Allosteric modulation of muscarinic acetylcholine receptors

Pharmaceuticals

Volumn 3, Issue 9, 2010, Pages 2838-2860

  Jakubík, Jan ^a   El Fakahany, Esam E ^b  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Allosteric modulation; Alzheimer's disease; Muscarinic acetylcholine receptors; Schizophrenia

Indexed keywords

17ALPHA ETHYNYL 17BETA HYDROXY 5ALPHA ANDROSTANO[3,2 B]PYRIMIDO[1,2 A]BENZIMIDAZOLE; 4 AMINOPYRIDINE; AC 260584; AC 42; ACETYLCHOLINE; ALCURONIUM; BENZYLQUINOLINE CARBOXYLIC ACID; BRUCINE; CARACURINE V; GALLAMINE; KT 5720; KT 5823; LY 2033298; MUSCARINIC AGENT; MUSCARINIC RECEPTOR; MUSCARINIC RECEPTOR BLOCKING AGENT; NEUROLEPTIC AGENT; NEUROMUSCULAR BLOCKING AGENT; NORCLOZAPINE; OBIDOXIME; PANCURONIUM; RAPACURONIUM BROMIDE; STAUROSPORINE; STRYCHNINE; TOXIFERINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERAPAMIL; VU 0010010; VU 0090157; WIN 62577;

ALLOSTERISM; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; BINDING AFFINITY; BINDING SITE; BRONCHOSPASM; CHOLINERGIC TRANSMISSION; CLINICAL TRIAL; CONFORMATIONAL TRANSITION; DRUG BIOAVAILABILITY; DRUG COMPETITION; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG RESEARCH; DRUG SELECTIVITY; DRUG STRUCTURE; HUMAN; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVIEW; SCHIZOPHRENIA;

EID: 77957282651     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph3092838     Document Type: Review

References (91)

