Exploring the positive allosteric modulation of human α7 nicotinic receptors from a single-channel perspective

Neuropharmacology

Volumn 107, Issue , 2016, Pages 189-200

  Andersen, Natalia D ^a   Nielsen, Beatriz E ^a   Corradi, Jeremías ^a   Tolosa, María F ^a   Feuerbach, Dominik ^b   Arias, Hugo R ^c   Bouzat, Cecilia ^a  

^a UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

^b NOVARTIS PHARMA AG   (Switzerland)

^c PLLC   (United States)

Author keywords

Cys loop receptors; Nicotinic receptors; Patch clamp; Positive allosteric modulators; Single channel recordings

Indexed keywords

1 (5 CHLORO 2,4 DIMETHOXYPHENYL) 3 (5 METHYL 3 ISOXAZOLYL)UREA; 3 FURAN 2 YL N 2 TOLYLACRYLAMIDE; 3 FURAN 2 YL N 4 TOLYLACRYLAMIDE; 3 FURAN 2 YL N PHENYLACRYLAMIDE; BUNGAROTOXIN RECEPTOR; MUTANT PROTEIN; N (5 CHLORO 2 HYDROXYPHENYL) N' [2 CHLORO 5 (TRIFLUOROMETHYL)PHENYL]UREA; NICOTINIC AGENT; UNCLASSIFIED DRUG; 1-(5-CHLORO-2,4-DIMETHOXYPHENYL)-3-(5-METHYLISOXAZOL-3-YL)UREA; CALCIUM; CARBANILAMIDE DERIVATIVE; CHOLINERGIC RECEPTOR STIMULATING AGENT; DIVALENT CATION; ISOXAZOLE DERIVATIVE;

ALLOSTERISM; ARTICLE; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; NERVOUS SYSTEM ELECTROPHYSIOLOGY; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TEMPERATURE SENSITIVITY; AGONISTS; ANIMAL; CELL LINE; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; KINETICS; MEMBRANE POTENTIAL; METABOLISM; MOLECULAR MODEL; MUTATION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROTEIN CONFORMATION; RAT; TEMPERATURE;

ALLOSTERIC REGULATION; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; CALCIUM; CATIONS, DIVALENT; CELL LINE; CHOLINERGIC AGENTS; HUMANS; ISOXAZOLES; KINETICS; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MUTATION; PATCH-CLAMP TECHNIQUES; PHENYLUREA COMPOUNDS; PROTEIN CONFORMATION; RATS; TEMPERATURE; TRANSFECTION;

EID: 84962209410     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.02.032     Document Type: Article

References (66)

