Binding-gating coupling in a nondesensitizing α7 nicotinic receptor. A single channel pharmacological study

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 2, 2009, Pages 410-416

  Bernal, José Antonio ^a   Mulet, José ^a   Castillo, Mar ^a   Criado, Manuel ^a   Sala, Salvador ^a   Sala, Francisco ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

Acetylcholine receptor; Channel gating; Cys loop receptor; Mutant; Single channel

Indexed keywords

1,1 DIMETHYL 4 PHENYLPIPERAZINIUM; ALANINE; BUNGAROTOXIN RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; KINETICS; MUTATION; NERVE CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL;

ACETYLCHOLINE; ANIMALS; CATTLE; DIMETHYLPHENYLPIPERAZINIUM IODIDE; ELECTROPHYSIOLOGICAL PHENOMENA; ION CHANNEL GATING; KINETICS; MUTATION; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; RECEPTORS, NICOTINIC;

EID: 59249099231     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.11.004     Document Type: Article

References (37)

1. Lester H.A., Dibas M.I., Dahan D.S., Leite J.F., and Dougherty D.A. Cys-loop receptors: new twists and turns. Trends Neurosci. 27 (2004) 329-336
2. Sine S.M., and Engel A.G. Recent advances in Cys-loop receptor structure and function. Nature 440 (2006) 448-455
3. Changeux J.P., and Edelstein S.J. Allosteric mechanisms of signal transduction. Science 308 (2005) 1424-1428
4. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4 A resolution. J. Mol. Biol. 346 (2005) 967-989
5. Dellisanti C.D., Yao Y., Stroud J.C., Wang Z.Z., and Chen L. Crystal structure of the extracellular domain of nAChR alpha1 bound to alpha-bungarotoxin at 1.94 A resolution. Nat. Neurosci. 10 (2007) 953-962
6. Brejc K., van Dijk W.J., Klaassen R.V., Schuurmans M., Oost van Der J., Smit A.B., and Sixma T.K. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411 (2001) 269-276
7. Hansen S.B., Sulzenbacher G., Huxford T., Marchot P., Taylor P., and Bourne Y. Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J. 24 (2005) 3635-3646
8. Wells G.B. Structural answers and persistent questions about how nicotinic receptors work. Front Biosci. 13 (2008) 5479-5510
9. Galzi J.L., Bertrand D., Devillers-Thiery A., Revah F., Bertrand S., and Changeux J.P. Functional significance of aromatic amino acids from three peptide loops of the alpha 7 neuronal nicotinic receptor site investigated by site-directed mutagenesis. FEBS Lett. 294 (1991) 198-202
10. Celie P.H., Rossum-Fikkert S.E., van Dijk W.J., Brejc K., Smit A.B., and Sixma T.K. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41 (2004) 907-914
11. Mukhtasimova N., Free C., and Sine S.M. Initial coupling of binding to gating mediated by conserved residues in the muscle nicotinic receptor. J. Gen. Physiol 126 (2005) 23-39
12. Criado M., Mulet J., Bernal J.A., Gerber S., Sala S., and Sala F. Mutations of a conserved lysine residue in the N-terminal domain of alpha7 nicotinic receptors affect gating and binding of nicotinic agonists. Mol. Pharmacol. 68 (2005) 1669-1677
13. Revah F., Bertrand D., Galzi J.L., Devillers-Thiery A., Mulle C., Hussy N., Bertrand S., Ballivet M., and Changeux J.P. Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature 353 (1991) 846-849
14. Bertrand D., Devillers-Thiery A., Revah F., Galzi J.L., Hussy N., Mulle C., Bertrand S., Ballivet M., and Changeux J.P. Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain. Proc. Natl. Acad. Sci. U. S. A 89 (1992) 1261-1265
15. Palma E., Mileo A.M., Eusebi F., and Miledi R. Threonine-for-leucine mutation within domain M2 of the neuronal alpha(7) nicotinic receptor converts 5-hydroxytryptamine from antagonist to agonist. Proc. Natl. Acad. Sci. U. S. A 93 (1996) 11231-11235
16. Palma E., Fucile S., Barabino B., Miledi R., and Eusebi F. Strychnine activates neuronal alpha7 nicotinic receptors after mutations in the leucine ring and transmitter binding site domains. Proc. Natl. Acad. Sci. U. S. A 96 (1999) 13421-13426
