Pharmacological and molecular studies on the interaction of varenicline with different nicotinic acetylcholine receptor subtypes. Potential mechanism underlying partial agonism at human α4β2 and α3β4 subtypes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 2, 2015, Pages 731-741

  Arias, Hugo R ^a   Feuerbach, Dominik ^b   Targowska Duda, Katarzyna ^c   Kaczor, Agnieszka A ^c   Poso, Antti ^d   Jozwiak, Krzysztof ^c  

^a California Northstate University   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^d UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Full agonist; Molecular modeling; Nicotinic acetylcholine receptors; Partial agonist; Varenicline

Indexed keywords

BUNGAROTOXIN RECEPTOR; CALCIUM ION; EPIBATIDINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA1BETA1GAMMADELTA; NICOTINIC RECEPTOR ALPHA3BETA4; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC RECEPTOR ALPHA4BETA4; NICOTINIC RECEPTOR TORPEDO ALPHA1BETA1GAMMADELTA; UNCLASSIFIED DRUG; VARENICLINE; BENZAZEPINE DERIVATIVE; CALCIUM; FUSED HETEROCYCLIC RINGS; ISOPROTEIN; NICOTINIC AGENT; PROTEIN BINDING; PYRIDINE DERIVATIVE; QUINOXALINE DERIVATIVE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM TRANSPORT; CONTROLLED STUDY; DRUG ACTIVITY; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; ALLOSTERISM; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; STRUCTURAL HOMOLOGY; TORPEDO; TRANSGENE;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; ANIMALS; BENZAZEPINES; BICYCLO COMPOUNDS, HETEROCYCLIC; CALCIUM; CHO CELLS; CRICETULUS; GENE EXPRESSION; HEK293 CELLS; HUMANS; HYDROGEN BONDING; MOLECULAR DOCKING SIMULATION; NICOTINIC AGONISTS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PYRIDINES; QUINOXALINES; RECEPTORS, NICOTINIC; STRUCTURAL HOMOLOGY, PROTEIN; TORPEDO; TRANSGENES;

EID: 84918570881     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.11.003     Document Type: Article

References (59)

