A structural model of agonist binding to the α3β4 neuronal nicotinic receptor

British Journal of Pharmacology

Volumn 140, Issue 5, 2003, Pages 921-931

  Costa, Valeria ^a,b   Nistri, Andrea ^a   Cavalli, Andrea ^c   Carloni, Paolo ^a,b  

^a SISSA   (Italy)

^b DEMOCRITOS NATIONAL SIMULATION CENTER   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Allosteric binding site; Cytisine; Docking; Eserine; Molecular modelling; Muscarine; Nicotine; Nicotinic acetylcholine receptor

Indexed keywords

ACETYLCHOLINE; ALPHA3 BETA4 NICOTINIC RECEPTOR; AMINO ACID; BINDING PROTEIN; CYTISINE; MUSCARINE; MUSCARINIC AGENT; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; PHYSOSTIGMINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BRAIN; DRUG BINDING; DRUG RECEPTOR BINDING; LIGAND BINDING; MOLECULAR MODEL; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; BINDING SITES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; NICOTINIC AGONISTS; PROTEIN BINDING; RECEPTORS, NICOTINIC;

EID: 0344441288     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705498     Document Type: Article

References (72)

1. ALBUQUERQUE, E.X., ALKONDON, M., PEREIRA, E.F., CASTRO, N.G., SCHRATTENHOLZ, A., BARBOSA, C.T., BONFANTE-CABARCAS, R., ARACAVA, Y., EISENBERG, H.M. & MAELICKE, A. (1997). Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J. Pharmacol. Exp. Ther., 280, 1117-1136.
2. ARIAS, H.R. (2000). Localization of agonist and competitive antagonist binding sites on nicotinic acetylcholine receptors. Neurochem. Int., 36, 595-645.
3. BAYLY, C., CIEPLACK, P., CORNELL, W. & KOLLMAN, P.A. (1993). A well-behaved electrostatic potential based method using charge restraints deriving atomic charges: the RESP model. J. Phys. Chem., 97, 10269-10280.
4. BARLOW, R.B., HOWARD, J.A.K. & JOHNSON, O. (1986). Structure of nicotine monomethyl iodide and nicotine monohydrogen iodide. Acta Crystallogr. C, 42, 852.
5. BARLOW, R.B. & JOHNSON, O. (1989). Relations between structure and nicotine-like activity: X-ray crystal structure analysis of (-)-cytisine and (-)-lobeline hydrochloride and a comparison with (-)-nicotine and other nicotine-like compounds. Br. J. Pharmacol., 98, 799-808.
6. BARNARD, E.A. (1996). The transmitter-gated channels: a range of receptor types and structures. Trends Pharmacol. Sci., 17, 305-309.
7. BEERS, W.H. & REICH, E. (1970). Structure and activity of acetylcholine. Nature, 228, 917-922.
8. BERENDSEN, H.J.C., POSTMA, J.P.M., VAN GUNSTEREN, W.F., DINOLA, A. & HAAK, J.R. (1984). Molecular dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
9. BEROUKHIM, R. & UNWIN, N. (1995). Three-dimensional location of the main immunogenic region of the acetylcholine receptor. Neuron, 15, 323-331.
10. 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.
11. CASE, D.A., PEARLMAN, D.A., CALDWELL, J.W., CHEATHAM III, T.E., ROSS, W.S., SIMMERLING, C.L., DARDEN, T.A., MERZ, K.M., STANTON, R.V., CHENG, A.L., VINCENT, J.J., CROWLEY, M.F., FERGUSON, D.M., RADMER, R.J., SINGH, U.C., WEINER, P.K. & KOLLMAN, P.A. (1997). AMBER 5. University of California, San Francisco.
12. CHANGEUX, J.P. & The TIPS Lecture (1990). The nicotinic acetylcholine receptor: an allosteric protein prototype of ligand-gated ion channels. Trends Pharmacol. Sci., 11, 485-492.
13. CHAVEZ-NORIEGA, L.E., CRONA, J.H., WASHBURN, M.S., URRUTIA, A., ELLIOTT, K.J. & JOHNSON, B.C. (1997). Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther., 280, 346-356.
14. 3H]nicotine photoincorporation in the gamma-subunit of the torpedo nicotinic acetylcholine receptor. FEBS Lett., 423, 223-226.
