Defining nicotinic agonist binding surfaces through photoaffinity labeling

Biochemistry

Volumn 46, Issue 30, 2007, Pages 8798-8806

  Tomizawa, Motohiro ^a   Maltby, David ^b   Medzihradszky, Katalin F ^b   Zhang, Nanjing ^a   Durkin, Kathleen A ^c   Presley, Jack ^d   Talley, Todd T ^e   Taylor, Palmer ^e   Burlingame, Alma L ^b   Casida, John E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SURFACES; NICOTINIC ACETYLCHOLINE (ACH); THERAPEUTIC AGENTS;

DERIVATIVES; DRUG THERAPY; NEUROLOGY; PHOTOACOUSTIC EFFECT; PROTEINS;

BINDING SITES;

AZIDOEPIBATIDINE; BINDING PROTEIN; CHOLINERGIC RECEPTOR; EPIBATIDINE; NICOTINIC AGENT; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; DERIVATIZATION; DRUG RECEPTOR BINDING; DRUG SYNTHESIS; ISOTOPE LABELING; MOLLUSC; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; RECEPTOR AFFINITY;

ACETYLCHOLINE; AMINO ACID SEQUENCE; ANIMALS; APLYSIA; BINDING SITES; BRIDGED COMPOUNDS; CROSS-LINKING REAGENTS; IMINES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; NICOTINIC AGONISTS; PEPTIDE FRAGMENTS; PHOTOAFFINITY LABELS; PROTEIN BINDING; PYRIDINES; RECEPTORS, NICOTINIC; TRITIUM; TRYPSIN;

EID: 34547620694     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700667v     Document Type: Article

References (55)

