. ed. Abrahams, D., pp. 357-405. New York: John Wiley.
37. CULL-CANDY, S.G. & USOWICZ, M.M. (1987). Multiple-conductance channels activated by excitatory amino acids in cerebellar neurons. Nature, 325, 525-528.
38. CYMES, G.D., GROSMAN, C. & AUERBACH, A. (2002). Structure of the transition state of gating in the acetylcholine receptor channel pore: a phi-value analysis. Biochemistry, 41, 5548-5555.
39. DEL CASTILLO, J. & KATZ, B. (1956). Biophysical aspects of neuromuscular transmission. Prog. Biophys. Biophys. Chem., 6, 121-170.
40. DEL CASTILLO, J. & KATZ, B. (1957). Interaction at end-plate receptors between different choline derivatives. Proc. R. Soc. Lond. B, 146, 369-381.
41. ENGEL, A.G., OHNO, K., SHEN, X.M. & SINE, S.M. (2003a). Congenital myasthenic syndromes: multiple molecular targets at the neuromuscular junction. Ann. NY Acad. Sci., 998, 138-160.
42. ENGEL, A.G., OHNO, K. & SINE, S.M. (2003b). Sleuthing molecular targets for neurological diseases at the neuromuscular junction. Nat. Rev. Neurosci., 4, 339-352.
43. ERREGER, K., DRAVID, S.M., BANKE, T.G., WYLLIE, D.J. & TRAYNELIS, S.F. (2005). Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J. Physiol., 563, 345-358.
44. FATT, P. & KATZ, B. (1951). An analysis of the end-plate potential recorded with an intra-cellular electrode. J. Physiol. (Lond.), 115, 320-370.
45. FATT, P. & KATZ, B. (1952). The electric activity of the motor endplate. pp. 183-186. Proc. Roy. Soc. Lond. B, 140, 183-186.
46. FERSHT, A.R. (1995). Characterizing transition states in protein folding: an essential step in the puzzle. Curr. Opin. Struct. Biol., 5, 79-84.
47. FERSHT, A.R. (2000). Transition-state structure as a unifying basis in protein-folding mechanisms: contact order, chain topology, stability, and the extended nucleus mechanism. Proc. Natl. Acad. Sci. U.S.A., 97, 1525-1529.
48. FERSHT, A.R. (2004). Relationship of Leffler (Bronsted) alpha values and protein folding Phi values to position of transition-state structures on reaction coordinates. Proc. Natl. Acad. Sci. U.S.A., 101, 14338-14342.
49. FERSHT, A.R. & SATO, S. (2004). Phi-value analysis and the nature of protein-folding transition states. Proc. Natl. Acad. Sci. U.S.A., 101, 7976-7981.
50. FREDKIN, D.R., MONTAL, M. & RICE, J.A. (1985). Identification of aggregated Markovian models: application to the nicotinic acetylcholine receptor. In: Proceedings of the Berkeley Conference in Honor of Jerzy Neyman and Jack Kiefer. ed. Le Cam, L.M., pp. 269-289. Monterey.: Wadsworth.
51. FURUKAWA, H. & GOUAUX, E. (2003). Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J., 22, 2873-2885.
52. GARDNER, P., OGDEN, D.C. & COLQUHOUN, D. (1984). Conductances of single ion channels opened by nicotinic agonists are indistinguishable. Nature, 309, 160-162.
53. GIBB, A.J. & COLQUHOUN, D. (1992). Activation of [N]-Methyl-D- Aspartate receptors by L-glutamate in cells dissociated from adult rat hippocampus. J. Physiol. (London), 456, 143-179.
54. GOUAUX, E. (2004). Structure and function of AMPA receptors. J Physiol. (London). 554, 249-253.
55. GROSMAN, C. & AUERBACH, A. (2000). Kinetic, mechanistic, and structural aspects of unliganded gating of acetylcholine receptor channels. A single-channel study of second transmembrane segment 12′ mutants. J. Gen. Physiol., 115, 621-635.