15. COHEN, B.N., FIGL, A., QUICK, M.W., LABARCA, C., DAVIDSON, N. & LESTER, H.A. (1995). Regions of beta 2 and beta 4 responsible for differences between the steady state dose-response relationships of the alpha 3 beta 2 and alpha 3 beta 4 neuronal nicotinic receptors. J. Gen. Physiol., 105, 745-764.
16. COHEN, J.B., SHARP, S.D. & LIU, W.S. (1991). Structure of the agonist-binding site of the nicotinic acetylcholine receptor. [3H]acetylcholine identifies residues in the cation-binding subsite. J. Biol. Chem., 266, 23354-23364.
17. CONNOLLY, M.L. (1983). Analytical molecular surface calculation. J. Appl. Crystallogr., 16, 548-558.
18. CORNELL, W.D., CIEPLAK, P., BAYLY, C.I., GOULD, I.R., MERZ JR, K.M., FERGUSON, D.M., SPELLMEYER, D.C., FOX, T., CALDWELL, J.W. & KOLLMAN, P.A. (1995). A second-generation force field for the simulation of proteins and nucleic acids. J. Chem. Phys., 117, 5179-5197.
19. CORRINGER, P.J., BERTRAND, S., GALZI, J.L., DEVILLERS-THIERY, A., CHANGEUX, J.P. & BERTRAND, D. (1999). Molecular basis of the charge selectivity of nicotinic acetylcholine receptor and related ligand-gated ion channels. Novartis Found. Symp., 225, 215-224.
20. CORRINGER, P.J., LE NOVERE, N. & CHANGEUX, J.P. (2000). Nicotinic receptors at the amino acid level. Annu. Rev. Pharmacol. Toxicol., 40, 431-458.
21. CZAJKOWSKI, C. & KARLIN, A. (1995). Structure of the nicotinic receptor acetylcholine-binding site. Identification of acidic residues in the delta subunit within 0.9 Nm of the 5 alpha subunit-binding. J. Biol. Chem., 270, 3160-3164.
22. DATTA, N., MONDAL, P. & PAULING, P. (1980). Acta Crystallogr. B, 36, 906.
23. DAYHOFF, M.O. (1978). A model of evolutionary change. In: Proteins in Atlas of Protein Sequence and Structure. ed. Dayhoff, M.O. Vol. 5, Suppl. 3, pp. 345-358. Washington: Georgetown University Medical Center, National Biomedical Research Foundation.
24. DI ANGELANTONIO, S., COSTA, V., CARLONI, P. & NISTRI, A. (2002). A novel class of peptides with facilitating action on neuronal nicotinic receptors of rat chromaffin cells in vitro: functional and molecular dynamics studies. Mol. Pharmacol., 61, 43-54.
25. DI ANGELANTONIO, S., NISTRI, A., MORETTI, M., CLEMENTI, F. & GOTTI, C. (2000). Antagonism of nicotinic receptors of rat chromaffin cells by N,N, N-trimethyl-1-(4-trans-stilbenoxy)-2-propylammonium iodide: a patch clamp and ligand binding study. Br. J. Pharmacol., 129, 1771-1779.
26. ESSMAN, U., PERERA, L., BERKOWITZ, M.L., DARDEN, T., LEE, H. & PEDERSEN, L.G. (1995). A smooth particle mesh Ewald method. J. Chem. Phys., 103, 8577-8593.
27. EWING, T.J.A. & KUNTZ, I.D. (1997). Critical evaluation of search algorithms for automated molecular docking and database screening. J. Comput. Chem., 18, 1175-1189.
28. 3H]epibatidine binding to bovine adrenal medulla: evidence for alpha3beta4* nicotinic receptors. Neurosci. Lett., 318, 98-102.
29. FRYDENVANG, K. (1990). J. Acta Crystallogr. C, 49, 985.
30. FRYDENVANG, K., GRONBORG, L. & JENSEN, B. (1988). Structures of acetylcholine picrate and methoxycarbonylcholine picrate hemi-hydrate. Acta Crystallogr. C, 44, 841-845.
31. GALZI, J.L., REVAH, F., BLACK, D., GOELDNER, M., HIRTH, C. & CHANGEUX, J.P. (1990). Identification of a novel amino acid alpha-tyrosine 93 within the cholinergic ligands-binding sites of the acetylcholine receptor by photoaffinity labeling. Additional evidence for a three-loop model of the cholinergic ligands-binding sites. J. Biol. Chem., 265, 10430-10437.
