Discovery of (2S,3R)-N-[2-(pyridin-3-ylmethyl)-1-azabicyclo[2.2.2]oct-3-yl] benzo[b]furan-2-carboxamide (TC-5619), a selective α7 nicotinic acetylcholine receptor agonist, for the treatment of cognitive disorders

Journal of Medicinal Chemistry

Volumn 55, Issue 22, 2012, Pages 9793-9809

  Mazurov, Anatoly A ^a   Kombo, David C ^a   Hauser, Terry A ^a   Miao, Lan ^a   Dull, Gary ^a   Genus, John F ^a   Fedorov, Nikolai B ^a   Benson, Lisa ^a   Sidach, Serguei ^a   Xiao, Yunde ^a   Hammond, Philip S ^a   James, John W ^a   Miller, Craig H ^a   Yohannes, Daniel ^a  

^a TARGACEPT INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (PYRIDIN 3 YLMETHYL) 1 AZABICYCLO[2.2.2]OCTAN 3 ONE DI 4 TOLUOYL DEXTRO TARTRATE; 2 (PYRIDIN 3 YLMETHYLENE) 1 AZABICYCLO[2.2.2]OCTAN 3 ONE; 3 AMINO 2 (PYRIDIN 3 YLMETHYL) 1 AZABICYCLO[2.2.2] OCTANE; ABT 107; AMIDE; AZD 0328; CLOZAPINE; EVP 6124; N (3 QUINUCLIDINYL)FURO[2,3 C]PYRIDINE 5 CARBOXAMIDE; N [2 (PYRIDIN 3 YLMETHYL) 1 AZABICYCLO(2.2.2)OCT 3 YL]BENZO[B]FURAN 2 CARBOXAMIDE; N [2 (PYRIDIN 3 YLMETHYL) 1 AZABICYCLO[2.2.2]OCT 3 YL]BENZO[B]FURAN 2 CARBOXAMIDE; NICOTINIC AGENT; NICOTINIC RECEPTOR ALPHA4BETA2; PHA 568487; RG 3487; UNCLASSIFIED DRUG;

ADD ON THERAPY; ARTICLE; CENTRAL NERVOUS SYSTEM; CLINICAL TRIAL (TOPIC); COGNITIVE DEFECT; HUMAN; IC 50; MOLECULAR DOCKING; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; RECEPTOR AFFINITY; SCHIZOPHRENIA; SYMPTOM;

ANIMALS; BENZOFURANS; CHO CELLS; COGNITION DISORDERS; CRICETINAE; ETHER-A-GO-GO POTASSIUM CHANNELS; HUMANS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; QUINUCLIDINES; RATS; RECEPTORS, NICOTINIC; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84870006985     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm301048a     Document Type: Article

References (83)

1. Lippiello, P. M.; Bencherif, M.; Hauser, T. A.; Jordan, K. G.; Letchworth, S. R.; Mazurov, A. A. Nicotinic Receptors as Targets for Therapeutic Discovery Expert Opin. Drug Discovery 2007, 2 (9) 1185-1203
2. Law, R. J.; Henchman, R. H.; McCammon, J. A. A gating mechanism proposed from a simulation of a human α7 nicotinic acetylcholine receptor Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 6813-6818
3. Schrattenholz, A.; Coban, T.; Schröder, B.; Okonjo, K. O.; Kuhlmann, J.; Pereira, E. F.; Albuquerque, E. X.; Maelicke, A. Biochemical Characterization of a Novel Channel-Activating Site on Nicotinic Acetylcholine Receptors J. Recept. Res. 1993, 13, 393-412
4. Tomizawa, M.; Maltby, D.; Medzihradszky, K. F.; Zhang, N.; Durkin, K. A.; Presley, J.; Talley, T. T.; Taylor, P.; Burlingame, A. L.; Casida, J. E. Defining Nicotinic Agonist Binding Surfaces through Photoaffinity Labeling Biochemistry 2007, 46, 8798-8806
5. Brejc, K.; van Dijk, W. J.; Klaassen, R. V.; Schuurmans, M.; van Der Oost, J.; Smit, A. B.; Sixma, T. K. Crystal Structure of an ACh-Binding Protein Reveals the Ligand-Binding Domain of Nicotinic Receptors Nature 2001, 411, 269-276
