Crystal structures of free and antagonist-bound states of human ± 9 nicotinic receptor extracellular domain

Nature Structural and Molecular Biology

Volumn 21, Issue 11, 2014, Pages 976-980

  Zouridakis, Marios ^a   Giastas, Petros ^a   Zarkadas, Eleftherios ^a,b   Chroni Tzartou, Dafni ^a   Bregestovski, Piotr ^c   Tzartos, Socrates J ^a,b  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b UNIVERSITY OF PATRAS   (Greece)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BUNGAROTOXIN; METHYLLYCACONITINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA9; PROTEIN VARIANT; UNCLASSIFIED DRUG; ACETYLCHOLINE; ACONITINE; BUNGAROTOXIN; COMPLEMENTARY RNA; NACHR ALPHA9; NICOTINE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; FEMALE; LIGAND BINDING; MOLECULAR INTERACTION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN SUBUNIT; STRUCTURAL HOMOLOGY; ACTION POTENTIAL; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MUTATION; OOCYTE; PATCH CLAMP TECHNIQUE; PICHIA; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY; XENOPUS LAEVIS;

ACETYLCHOLINE; ACONITINE; ACTION POTENTIALS; ANIMALS; BUNGAROTOXINS; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION; HUMANS; MODELS, MOLECULAR; MUTATION; NICOTINE; OOCYTES; PATCH-CLAMP TECHNIQUES; PICHIA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, NICOTINIC; RECOMBINANT PROTEINS; RNA, COMPLEMENTARY; XENOPUS LAEVIS;

EID: 84909942884     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2900     Document Type: Article

References (45)