32. GALZI, J.L., BERTRAND, D., DEVILLERS-THIERY, A., REVAH, F., BERTRAND, S. & CHANGEUX, J.P. (1991). 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, 198-202.
33. GILSON, M.K. & HONIG, B. (1988). Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis. Proteins, 4, 7-18.
34. GREEN, W.N. & WANAMAKER, C.P. (1998). Formation of the nicotinic acetylcholine receptor binding sites. J. Neurosci., 18, 5555-5564.
35. GROOT-KORMELINK, P.J., BOORMAN, J.P. & SIVILOTTI, L.G. (2001). Formation of functional alpha3beta4alpha5 human neuronal nicotinic receptors in Xenopus oocytes: a reporter mutation approach. Br. J. Pharmacol., 134, 789-796.
36. GRUTTER, T., EHRET-SABATIER, L., KOTZYBA-HIBERT, F. & GOELDNER, M. (2000). Photoaffinity labeling of torpedo nicotinic receptor with the agonist [3H]DCTA: identification of amino acid residues which contribute to the binding of the ester moiety of acetylcholine. Biochemistry, 39, 3034-3043.
37. HAGHIGHI, A.P. & COOPER, E. (2000). A molecular link between inward rectification and calcium permeability of neuronal nicotinic acetylcholine α3β4 and α4β2 receptors. J. Neurosci., 20, 529-541.
38. HERDKLOTZ, J.K. & SASS, R.L. (1970). The crystal structure of acetylcholine chloride: a new conformation for acetylcholine. Biochem. Biophys. Res. Commun., 40, 583-588.
39. HONIG, B. & NICHOLLS, A. (1995). Classical electrostatics in biology and chemistry. Science, 268, 1144-1149.
40. HUCHO, F., TSETLIN, V.I. & MACHOLD, J. (1996). The emerging three-dimensional structure of a receptor. The nicotinic acetylcholine receptor. Eur. J. Biochem., 239, 539-557.
41. ITIER, V. & BERTRAND, D. (2001). Neuronal nicotinic receptors: from protein structure to function. FEBS Lett., 504, 118-125.
42. A receptor agonists from antagonists. Biophys. J., 81, 2660-2670.
43. JORGENSEN, W.L., CHANDRASEKHAR, J. & MADURA, J.D. (1983). Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
44. KARLIN, A. (1969). Chemical modification of the active site of the acetylcholine receptor. J. Gen. Physiol., 54, 245S-264S.
45. KARLIN, A. (2002). Emerging structure of the nicotinic acetylcholine receptors. Nat. Rev. Neurosci., 3, 102-114.
46. KEARNEY, P.C., NOWAK, M.W., ZHONG, W., SILVERMAN, S.K., LESTER, H.A. & DOUGHERTY, D.A. (1996). Dose-response relations for unnatural amino acids at the agonist binding site of the nicotinic acetylcholine receptor: tests with novel side chains and with several agonists. Mol. Pharmacol., 50, 1401-1412.
47. LE NOVERE, N., CORRINGER, P.J. & CHANGEUX, J.P. (1999). Improved secondary structure predictions for a nicotinic receptor subunit: incorporation of solvent accessibility and experimental data into a two-dimensional representation. Biophys. J., 76, 2329-2345.
48. LE NOVERE, N., GRUTTER, T. & CHANGEUX, J.P. (2002). Models of the extracellular domain of the nicotinic receptors and of Ago. Proc. Natl. Acad. Sci. U.S.A., 99, 3210-3215.
49. LINDSTROM, J. (1997). Nicotinic acetylcholine receptors in health and disease. Mol. Neurobiol., 15, 193-222.
50. LUETJE, C.W. & PATRICK, J. (1991). Both alpha-and beta-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J. Neurosci., 11, 837-845.
51. LUO, S., KULAK, J.M., CARTIER, G.E., JACOBSEN, R.B., YOSHIKAMI, D., OLIVERA, B.M. & MCINTOSH, J.M. (1998). α-Conotoxin AuIB selectively blocks α3β4 nicotinic acetylcholine receptors and nicotine-evoked norepinephrine release. J. Neurosci., 18, 8571-8579.
52. MARTIN, M., CZAJKOWSKI, C. & KARLIN, A. (1996). The contributions of aspartyl residues in the acetylcholine receptor gamma and delta subunits to the binding of agonists and competitive antagonists. J. Biol. Chem., 271, 13497-13503.
