NMR structures of the human α7 nAChR transmembrane domain and associated anesthetic binding sites

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 5, 2014, Pages 1389-1395

  Bondarenko, Vasyl ^a   Mowrey, David D ^a   Tillman, Tommy S ^a   Seyoum, Edom ^a   Xu, Yan ^a   Tang, Pei ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

General anesthetics; Halothane; Ketamine; NMR; Protein dynamics; 7 nAChR structure

Indexed keywords

BUNGAROTOXIN RECEPTOR; HALOTHANE; KETAMINE;

ANIMAL CELL; ARTICLE; BINDING SITE; CHANNEL GATING; DRUG PROTEIN BINDING; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR DOCKING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; XENOPUS;

GENERAL ANESTHETICS; HALOTHANE; KETAMINE; NMR; PROTEIN DYNAMICS; Α7 NACHR STRUCTURE;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANESTHETICS; ANIMALS; BINDING SITES; CELL MEMBRANE; HALOTHANE; HUMANS; KETAMINE; MEMBRANE PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; XENOPUS;

EID: 84894622604     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.12.018     Document Type: Article

References (67)

1. S. Couturier, D. Bertrand, J.M. Matter, M.C. Hernandez, S. Bertrand, N. Millar, S. Valera, T. Barkas, and M. Ballivet A neuronal nicotinic acetylcholine receptor subunit (alpha 7) is developmentally regulated and forms a homo-oligomeric channel blocked by alpha-BTX Neuron 5 1990 847 856
2. F. Rubboli, J.A. Court, C. Sala, C. Morris, B. Chini, E. Perry, and F. Clementi Distribution of nicotinic receptors in the human hippocampus and thalamus Eur. J. Neurosci. 6 1994 1596 1604
3. A. Wevers, A. Jeske, C. Lobron, C. Birtsch, S. Heinemann, A. Maelicke, R. Schroder, and H. Schroder Cellular distribution of nicotinic acetylcholine receptor subunit mRNAs in the human cerebral cortex as revealed by non-isotopic in situ hybridization Brain Res. Mol. Brain Res. 25 1994 122 128
4. E.D. Levin, and A.H. Rezvani Nicotinic treatment for cognitive dysfunction, current drug targets Curr. Drug Targets CNS Neurol. Disord. 1 2002 423 431
5. C. Gotti, L. Riganti, S. Vailati, and F. Clementi Brain neuronal nicotinic receptors as new targets for drug discovery Curr. Pharm. Des. 12 2006 407 428
6. H. Wang, M. Yu, M. Ochani, C.A. Amella, M. Tanovic, S. Susarla, J.H. Li, H. Wang, H. Yang, L. Ulloa, Y. Al-Abed, C.J. Czura, and K.J. Tracey Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation Nature 421 2003 384 388
7. C. Heeschen, M. Weis, A. Aicher, S. Dimmeler, and J.P. Cooke A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors J. Clin. Invest. 110 2002 527 536
8. K. Brejc, W.J. van Dijk, R.V. Klaassen, M. Schuurmans, J. van Der Oost, A.B. Smit, and T.K. Sixma Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Nature 411 2001 269 276
9. P.H. Celie, S.E. van Rossum-Fikkert, W.J. van Dijk, K. Brejc, A.B. Smit, and T.K. Sixma Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures Neuron 41 2004 907 914
10. S.B. Hansen, G. Sulzenbacher, T. Huxford, P. Marchot, P. Taylor, and Y. Bourne Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations EMBO J. 24 2005 3635 3646
11. S.X. Li, S. Huang, N. Bren, K. Noridomi, C.D. Dellisanti, S.M. Sine, and L. Chen Ligand-binding domain of an alpha7-nicotinic receptor chimera and its complex with agonist Nat. Neurosci. 14 2011 1253 1259