1. Changeux, J.-P., and Edelstein, S. J. (2005) Nicotinic Acetylcholine Receptors: From Molecular Biology to Cognition, 284 pp, Odile Jacob, New York.
2. Cassels, B. K., Bermúdez, I., Dajas, F., Abin-Carriquiry, J. A., and Wonnacott, S. (2005) From ligand design to therapeutic efficacy: The challenge for nicotinic receptor research, Drug Discov. Today 10, 1657-1665.
3. Whiting, P. J., and Lindstrom, J. M. (1988) Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies, J. Neurosci. 8, 3395-3404.
4. Anand, R., Conroy, W. G., Schoepfer, R., Whiting, P., and Lindstrom, J. (1991) Neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes have a pentameric quaternary structure, J. Biol. Chem. 266, 11192-11198.
5. Cooper, E., Couturier, S., and Ballivet, M. (1991) Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 350, 235-238.
6. Flores, C. M., Rogers, S. W., Pabreza, L. A., Wolfe, B. B., and Kellar, K. J. (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of α4 and β2 subunits and is up-regulated by chronic nicotine treatment, Mol. Pharmacol. 41, 31-37.
7. Bunnelle, W. H., Dart, M. J., and Schrimpf, M. R. (2004) Design of ligands for the nicotinic acetylcholine receptors: The quest for selectivity, Curr. Top. Med. Chem. 4, 299-334.
8. Tomizawa, M., and Casida, J. E. (2005) Neonicotinoid insecticide toxicology: Mechanism of selective action, Annu. Rev. Pharmacol. Toxicol. 45, 247-268.
9. Arias, H. R. (2000) Localization of agonist and competitive antagonist binding sites on nicotinic acetylcholine receptors, Neurochem. Int. 36, 595-645.
10. Karlin, A. (2002) Emerging structure of the nicotinic acetylcholine receptors, Nat. Rev. Neurosci. 3, 102-114.
11. 3H]DCTA: Identification of amino acid residues which contribute to the binding of the ester moiety of acetylcholine, Biochemistry 39, 3034-3043.
12. Nirthanan, S., Ziebell, M. R., Chiara, D. C., Hong, F., and Cohen, J. B. (2005) Photolabeling the Torpedo nicotinic acetylcholine receptor with 4-azido-2,3,5,6-tetrafluorobenzoylcholine, a partial agonist, Biochemistry 44, 13447-13456.
13. Dougherty, D. A. (1996) Cation-π interactions in chemistry and biology: A new view of benzene, Phe, Tyr, and Trp, Science 271, 163-168.
14. Zhong, W., Gallivan, J. P., Zhang, Y., Li, L., Lester, H. A., and Dougherty, D. A. (1998) From ab initio quantum mechanics to molecular biology: A cation-π binding site in the nicotinic receptor, Proc. Natl. Acad. Sci. U.S.A. 95, 12088-12093.
15. Dougherty, D. A., and Lester, H. A. (2001) Snail, synapses and smokers, Nature 411, 252-255.
16. Cashin, A. L., Petersson, E. J., Lester, H. A., and Dougherty, D. A. (2005) Using physical chemistry to differentiate nicotinic from cholinergic agonists at the nicotinic acetylcholine receptor, J. Am. Chem. Soc. 127, 350-356.
17. Spande, T. F., Garraffo, H. M., Edwards, M. W., Yeh, H. J. C., Pannell, L., and Daly, J. W. (1992) Epibatidine: A novel (chloropyridyl)azabicycloheptane with potent analgesic activity from an Ecuadoran poison frog, J. Am. Chem. Soc. 114, 3475-3478.
18. Badio, B., and Daly, J. W. (1994) Epibatidine, a potent analgetic and nicotinic agonist, Mol. Pharmacol. 45, 563-569.
19. Brejc, K., van Dijk, W. J., Klaassen, R. V., Schuurmans, M., van der Oost, J., Smit, A. B., and Sixma, T. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptor, Nature 411, 269-276.
20. Celie, P. H. N., van Rossum-Fikkert, S. E., van Dijk, W. J., Brejc, K., Smit, A. B., and Sixma, T. K. (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures, Neuron 41, 907-914.
21. Hansen, S. B., Talley, T. T., Radić, Z., and Taylor, P. (2004) Structural and ligand recognition characteristics of an acetylcholine-binding protein from Aplysia californica, J. Biol. Chem. 279, 24197-24202.
22. Hansen, S. B., Sulzenbacher, G., Huxford, T., Marchot, P., Taylor, P., and Bourne, Y. (2005) Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations, EMBO J. 24, 3635-3646.
23. Zhang, N., Tomizawa, M., and Casida, J. E. (2003) 5-Azidoepibatidine: An exceptionally potent photoaffinity ligand for neuronal α4β2 and α7 nicotinic acetylcholine receptors, Bioorg. Med. Chem. Lett. 13, 525-527.
24. Carroll, F. I., Liang, F., Navarro, H. A., Brieaddy, L. E., Abraham, P., Damaj, M. I., and Martin, B. R. (2001) Synthesis, nicotinic acetylcholine receptor binding, and antinociceptive properties of 2-exo-2-(2′- substituted 5′-pyridinyl)-7-azabicyclo[2.2.1]heptanes. Epibatidine analogues, J. Med. Chem. 44, 2229-2237.
25. Whiting, P., Schoepfer, R., Lindstrom, J., and Priestley, T. (1991) Structural and pharmacological characterization of the major brain nicotinic acetylcholine receptor subtype stably expressed in mouse fibroblasts, Mol. Pharmacol. 40, 463-472.
26. Talley, T. T., Yalda, S., Ho, K.-Y., Tor, Y., Soti, F. S., Kem, W. R., and Taylor, P. (2006) Spectroscopic analysis of benzylidene anabaseine complexes with acetylcholine binding proteins as models for ligand-nicotinic receptor interactions, Biochemistry 45, 8894-8902.
27. 50) of an enzymatic reaction, Biochem. Pharmacol. 22, 3099-3108.
28. Nef, P., Oneyser, C., Alliod, C., Couturier, S., and Ballivet, M. (1988) Genes expressed in the brain define 3 distinct neuronal nicotinic acetylcholine-receptors, EMBO J. 7, 595-601.
