Functional evaluation of key interactions evident in the structure of the eukaryotic Cys-loop receptor GluCl

ACS Chemical Biology

Volumn 9, Issue 10, 2014, Pages 2283-2290

  Daeffler, Kristina N M ^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

AMINE; CATION; CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR; CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR GLUCL ALPHA; CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR GLUCL BETA; GLUTAMIC ACID; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; CHLORIDE CHANNEL; GLUTAMATE-GATED CHLORIDE CHANNELS; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FEMALE; HUMAN; HUMAN CELL; HYDROGEN BOND; LIGAND BINDING; MUTAGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; CAENORHABDITIS ELEGANS; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; EVALUATION STUDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OOCYTE; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; XENOPUS LAEVIS;

EUKARYOTA;

ANIMALS; CAENORHABDITIS ELEGANS; CHLORIDE CHANNELS; CYSTEINE LOOP LIGAND-GATED ION CHANNEL RECEPTORS; GLUTAMIC ACID; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; OOCYTES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; XENOPUS LAEVIS;

EID: 84908140914     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500323d     Document Type: Article

References (46)

1. Thompson, A. J., Lester, H. A., and Lummis, S. C. (2010) The structural basis of function in Cys-loop receptors. Q. Rev. Biophys. 43, 449-499.
2. Coe, J. W., Brooks, P. R., Vetelino, M. G., Wirtz, M. C., Arnold, E. P., Huang, J., Sands, S. B., Davis, T. I., Lebel, L. A., Fox, C. B., Shrikhande, A., Heym, J. H., Schaeffer, E., Rollema, H., Lu, Y., Mansbach, R. S., Chambers, L. K., Rovetti, C. C., Schulz, D. W., Tingley, F. D., 3rd, and O'Neill, B. T. (2005) Varenicline: An α4β2 nicotinic receptor partial agonist for smoking cessation. J. Med. Chem. 48, 3474-3477.
3. Cupp, E. W., Bernardo, M. J., Kiszewski, A. E., Collins, R. C., Taylor, H. R., Aziz, M. A., and Greene, B. M. (1986) The effects of ivermectin on transmission of Onchocerca volvulus. Science 231, 740-742.
4. Miyazawa, A., Fujiyoshi, Y., Stowell, M., and Unwin, N. (1999) Nicotinic acetylcholine receptor at 4.6 A resolution: Transverse tunnels in the channel wall. J. Mol. Biol. 288, 765-786.
5. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346, 967-689.
6. 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 receptors. Nature 411, 269-276.
7. Hilf, R. J., and Dutzler, R. (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452, 375-379.
8. Hilf, R. J., and Dutzler, R. (2009) Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 457, 115-118.
9. Bocquet, N., Nury, H., Baaden, M., Le Poupon, C., Changeux, J. P., Delarue, M., and Corringer, P. J. (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457, 111-114.
10. Hibbs, R. E., and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60.
11. Campbell, W. C. (1985) Ivermectin: An update. Parasitol Today 1, 10-16.
12. Campbell, W. C., Fisher, M. H., Stapley, E. O., Albers-Schonberg, G., and Jacob, T. A. (1983) Ivermectin: A potent new antiparasitic agent. Science 221, 823-828.
13. Aziz, M. A., Diallo, S., Diop, I. M., Lariviere, M., and Porta, M. (1982) Efficacy and tolerance of ivermectin in human onchocerciasis. Lancet 2, 171-173.
14. Lester, H. A., Dibas, M. I., Dahan, D. S., Leite, J. F., and Dougherty, D. A. (2004) Cys-loop receptors: New twists and turns. Trends Neurosci. 27, 329-336.
15. Miller, P. S., and Smart, T. G. (2010) Binding, activation, and modulation of Cys-loop receptors. Trends Pharmacol. Sci. 31, 161-174.
16. Van Arnam, E. B., and Dougherty, D. A. (2014) Functional probes of drug-receptor interactions implicated by structural studies: Cys-loop receptors provide a fertile testing ground. J. Med. Chem., DOI: 10.1021/jm500023m.
17. Etter, A., Cully, D. F., Schaeffer, J. M., Liu, K. K., and Arena, J. P. (1996) An amino acid substitution in the pore region of a glutamate-gated chloride channel enables the coupling of ligand binding to channel gating. J. Biol. Chem. 271, 16035-16039.
18. Slimko, E. M., and Lester, H. A. (2003) Codon optimization of Caenorhabditis elegans GluCl ion channel genes for mammalian cells dramatically improves expression levels. J. Neurosci. Methods 124, 75-81.
19. Kao, C., Zheng, M., and Rudisser, S. (1999) A simple and efficient method to reduce nontemplated nucleotide addition at the 3′ terminus of RNAs transcribed by T7 RNA polymerase. RNA 5, 1268-1272.
20. Nowak, M. W., Gallivan, J. P., Silverman, S. K., Labarca, C. G., Dougherty, D. A., and Lester, H. A. (1998) In vivo incorporation of unnatural amino acids into ion channels in Xenopus oocyte expression system. Methods Enzymol. 293, 504-529.
21. Pertzoff, V. A. (1933) The solubility of glutamic acid in water and certain organic solvents. J. Biol. Chem. 100, 97-104.
22. Filatov, G. N., and White, M. M. (1995) The role of conserved leucines in the M2 domain of the acetylcholine receptor in channel gating. Mol. Pharmacol. 48, 379-384.