56. GROSMAN, C., SALAMONE, F.N., SINE, S.M. & AUERBACH, A. (2000a). The extracellular linker of musle acetylcholine receptor channels is a gating control element. J. Gen. Physiol., 116, 327-339.
57. GROSMAN, C., ZHOU, M. & AUERBACH, A. (2000b). Mapping the conformational wave of acetylcholine receptor channel gating. Nature, 403, 773-776.
58. HAMILL, O.P., MARTY, A., NEHER, E., SAKMANN, B. & SIGWORTH, F.J. (1981). Improved patch clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch., 391, 85-100.
59. HATTON, C.J., SHELLEY, C, BRYDSON, M., BEESON, D. & COLQUHOUN, D. (2003). Properties of the human muscle nicotinic receptor, and of the slow-channel myasthenic syndrome mutant epsilonL221F, inferred from maximum likelihood fits. J Physiol. (Lond.), 547, 729-760.
60. HAWKES, A.G., JALALI, A. & COLQUHOUN, D. (1990). The distributions of the apparent open times and shut times in a single channel record when brief events can not be detected. Philos. Trans. R. Soc. Lond. A, 332, 511-538.
61. HAWKES, A.G., JALALI, A. & COLQUHOUN, D. (1992). Asymptotic distributions of apparent open times and shut times in a single channel record allowing for the omission of brief events. Philos. Trans. R. Soc. Lond. B Biol. Sci., 337, 383-404.
62. HILL, A.V. (1909). The mode of action of nicotine and curari determined by the form of the contraction curve and the method of temperature coefficients. J. Physiol. (London), 39, 361-373.
63. HLADKY, S.B. & HAYDON, D.A. (1970). Discreteness of conductance change in bimolecular lipid membranes in the presence of certain antibiotics. Nature, 225, 451-453.
64. HORN, R. & LANGE, K. (1983). Estimating kinetic constants from single channel data. Biophys. J., 43, 207-223.
65. HOSIE, A.M., DUNNE, E.L., HARVEY, R.J. & SMART, T.G. (2003). Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat. Neurosci., 6, 362-369.
66. IFUNE, C.K. & STEINBACH, J.H. (1990). Rectification of acetylcholine-elicited currents in PC12 pheochromoctyoma cells. Proc. Natl. Acad. Sci. U.S.A., 87, 4794-4798.
67. IMOTO, K., BUSCH, C., SAKMANN, B., MISHINA, M., KONNO, T., NAKAI, I., BUJO, H., MORI, Y., FUKUDA, K. & NUMA, S. (1988). Rings of negatively charged amino acids as determinants of acetylcholine receptor channel conductance. Nature, 335, 645-648.
68. IMOTO, K., METHFESSEL, C., SAKMANN, B., MISHINA, M., MORI, Y., KONNO, T., FUKUDA, K., KURASAKI, M., BUJO, H., FUJITA, Y. & NUMA, S. (1986). Location of a delta-subunit region determining ion transport through the acetylcholine receptor channel. Nature, 324, 670-674.
69. JIN, R., BANKE, T.G., MAYER, M.L., TRAYNELIS, S.F. & GOUAUX, E. (2003). Structural basis for partial agonist action at ionotropic glutamate receptors. Nature Neurosci., 6, 803-810.
70. A channel responses to brief agonist pulses. Neuron, 15, 181-191.
71. KATZ, B. & MILEDI, R. (1970). Membrane noise produced by acetylcholine. Nature, 226, 962-963.
72. KATZ, B. & MILEDI, R. (1972). The statistical nature of the acetylcholine potential and its molecular components. J. Physiol. (London), 224, 665-699.
73. KIRSCHNER, L.B. & STONE, W.E. (1951). Action of inhibitors at the myoneural junction. J. Gen. Physiol., 34, 821-834.
74. LANGMUIR, I. (1918). The adsorption of gases on plane surfaces of Glass, mica and platinum. J. Amer. Chem. Soc., 40, 1361-1403.