12. A. Nemecz, and P. Taylor Creating an alpha7 nicotinic acetylcholine recognition domain from the acetylcholine-binding protein: crystallographic and ligand selectivity analyses J. Biol. Chem. 286 2011 42555 42565
13. N. Unwin Refined structure of the nicotinic acetylcholine receptor at 4A resolution J. Mol. Biol. 346 2005 967 989
14. R.J. Hilf, and R. Dutzler X-ray structure of a prokaryotic pentameric ligand-gated ion channel Nature 452 2008 375 379
15. N. Bocquet, H. Nury, M. Baaden, C. Le Poupon, J.P. Changeux, M. Delarue, and P.J. Corringer X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation Nature 457 2009 111 114
16. R.J. Hilf, and R. Dutzler Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel Nature 457 2009 115 118
17. R.E. Hibbs, and E. Gouaux Principles of activation and permeation in an anion-selective Cys-loop receptor Nature 474 2011 54 60
18. X. Cheng, B. Lu, B. Grant, R.J. Law, and J.A. McCammon Channel opening motion of alpha7 nicotinic acetylcholine receptor as suggested by normal mode analysis J. Mol. Biol. 355 2006 310 324
19. D. Mowrey, E.J. Haddadian, L.T. Liu, D. Willenbring, Y. Xu, and P. Tang Unresponsive correlated motion in alpha7 nAChR to halothane binding explains its functional insensitivity to volatile anesthetics J. Phys. Chem. B 114 2010 7649 7655
20. T. Mori, X. Zhao, Y. Zuo, G.L. Aistrup, K. Nishikawa, W. Marszalec, J.Z. Yeh, and T. Narahashi Modulation of neuronal nicotinic acetylcholine receptors by halothane in rat cortical neurons Mol. Pharmacol. 59 2001 732 743
21. L. Zhang, M. Oz, R.R. Stewart, R.W. Peoples, and F.F. Weight Volatile general anaesthetic actions on recombinant nACh alpha 7, 5-HT3 and chimeric nACh alpha 7-5-HT3 receptors expressed in Xenopus oocytes Br. J. Pharmacol. 120 1997 353 355
22. R.S. Hurst, M. Hajos, M. Raggenbass, T.M. Wall, N.R. Higdon, J.A. Lawson, K.L. Rutherford-Root, M.B. Berkenpas, W.E. Hoffmann, D.W. Piotrowski, V.E. Groppi, G. Allaman, R. Ogier, S. Bertrand, D. Bertrand, and S.P. Arneric A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization J. Neurosci. 25 2005 4396 4405
23. G.T. Young, R. Zwart, A.S. Walker, E. Sher, and N.S. Millar Potentiation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site Proc. Natl. Acad. Sci. U. S. A. 105 2008 14686 14691
24. D. Bertrand, S. Bertrand, S. Cassar, E. Gubbins, J. Li, and M. Gopalakrishnan Positive allosteric modulation of the alpha7 nicotinic acetylcholine receptor: ligand interactions with distinct binding sites and evidence for a prominent role of the M2-M3 segment Mol. Pharmacol. 74 2008 1407 1416
25. J.H. Gronlien, M. Hakerud, H. Ween, K. Thorin-Hagene, C.A. Briggs, M. Gopalakrishnan, and J. Malysz Distinct profiles of alpha7 nAChR positive allosteric modulation revealed by structurally diverse chemotypes Mol. Pharmacol. 72 2007 715 724
26. J.K. Gill, M. Savolainen, G.T. Young, R. Zwart, E. Sher, and N.S. Millar Agonist activation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site Proc. Natl. Acad. Sci. U. S. A. 108 2011 5867 5872
27. V. Bondarenko, D. Mowrey, T. Tillman, T. Cui, L.T. Liu, Y. Xu, and P. Tang NMR structures of the transmembrane domains of the alpha4beta2 nAChR Biochim. Biophys. Acta 1818 2012 1261 1268
28. S. Kracun, P.C. Harkness, A.J. Gibb, and N.S. Millar Influence of the M3-M4 intracellular domain upon nicotinic acetylcholine receptor assembly, targeting and function Br. J. Pharmacol. 153 2008 1474 1484