1. E.X. Albuquerque, E.F. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
2. N. Andersen, J. Corradi, M. Bartos, S.M. Sine, and C. Bouzat Functional relationships between agonist binding sites and coupling regions of homomeric Cys-loop receptors J. Neurosci. 31 2011 3662 3669
3. N. Andersen, J. Corradi, S.M. Sine, and C. Bouzat Stoichiometry for activation of neuronal alpha7 nicotinic receptors Proc. Natl. Acad. Sci. U. S. A. 110 2013 20819 20824
4. H.R. Arias Positive and negative modulation of nicotinic receptors Adv. Protein Chem. Struct. Biol. 80 2010 153 203
5. H.R. Arias, R.X. Gu, D. Feuerbach, B.B. Guo, Y. Ye, and D.Q. Wei Novel positive allosteric modulators of the human alpha7 nicotinic acetylcholine receptor Biochemistry 50 2011 5263 5278
6. H.R. Arias, K.M. Targowska-Duda, D. Feuerbach, and K. Jozwiak The Antidepressant-like Activity of Nicotine, but Not of 3-furan-2-yl-n-p-tolyl-acrilamide, Is Regulated by the Nicotinic Receptor β4 Subunit 2015
7. D. Bagdas, K.M. Targowska-Duda, J.J. Lopez, E.G. Perez, H.R. Arias, and M.I. Damaj The antinociceptive and antiinflammatory properties of 3-furan-2-yl-N-p-tolyl-acrylamide, a positive allosteric modulator of alpha7 nicotinic acetylcholine receptors in mice Anesth. Analg. 121 2015 1369 1377
8. D. Bertrand, and M. Gopalakrishnan Allosteric modulation of nicotinic acetylcholine receptors Biochem. Pharmacol. 74 2007 1155 1163
9. 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
10. C. Bouzat, N. Bren, and S.M. Sine Structural basis of the different gating kinetics of fetal and adult acetylcholine receptors Neuron 13 1994 1395 1402
11. C. Bouzat, F. Gumilar, G. Spitzmaul, H.L. Wang, D. Rayes, S.B. Hansen, P. Taylor, and S.M. Sine Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel Nature 430 2004 896 900
12. C. Bouzat, M. Bartos, J. Corradi, and S.M. Sine The interface between extracellular and transmembrane domains of homomeric Cys-loop receptors governs open-channel lifetime and rate of desensitization J. Neurosci. 28 2008 7808 7819
13. A. Chatzidaki, and N.S. Millar Allosteric modulation of nicotinic acetylcholine receptors Biochem. Pharmacol. 97 2015 408 417
14. A. Chatzidaki, J.M. D'Oyley, J.K. Gill-Thind, T.D. Sheppard, and N.S. Millar The influence of allosteric modulators and transmembrane mutations on desensitisation and activation of alpha7 nicotinic acetylcholine receptors Neuropharmacology 97 2015 75 85
15. T. Collins, G.T. Young, and N.S. Millar Competitive binding at a nicotinic receptor transmembrane site of two alpha7-selective positive allosteric modulators with differing effects on agonist-evoked desensitization Neuropharmacology 61 2011 1306 1313
16. J. Corradi, F. Gumilar, and C. Bouzat Single-channel kinetic analysis for activation and desensitization of homomeric 5-HT(3)A receptors Biophys. J. 97 2009 1335 1345
17. C.J. daCosta, C.R. Free, J. Corradi, C. Bouzat, and S.M. Sine Single-channel and structural foundations of neuronal alpha7 acetylcholine receptor potentiation J. Neurosci. 31 2011 13870 13879
18. C.J. daCosta, and S.M. Sine Stoichiometry for drug potentiation of a pentameric ion channel Proc. Natl. Acad. Sci. U. S. A. 110 2013 6595 6600
19. C.J. daCosta, C.R. Free, and S.M. Sine Stoichiometry for alpha-bungarotoxin block of alpha7 acetylcholine receptors Nat. Commun. 6 2015 8057