23. Labarca, C., Nowak, M. W., Zhang, H., Tang, L., Deshpande, P., and Lester, H. A. (1995) Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature 376, 514-516.
24. Frazier, S. J., Cohen, B. N., and Lester, H. A. (2013) An engineered glutamate-gated chloride (GluCl) channel for sensitive, consistent neuronal silencing by ivermectin. J. Biol. Chem. 288, 21029-21042.
25. Placzek, A. N., Grassi, F., Meyer, E. M., and Papke, R. L. (2005) An α7 nicotinic acetylcholine receptor gain-of-function mutant that retains pharmacological fidelity. Mol. Pharmacol. 68, 1863-1876.
26. Yakel, J. L., Lagrutta, A., Adelman, J. P., and North, R. A. (1993) Single amino acid substitution affects desensitization of the 5-hydroxytryptamine type 3 receptor expressed in Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 90, 5030-5033.
27. Xiu, X., Puskar, N. L., Shanata, J. A., Lester, H. A., and Dougherty, D. A. (2009) Nicotine binding to brain receptors requires a strong cation-π interaction. Nature 458, 534-537.
28. Marotta, C. B., Dilworth, C. N., Lester, H. A., and Dougherty, D. A. (2014) Probing the noncanonical interface for agonist interaction with an α5 containing nicotinic acetylcholine receptor. Neuropharmacology 77, 342-349.
29. Zhong, W. G., Gallivan, J. P., Zhang, Y. O., Li, L. T., Lester, H. A., and Dougherty, D. A. (1998) From ab initio quantum mechanics to molecular neurobiology: A cation-π binding site in the nicotinic receptor. Proc. Natl. Acad. Sci. U.S.A. 95, 12088-12093.
30. Kearney, P. C., Zhang, H., Zhong, W., Dougherty, D. A., and Lester, H. A. (1996) Determinants of nicotinic receptor gating in natural and unnatural side chain structures at the M2 9′ position. Neuron 17, 1221-1229.
31. Zerangue, N., Schwappach, B., Jan, Y. N., and Jan, L. Y. (1999) A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22, 537-548.
32. Boyd, G. W., Doward, A. I., Kirkness, E. F., Millar, N. S., and Connolly, C. N. (2003) Cell surface expression of 5-hydroxytryptamine type 3 receptors is controlled by an endoplasmic reticulum retention signal. J. Biol. Chem. 278, 27681-27687.
33. Mossessova, E., Bickford, L. C., and Goldberg, J. (2003) SNARE selectivity of the COPII coat. Cell 114, 483-495.
34. Xu, J., Zhu, Y., and Heinemann, S. F. (2006) Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J. Neurosci. 26, 9780-9793.
35. Kracun, S., Harkness, P. C., Gibb, A. J., and Millar, N. S. (2008) Influence of the M3-M4 intracellular domain upon nicotinic acetylcholine receptor assembly, targeting, and function. Br. J. Pharmacol. 153, 1474-1484.
36. Castillo, M., Mulet, J., Aldea, M., Gerber, S., Sala, S., Sala, F., and Criado, M. (2009) Role of the N-terminal α-helix in biogenesis of α7 nicotinic receptors. J. Neurochem 108, 1399-1409.
37. Pons, S., Sallette, J., Bourgeois, J. P., Taly, A., Changeux, J. P., and Devillers-Thiery, A. (2004) Critical role of the C-terminal segment in the maturation and export to the cell surface of the homopentameric α7-5HT3A receptor. Eur. J. Neurosci 20, 2022-2030.
38. Beene, D. L., Brandt, G. S., Zhong, W., Zacharias, N. M., Lester, H. A., and Dougherty, D. A. (2002) Cation-π interactions in ligand recognition by serotonergic (5-HT3A) and nicotinic acetylcholine receptors: The anomalous binding properties of nicotine. Biochemistry 41, 10262-10269.
39. Puskar, N. L., Xiu, X. A., Lester, H. A., and Dougherty, D. A. (2011) Two neuronal nicotinic acetylcholine receptors, α4, β4, and α7, show differential agonist binding modes. J. Biol. Chem. 286, 14618-14627.
40. Lummis, S. C., D, L. B., Harrison, N. J., Lester, H. A., and Dougherty, D. A. (2005) A cation-π binding interaction with a tyrosine in the binding site of the GABAC receptor. Chem. Biol. 12, 993-997.
41. Pless, S. A., Millen, K. S., Hanek, A. P., Lynch, J. W., Lester, H. A., Lummis, S. C., and Dougherty, D. A. (2008) A cation-π interaction in the binding site of the glycine receptor is mediated by a phenylalanine residue. J. Neurosci. 28, 10937-10942.
42. Gleitsman, K. R., Kedrowski, S. M. A., Lester, H. A., and Dougherty, D. A. (2008) An intersubunit hydrogen bond in the nicotinic acetylcholine receptor that contributes to channel gating. J. Biol. Chem. 283, 35638-35643.
43. Blum, A. P., Gleitsman, K. R., Lester, H. A., and Dougherty, D. A. (2011) Evidence for an extended hydrogen bond network in the binding site of the nicotinic receptor: Role of the vicinal disulfide of the α1 subunit. J. Biol. Chem. 286, 32251-32258.
44. Mecozzi, S., West, A. P., and Dougherty, D. A. (1996) Cation-π interactions in aromatics of biological and medicinal interest: Electrostatic potential surfaces as a useful qualitative guide. Proc. Natl. Acad. Sci. U.S.A. 93, 10566-10571.
45. Padgett, C. L., Hanek, A. P., Lester, H. A., Dougherty, D. A., and Lummis, S. C. (2007) Unnatural amino acid mutagenesis of the GABA(A) receptor binding site residues reveals a novel cation-π interaction between GABA and β 2Tyr97. J. Neurosci. 27, 886-892.
46. Mu, T. W., Lester, H. A., and Dougherty, D. A. (2003) Different binding orientations for the same agonist at homologous receptors: A lock and key or a simple wedge? J. Am. Chem. Soc. 125, 6850-6851.