1. M. Nides, E.D. Glover, V.I. Reus, A.G. Christen, B.J. Make, C.B. Billing Jr., and K.E. Williams Varenicline versus bupropion SR or placebo for smoking cessation: a pooled analysis Am. J. Health Behav. 32 2008 664 675
2. H.R. Arias Is the inhibition of nicotinic acetylcholine receptors by bupropion involved in its clinical actions? Int. J. Biochem. Cell Biol. 41 2009 2098 2108
3. M.O. Ortells, and H.R. Arias Neuronal networks of nicotine addiction Int. J. Biochem. Cell Biol. 42 2010 1931 1935
4. H. Rollema, J.W. Coe, L.K. Chambers, R.S. Hurst, S.M. Stahl, and K.E. Williams Rationale, pharmacology and clinical efficacy of partial agonists of α4β2 nACh receptors for smoking cessation Trends Pharmacol. Sci. 28 2007 316 325
5. J.W. Smith, A. Mogg, E. Tafi, E. Peacey, I.A. Pullar, P. Szekeres, and M. Tricklebank Ligands selective for α4β2 but not α3β4 or α7 nicotinic receptors generalise to the nicotine discriminative stimulus in the rat Psychopharmacology (Berl) 190 2007 157 170
6. M.R. Picciotto, M. Zoli, R. Rimondini, C. Lena, L.M. Marubio, E.M. Pich, K. Fuxe, and J.P. Changeux Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine Nature 391 1998 173 177
7. M. Shoaib, J. Gommans, A. Morley, I.P. Stolerman, R. Grailhe, and J.P. Changeux The role of nicotinic receptor β2 subunits in nicotine discrimination and conditioned taste aversion Neuropharmacology 42 2002 530 539
8. S.R. Grady, N.M. Meinerz, J. Cao, A.M. Reynolds, M.R. Picciotto, J.P. Changeux, J.M. McIntosh, M.J. Marks, and A.C. Collins Nicotinic agonists stimulate acetylcholine release from mouse interpeduncular nucleus: a function mediated by a different nAChR than dopamine release from striatum J. Neurochem. 76 2001 258 268
9. J.W. Coe, P.R. Brooks, M.G. Vetelino, M.C. Wirtz, E.P. Arnold, J. Huang, S.B. Sands, T.I. Davis, L.A. Lebel, C.B. Fox, A. Shrikhande, J.H. Heym, E. Schaeffer, H. Rollema, Y. Lu, R.S. Mansbach, L.K. Chambers, C.C. Rovetti, D.W. Schulz, F.D. Tingley III, and B.T. O'Neill Varenicline: an α4β2 nicotinic receptor partial agonist for smoking cessation J. Med. Chem. 48 2005 3474 3477
10. K.B. Mihalak, F.I. Carroll, and C.W. Luetje Varenicline is a partial agonist at α4β2 and a full agonist at α7 neuronal nicotinic receptors Mol. Pharmacol. 7 2006 801 805
11. H. Rollema, L.K. Chambers, J.W. Coe, J. Glowa, R.S. Hurst, L.A. Lebel, Y. Lu, R.S. Mansbach, R.J. Mather, C.C. Rovetti, S.B. Sands, E. Schaeffer, D.W. Schulz, F.D. Tingley III, and K.E. Williams Pharmacological profile of the α4β2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid Neuropharmacology 52 2007 985 994
12. H. Rollema, A. Shrikhande, K.M. Ward, F.D. Tingley III, J.W. Coe, B.T. O'Neill, E. Tseng, E.Q. Wang, R.J. Mather, R.S. Hurst, K.E. Williams, M. de Vries, T. Cremers, S. Bertrand, and D. Bertrand Pre-clinical properties of the α4β2 nicotinic acetylcholine receptor partial agonists varenicline, cytisine and dianicline translate to clinical efficacy for nicotine dependence Br. J. Pharmacol. 160 2010 334 345
13. R.C. Jiloha Pharmacotherapy of smoking cessation Indian J. Psychiatry 5 2014 87 95
14. E.C. O'Connor, D. Parker, H. Rollema, and A.N. Mead The α4β2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats Psychopharmacology (Berl) 208 2010 365 376
15. C. Reperant, S. Pons, E. Dufour, H. Rollema, A.M. Gardier, and U. Maskos Effect of the α4β2∗ nicotinic acetylcholine receptor partial agonist varenicline on dopamine release in β2 knock-out mice with selective re-expression of the β2 subunit in the ventral tegmental area Neuropharmacology 58 2010 346 350
16. L. Azam, U.H. Winzer-Serhan, Y. Chen, and F.M. Leslie Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons J. Comp. Neurol. 444 2002 260 274
17. M. Quik, Y. Polonskaya, A. Gillespie, M. Jakowec, G.K. Lloyd, and J.W. Langston Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization J. Comp. Neurol. 425 2000 58 69
18. H.R. Arias, N.B. Fedorov, L.C. Benson, P. Lippiello, G.J. Gatto, D. Feuerbach, and M.O. Ortells Functional and structural interaction of (-)-reboxetine with the human α4β2 nicotinic acetylcholine receptor J. Pharmacol. Exp. Ther. 344 2013 113 123