1. Dale, H.H. The action of certain esters and ethers of choline and their relation to muscarine. J. Pharmacol. 1914, 6, 147-190.
2. Loewi, O. Über humorale Übertragbarkeit der Herznervenwirkung. I. Pflügers Archiv. 1921, 189, 239-242.
3. Bonner, T.I.; Buckley, N.J.; Young, A.C.; Brann, M.R. Identification of a family of muscarinic acetylcholine receptor genes. Science 1987, 237, 527-532.
4. Caulfield, M.P. Muscarinic receptors--characterization, coupling and function. Pharmacol. Ther. 1993, 58, 319-379.
5. Levey, A.I. Immunological localization of m1-m5 muscarinic acetylcholine receptors in peripheral tissues and brain. Life Sci. 1993, 52, 441-448.
6. Felder, C.C.; Porter, A.C.; Skillman, T.L.; Zhang, L.; Bymaster, F.P.; Nathanson, N.M.; Hamilton, S.E.; Gomeza, J.; Wess, J.; McKinzie, D.L. Elucidating the role of muscarinic receptors in psychosis. Life Sci. 2001, 68, 2605-2613.
7. Langmead, C.J.; Watson, J.; Reavill, C. Muscarinic acetylcholine receptors as CNS drug targets. Pharmacol. Ther. 2008, 117, 232-243.
8. Brito, G.N.; Davis, B.J.; Stopp, L.C.; Stanton, M.E. Memory and the septo-hippocampal cholinergic system in the rat. Psychopharmacology (Berl) 1983, 81, 315-320.
9. Meck, W.H.; Church, R.M.; Wenk, G.L.; Olton, D.S. Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory. J. Neurosci. 1987, 7, 3505-3511.
10. Christie, J.E.; Shering, A.; Ferguson, J.; Glen, A.I. Physostigmine and arecoline, effects of intravenous infusions in Alzheimer presenile dementia. Br. J. Psychiatry. 1981, 138, 46-50.
11. Bymaster, F.P.; McKinzie, D.L.; Felder, C.C.; Wess, J. Use of M1-M5 muscarinic receptor knockout mice as novel tools to delineate the physiological roles of the muscarinic cholinergic system. Neurochem. Res. 2003, 28, 437-442.
12. Wess, J.; Eglen, R.M.; Gautam, D. Muscarinic acetylcholine receptors, mutant mice provide new insights for drug development. Nat. Rev. Drug Discov. 2007, 6, 721-733.
13. Caccamo, A.; Oddo, S.; Billings, L.M.; Green, K.N.; Martinez-Coria, H.; Fisher, A.; LaFerla, F.M. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 2006, 49, 671-682.
14. Jones, C.K.; Brady, A.E.; Davis, A.A.; Xiang, Z.; Bubser, M.; Tantawy, M.N.; Kane, A.S.; Bridges, T.M.; Kennedy, J.P.; Bradley, S.R.; Peterson, T.E.; Ansari, M.S.; Baldwin, R.M.; Kessler, R.M.; Deutch, A.Y.; Lah, J.J.; Levey, A.I.; Lindsley, C.W.; Conn, P.J. Novel selective allosteric activator of the M1 muscarinic acetylcholine receptor regulates amyloid processing and produces antipsychotic-like activity in rats. J. Neurosci. 2008, 28, 10422-10433.
15. Perry E.K.; Kilford L.; Lees A.J.; Burn D.J.; Perry R.H. Increased Alzheimer pathology in Parkinson's disease related to antimuscarinic drugs. Ann. Neurol. 2003, 54, 235-238.
16. Machová, E.; Jakubík, J.; Michal, P.; Oksman, M.; Iivonen, H.; Tanila, H.; Doležal, V. Impairment of muscarinic transmission in transgenic APPswe/PS1dE9 mice. Neurobiol. Aging 2008, 29, 368-378.
17. Machová, E.; Rudajev, V.; Smycková, H.; Koivisto, H.; Tanila, H.; Dolezal, V. Functional cholinergic damage develops with amyloid accumulation in young adult APPswe/PS1dE9 transgenic mice. Neurobiol. Dis. 2010, 38, 27-35.
18. Biel, J.H.; Nuhfer, P.A.; Hoya, W.K.; Leiser, H.A.; Abood, L.G. Cholinergic blockade as an approach to the development of new psychotropic agents. Ann. N. Y. Acad. Sci. 1962, 96, 251-262.
19. Mego, D.M.; Omori, J.M.; Hanley, J.F. Transdermal scopolamine as a cause of transient psychosis in two elderly patients. South. Med. J. 1988, 81, 394-395.
20. Dean, B.; Crook, J.M.; Opeskin, K.; Hill, C.; Keks, N.; Copolov, D.L. The density of muscarinic M1 receptors is decreased in the caudate-putamen of subjects with schizophrenia. Mol. Psychiatry 1996, 1, 54-58.
21. Dean, B.; Crook, J.M.; Pavey, G.; Opeskin, K.; Copolov, D.L. Muscarinic1 and 2 receptor mRNA in the human caudate-putamen, no change in m1 mRNA in schizophrenia. Mol. Psychiatry 2000, 5, 203-207.
22. Crook, J.M.; Dean, B.; Pavey, G.; Copolov, D. The binding of [3H]AF-DX 384 is reduced in the caudate-putamen of subjects with schizophrenia. Life Sci. 1999, 64, 1761-1771.