20. J.A. Dani, and D. Bertrand Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system Annu. Rev. Pharmacol. Toxicol. 47 2007 699 729
21. J.P. Dilger, R.S. Brett, D.M. Poppers, and Y. Liu The temperature dependence of some kinetic and conductance properties of acetylcholine receptor channels Biochim. Biophys. Acta 1063 1991 253 258
22. K.T. Dineley, A.A. Pandya, and J.L. Yakel Nicotinic ACh receptors as therapeutic targets in CNS disorders Trends Pharmacol. Sci. 36 2015 96 108
23. T. Dinklo, H. Shaban, J.W. Thuring, H. Lavreysen, K.E. Stevens, L. Zheng, C. Mackie, C. Grantham, I. Vandenberk, G. Meulders, L. Peeters, H. Verachtert, P.E. De, and A.S. Lesage Characterization of 2-[[4-fluoro-3-(trifluoromethyl)phenyl]amino]-4-(4-pyridinyl)-5-thiazolemethanol (JNJ-1930942), a novel positive allosteric modulator of the {alpha}7 nicotinic acetylcholine receptor J. Pharmacol. Exp. Ther. 336 2011 560 574
24. J. Dunlop, T. Lock, B. Jow, F. Sitzia, S. Grauer, F. Jow, A. Kramer, M.R. Bowlby, A. Randall, D. Kowal, A. Gilbert, T.A. Comery, J. Larocque, V. Soloveva, J. Brown, and R. Roncarati Old and new pharmacology: positive allosteric modulation of the alpha7 nicotinic acetylcholine receptor by the 5-hydroxytryptamine(2B/C) receptor antagonist SB-206553 (3,5-dihydro-5-methyl-N-3-pyridinylbenzo[1,2-b:4,5-b′]di pyrrole-1(2H)-carboxamide) J. Pharmacol. Exp. Ther. 328 2009 766 776
25. H. Fan, R. Gu, and D. Wei The alpha7 nAChR selective agonists as drug candidates for Alzheimer's disease Adv. Exp. Med. Biol. 827 2015 353 365
26. R. Freedman alpha7-nicotinic acetylcholine receptor agonists for cognitive enhancement in schizophrenia Annu. Rev. Med. 65 2014 245 261
27. 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
28. J.H. Gronlien, H. Ween, K. Thorin-Hagene, S. Cassar, J. Li, C.A. Briggs, M. Gopalakrishnan, and J. Malysz Importance of M2-M3 loop in governing properties of genistein at the alpha7 nicotinic acetylcholine receptor inferred from alpha7/5-HT3A chimera Eur. J. Pharmacol. 647 2010 37 47
29. M. Guerra-Alvarez, A.J. Moreno-Ortega, E. Navarro, J.C. Fernandez-Morales, J. Egea, M.G. Lopez, and M.F. Cano-Abad Positive allosteric modulation of alpha-7 nicotinic receptors promotes cell death by inducing Ca(2+) release from the endoplasmic reticulum J. Neurochem. 133 2015 309 319
30. F. Gumilar, and C. Bouzat Tricyclic antidepressants inhibit homomeric Cys-loop receptors by acting at different conformational states Eur. J. Pharmacol. 584 2008 30 39
31. S. Gupta, and A. Auerbach Temperature dependence of acetylcholine receptor channels activated by different agonists Biophys. J. 100 2011 895 903
32. M. Hu, M. Gopalakrishnan, and J. Li Positive allosteric modulation of alpha7 neuronal nicotinic acetylcholine receptors: lack of cytotoxicity in PC12 cells and rat primary cortical neurons Br. J. Pharmacol. 158 2009 1857 1864
33. X.Q. Hu, and D.M. Lovinger The L293 residue in transmembrane domain 2 of the 5-HT3A receptor is a molecular determinant of allosteric modulation by 5-hydroxyindole Neuropharmacology 54 2008 1153 1165
34. R. Hurst, H. Rollema, and D. Bertrand Nicotinic acetylcholine receptors: from basic science to therapeutics Pharmacol. Ther. 137 2013 22 54
35. 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
36. M. Jindrichova, S.J. Lansdell, and N.S. Millar Changes in temperature have opposing effects on current amplitude in alpha7 and alpha4beta2 nicotinic acetylcholine receptors PLoS One 7 2012 e32073
