Nicotine binding to brain receptors requires a strong cation- interaction

Nature

Volumn 458, Issue 7237, 2009, Pages 534-537

  Xiu, Xinan ^a   Puskar, Nyssa L ^a   Shanata, Jai A P ^a   Lester, Henry A ^b   Dougherty, Dennis A ^a  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN RECEPTOR; NICOTINE; NICOTINIC RECEPTOR ALPHA4BETA2; TRYPTOPHAN;

AMINO ACID; BRAIN; CATION; DISEASE; DRUG; MORTALITY; MUSCLE; SMOKING;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROGEN BOND; NEUROMUSCULAR SYNAPSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; TOBACCO DEPENDENCE; XENOPUS LAEVIS;

ACETYLCHOLINE; ANIMALS; BINDING SITES; BRAIN; CATIONS; HALOGENATION; MICE; MODELS, MOLECULAR; NICOTINE; NICOTINIC AGONISTS; OOCYTES; ORGAN SPECIFICITY; PROTEIN BINDING; PROTEIN CONFORMATION; RATS; RECEPTORS, NICOTINIC; SMOKING; SUBSTANCE-RELATED DISORDERS; TRYPTOPHAN; XENOPUS LAEVIS;

EID: 63649149427     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature07768     Document Type: Article

References (31)

1. Romanelli, M. N. et al. Central nicotinic receptors: structure, function, ligands, and therapeutic potential. ChemMedChem 2, 746-767 (2007).
2. Corringer, P. J., Le Novere, N. & Changeux, J. P. Nicotinic receptors at the amino acid level. Annu. Rev. Pharmacol. Toxicol. 40, 431-458 (2000).
3. Coe, J. W. et al. Varenicline: An a4b2 nicotinic receptor partial agonist for smoking cessation. J. Med. Chem. 48, 3474-3477 (2005).
4. Gotti, C., Zoli, M. & Clementi, F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol. Sci. 27, 482-491 (2006).
5. Mansvelder, H. D., Keath, J. R. & McGehee, D. S. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33, 905-919 (2002).
6. Nashmi, R. et al. Chronic nicotine cell specifically upregulates functional α4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J. Neurosci. 27, 8202-8218 (2007).
7. Tapper, A. R. et al. Nicotine activation of a4*receptors: sufficient for reward, tolerance, and sensitization. Science 306, 1029-1032 (2004).
8. Kuryatov, A., Luo, J., Cooper, J. & Lindstrom, J. Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol. Pharm. 68, 1839-1851 (2005).
9. Zhong, W. et al. From ab initio quantum mechanics to molecular neurobiology: A cation-p binding site in the nicotinic receptor. Proc. Natl Acad. Sci. USA 95, 12088-12093 (1998).
10. Brejc, K. et al. Crystal structure of an ACh-binding protein reveals the ligandbinding domain of nicotinic receptors. Nature 411, 269-276 (2001).
11. Sixma, T. K. & Smit, A. B. Acetylcholine binding protein (AChBP): a secreted glial protein that provides a high-resolution model for the extracellular domain of pentameric ligand-gated ion channels. Annu. Rev. Biophys. Biomol. Struct. 32, 311-334 (2003).
12. Dougherty, D. A. Cys-loop neuroreceptors: structure to the rescue? Chem. Rev. 108, 1642-1653 (2008).
13. 3A) and nicotinic acetylcholine receptors: The anomalous binding properties of nicotine. Biochemistry 41, 10262-10269 (2002).
14. Dougherty, D. A. Physical organic chemistry on the brain. J. Org. Chem. 73, 3667-3673 (2008).
15. Nowak, M. W. et al. In vivo incorporation of unnatural amino acids into ion channels in a Xenopus oocyte expression system. Methods Enzymol. 293, 504-529 (1998).
16. Fonck, C. et al. Novel seizure phenotype and sleep disruptions in knock-in mice with hypersensitive a4*nicotinic receptors. J. Neurosci. 25, 11396-11411 (2005).
17. Filatov, G. N. & White, M. M. The role of conserved leucines in the M2 domain of the acetylcholine receptor in channel gating. Mol. Pharmacol. 48, 379-384 (1995).
18. Labarca, C. et al. Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature 376, 514-516 (1995).
19. Kearney, P. et al. 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 (1996).
20. Moroni, M., Zwart, R., Sher, E., Cassels, B. K. & Bermudez, I. α4β2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol. Pharmacol. 70, 755-768 (2006).
21. Nelson, M. E., Kuryatov, A., Choi, C. H., Zhou, Y. & Lindstrom, J. Alternate stoichiometries of α4β2 nicotinic acetylcholine receptors. Mol. Pharmacol. 63, 332-341 (2003).
22. Celie, P. H. et al. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41, 907-914 (2004).
23. Hansen, S. B. et al. Structures of aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J. 24, 3635-3646 (2005).
24. Talley, T. T. et al. Spectroscopic analysis of benzylidene anabaseine complexes with acetylcholine binding proteins as models for ligand-nicotinic receptor interactions. Biochemistry 45, 8894-8902 (2006).
25. Cashin, A. L., Petersson, E. J., Lester, H. A. & Dougherty, D. A. Using physical chemistry to differentiate nicotinic from cholinergic agonists at the nicotinic acetylcholine receptor. J. Am. Chem. Soc. 127, 350-356 (2005).
26. Deechongkit, S. et al. Context-dependent contributions of backbone hydrogen bonding to b-sheet folding energetics. Nature 430, 101-105 (2004).
27. England, P. M., Zhang, Y., Dougherty, D. A. & Lester, H. A. Backbone mutations in transmembrane domains of a ligand-gated ion channel: implications for the mechanism of gating. Cell 96, 89-98 (1999).
28. Koh, J. T., Cornish, V. W. & Schultz, P. G. An experimental approach to evaluating the role of backbone interactions in proteins using unnatural amino acid mutagenesis. Biochemistry 36, 11314-11322 (1997).
29. Grutter, T. et al. An H-bond between two residues from different loops of the acetylcholine binding site contributes to the activation mechanism of nicotinic receptors. EMBO J. 22, 1990-2003 (2003).
30. Sine, S. M. et al. Mutation of the acetylcholine receptor a subunit causes a slowchannel myasthenic syndrome by enhancing agonist binding affinity. Neuron 15, 229-239 (1995).
31. McManus, O. B., Blatz, A. L. & Magleby, K. L. Sampling, log binning, fitting, and plotting durations of open-and-shut intervals from single channels and the effects of noise. Pflugers Archiv-Eur. J. Physiol. 410, 530-553 (1987).