53. OSAKA, H., SUGIYAMA, N. & TAYLOR, P. (1998). Distinctions in agonist and antagonist specificity conferred by anionic residues of the nicotinic acetylcholine receptor. J. Biol. Chem., 273, 12758-12765.
54. PARKER, M.J., BECK, A. & LUETJE, C.W. (1998). Neuronal nicotinic receptor beta2 and beta4 subunits confer large differences in agonist binding affinity. Mol. Pharmacol., 54, 1132-1139.
55. PARKER, M.J., HARVEY, S.C. & LUETJE, C.W. (2001). Determinants of agonist binding affinity on neuronal nicotinic receptor beta subunits. J. Pharmacol. Exp. Ther., 299, 385-391.
56. PATERSON, D. & NORDBERG, A. (2000). Neuronal nicotinic receptors in the human brain. Prog. Neurobiol., 61, 75-111.
57. PAULING, P. & PETCHER, T.J. (1973). Neuromuscular blocking agents: structure and activity. Chem. Biol. Interact., 6, 351-365.
58. PEREIRA, E.F., REINHARDT-MAELICKE, S., SCHRATTENHOLZ, A., MAELICKE, A. & ALBUQUERQUE, E.X. (1993). Identification and functional characterization of a new agonist site on nicotinic acetylcholine receptors of cultured hippocampal neurons. J. Pharmacol. Exp. Ther., 265, 1474-1491.
59. SALI, A. & BLUNDELL, T.L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol., 234, 779-815.
60. SANCHEZ, R. & SALI, A. (1997). Evaluation of comparative protein structure modeling by MODELLER-3. Proteins (Suppl. 1), 50-58.
61. SCHAPIRA, M., ABAGYAN, R. & TOTROV, M. (2002). Structural model of nicotinic acetylcholine receptor isotypes bound to acetylcholine and nicotine. BMC Struct. Biol., 2, 1.
62. SCHRATTENHOLZ, A., GODOVAC-ZIMMERMANN, J., SCHAFER, H.J., ALBUQUERQUE, E.X. & MAELICKE, A. (1993). Photoaffinity labeling of torpedo acetylcholine receptor by physostigmine. Eur. J. Biochem., 216, 671-677.
63. SINE, S.M., QUIRAM, P., PAPANIKOLAOU, F., KREIENKAMP, H.J. & TAYLOR, P. (1994). Conserved tyrosines in the alpha subunit of the nicotinic acetylcholine receptor stabilize quaternary ammonium groups of agonists and curariform antagonists. J. Biol. Chem., 269, 8808-8816.
64. SMIT, A.B., SYED, N.I., SCHAAP, D., VAN MINNEN, J., KLUMPERMAN, J., KITS, K.S., LODDER, H., VAN DER SCHORS, R.C., VAN ELK, R., SORGEDRAGER, B., BREJC, K., SIXMA, T.K. & GERAERTS, W.P. (2001). A glia-derived acetylcholine- binding protein that modulates synaptic transmission. Nature, 411, 261-268.
65. STAUFFER, D.A. & KARLIN, A. (1994). Electrostatic potential of the acetylcholine binding sites in the nicotinic receptor probed by reactions of binding-site cysteines with charged methanethiosulfonates. Biochemistry, 33, 6840-6849.
66. SUDWEEKS, S.N. & YAKEL, J.L. (2000). Functional and molecular characterization of neuronal nicotinic ACh receptors in Rat CA1 hippocampal neurons. J. Physiol., 527, 515-528.
67. SUGIYAMA, N., BOYD, A.E. & TAYLOR, P. (1996). Anionic residue in the alpha-subunit of the nicotinic acetylcholine receptor contributing to subunit assembly and ligand binding. J. Biol. Chem., 271, 26575-26581.
68. SVINNING, T. & SOURUM, H. (1975). Acta Crystallogr., 31, 1581.
69. THOMPSON, J.D., GIBSON, T.J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
70. UNWIN, N. (1993). Nicotinic acetylcholine receptor at 9 A resolution. J. Mol. Biol., 229, 1101-1124.
71. UNWIN, N. (1995). Acetylcholine receptor channel imaged in the open state. Nature, 373, 37-43.
72. ZHONG, W., GALLIVAN, J.P., ZHANG, Y., LI, L., LESTER, H.A. & DOUGHERTY, D.A. (1998). From ab initio quantum mechanics to molecular neurobiology: a cation-Pi binding site in the nicotinic receptor. Proc. Natl. Acad. Sci. U.S.A., 95, 12088-12093.