17. Palma E., Maggi L., Eusebi F., and Miledi R. Neuronal nicotinic threonine-for-leucine 247 alpha7 mutant receptors show different gating kinetics when activated by acetylcholine or by the noncompetitive agonist 5-hydroxytryptamine. Proc. Natl. Acad. Sci. U. S. A 94 (1997) 9915-9919
18. +, lines the extracellular vestibule. Am. J. Physiol. Cell Physiol. 283 (2002) C1454-C1460
19. Lyford L.K., Sproul A.D., Eddins D., McLaughlin J.T., and Rosenberg R.L. Agonist-induced conformational changes in the extracellular domain of alpha 7 nicotinic acetylcholine receptors. Mol. Pharmacol. 64 (2003) 650-658
20. Krieg P.A., and Melton D.A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12 (1984) 7057-7070
21. Sala F., Mulet J., Sala S., Gerber S., and Criado M. Charged amino acids of the N-terminal domain are involved in coupling binding and gating in {alpha}7 nicotinic receptors. J. Biol. Chem. 280 (2005) 6642-6647
22. Garcia-Guzman M., Sala F., Sala S., Campos-Caro A., and Criado M. Role of two acetylcholine receptor subunit domains in homomer formation and intersubunit recognition, as revealed by alpha 3 and alpha 7 subunit chimeras. Biochemistry 33 (1994) 15198-15203
23. Stühmer W. Electrophysiological recording from Xenopus oocytes. Methods Enzymol. 207 (1992) 319-339
24. Yang X.C., and Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243 (1989) 1068-1071
25. Qin F., Auerbach A., and Sachs F. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70 (1996) 264-280
26. + channel pore through mutant cycles with a peptide inhibitor. Science 268 (1995) 307-310
27. Criado M., Mulet J., Castillo M., Aldea M., Sala S., and Sala F. Interactions between loop 5 and beta-strand beta 6′ are involved in alpha7 nicotinic acetylcholine receptors channel gating. J. Neurochem. 104 (2008) 719-730
28. Colquhoun D. Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol 125 (1998) 924-947
29. Tonini R., Palma E., Miledi R., and Eusebi F. Properties of neuronal alpha7 mutant nicotinic acetylcholine receptors gated by bicuculline. Neuropharmacology 44 (2003) 765-771
30. Rovira J.C., Vicente-Agullo F., Campos-Caro A., Criado M., Sala F., Sala S., and Ballesta J.J. Gating of alpha3beta4 neuronal nicotinic receptor can be controlled by the loop M2-M3 of both alpha3 and beta4 subunits. Pflugers Arch. 439 (1999) 86-92
31. Aldea M., Mulet J., Sala S., Sala F., and Criado M. Non-charged amino acids from three different domains contribute to link agonist binding to channel gating in alpha7 nicotinic acetylcholine receptors. J. Neurochem. 103 (2007) 725-735
32. Luetje C.W., and Patrick J. Both alpha- and beta-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J. Neurosci. 11 (1991) 837-845
33. Figl A., Cohen B.N., Quick M.W., Davidson N., and Lester H.A. Regions of beta 4.beta 2 subunit chimeras that contribute to the agonist selectivity of neuronal nicotinic receptors. FEBS Lett. 308 (1992) 245-248
34. Papke R.L., and Heinemann S.F. Partial agonist properties of cytisine on neuronal nicotinic receptors containing the beta 2 subunit. Mol. Pharmacol. 45 (1994) 142-149
35. Anand R., Nelson M.E., Gerzanich V., Wells G.B., and Lindstrom J. Determinants of channel gating located in the N-terminal extracellular domain of nicotinic alpha7 receptor. J.Pharmacol.Exp.Ther. 287 (1998) 469-479
36. Hussy N., Ballivet M., and Bertrand D. Agonist and antagonist effects of nicotine on chick neuronal nicotinic receptors are defined by alpha and beta subunits. J. Neurophysiol. 72 (1994) 1317-1326
37. Horenstein N.A., McCormack T.J., Stokes C., Ren K., and Papke R.L. Reversal of agonist selectivity by mutations of conserved amino acids in the binding site of nicotinic acetylcholine receptors. J. Biol. Chem. 282 (2007) 5899-5909