75. LAUBE, B., MAKSAY, G., SCHEMM, R. & BETZ, H. (2002). Modulation of glycine receptor function: a novel approach for therapeutic intervention at inhibitory synapses? Trends Pharmacol. Sci., 23, 519-527.
76. LEWIS, T.M., SIVILOTTI, L.G., COLQUHOUN, D., GARDINER, R.M., SCHOEPFER, R. & REES, M. (1998). Properties of human glycine receptors containing the hyperekplexia mutation alpha1(K276E), expressed in Xenopus oocytes. J. Physiol., 507 (Part 1), 25-40.
77. LYNCH, J.W. (2004). Molecular structure and function of the glycine receptor chloride channel. Physiol. Rev., 84, 1051-1095.
78. MAGLEBY, K.L. & STEVENS, C.F. (1972a). A quantitative description of end-plate currents. J. Physiol., 223, 173-197.
79. MAGLEBY, K.L. & STEVENS, C.F. (1972b). The effect of voltage on the time course of end-plate currents. J. Physiol., 223, 151-171.
80. MAGLEBY, K.L. (2003). Gating mechanism of BK (Slo1) channels: so near, yet so far. J. Gen. Physiol., 121, 81-96.
81. MAYER, M.L., OLSON, R. & GOUAUX, E. (2001). Mechanisms for ligand binding to GluR0 ion channels: crystal structures of the glutamate and serine complexes and a closed apo state. J. Mol. Biol., 311, 815-836.
82. MISHINA, M., TAKAI, T., IMOTO, K., NODA, M., TAKAHASHI, T., NUMA, S., METHFESSEL, C. & SAKMANN, B. (1986). Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature, 321, 406-411.
83. MIYAZAWA, A., FUJIYOSHI, Y. & UNWIN, N. (2003). Structure and gating mechanism of the acetylcholine receptor pore. Nature, 424, 949-955.
84. NEHER, E. & SAKMANN, B. (1976). Single channel currents recorded from membrane of denervated frog muscle fibres. Nature, 260, 799-802.
85. NODA, M., TAKAHASHI, H., TANABE, T., TOYOSATO, M., FURUTANI, Y., HIROSE, T., ASAI, M., INAYAMA, S., MIYATA, T. & NUMA, S. (1982). Primary structure of alpha-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature, 299, 793-797.
86. NORTH, R.A. (2002). Molecular physiology of P2X receptors. Physiol. Rev., 82, 1013-1067.
87. OHNO, K., QUIRAM, P.A., MILONE, M., WANG, H.L., HARPER, M.C., PRUITT, J.N., BRENGMAN, J.M., PAO, L., FISCHBECK, K.H., CRAWFORD, T.O., SINE, S.M. & ENGEL, A.G. (1997). Congenital myasthenic syndromes due to heteroallelic nonsense/missense mutations in the acetylcholine receptor ε subunit gene: identification and functional characterization of six new mutations. Human Molecular Genetics, 6, 753-766.
88. POPESCU, G. & AUERBACH, A. (2003). Modal gating of NMDA receptors and the shape of their synaptic response. Nature Neurosci., 6, 476-483.
89. ROTHBERG, B.S. & MAGLEBY, K.L. (1999). Gating kinetics of single large-conductance Ca2+-activated K+ channels in high Ca2+ suggest a two-tiered allosteric gating mechanism. J. Gen. Physiol., 114, 93-124.
90. SALAMONE, F.N., ZHOU, M. & AUERBACH, A. (1999). A reexamination of adult mouse nicotinic acetylcholine receptor channel activation kinetics. J. Physiol. (London), 516, 315-330.
91. SANCHEZ, I.E. & KIEFHABER, T. (2003). Origin of unusual phi-values in protein folding: evidence against specific nucleation sites. J. Mol. Biol., 334, 1077-1085.
92. SCHOFIELD, P.R. (2002). The role of glycine and glycine receptors in myoclonus and startle syndromes. Adv. Neurol., 89, 263-274.