29. L.M. Valor, J. Mulet, F. Sala, S. Sala, J.J. Ballesta, and M. Criado Role of the large cytoplasmic loop of the alpha 7 neuronal nicotinic acetylcholine receptor subunit in receptor expression and function Biochemistry 41 2002 7931 7938
30. M. Jansen, M. Bali, and M.H. Akabas Modular design of Cys-loop ligand-gated ion channels: functional 5-HT3 and GABA rho1 receptors lacking the large cytoplasmic M3M4 loop J. Gen. Physiol. 131 2008 137 146
31. J. Marley, M. Lu, and C. Bracken A method for efficient isotopic labeling of recombinant proteins J. Biomol. NMR 20 2001 71 75
32. Y. Xu, T. Seto, P. Tang, and L. Firestone NMR study of volatile anesthetic binding to nicotinic acetylcholine receptors Biophys. J. 78 2000 746 751
33. N.J. Baxter, and M.P. Williamson Temperature dependence of 1H chemical shifts in proteins J. Biomol. NMR 9 1997 359 369
34. M. Mayer, and B. Meyer Characterization of ligand binding by saturation transfer difference NMR spectroscopy Angew. Chem. Int. Ed. 38 1999 1784 1788
35. T. Cui, V. Bondarenko, D. Ma, C. Canlas, N.R. Brandon, J.S. Johansson, Y. Xu, and P. Tang Four-alpha-helix bundle with designed anesthetic binding pockets. Part II: halothane effects on structure and dynamics Biophys. J. 94 2008 4464 4472
36. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6 1995 135 140
37. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
38. T.D. Goddard, and D.G. Kneller SPARKY 3 2001 University of California San Francisco
39. P. Guntert, C. Mumenthaler, and K. Wuthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
40. G. Cornilescu, F. Delaglio, and A. Bax Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13 1999 289 302
41. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 [27-38]
42. R. Koradi, M. Billeter, and K. Wuthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55 [29-32]
43. V. Sobolev, E. Eyal, S. Gerzon, V. Potapov, M. Babor, J. Prilusky, and M. Edelman SPACE: a suite of tools for protein structure prediction and analysis based on complementarity and environment Nucleic Acids Res. 33 2005 W39 W43
44. J.D. Durrant, C.A.D. Oliveira, and J.A. McCammon POVME: an algorithm for measuring binding-pocket volumes J. Mol. Graph. Model. 29 2011 773 776
45. G.M. Morris, D.S. Goodsell, R.S. Halliday, R. Huey, W.E. Hart, R.K. Belew, and A.J. Olson Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 19 1998 1639 1662
46. E. Folta-Stogniew, and K.R. Williams Determination of molecular masses of proteins in solution: implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory J. Biomol. Tech. 10 1999 51 63
47. P. Strop, and A.T. Brunger Refractive index-based determination of detergent concentration and its application to the study of membrane proteins Protein Sci. 14 2005 2207 2211
48. N. Dascal Voltage clamp recordings from Xenopus oocytes Current protocols in neuroscience 2001 John Wiley and Sons Hoboken, NJ [Chapter 6, Unit 6.12]
49. R.M. Krause, B. Buisson, S. Bertrand, P.J. Corringer, J.L. Galzi, J.P. Changeux, and D. Bertrand Ivermectin: a positive allosteric effector of the alpha7 neuronal nicotinic acetylcholine receptor Mol. Pharmacol. 53 1998 283 294
50. T. Collins, and N.S. Millar Nicotinic acetylcholine receptor transmembrane mutations convert ivermectin from a positive to a negative allosteric modulator Mol. Pharmacol. 78 2010 198 204