6. Celie, P. H.; van Rossum-Fikkert, S. E.; van Dijk, W. J.; Brejc, K.; Smit, A. B.; Sixma, T. K. Nicotine and carbamylcholine Binding to Nicotinic Acetylcholine Receptors as Studied in AChBP Crystal Structures Neuron 2004, 41, 907-914
7. Hansen, S. B.; Talley, T. T.; Radic, Z.; Taylor, P. Structural and Ligand recognition Characteristics of an Acetylcholine-Binding Protein from Aplysia Californica J. Biol. Chem. 2004, 279, 24197-24202
8. Celie, P. H.; Klaassen, R. V.; van Rossum-Fikkert, S. E.; van Elk, R.; van Nierop, P.; Smit, A. B.; Sixma, T. K. Crystal Structure of Acetylcholine-Binding Protein from Bulinus Truncatus Reveals the Conserved Structural Scaffold and Sites of Variation in Nicotinic Acetylcholine Receptors J. Biol. Chem. 2005, 280, 26457-26466
9. Celie, P. H.; Kasheverov, I. E.; Mordvintsev, D. Y.; Hogg, R. C.; van Nierop, P.; van Elk, R.; van Rossum-Fikkert, S. E.; Zhmak, M. N.; Bertrand, D.; Tsetlin, V.; Sixma, T. K.; Smit, A. B. Crystal Structure of Nicotinic Acetylcholine Receptor Homolog AChBP in Complex with an Alpha-Conotoxin PnIA Variant Nature Struct. Mol. Biol. 2005, 12, 582-588
10. Hansen, S. B.; Sulzenbacher, G.; Huxford, T.; Marchot, P.; Taylor, P.; Bourne, Y. Structures of Aplysia AChBP Complexes with Nicotinic Agonists and Antagonists Reveal Distinctive Binding Interfaces and Conformations EMBO J. 2005, 24, 3635-3646
11. Ulens, C.; Hogg, R. C.; Celie, P. H.; Bertrand, D.; Tsetlin, V.; Smit, A. B.; Sixma, T. K. Structural Determinants of Selective Alpha-Conotoxin Binding to a Nicotinic Acetylcholine Receptor Homolog AChBP Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 3615-3620
12. Dutertre, S.; Ulens, C.; Buttner, R.; Fish, A.; van Elk, R.; Kendel, Y.; Hopping, G.; Alewood, P. F.; Schroeder, C.; Nicke, A.; Smit, A. B.; Sixma, T. K.; Lewis, R. J. AChBP-Targeted Alpha-Conotoxin Correlates Distinct Binding Orientations with nAChR Subtype Selectivity EMBO J. 2007, 26, 3858-3867
13. Nemecz, A.; Taylor, P. Creating an α7 Nicotinic Acetylcholine Recognition Domain from the Acetylcholine-Binding Protein: Crystallographic and Ligand Selectivity Analyses J. Biol. Chem. 2011, 286, 4255-4265
14. Li, S. X.; Huang, S.; Bren, N.; Noridomi, K.; Dellisanti, C. D.; Sine, S. M.; Chen, L. Ligand-Binding Domain of an α7-Nicotinic Receptor Chimera and its Complex with Agonist Nature Neurosci. 2011, 14, 1253-1259
15. Tasso, B.; Canu Boido, C.; Terranova, E.; Gotti, C.; Riganti, L.; Clementi, F.; Artali, R.; Bombieri, G.; Meneghetti, F.; Sparatore, F. Synthesis, Binding, and Modeling Studies of New Cytisine Derivatives, as Ligands for Neuronal Nicotinic Acetylcholine Receptor Subtypes J. Med. Chem. 2009, 52, 4345-4357
16. 3H] Epibatidine Photolabels Nonequivalent Amino Acids in the Agonist Binding Site of Torpedo and α4β2 Nicotinic Acetylcholine Receptors J. Biol. Chem. 2009, 284, 24939-24947
17. Bisson, W. H; Scapozza, L.; Westera, G.; Mu, L.; Schubiger, P. A. Ligand Selectivity for the Acetylcholine Binding Site of the Rat α4β2 and α3β4 Nicotinic Subtypes Investigated by Molecular Docking J. Med. Chem. 2005, 48, 5123-5130