23. Crook, J.M.; Tomaskovic-Crook, E.; Copolov, D.L.; Dean, B. Decreased muscarinic receptor binding in subjects with schizophrenia, a study of the human hippocampal formation. Biol. Psychiatry 2000, 48, 381-388.
24. Crook, J.M.; Tomaskovic-Crook, E.; Copolov, D.L.; Dean, B. Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia, a study of Brodmann's areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. Am. J. Psychiatry 2001, 158, 918-925.
25. Raedler, T.J.; Bymaster, F.P.; Tandon, R.; Copolov, D.; Dean, B. Towards a muscarinic hypothesis of schizophrenia. Mol. Psychiatry 2007, 12, 232-246.
26. Tzavara, E.T.; Bymaster, F.P.; Davis, R.J.; Wade, M.R.; Perry, K.W.; Wess, J.; McKinzie, D.L.; Felder, C.; Nomikos, G.G. M4 muscarinic receptors regulate the dynamics of cholinergic and dopaminergic neurotransmission, relevance to the pathophysiology and treatment of related CNS pathologies. FASEB J. 2004, 18, 1410-1412.
27. Kenakin, T. Allosteric agonist modulators. J. Recept. Signal. Transduct. Res. 2007, 27, 247-259.
28. Clark, A.L.; Mitchelson, F. The inhibitory effect of gallamine on muscarinic receptors. Br. J. Pharmacol. 1976, 58, 323-331.
29. Stockton J.M.; Birdsall N.J.; Burgen A.S.; Hulme E.C. Modification of the binding properties of muscarinic receptors by gallamine. Mol. Pharmacol. 1983, 23, 551-557.
30. Nedoma, J.; Dorofeeva, N.A.; Tuček, S.; Shelkovnikov, S.A.; Danilov, A.F. Interaction of the neuromuscular blocking drugs alcuronium, decamethonium, gallamine, pancuronium, ritebronium, tercuronium and d-tubocurarine with muscarinic acetylcholine receptors in the heart and ileum. Naunyn Schmiedebergs Arch. Pharmacol. 1985, 329, 176-181.
31. Nedoma, J.; Tucek, S.; Danilov, A.F.; Shelkovnikov, S.A. Stabilization of antagonist binding to cardiac muscarinic acetylcholine receptors by gallamine and other neuromuscular blocking drugs. J. Pharmacol. Exp. Ther. 1986, 236, 219-223.
32. Waelbroeck, M.; Robberecht, P.; De Neef, P.; Christophe, J. Effects of verapamil on the binding properties of rat heart muscarinic receptors, evidence for an allosteric site. Biochem. Biophys. Res. Commun. 1984, 121, 340-345.
33. Lai, W.S.; Ramkumar, V.; el-Fakahany, E.E. Possible allosteric interaction of 4-aminopyridine with rat brain muscarinic acetylcholine receptors. J. Neurochem. 1985, 44, 1936-1942.
34. Kloog, Y.; Sokolovsky, M. Allosteric interactions between muscarinic agonist binding sites and effector sites demonstrated by the use of bisquaternary pyridinium oximes. Life Sci. 1985, 36, 2127-2136.
35. Flynn, D.D.; Mash, D.C. Multiple in vitro interactions with and differential in vivo regulation of muscarinic receptor subtypes by tetrahydroaminoacridine. J. Pharmacol. Exp. Ther. 1989, 250, 573-581.
36. Jooste, E.; Klafter, F.; Hirshman, C.A.; Emala, C.W. A mechanism for rapacuronium-induced bronchospasm, M2 muscarinic receptor antagonism. Anesthesiology 2003, 98, 906-911.
37. Hu, J.; el-Fakahany, E.E. Allosteric interaction of dynorphin and myelin basic protein with muscarinic receptors. Pharmacology 1993, 47, 351-359.
38. Dalton, D.W.; Tyers, M.B. A comparison of the muscarinic antagonist actions of pancuronium and alcuronium. J. Auton. Pharmacol. 1982, 2, 261-266.
39. Jakubík, J.; Bacáková, L.; El-Fakahany, E.E.; Tuček, S. Positive cooperativity of acetylcholine and other agonists with allosteric ligands on muscarinic acetylcholine receptors. Mol. Pharmacol. 1997, 52, 172-179.
40. Lazareno, S.; Popham, A.; Birdsall, N.J. Allosteric interactions of staurosporine and other indolocarbazoles with N-[methyl-(3)H]scopolamine and acetylcholine at muscarinic receptor subtypes, identification of a second allosteric site. Mol. Pharmacol. 2000, 58, 194-207.
41. Lazareno, S.; Doležal, V.; Popham, A.; Birdsall, N.J.M. Thiochrome enhances acetylcholine affinity at muscarinic M4 receptors, receptor subtype selectivity via cooperativity rather than affinity. Mol. Pharmacol. 2004, 65, 257-266.
42. Zlotos, D.P.; Buller, S.; Stiefl, N.; Baumann, K.; Mohr, K. Probing the pharmacophore for allosteric ligands of muscarinic M2 receptors, SAR and QSAR studies in a series of bisquaternary salts of caracurine V and related ring systems. J. Med. Chem. 2004, 47, 3561-3571.