29. Schoepfer, R., Whiting, P., Esch, F., Blacher, R., Shimasaki, S., and Lindstrom, J. (1988) cDNA clones coding for the structural subunit of a chicken brain nicotinic acetylcholine receptor, Neuron 1, 241-248.
30. Bairoch, A., Apweiler, R., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M., Martin, M. J., Natale, D. A., O'Donovan, C., Redaschi, N., and Yeh, L.-S. L. (2005) The universal protein resource (UniProt), Nucleic Acids Res. 33, D154-D159.
31. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22, 4673-4680.
32. Lassmann, T., and Sonnhammer, E. L. L. (2005) Kalign - an accurate and fast multiple sequence alignment algorithm, BMC Bioinformatics 6, 298.
33. Lassmann, T., and Sonnhammer, E. L. L. (2006) Kalign, Kalignvu and Mumsa: Web servers for multiple sequence alignment, Nucleic Acids Res. 34, W596-W599.
34. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: An automated protein homology-modeling server, Nucleic Acids Res. 31, 3381-3385.
35. Mohamadi, F., Richard, N. G. J., Guida, W. C., Liskamp, R., Lipton, M., Caufield, C., Chang, G., Hendrickson, T., and Still, W. C. (1990) Macromodels - an integrated software system for modeling organic and bioorganic molecules using molecular mechanics, J. Comput. Chem. 11, 440-467.
36. Jorgensen, W. L., Maxwell, D. S., and Tirado-Rives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids, J. Am. Chem. Soc. 118, 11225-11236.
37. Morris, G. M., Goodsell, D. S., Huey, R., and Olson, A. J. (1996) Distributed automated docking of flexible ligands to proteins: Parallel applications of AutoDock 2.4, J. Comput.-Aided Mol. Des. 10, 293-304.
38. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function, J. Comput. Chem. 19, 1639-1662.
39. Biemann, K. (1990) Nomenclature for peptide fragment ions (positive ions), Methods Enzymol. 193, 886-887.
40. Kagabu, S., Maienfisch, P., Zhang, A., Granda-Minones, J., Haettenschwiler, J., Kayser, H., Maetzke, T., and Casida, J. E. (2000) 5-Azidoimidacloprid and an acyclic analogue as candidate photoaffinity probes for mammalian and insect nicotinic acetyl-choline receptors, J. Med. Chem. 43, 5003-5009.
41. Zhang, N., Tomizawa, M., and Casida, J. E. (2002) Structural features of azidopyridinyl neonicotinoid probes conferring high affinity and selectivity for mammalian α4β2 and Drosophila nicotinic receptors, J. Med. Chem. 45, 2832-2840.
42. Bouzat, C., Gumilar, F., Spitzmaul, G., Wang, H.-L., Rayes, D., Hansen, S. B., Taylor, P., and Sine, S. M. (2004) Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel, Nature 430, 896-900.
43. Celie, P. H. N., Klaassen, R. V., van Rossum-Fikkert, S. E., van Elk, R., van Nierop, P., Smit, A. B., and Sixma, T. K. (2005) Crystal structure of acetylcholine-binding protein from Bulinus truncates reveals the conserved structural scaffold and sites of variation in nicotinic acetylcholine receptors, J. Biol. Chem. 280, 26457-26466.
44. Bourne, Y., Talley, T. T., Hansen, S. B., Taylor, P., and Marchot, P. (2005) Crystal structure of a Cbtx-AChBP complex reveals essential interactions between snake α-neurotoxins and nicotinic receptors, EMBO J. 24, 1512-1522.
45. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution, J. Mol. Biol. 346, 967-989.
46. Gao, F., Bren, N., Burghardt, T. P., Hansen, S., Henchman, R. H., Taylor, P., McCammon, J. A., and Sine, S. M. (2005) Agonist-mediated conformational changes in acetylcholine-binding protein revealed by simulation and intrinsic tryptophan fluorescence, J. Biol. Chem. 280, 8443-8451.
47. Gao, F., Mer, G., Tonelli, M., Hansen, S. B., Burghardt, T. P., Taylor, P., and Sine, S. M. (2006) Solution NMR of acetylcholine binding protein reveals agonist-mediated conformational change of the C-loop, Mol. Pharmacol. 70, 1230-1235.
48. Shi, J., Koeppe, J. R., Komives, E. A., and Taylor, P. (2006) Ligand-induced conformational changes in the acetylcholine-binding protein analyzed by hydrogen-deuterium exchange mass spectrometry, J. Biol. Chem. 281, 12170-12177.
49. Grutter, T., Bertrand, S., Kotzyba-Hibert, F., Bertrand, D., and Goeldner, M. (2002) Structural reorganization of the acetylcholine binding site of the Torpedo nicotinic receptor as revealed by dynamic photoaffinity labeling, ChemBioChem 3, 652-658.
50. 3H]AC5, a photoactivatable agonist, Mol. Pharmacol. 69, 452-461.
51. Rihakova, L., Deraët, M., Auger-Messier, M., Pérodin, J., Boucard, A. A., Guillemette, G., Leduc, R., Lavigne, P., and Escher, E. (2002) Methionine proximity assay, a novel method for exploring peptide ligand-receptor interaction, J. Recept. Signal Transduction 22, 297-313.
52. Wittelsberger, A., Thomas, B. E., Mierke, D. F., and Rosenblatt, M. (2006) Methionine acts as a "magnet" in photoaffinity crosslinking experiments, FEBS Lett. 580, 1872-1876.
53. 2+-binding sites, Proc. Natl. Acad. Sci. U.S.A. 99, 3210-3215.
54. Schapira, M., Abagyan, R., and Totrov, M. (2002) Structural model of nicotinic acetylcholine receptor isotypes bound to acetylcholine and nicotine, BMC Struct. Biol. 2, 1.
55. Huang, X., Zheng, F., Crooks, P. A., Dwoskin, L. P., and Zhan, C.-G. (2005) Modeling multiple species of nicotine and deschloroepibatidine interacting with α4β2 nicotinic acetylcholine receptor: From microscopic binding to phenomenological binding affinity, J. Am. Chem. Soc. 127, 14401-14414.