18. Huang, X.; Zheng, F.; Stokes, C.; Papke, R. L.; Zhan, C.-G. Modeling Binding Modes of R7 Nicotinic Acetylcholine Receptor with Ligands: The Roles of Gln117 and Other Residues of the Receptor in Agonist Binding J. Med. Chem. 2008, 51, 6293-6302
19. 2+-Binding Sites Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 3210-3215
20. Huang, X.; Zheng, F.; Chen, X.; Crooks, P. A.; Dwoskin, L. P.; Zhan, C.-G. Modeling Subtype-Selective Agonists Binding with α4β2 and α7 Nicotinic Acetylcholine Receptors: Effects of Local Binding and Long-Range Electrostatic Interactions J. Med. Chem. 2006, 49, 7661-7674
21. Bisson, W. H.; Westera, G.; Schubiger, P. A.; Scapozza, L. Homology Modeling and Dynamics of the Extracellular Domain of Rat and Human Neuronal Nicotinic Acetylcholine Receptor Subtypes α4β2 and α7 J. Mol. Model. 2008, 14, 891-899
22. Taly, A.; Corringer, P.-J.; Guedin, D.; Lestage, P.; Changeux, J. P. Nicotinic Receptors: Allosteric Transitions and Therapeutic Targets in the Nervous System Nature Rev. 2009, 8, 733-750
23. Guandalini, L.; Martini, E.; Dei, S.; Manetti, D.; Scapecchi, S.; Teodori, E.; Romanelli, M. N; Varani, K.; Greco, G.; Spadola, L.; Novellino, E. Design of Novel Nicotinic Ligands through 3D Database Searching Bioorg. Med. Chem. 2005, 13, 799-807
24. Nicolotti, O.; Pellegrini-Calace, M.; Carrie, A.; Altomare, C.; Centeno, N. B.; Sanz, F.; Carottia, A. Neuronal Nicotinic Receptor Agonists: a Multi-Approach Development of the Pharmacophore J. Comput.-Aided Mol. Des. 2001, 15, 859-872
25. Erratum in: J. Comput.-Aided Mol. Des. 2001, 15, 1153.
26. Beers, W. H.; Reich, E. Structure and Activity of Acetylcholine Nature 1970, 228, 917-922
27. Sheridan, R. P.; Nilakantan, R.; Dixon, J. S.; Venkataraghavan, R. J. The Ensemble Approach to Distance Geometry: Application to the Nicotinic Pharmacophore J. Med. Chem. 1986, 29, 899-906
28. Nicolotti, O.; Pellegrini-Calace, M.; Carrieri, A.; Altomare, C.; Centeno, N. B.; Sanz, F.; Carotti, A. Neuronal nicotinic Receptor Agonists: a Multi-Approach Development of the Pharmacophore J. Comput.-Aided Mol. Des. 2001, 15, 859-872
29. Marks, M. J.; Collins, A. C. Characterization of nicotine binding in mouse brain and comparison with the binding of alpha-bungarotoxin and quinuclidinyl benzilate Mol. Pharmacol. 1982, 3, 554-564
30. Freedman, R.; Hall, M.; Adler, L. E.; Leonard, S. Evidence in Post-Mortem Brain Tissue for Decreased Numbers of Hippocampal Nicotinic Receptors in Schizophrenia Biol. Psychiatry 1995, 38, 22-33
31. Bertrand, D.; Gopalakrishnan, M. Allosteric modulation of nicotinic acetylcholine receptors Biochem. Pharmacol. 2007, 74, 1155-1163
32. Freedman, R.; Coon, H.; Myles-Worsley, M.; Orr-Urtreger, A.; Olincy, A.; Davis, A.; Polymeropoulos, M.; Holil, J.; Hopkins, J.; Hoff, M.; Rosenthal, J.; Waldo, M. C.; Reimherr, F.; Wender, P.; Yaw, J.; Young, D. A.; Breese, C. R.; Adams, C.; Patterson, D.; Adler, L. E.; Kruglyak, L.; Leonard, S.; Byerley, W. Linkage of a Neurophysiological Deficit in Schizophrenia to a Chromosome 15 Locus Proc. Natl. Acad. Sci.U. S. A. 1997, 94, 587-592