19. 2,6]decan-2-amine enantiomers interact with the human α4β2 nicotinic acetylcholine receptor at luminal and non-luminal domains OA Biochemistry 1 2013 11
20. H.R. Arias, D. Feuerbach, P. Bhumireddy, and M.O. Ortells Inhibitory mechanisms and binding site location for serotonin selective reuptake inhibitors on nicotinic acetylcholine receptors Int. J. Biochem. Cell Biol. 42 2010 712 724
21. H.R. Arias, J.R. Trudell, E.Z. Bayer, B. Hester, E.A. McCardy, and M.P. Blanton Noncompetitive antagonist binding sites in the Torpedo nicotinic acetylcholine receptor ion channel. Structure-activity relationship studies using adamantane derivatives Biochemistry 42 2003 7358 7370
22. H.R. Arias, H. Xing, K. Macdougall, M.P. Blanton, F. Soti, and W.R. Kem Interaction of benzylidene-anabaseine analogues with agonist and allosteric sites on muscle nicotinic acetylcholine receptors Br. J. Pharmacol. 157 2009 320 330
23. H.R. Arias, D. Feuerbach, K.M. Targowska-Duda, M. Russell, and K. Jozwiak Interaction of selective serotonin reuptake inhibitors with neuronal nicotinic acetylcholine receptors Biochemistry 49 2010 5734 5742
24. Y. Aracava, and E.X. Albuquerque Meproadifen enhances activation and desensitization of the acetylcholine receptor-ionic channel complex (AChR): single channel studies FEBS Lett. 17 1984 267 274
25. 50) of an enzymatic reaction Biochem. Pharmacol. 22 1973 3099 3108
26. 3H]methyllycaconitine: a new radioligand for labelling α7-type neuronal nicotinic acetylcholine receptors Neuropharmacology 38 1999 679 690
27. Y.E. Slater, L.M. Houlihan, P.D. Maskell, R. Exley, I. Bermudez, R.J. Lukas, A.C. Valdivia, and B.K. Cassels Halogenated cytisine derivatives as agonists at human neuronal nicotinic acetylcholine receptor subtypes Neuropharmacology 44 2003 503 515
28. J. Zhang, and J.H. Steinbach Cytisine binds with similar affinity to nicotinic α4β2 receptors on the cell surface and in homogenates Brain Res. 959 2003 98 102
29. S. Michelmore, K. Croskery, J. Nozulak, D. Hoyer, R. Longato, A. Weber, R. Bouhelal, and D. Feuerbach Study of the calcium dynamics of the human α4β2, α3β4 and α1β1γδ nicotinic acetylcholine receptors Naunyn Schmiedeberg's Arch. Pharmacol. 366 2002 235 245
30. P. Rucktooa, C.A. Haseler, R. van Elk, A.B. Smit, T. Gallagher, and T.K. Sixma Structural characterization of binding mode of smoking cessation drugs to nicotinic acetylcholine receptors through study of ligand complexes with acetylcholine-binding protein J. Biol. Chem. 28 2012 23283 23293
31. N. Unwin Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution J. Mol. Biol. 346 2005 967 989
32. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680
33. N. Eswar, B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M.Y. Shen, U. Pieper, and A. Sali Comparative protein structure modeling using Modeller Curr. Protoc. Bioinformatics Supplement 15 2006 John Wiley & Sons, Inc. (5.6.1-5.6.30)
34. M.Y. Shen, and A. Sali Statistical potential for assessment and prediction of protein structures Protein Sci. 15 2006 2507 2524
35. F. Melo, and E. Feytmans Assessing protein structures with a non-local atomic interaction energy J. Mol. Biol. 27 1998 1141 1152
36. J.U. Bowie, R. Luthy, and D. Eisenberg A method to identify protein sequences that fold into a known three-dimensional structure Science 253 1991 164 170
37. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK - a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
38. H.R. Arias, D. Feuerbach, K.M. Targowska-Duda, S. Aggarwal, D. Lapinsky, and K. Jozwiak Structural and functional interaction of (±)-2-(N-tert-butylamino)-3′-iodo-4′-azidopropiophenone, a photoreactive bupropion derivative, with nicotinic acetylcholine receptors Neurochem. Int. 61 2012 1433 1441
39. K.J. Bowers, E. Chow, H. Xu, R.O. Dror, M.P. Eastwood, B.A. Gregersen, J.L. Klepeis, I. Kolossváry, M.A. Moraes, F.D. Sacerdoti, J.K. Salmon, Y. Shan, and D.E. Shaw Scalable algorithms for molecular dynamics simulations on commodity clusters Proceedings of the ACM/IEEE Conference on Supercomputing (SC06) November 11-17, 2006 (Tampa, Florida)