37. B.I. Kalappa, F. Sun, S.R. Johnson, K. Jin, and V.V. Uteshev A positive allosteric modulator of alpha7 nAChRs augments neuroprotective effects of endogenous nicotinic agonists in cerebral ischaemia Br. J. Pharmacol. 169 2013 1862 1878
38. D.M. Lovinger, S. Sikes, and Q. Zhou Rapid drug Superfusion and kinetic analysis Y. Liu, D.M. Lovinger, Methods in Alcohol-related Neuroscience Research 2002 CRC Press Boca Raton, Florida 159 187
39. J. Malysz, J.H. Gronlien, D.J. Anderson, M. Hakerud, K. Thorin-Hagene, H. Ween, C. Wetterstrand, C.A. Briggs, R. Faghih, W.H. Bunnelle, and M. Gopalakrishnan In vitro pharmacological characterization of a novel allosteric modulator of alpha 7 neuronal acetylcholine receptor, 4-(5-(4-chlorophenyl)-2-methyl-3-propionyl-1H-pyrrol-1-yl)benzenesulfonamide (A-867744), exhibiting unique pharmacological profile J. Pharmacol. Exp. Ther. 330 2009 257 267
40. H.J. Ng, E.R. Whittemore, M.B. Tran, D.J. Hogenkamp, R.S. Broide, T.B. Johnstone, L. Zheng, K.E. Stevens, and K.W. Gee Nootropic alpha7 nicotinic receptor allosteric modulator derived from GABAA receptor modulators Proc. Natl. Acad. Sci. U. S. A. 104 2007 8059 8064
41. M.M. Palczynska, M. Jindrichova, A.J. Gibb, and N.S. Millar Activation of alpha7 nicotinic receptors by orthosteric and allosteric agonists: influence on single-channel kinetics and conductance Mol. Pharmacol. 82 2012 910 917
42. R.L. Papke, and J.K. Porter Papke Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis Br. J. Pharmacol. 137 2002 49 61
43. A.N. Placzek, F. Grassi, T. Papke, E.M. Meyer, and R.L. Papke A single point mutation confers properties of the muscle-type nicotinic acetylcholine receptor to homomeric alpha7 receptors Mol. Pharmacol. 66 2004 169 177
44. A. Potasiewicz, T. Kos, F. Ravazzini, G. Puia, H.R. Arias, P. Popik, and A. Nikiforuk Pro-cognitive activity in rats of 3-furan-2-yl-N-p-tolyl-acrylamide, a positive allosteric modulator of the alpha7 nicotinic acetylcholine receptor Br. J. Pharmacol. 172 2015 5123 5135
45. D. Rayes, G. Spitzmaul, S.M. Sine, and C. Bouzat Single-channel kinetic analysis of chimeric alpha7-5HT3A receptors Mol. Pharmacol. 68 2005 1475 1483
46. S. Sahdeo, T. Wallace, R. Hirakawa, F. Knoflach, D. Bertrand, H. Maag, D. Misner, G.C. Tombaugh, L. Santarelli, K. Brameld, M.E. Milla, and D.C. Button Characterization of RO5126946, a Novel alpha7 nicotinic acetylcholine receptor-positive allosteric modulator J. Pharmacol. Exp. Ther. 350 2014 455 468
47. F. Sitzia, J.T. Brown, A.D. Randall, and J. Dunlop Voltage- and temperature-dependent allosteric modulation of alpha7 nicotinic receptors by PNU120596 Front. Pharmacol. 2 2011 81
48. R. Spurny, S. Debaveye, A. Farinha, K. Veys, A.M. Vos, T. Gossas, J. Atack, S. Bertrand, D. Bertrand, U.H. Danielson, G. Tresadern, and C. Ulens Molecular blueprint of allosteric binding sites in a homologue of the agonist-binding domain of the alpha7 nicotinic acetylcholine receptor Proc. Natl. Acad. Sci. U. S. A. 112 2015 E2543 E2552
49. Y.G. Sun, J.D. Pita-Almenar, C.S. Wu, J.J. Renger, V.N. Uebele, H.C. Lu, and M. Beierlein Biphasic cholinergic synaptic transmission controls action potential activity in thalamic reticular nucleus neurons J. Neurosci. 33 2013 2048 2059
50. A.K. Szabo, K. Pesti, A. Mike, and E.S. Vizi Mode of action of the positive modulator PNU-120596 on alpha7 nicotinic acetylcholine receptors Neuropharmacology 81 2014 42 54