33. 3 Receptors Expressed in Xenopus Oocytes Neurosci. Lett. 1998, 247, 107-110
34. Karlin, A.; Akabas, M. H. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins Neuron 1995, 15, 1231-1244
35. Phillips, E.; Mack, R.; Macor, J.; Semus, S. Novel Spiroazabicyclic Heterocyclic Compounds. WO Patent 9903859, 1999.
36. 3 Receptor Bioorg. Med. Chem. Lett. 2005, 15, 4727-4730
37. 3 Antagonist Tropisetron (ICS 205-930) is a Potent and Selective α7 Nicotinic Receptor Partial Agonist Bioorg. Med. Chem. Lett. 2001, 11, 319-321
38. 3 Receptors Curr. Pharm. Des. 2006, 12, 3615-3630
39. 3 Receptors with Arylpiperazine, Tropane, and Quinuclidine Ligands Curr. Top. Med. Chem 2002, 2, 599-624
40. Romanelli, M. N.; Gratteri, L.; Guandalini, L.; Martini, E.; Bonaccini, C.; Gualtieri, F. Central Nicotinic Receptors: Structure, Function, Ligands, and Therapeutic Potential ChemMedChem. 2007, 2, 2-24
41. Dolasetron (Anzemet) Product Information; Aventis: Bridgewater, NJ, February 2002.
42. Granisetron (Kytril) Product Information; Roche: Basel, August 2002.
43. Ondansetron (Zofran) Product Information; GlaxoSmithKline: Research Triangle Park, NC, May 2001.
44. Lisi, D. M. Lotronex Withdrawal Arch. Intern. Med. 2002, 162, 101
45. Mazurov, A. A; Speake, J. D.; Yohannes, D. Discovery and Development of α7 Nicotinic Acetylcholine Receptor Modulators J. Med. Chem. 2011, 54, 7943-7961
46. Wishka, D. G.; Walker, D. P.; Yates, K. M.; Reitz, S. C.; Jia, S.; Myers, J. K.; Olson, K. I.; Jacobsen, E. J.; Wolfe, M. L.; Groppi, V. E.; Hanchar, A. J.; Thornburgh, B. A.; Cortes, B.; Luz, A.; Wong, E. H. F.; Staton, B. A.; Raub, T. J.; Higdon, N. R.; Wall, T. M.; Hurst, R. S.; Walters, R. R.; Hoffmann, W. E.; Hajos, M.; Franklin, S.; Carey, G.; Gold, L. H.; Cook, K. K.; Sands, S. B.; Zhao, S. X.; Soglia, J. R.; Kalgutkar, A. S.; Arneric, S. P.; Rogers, B. N. Discovery of N -[(3 R)-1-Azabicyclo-[2.2.2]oct-3-yl]furo[2,3- c ]pyridine-5-carboxamide, an Agonist of the α7 Nicotinic Acetylcholine Receptor, for the Potential Treatment of Cognitive Deficits in Schizophrenia: Synthesis and Structure-Activity Relationship J. Med. Chem. 2006, 49, 4425-4436
47. Wall, T. M.; Hurst, R. S.; Wong, E. H. F.; Rogers, B. N. Design, Synthesis, Structure-Activity Relationship, and in Vivo Activity of Azabicyclic Aryl Amides as α7 Nicotinic Acetylcholine Receptor Agonists Bioorg. Med. Chem. 2006, 14, 8219-8248
48. Malysz, J.; Anderson, D. J.; Grønlien, J. H.; Ji, J.; Bunnelle, W. H.; Håkerud, M.; Thorin-Hagene, K.; Ween, H.; Helfrich, R.; Hu, M.; Gubbins, E.; Gopalakrishnan, S.; Puttfarcken, P. S.; Briggs, C. A.; Li, J.; Meyer, M. D.; Dyhring, T.; Ahring, P. K.; Nielsen, E. Ø.; Peters, D.; Timmermann, D. B.; Gopalakrishnan, M. In Vitro Pharmacological Characterization of a Novel Selective α7 Neuronal Nicotinic Acetylcholine Receptor Agonist ABT-107 J. Pharm. Exp. Ther. 2010, 334, 863-874
49. Sydserff, S.; Sutton, E. J.; Song, D.; Quirk, M. C.; Maciag, C.; Li, C.; Gerald Jonak, G.; Gurley, D.; Gordon, J. C.; Christian, E. P.; Doherty, J. J.; Hudzik, T.; Johnson, E.; Mrzljak, L.; Piser, T.; Smagin, G. N.; Wang, Y.; Widzowski, D.; Smith, J. S. Selective α7 Nicotinic Receptor Activation by AZD0328 Enhances Cortical Dopamine Release and Improves Learning and Attentional Processes Biochem. Pharmacol. 2009, 78, 880-888
50. Mazurov, A.; Hauser, T.; Miller, C. H. Selective α7 Nicotinic Acetylcholine Receptor Ligands Curr. Med. Chem. 2006, 13, 1567-1584
51. Langlois, M.; Meyer, C.; Soulier, J. L. Synthesis of (R)- and (S)-3-Aminoquinuclidinone from 3-Quinuclidine and (S)- and (R)-1-Phenethylamine Synth. Commun. 1992, 22, 1895-1911
52. Wong, E.; Cortes-Burgos, L. A.; Rogers, B. N.; Piotrowski, D. W.; Walker, D. P.; Jacobsen, E. J.; Wishka, D. G.; Acker, B. A. Compounds Having both α7 Nicotinic Agonist Activity and 5HT3 Antagonist Activity for Treatment of CNS Diseases. WO Patent 04039815, 2004.