93. SCHORGE, S., ELENES, S. & COLQUHOUN, D. (2005). Maximum likelihood fitting of single channel NMDA activity with a mechanism composed of independent dimers of subunits. J. Physiol. (London), 569, 395-418.
94. SHEN, X.M., OHNO, K., TSUJINO, A., BRENGMAN, J.M., GINGOLD, M., SINE, S.M. & ENGEL, A.G. (2003). Mutation causing severe myasthenia reveals functional asymmetry of AChR signature cystine loops in agonist binding and gating. J. Clin. Invest., 111, 497-505.
95. SINE, S.M. & STEINBACH, J.H. (1986). Activation of acetylcholine receptors on clonal mammalian BC3H-1 cells by low concentrations of agonist. J. Physiol. (London), 373, 129-162.
96. SINE, S.M. & STEINBACH, J.H. (1987). Activation of acetylcholine receptors on clonal mammalian BC3H-1 cells by high concentrations of agonist. J. Physiol. (London), 385, 325-359.
97. SINE, S.M., SHEN, X.M., WANG, H.L., OHNO, K., LEE, W.Y., TSUJINO, A., BRENGMANN, J., BREN, N., VAJSAR, J. & ENGEL, A.G. (2002). Naturally Occurring Mutations at the Acetylcholine Receptor Binding Site Independently Alter ACh Binding and Channel Gating. J. Gen. Physiol., 120, 483-496.
98. SIVILOTTI, L.G. & COLQUHOUN, D. (1995). Acetylcholine receptors: too many channels, too few functions. Science, 269, 1681-1682.
99. STEPHENSON, R.P. (1956). A modification of receptor theory. Br. J. Pharmacol., 11, 379-393.
100. SUNDERMAN, E.R. & ZAGOTTA, W.N. (1999). Mechanism of allosteric modulation of rod cyclic nucleotide-gated channels. J. Gen. Physiol., 113, 601-620.
101. TWYMAN, R.E. & MACDONALD, R.L. (1991). Kinetic properties of the glycine receptor main- and sub-conductance states of mouse spinal cord neurones in culture. J. Physiol. (London), 435, 303-331.
102. UNWIN, N. (2005). Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346, 967-989.
103. UNWIN, N., TOYOSHIMA, C. & KUBALEK, E. (1988). Arrangement of the acetylcholine receptor subunits in the resting and desensitized states, determined by cryoelectron microscopy of crystallized Torpedo postsynaptic membranes. J. Cell Biol., 107, 1123-1138.
104. VINCENT, A., NEWLAND, C., CROXEN, R. & BEESON, D. (1997). Genes at the junction - candidates for congenital myasthenic syndromes. Trends Neurosci., 20, 15-22.
105. WANG, H.L., AUERBACH, A., BREN, N., OHNO, K., ENGEL, A.G. & SINE, S.M. (1997). Mutation in the M1 domain of the acetylcholine receptor α subunit decreases the rate of agonist dissociation. J. Gen. Physiol., 109, 757-766.
106. WYLLIE, D.J.A., BÉHÉ, P. & COLQUHOUN, D. (1998). Single-channel activations and concentration jumps: comparison of recombinant NR1/NR2A and NR1/NR2D NMDA receptors. J. Physiol. (Lond.), 510, 1-18.
107. WYMAN, J. & ALLEN, D.W. (1951). The problem of the heme Interactions in hemoglobin and the basis of the Bohr effect. J. Polym. Sci., VII, 499-518.
108. ZAGOTTA, W.N. & SIEGELBAUM, S.A. (1996). Structure and func tion of cyclic nucleotide-gated channels. Annu. Rev. Neurosci., 19, 235-263.
109. ZHOU, Y., PEARSON, J.E. & AUERBACH, A. (2005). φ-value analysis of a linear, sequential reaction mechanism: theory and application to ion channel gating. Biophys. J., 89, 3680-3685.