1. Changeux, J.P. The nicotinic acetylcholine receptor: the founding father of the pentameric ligand-gated ion channel superfamily. J. Biol. Chem. 287, 40207-40215 (2012).
2. Unwin, N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346, 967-989 (2005).
3. Brejc, K. et al. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411, 269-276 (2001).
4. Celie, P.H. et al. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41, 907-914 (2004).
5. 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).
6. Dellisanti, C.D., Yao, Y., Stroud, J.C., Wang, Z.Z. &Chen, L. Crystal structure of the extracellular domain of nAChR α1 bound to α-bungarotoxin at 1.94 A resolution. Nat. Neurosci. 10, 953-962 (2007).
7. Bocquet, N. et al. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457, 111-114 (2009).
8. Hilf, R.J. &Dutzler, R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452, 375-379 (2008).
9. Li, S.X. et al. Ligand-binding domain of an α7-nicotinic receptor chimera and its complex with agonist. Nat. Neurosci. 14, 1253-1259 (2011).
10. Nemecz, A. &Taylor, P. Creating an α7 nicotinic acetylcholine recognition domain from the acetylcholine-binding protein: crystallographic and ligand selectivity analyses. J. Biol. Chem. 286, 42555-42565 (2011).
11. Huang, S. et al. Complex between α-bungarotoxin and an α7 nicotinic receptor ligand-binding domain chimaera. Biochem. J. 454, 303-310 (2013).
12. Hibbs, R.E. &Gouaux, E. Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60 (2011).
13. Althoff, T., Hibbs, R.E., Banerjee, S. &Gouaux, E. X-ray structures of GluCl in apo states reveal a gating mechanism of Cys-loop receptors. Nature 512, 333-337 (2014).
14. Miller, P.S. &Aricescu, A.R. Crystal structure of a human GABAA receptor. Nature 512, 270-275 (2014).
15. Hassaine, G. et al. X-ray structure of the mouse serotonin 5-HT3 receptor. Nature 512, 276-281 (2014).
16. Elgoyhen, A.B., Johnson, D.S., Boulter, J., Vetter, D.E. &Heinemann, S. α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79, 705-715 (1994).
17. Rothlin, C.V., Katz, E., Verbitsky, M. &Elgoyhen, A.B. The α9 nicotinic acetylcholine receptor shares pharmacological properties with type A γ-aminobutyric acid, glycine, and type 3 serotonin receptors. Mol. Pharmacol. 55, 248-254 (1999).
18. Lustig, L.R., Peng, H., Hiel, H., Yamamoto, T. &Fuchs, P.A. Molecular cloning and mapping of the human nicotinic acetylcholine receptor α10 (CHRNA10). Genomics 73, 272-283 (2001).
19. Elgoyhen, A.B. et al. α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc. Natl. Acad. Sci. USA 98, 3501-3506 (2001).
20. Sgard, F. et al. A novel human nicotinic receptor subunit, α10, that confers functionality to the α9-subunit. Mol. Pharmacol. 61, 150-159 (2002).
21. Plazas, P.V., Katz, E., Gomez-Casati, M.E., Bouzat, C. &Elgoyhen, A.B. Stoichiometry of the α9α10 nicotinic cholinergic receptor. J. Neurosci. 25, 10905-10912 (2005).
22. Indurthi, D.C. et al. Presence of multiple binding sites on α9α10 nAChR receptors alludes to stoichiometric-dependent action of the α-conotoxin, Vc1.1. Biochem. Pharmacol. 89, 131-140 (2014).
23. McIntosh, J.M., Absalom, N., Chebib, M., Elgoyhen, A.B. &Vincler, M. α9 nicotinic acetylcholine receptors and the treatment of pain. Biochem. Pharmacol. 78, 693-702 (2009).
24. Elgoyhen, A.B., Katz, E. &Fuchs, P.A. The nicotinic receptor of cochlear hair cells: a possible pharmacotherapeutic target Biochem. Pharmacol. 78, 712-719 (2009).
25. Psaridi-Linardaki, L., Mamalaki, A., Remoundos, M. &Tzartos, S.J. Expression of soluble ligand-and antibody-binding extracellular domain of human muscle acetylcholine receptor α subunit in yeast Pichia pastoris: role of glycosylation in α-bungarotoxin binding. J. Biol. Chem. 277, 26980-26986 (2002).
26. Zouridakis, M., Zisimopoulou, P., Eliopoulos, E., Poulas, K. &Tzartos, S.J. Design and expression of human α7 nicotinic acetylcholine receptor extracellular domain mutants with enhanced solubility and ligand-binding properties. Biochim. Biophys. Acta 1794, 355-366 (2009).
27. Stergiou, C., Zisimopoulou, P. &Tzartos, S.J. Expression of water-soluble, ligand-binding concatameric extracellular domains of the human neuronal nicotinic receptor α4 and β2 subunits in the yeast Pichia pastoris: glycosylation is not required for ligand binding. J. Biol. Chem. 286, 8884-8892 (2011).
28. Mukhtasimova, N., Free, C. &Sine, S.M. Initial coupling of binding to gating mediated by conserved residues in the muscle nicotinic receptor. J. Gen. Physiol. 126, 23-39 (2005).
29. Sine, S.M. &Engel, A.G. Recent advances in Cys-loop receptor structure and function. Nature 440, 448-455 (2006).
30. Verbitsky, M., Rothlin, C.V., Katz, E. &Elgoyhen, A.B. Mixed nicotinic-muscarinic properties of the α9 nicotinic cholinergic receptor. Neuropharmacology 39, 2515-2524 (2000).
31. Chen, L. In pursuit of the high-resolution structure of nicotinic acetylcholine receptors. J. Physiol. (Lond.) 588, 557-564 (2010).
32. Lee, W.Y. &Sine, S.M. Principal pathway coupling agonist binding to channel gating in nicotinic receptors. Nature 438, 243-247 (2005).
33. Mukhtasimova, N. &Sine, S.M. Nicotinic receptor transduction zone: invariant arginine couples to multiple electron-rich residues. Biophys. J. 104, 355-367 (2013).
34. Azam, L. &McIntosh, J.M. Molecular basis for the differential sensitivity of rat and human α9α10 nAChRs to α-conotoxin RgIA. J. Neurochem. 122, 1137-1144 (2012).
35. Yu, R., Kompella, S.N., Adams, D.J., Craik, D.J. &Kaas, Q. Determination of the α-conotoxin Vc1.1 binding site on the α9α10 nicotinic acetylcholine receptor. J. Med. Chem. 56, 3557-3567 (2013).
36. Karplus, P.A. &Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030-1033 (2012).
37. Stothard, P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28, 1102, 1104 (2000).
38. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
39. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006).
40. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
41. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
42. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
43. Emsley, P. &Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
44. Evans, P.R. &Murshudov, G.N. How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013).
45. Filchakova, O. &McIntosh, J.M. Functional expression of human α9 nicotinic acetylcholine receptors in X. laevis oocytes is dependent on the α9 subunit 5-UTR. PLoS ONE 8, e64655 (2013).