53. Dwoskin, L. P.; Xu, R.; Ayers, J. T.; Crooks, P. A. Recent Developments in Neuronal Nicotinic Acetylcholine Receptor Antagonists Exp. Opin. Ther. Pat. 2000, 10, 1561-1581
54. Jacobsen, E. J.; Walker, D. P.; Myers, J. K.; Piotrowski, D. W.; Groppi, V. E. Substituted 2-Azabicyclic Moieties for the Treatment of Disease (Nicotinic Acetylcholine Receptor Antagonists). PCT WO 02/085901, 2002.
55. Mazurov, A, A.; Klucik, J.; Miao, L.; Phillips, T. Y.; Seamans, A.; Schmitt, J. D.; Hauser, T. A.; Johnson, R. T.; Miller, C. 2-(Arylmethy)l-3- Substituted Quinuclidines as Selective α7 Nicotinic Receptor Ligands Bioorg. Med. Chem. Lett. 2005, 15, 2073-2077
56. O'Donnell, C. J.; Rogers, B. N.; Bronk, B. S.; Bryce, D. K.; Coe, J. W.; Cook, K. K.; Duplantier, A. J.; Evrard, E.; Hajós, M.; Hoffmann, W. E.; Hurst, R. S.; Maklad, N.; Mather, R. J.; McLean, S.; Nedza, F. M.; O'Neill, B. T.; Peng, L.; Qian, W.; Rottas, M. M.; Sands, S. B.; Schmidt, A. W.; Shrikhande, A. V.; Spracklin, D. K.; Wong, D. F.; Zhang, A.; Zhang, L. Discovery of 4-(5-Methyloxazolo[4,5- b ]pyridin-2-yl)-1,4-diazabicyclo[3.2.2]nonane (CP-810,123), a Novel α7 Nicotinic Acetylcholine Receptor Agonist for the Treatment of Cognitive Disorders in Schizophrenia: Synthesis, SAR Development, and in Vivo Efficacy in Cognition Models J. Med. Chem. 2010, 53, 1222-1237
57. Callahan, P. M.; Wang, S.; Xie, W.; Dragan, S.; Sun, S.; Michael, T.; Herbert, B.; Rowe, W.; Tehim, A.; Lowe, D.; Barrett, J. E. Pharmacological Characterization of MEM-3454, a Novel Nicotinic Alpha7 Receptor Partial Agonist. Therapeutic Potential for the Cognitive Deficits Associated with Alzheimer's Disease and Schizophrenia Neuropsychopharmacology 2006, 31, S198
58. Kalgutkar, A. S.; Gardner, I.; Obach, R. S.; Shaffer, C. I.; Callegari, E.; Henne, K.; Mutlib, A.; Dalvie, D.; Lee, J.; Nakai, Y.; O'Donell, J.; Boer, J.; Harriman, S. A. Comprehensive Listing of Bioactivation Pathways of Organic Functional Groups Curr. Drug Metab. 2005, 6, 161-225
59. Deepak, K. D.; Kalgutkar, A. S.; Khojasteh-Bakht, S. C.; Obach, R. S.; O'Donell, J. P. Biotransformation Reactions of Five-Membered Aromatic Heterocyclic Rings Chem. Res. Toxicol. 2002, 15, 269-299
60. Hauser, T. A.; Kucinski, A.; Jordan, K. G.; Gatto, G. J.; Wersinger, S. R.; Hesse, R. A.; Stachowiak, E. K.; Stachowiak, M. K.; Papke, R. L.; Lippiello, P. M.; Bencherif, M. TC-5619: An Alpha7 Neuronal Nicotinic Receptor-Selective Agonist that Demonstrates Efficacy in Animal Models of the Positive and Negative Symptoms and Cognitive Dysfunction of Schizophrenia Biochem. Pharmacol. 2009, 78, 803-812