43. Proška, J.; Tuček, S. Mechanisms of steric and cooperative actions of alcuronium on cardiac muscarinic acetylcholine receptors. Mol. Pharmacol. 1994, 45, 709-717.
44. Ellis, J.; Huyler, J.; Brann, M.R. Allosteric regulation of cloned m1-m5 muscarinic receptor subtypes. Biochem. Pharmacol. 1991, 42, 1927-1932.
45. Jakubík, J.; Bacáková, L.; el-Fakahany, E.E.; Tuček, S. Subtype selectivity of the positive allosteric action of alcuronium at cloned M1-M5 muscarinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 1995, 274, 1077-1083.
46. Leppik, R.A.; Miller, R.C.; Eck, M.; Paquet, J.L. Role of acidic amino acids in the allosteric modulation by gallamine of antagonist binding at the m2 muscarinic acetylcholine receptor. Mol. Pharmacol. 1994, 45, 983-990.
47. Krejcí, A.; Tuček, S. Changes of cooperativity between N-methylscopolamine and allosteric modulators alcuronium and gallamine induced by mutations of external loops of muscarinic M(3) receptors. Mol. Pharmacol. 2001, 60, 761-767.
48. Huang, X.; Prilla, S.; Mohr, K.; Ellis, J. Critical amino acid residues of the common allosteric site on the M2 muscarinic acetylcholine receptor, more similarities than differences between the structurally divergent agents gallamine and bis(ammonio)alkane-type hexamethylene-bis- [dimethyl-(3-phtha)]. Mol. Pharmacol. 2005, 68, 769-778.
49. Matsui, H.; Lazareno, S.; Birdsall, N.J. Probing of the location of the allosteric site on m1 muscarinic receptors by site-directed mutagenesis. Mol. Pharmacol. 1995, 47, 88-98.
50. Jakubík, J.; Krejcí, A.; Doležal, V. Asparagine, valine, and threonine in the third extracellular loop of muscarinic receptor have essential roles in the positive cooperativity of strychnine-like allosteric modulators. J. Pharmacol. Exp. Ther. 2005, 313, 688-696.
51. Voigtländer, U.; Jöhren, K.; Mohr, M.; Raasch, A.; Tränkle, C.; Buller, S.; Ellis, J.; Höltje, H.; Mohr, K. Allosteric site on muscarinic acetylcholine receptors, identification of two amino acids in the muscarinic M2 receptor that account entirely for the M2/M5 subtype selectivities of some structurally diverse allosteric ligands in N-methylscopolamine-occupie. Mol. Pharmacol. 2003, 64, 21-31.
52. Prilla, S.; Schrobang, J.; Ellis, J.; Höltje, H.; Mohr, K. Allosteric interactions with muscarinic acetylcholine receptors, complex role of the conserved tryptophan M2422Trp in a critical cluster of amino acids for baseline affinity, subtype selectivity, and cooperativity. Mol. Pharmacol. 2006, 70, 181-193.
53. Tränkle, C.; Dittmann, A.; Schulz, U.; Weyand, O.; Buller, S.; Jöhren, K.; Heller, E.; Birdsall, N.J.M.; Holzgrabe, U.; Ellis, J.; Höltje, H.D.; Mohr, K. Atypical muscarinic allosteric modulation, cooperativity between modulators and their atypical binding topology in muscarinic M2 and M2/M5 chimeric receptors. Mol. Pharmacol. 2005, 68, 1597-1610.
54. Lazareno, S.; Popham, A.; Birdsall, N.J.M. Analogs of WIN 62,577 define a second allosteric site on muscarinic receptors. Mol. Pharmacol. 2002, 62, 1492-1505.
55. Lanzafame, A.A.; Sexton, P.M.; Christopoulos, A. Interaction studies of multiple binding sites on m4 muscarinic acetylcholine receptors. Mol. Pharmacol. 2006, 70, 736-746.
56. Tränkle, C.; Mies-Klomfass, E.; Cid, M.H.; Holzgrabe, U.; Mohr, K. Identification of a [3H]Ligand for the common allosteric site of muscarinic acetylcholine M2 receptors. Mol. Pharmacol. 1998, 54, 139-145.
57. Lysíková, M.; Fuksová, K.; Elbert, T.; Jakubík, J.; Tuček, S. Subtype-selective inhibition of [methyl-3H]-N-methylscopolamine binding to muscarinic receptors by alpha-truxillic acid esters. Br. J. Pharmacol. 1999, 127, 1240-1246.
58. Mohr, K.; Tränkle, C.; Holzgrabe, U. Structure/activity relationships of M2 muscarinic allosteric modulators. Receptors Channels 2003, 9, 229-240.
59. Birdsall N.J.M.; Lazareno S. Allosterism at muscarinic receptors, ligands and mechanisms. Mini. Rev. Med. Chem. 2005, 5, 523-543.
60. Lazareno, S.; Gharagozloo, P.; Kuonen, D.; Popham, A.; Birdsall, N.J. Subtype-selective positive cooperative interactions between brucine analogues and acetylcholine at muscarinic receptors, radioligand binding studies. Mol. Pharmacol. 1998, 53, 573-589.