51. K.M. Targowska-Duda, D. Feuerbach, G. Biala, K. Jozwiak, and H.R. Arias Antidepressant activity in mice elicited by 3-furan-2-yl-N-p-tolyl-acrylamide, a positive allosteric modulator of the alpha7 nicotinic acetylcholine receptor Neurosci. Lett. 569 2014 126 130
52. M.S. Thomsen, H.H. Hansen, D.B. Timmerman, and J.D. Mikkelsen Cognitive improvement by activation of alpha7 nicotinic acetylcholine receptors: from animal models to human pathophysiology Curr. Pharm. Des. 16 2010 323 343
53. M.S. Thomsen, M. El-Sayed, and J.D. Mikkelsen Differential immediate and sustained memory enhancing effects of alpha7 nicotinic receptor agonists and allosteric modulators in rats PLoS One 6 2011 e27014
54. D.B. Timmermann, J.H. Gronlien, K.L. Kohlhaas, E.O. Nielsen, E. Dam, T.D. Jorgensen, P.K. Ahring, D. Peters, D. Holst, J.K. Christensen, J. Malysz, C.A. Briggs, M. Gopalakrishnan, and G.M. Olsen An allosteric modulator of the alpha7 nicotinic acetylcholine receptor possessing cognition-enhancing properties in vivo J. Pharmacol. Exp. Ther. 323 2007 294 307
55. V. Uteshev Are positive allosteric modulators of alpha7 nAChRs clinically safe? J. Neurochem. 136 2015 217 219
56. V.V. Uteshev The therapeutic promise of positive allosteric modulation of nicotinic receptors Eur. J. Pharmacol. 727 2014 181 185
57. T.L. Wallace, and R.H. Porter Targeting the nicotinic alpha7 acetylcholine receptor to enhance cognition in disease Biochem. Pharmacol. 82 2011 891 903
58. T.L. Wallace, and D. Bertrand Alpha7 neuronal nicotinic receptors as a drug target in schizophrenia Expert Opin. Ther. Targets 17 2013 139 155
59. D.K. Williams, J. Wang, and R.L. Papke Positive allosteric modulators as an approach to nicotinic acetylcholine receptor-targeted therapeutics: advantages and limitations Biochem. Pharmacol. 82 2011 915 930
60. D.K. Williams, J. Wang, and R.L. Papke Investigation of the molecular mechanism of the alpha7 nicotinic acetylcholine receptor positive allosteric modulator PNU-120596 provides evidence for two distinct desensitized states Mol. Pharmacol. 80 2011 1013 1032
61. D.K. Williams, C. Peng, M.R. Kimbrell, and R.L. Papke Intrinsically low open probability of alpha7 nicotinic acetylcholine receptors can be overcome by positive allosteric modulation and serum factors leading to the generation of excitotoxic currents at physiological temperatures Mol. Pharmacol. 82 2012 746 759
62. H. Yan, N. Pan, F. Xue, Y. Zheng, C. Li, Y. Chang, Z. Xu, H. Yang, and J. Zhang The coupling interface and pore domain codetermine the single-channel activity of the alpha7 nicotinic receptor Neuropharmacology 95 2015 448 458
63. J.S. Yang, S.W. Seo, S. Jang, G.Y. Jung, and S. Kim Rational engineering of enzyme allosteric regulation through sequence evolution analysis PLoS Comput. Biol. 8 2012 e1002612
64. 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
65. Q. Zhou, T.A. Verdoorn, and D.M. Lovinger Alcohols potentiate the function of 5-HT3 receptor-channels on NCB-20 neuroblastoma cells by favouring and stabilizing the open channel state J. Physiol. 507 Pt 2 1998 335 352
66. R. Zwart, F.G. De, L.M. Broad, G.I. McPhie, K.H. Pearson, T. Baldwinson, and E. Sher 5-Hydroxyindole potentiates human alpha 7 nicotinic receptor-mediated responses and enhances acetylcholine-induced glutamate release in cerebellar slices Neuropharmacology 43 2002 374 384