61. Tcheremissine, O. V.; Castro, M. A.; Dineen, R; Gardne, D. R. Targeting cognitive deficits in schizophrenia: a review of the development of a new class of medicines from the perspective of community mental health researchers Exp. Opin. Invest. Drugs 2012, 21, 7-14
62. Dunbar, G.; Hosford, D.; Segreti, A.; Lieberman, J. Effects of alpha7 nicotinic receptor agonist TC-5619 in cognitive dysfunction in schizophrenia Eur. Neuropsychopharmacology 2011, 21, S522
63. Prickaerts, J.; van Goethem, N. P.; Chesworth, R.; Shapiro, G.; Boess, F. G.; Methfessel, C.; Reneerkens, O. A. H.; Flood, D. G.; Hilt, D.; Gawryl, M.; Bertrand, S.; Bertrand, D.; König, G. EVP-6124, a Novel and Selective α7 Nicotinic Acetylcholine Receptor Partial Agonist, Improves Memory Performance by Potentiating the Acetylcholine Response of α7 Nicotinic Acetylcholine Receptors Neuropharmacology 2012, 62, 1099-1110
64. Biton, B.; Bergis, O.; Galli, F.; Nedelec, A.; Lochead, A.; Jegham, S.; Godet, D.; Laneau, C.; Santamaria, R.; Chesney, F.; Leonardon, J.; Granger, P.; Debono, M. W.; Bohme, G. A.; Sgard, F.; Besnard, F.; Graham, D.; Coste, A.; Oblin, A.; Curet, O.; Vige, X.; Voltz, C.; Rouquie, L.; Souilhac, J.; Santucci, V.; Gueudet, C.; Francon, D.; Steinberg, R.; Griebel, G.; Oury-Donat, F.; George, P.; Avenet, P.; Scatton, B. SSR180711, a novel selective α7 nicotinic receptor partial agonist: (1) binding and functional profile Neuropsychopharmacology 2007, 32, 1-16
65. Wallace, T. L.; Callahan, P. M.; Tehim, A.; Bertrand, D.; Tombaugh, G.; Wang, S.; Xie, W.; Rowe, W. B.; Ong, V.; Graham, E.; Terry, A. V., Jr.; Rodefer, J.; Herbert, B.; Murray, M.; Porter, R.; Santarelli, L.; Lowe, D. A. RG3487, a novel nicotinic α7 receptor partial agonist, improves cognition and sensorimotor gating in rodents J. Pharmacol. Exp. Ther. 2011, 336 (1) 242-253
66. Celie, P. H. N.; Rossum-Fikkert, S. E.; Dijk, W. J.; Brejc, K.; Smit, A. B.; Sixma, T. K. Nicotine and Carbamylcholine Binding to Nicotinic Acetylcholine Receptors as Studied in AChBP Crystal Structures Neuron 2004, 41, 907-914
67. Jeffrey, G. A. An Introduction to Hydrogen Bonding (Topics in Physical Chemistry); Oxford University Press: New York, 1997.