40. H. Nury, F. Poitevin, C. Van Renterghem, J.P. Changeux, P.J. Corringer, M. Delarue, and M. Baaden One-microsecond molecular dynamics simulation of channel gating in a nicotinic receptor homologue Proc. Natl. Acad. Sci. U. S. A. 10 2010 6275 6280
41. A.A. Kaczor, Z. Karczmarzyk, A. Fruzinski, K. Pihlaja, J. Sinkkonen, K. Wiinamaki, C. Kronbach, K. Unverferth, A. Poso, and D. Matosiuk Structural studies, homology modeling and molecular docking of novel non-competitive antagonists of GluK1/GluK2 receptors Bioorg. Med. Chem. 22 2014 787 795
42. Y. Xiao, H. Fan, J.L. Musachio, Z.L. Wei, S.K. Chellappan, A.P. Kozikowski, and K.J. Kellar Sazetidine-A, a novel ligand that desensitizes α4β2 nicotinic acetylcholine receptors without activating them Mol. Pharmacol. 70 2006 1454 1460
43. D. Rayes, M.J. De Rosa, S.M. Sine, and C. Bouzat Number and locations of agonist binding sites required to activate homomeric Cys-loop receptors J. Neurosci. 29 2009 6022 6032
44. S.R. Grady, R.M. Drenan, S.R. Breining, D. Yohannes, C.R. Wageman, N.B. Fedorov, S. McKinney, P. Whiteaker, M. Bencherif, H.A. Lester, and M.J. Marks Structural differences determine the relative selectivity of nicotinic compounds for native α4β2∗-, α6β2∗-, α3β4∗- and α7-nicotine acetylcholine receptors Neuropharmacology 58 2010 1054 1066
45. J. Wu, Q. Liu, K. Yu, J. Hu, Y.P. Kuo, M. Segerberg, P.A. St John, and R.J. Lukas Roles of nicotinic acetylcholine receptor beta subunits in function of human α4-containing nicotinic receptors J. Physiol. 576 2006 103 118
46. C.L. Gentry, L.H. Wilkins Jr., and R.J. Lukas Effects of prolonged nicotinic ligand exposure on function of heterologously expressed, human α4β2- and α4β4-nicotinic acetylcholine receptors J. Pharmacol. Exp. Ther. 304 2003 206 216
47. Y. Xiao, and K.J. Kellar The comparative pharmacology and up-regulation of rat neuronal nicotinic receptor subtype binding sites stably expressed in transfected mammalian cells J. Pharmacol. Exp. Ther. 310 2004 98 107
48. R. Salas, F. Pieri, and M. De Biasi Decreased signs of nicotine withdrawal in mice null for the β4 nicotinic acetylcholine receptor subunit J. Neurosci. 24 2004 10035 10039
49. Y. Liang, R. Salas, L. Marubio, D. Bercovich, M. De Biasi, A.L. Beaudet, and J.A. Dani Functional polymorphisms in the human β4 subunit of nicotinic acetylcholine receptors Neurogenetics 6 2005 37 44
50. H. Rollema, C. Russ, T.C. Lee, R.S. Hurst, and D. Bertrand Functional interactions of varenicline and nicotine with nAChR subtypes implicated in cardiovascular control Nicotine Tob. Res. 1 2014 733 742
51. H.R. Arias, K.M. Targowska-Duda, D. Feuerbach, and K. Jozwiak Mecamylamine inhibits muscle nicotinic acetylcholine receptors by competitive and noncompetitive mechanisms OA Biochemistry 1 2013 7
52. H.R. Arias, P. Bhumireddy, and C. Bouzat Molecular mechanisms and binding site locations for noncompetitive antagonists of nicotinic acetylcholine receptors Int. J. Biochem. Cell Biol. 38 2006 1254 1276
53. S.M. Sine, and A.G. Engel Recent advances in Cys-loop receptor structure and function Nature 440 2006 448 455
54. 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
55. H.R. Arias Positive and negative modulation of nicotinic receptors Adv. Protein Chem. Struct. Biol. 80 2010 153 203
56. H.R. Arias Molecular interactions between ligands and nicotinic acetylcholine receptors revealed by studies with acetylcholine binding proteins J. Thermodynam. Cat. 3 2012 116
57. C. Shi, R. Yu, S. Shao, and Y. Li Partial activation of α7 nicotinic acetylcholine receptors: insights from molecular dynamics simulations J. Mol. Model. 19 2013 871 878
58. 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
59. L.T. Liu, D. Willenbring, Y. Xu, and P. Tang General anesthetic binding to neuronal α4β2 nicotinic acetylcholine receptor and its effects on global dynamics J. Phys. Chem. B 113 2009 12581 12589