51. P. Flood, and M.D. Krasowski Intravenous anesthetics differentially modulate ligand-gated ion channels Anesthesiology 92 2000 1418 1425
52. K.M. Coates, and P. Flood Ketamine and its preservative, benzethonium chloride, both inhibit human recombinant alpha7 and alpha4beta2 neuronal nicotinic acetylcholine receptors in Xenopus oocytes Br. J. Pharmacol. 134 2001 871 879
53. T. Yamakura, L.E. Chavez-Noriega, and R.A. Harris Subunit-dependent inhibition of human neuronal nicotinic acetylcholine receptors and other ligand-gated ion channels by dissociative anesthetics ketamine and dizocilpine Anesthesiology 92 2000 1144 1153
54. V. Bondarenko, D. Mowrey, L.T. Liu, Y. Xu, and P. Tang NMR resolved multiple anesthetic binding sites in the TM domains of the alpha4beta2 nAChR Biochim. Biophys. Acta 1828 2013 398 404
55. J.M. Violet, D.L. Downie, R.C. Nakisa, W.R. Lieb, and N.P. Franks Differential sensitivities of mammalian neuronal and muscle nicotinic acetylcholine receptors to general anesthetics Anesthesiology 86 1997 866 874
56. R.A. Smith, E.G. Porter, and K.W. Miller The solubility of anesthetic gases in lipid bilayers Biochim. Biophys. Acta 645 1981 327 338
57. C.G. Canlas, T. Cui, L. Li, Y. Xu, and P. Tang Anesthetic modulation of protein dynamics: insight from an NMR study J. Phys. Chem. B 112 2008 14312 14318
58. D.P. Frueh, H. Arthanari, A. Koglin, D.A. Vosburg, A.E. Bennett, C.T. Walsh, and G. Wagner Dynamic thiolation-thioesterase structure of a non-ribosomal peptide synthetase Nature 454 2008 903 906
59. V. Bondarenko, T. Tillman, Y. Xu, and P. Tang NMR structure of the transmembrane domain of the n-acetylcholine receptor beta2 subunit Biochim. Biophys. Acta 1798 2010 1608 1614
60. L. Li, Y.H. Lee, P. Pappone, A. Palma, and M.G. McNamee Site-specific mutations of nicotinic acetylcholine receptor at the lipid-protein interface dramatically alter ion channel gating Biophys. J. 62 1992 61 63
61. Y.H. Lee, L. Li, J. Lasalde, L. Rojas, M. McNamee, S.I. Ortiz-Miranda, and P. Pappone Mutations in the M4 domain of Torpedo californica acetylcholine receptor dramatically alter ion channel function Biophys. J. 66 1994 646 653
62. J.A. Lasalde, S. Tamamizu, D.H. Butler, C.R. Vibat, B. Hung, and M.G. McNamee Tryptophan substitutions at the lipid-exposed transmembrane segment M4 of Torpedo californica acetylcholine receptor govern channel gating Biochemistry 35 1996 14139 14148
63. C.J. daCosta, and J.E. Baenziger A lipid-dependent uncoupled conformation of the acetylcholine receptor J. Biol. Chem. 284 2009 17819 17825
64. N. Unwin, and Y. Fujiyoshi Gating movement of acetylcholine receptor caught by plunge-freezing J. Mol. Biol. 422 2012 617 634
65. M.S. Prevost, L. Sauguet, H. Nury, C. Van Renterghem, C. Huon, F. Poitevin, M. Baaden, M. Delarue, and P.J. Corringer A locally closed conformation of a bacterial pentameric proton-gated ion channel Nat. Struct. Mol. Biol. 19 2012 642 649
66. D.D. Mowrey, Q. Liu, V. Bondarenko, Q. Chen, E. Seyoum, Y. Xu, J. Wu, and P. Tang Insights into distinct modulation of alpha7 and alpha7beta2 nAChRs by the volatile anesthetic isoflurane J. Biol. Chem. 288 2013 35793 35800
67. J. Pan, Q. Chen, D. Willenbring, D. Mowrey, X.-P. Kong, A. Cohen, C.B. Divito, Y. Xu, and P. Tang Structure of the pentameric ligand-gated ion channel GLIC bound with anesthetic ketamine Structure 20 2012 1463 1469