68. Beene, D. L.; Brandt, G. S.; Zhong, W.; Zacharias, N. M.; Lester, H. A.; Dougherty, D. A. Cation-π Interactions in Ligand Recognition by Serotonergic (5-HT3A) and Nicotinic Acetylcholine Receptors: The Anomalous Binding Properties of Nicotine Biochemistry 2002, 41, 10262-10269
69. Xiu, X.; Puskar, N. L.; Shanata, J. A. P.; Lester, H. A.; Dougherty, D. A. Nicotine Binding to Brain Receptors Requires a Strong Cation-π Interaction Nature 2009, 458, 534-537
70. Legendre, L. Numerical Ecology; Elsevier: Amsterdam, 1998; pp 319-321.
71. 3H]methyllycaconitine: A New Radioligand for Labelling of Alpha 7-Type Neuronal Nicotinic Acetylcholine Receptors Neuropharmacology 1999, 38, 679-690
72. Hauser, T. A.; Hepler, C. D.; Kombo, D. C.; Grinevich, V. P.; Kiser, M. N.; Hooker, D. N.; Zhang, J.; Mountfort, D.; Selwood, A.; Akireddy, S. R.; Letchworth, S. R.; Yohannes, D. Comparison of Acetylcholine Receptor Interactions of the Marine Toxins, 13-Desmethylspirolide C and Gymnodimine Neuropharmacology 2012, 62, 2238-2249
73. Bencherif, M.; Schmitt, J. D.; Bhatti, B. S.; Crooks, P.; Caldwell, W. S.; Lovette, M. E.; Fowler, K.; Reeves, L.; Lippiello, P. M. The Heterocyclic Substituted Pyridine Derivative (±)-2-(3-Pyridinyl-1)-1-azabicyclo[2.2.2] octane (RJR-2429): A Selective Ligand at Nicotinic Acetylcholine Receptors J. Pharmacol. Exp. Ther. 1998, 284, 886-894
74. Placzek, A. N.; Grassi, F.; Meyer, E. M.; Papke, R. L. An α7 Nicotinic Acetylcholine Receptor Gain-of-Function Mutant That Retains Pharmacological Fidelity Mol. Pharmacol. 2005, 68, 1863-1876
75. Hooft, R. W. W.; Straver, L. H.; Spek, A. L. Determination of Absolute Structure Using Bayesian Statistics on Bijvoet Differences J. Appl. Crystallogr. 2008, 41, 96-103
76. Biology Workbench 3.2; San Diego Supercomputer Center, UCSD: San Diego, CA.
77. Eswar, N.; Marti-Renom, M. A.; Webb, B.; Madhusudhan, M. S.; Eramian, D.; Shen, M.; Pieper, U.; Sali, A. Comparative Protein Structure Modeling With MODELLER. In Current Protocols in Bioinformatics; John Wiley & Sons, Inc.: New York, 2006; Supplement 15) 5.6.1-5.6.30, 200.
78. Marti-Renom, M. A.; Stuart, A.; Fiser, A.; Sánchez, R.; Melo, F.; Sali, A. Comparative Protein Structure Modeling of Genes and Genomes Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325
79. MODELER; Accelrys, Inc: San Diego, CA, USA.
80. Maestro; Schrodinger, Inc.: 101 SW Main Street, Suite 1300, Portland, OR 97204.
81. Kombo, D. C.; Mazurov, A. A.; Tallapragada, K.; Hammond, P. S.; Chewning, J.; Hauser, T. A.; Vasquez-Valdivieso, M.; Yohannes, D.; Talley, T. T.; Taylor, P.; Caldwell, W. S. Computational Studies of Benzylidene Anabaseine Interactions with α7 Nicotinic Acetylcholine Receptor (nAChR) and Acetylcholine Binding Proteins (AChBPs): Application to the Design of Related α7 Selective Ligands Eur. J. Med. Chem. 2011, 46, 5625-5635
82. Friesner, R. A.; Banks, J. L.; Murphy, R. B.; Halgren, T. A.; Klicic, J. J.; Mainz, D. T.; Repasky, M. P.; Knoll, E. H.; Mee, S.; Perry, J. K.; Shaw, D. E.; Francis, P.; Shenkin, P. S. Glide: a New Approach for Rapid, Accurate Docking and Scoring. 1. Method and Assessment of Docking Accuracy J. Med. Chem. 2004, 47, 1739-1749
83. Halgren, T. A.; Murphy, R. B.; Friesner, R. A.; Beard, H. S.; Frye, L. L.; Pollard, W. T.; Banks, J. L. Glide: a New Approach for Rapid, Accurate Docking and Scoring. 2. Enrichment Factors in Database Screening J. Med. Chem. 2004, 47, 1750-1759