61. Lysíková M.; Havlas Z.; Tuček S. Interactions between allosteric modulators and 4-DAMP and other antagonists at muscarinic receptors, potential significance of the distance between the N and carboxyl C atoms in the molecules of antagonists. Neurochem Res 2001, 26, 383-394.
62. Jöhren, K.; Höltje, H. A model of the human M2 muscarinic acetylcholine receptor. J. Comput. Aided Mol. Des. 2002, 16, 795-801.
63. Jakubík, J.; Tuček, S. Positive allosteric interactions on cardiac muscarinic receptors, effects of chemical modifications of disulphide and carboxyl groups. Eur. J. Pharmacol. 1995, 289, 311-319.
64. Huang, X.; Ellis, J. Mutational disruption of a conserved disulfide bond in muscarinic acetylcholine receptors attenuates positive homotropic cooperativity between multiple allosteric sites and has subtype-dependent effects on the affinities of muscarinic allosteric ligands. Mol. Pharmacol. 2007, 71, 759-768.
65. Diaz-Arrastia, R.; Ashizawa, T.; Appel, S.H. Endogenous inhibitor of ligand binding to the muscarinic acetylcholine receptor. J. Neurochem. 1985, 44, 622-628.
66. Maslinski, W.; Ryzewski, J.; Bartfai, T. Rat thymocytes release a factor which inhibits muscarinic ligand binding. J. Neuroimmunol. 1988, 17, 275-285.
67. Fryer, A.D.; el-Fakahany, E.E. An endogenous factor induces heterogeneity of binding sites of selective muscarinic receptor antagonists in rat heart. Membr. Biochem. 1989, 8, 127-132.
68. Frey, W.H.2.; Emory, C.R.; Wiebenga, M.E.; Saxena, S.; Cardelli, D.; Ala, T.A.; Tollefson, G.D. Inhibitor of antagonist binding to the muscarinic receptor is elevated in Alzheimer's brain. Brain Res. 1994, 655, 153-160.
69. Fang Y.I.; Suzuki T.; Momose K. Partial purification of an endogenous inhibitor of muscarinic ligand binding. Biochem. Mol. Biol. Int. 1996, 38, 501-507.
70. Jacoby, D.B.; Gleich, G.J.; Fryer, A.D. Human eosinophil major basic protein is an endogenous allosteric antagonist at the inhibitory muscarinic M2 receptor. J. Clin. Invest. 1993, 91, 1314-1318.
71. Kjome, J.R.; Swenson, K.A.; Johnson, M.N.; Bordayo, E.Z.; Anderson, L.E.; Klevan, L.C.; Fraticelli, A.I.; Aldrich, S.L.; Fawcett, J.R.; Venters, H.D.J.; Ala, T.A.; Frey, W.H.2. Inhibition of antagonist and agonist binding to the human brain muscarinic receptor by arachidonic acid. J. Mol. Neurosci. 1998, 10, 209-217.
72. Frey, W.H.2.; Najarian, M.M.; Kumar, K.S.; Emory, C.R.; Menning, P.M.; Frank, J.C.; Johnson, M.N.; Ala, T.A. Endogenous Alzheimer's brain factor and oxidized glutathione inhibit antagonist binding to the muscarinic receptor. Brain Res. 1996, 714, 87-94.
73. Fawcett, J.R.; Bordayo, E.Z.; Jackson, K.; Liu, H.; Peterson, J.; Svitak, A.; Frey, W.H.2. Inactivation of the human brain muscarinic acetylcholine receptor by oxidative damage catalyzed by a low molecular weight endogenous inhibitor from Alzheimer's brain is prevented by pyrophosphate analogs, bioflavonoids and other antioxidants. Brain Res. 2002, 950, 10-20.
74. Ma, L.; Seager, M.A.; Wittmann, M.; Jacobson, M.; Bickel, D.; Burno, M.; Jones, K.; Graufelds, V.K.; Xu, G.; Pearson, M.; McCampbell, A.; Gaspar, R.; Shughrue, P.; Danziger, A.; Regan, C.; Flick, R.; Pascarella, D.; Garson, S.; Doran, S.; Kreatsoulas, C.; Veng, L.; Lindsley, C.W.; Shipe, W.; Kuduk, S.; Sur, C.; Kinney, G.; Seabrook, G.R.; Ray, W.J. Selective activation of the M1 muscarinic acetylcholine receptor achieved by allosteric potentiation. Proc. Natl. Acad. Sci. USA 2009, 106, 15950-15955.
75. Shirey, J.K.; Brady, A.E.; Jones, P.J.; Davis, A.A.; Bridges, T.M.; Kennedy, J.P.; Jadhav, S.B.; Menon, U.N.; Xiang, Z.; Watson, M.L.; Christian, E.P.; Doherty, J.J.; Quirk, M.C.; Snyder, D.H.; Lah, J.J.; Levey, A.I.; Nicolle, M.M.; Lindsley, C.W.; Conn, P.J. A selective allosteric potentiator of the M1 muscarinic acetylcholine receptor increases activity of medial prefrontal cortical neurons and restores impairments in reversal learning. J. Neurosci. 2009, 29, 14271-14286.
76. Marlo, J.E.; Niswender, C.M.; Days, E.L.; Bridges, T.M.; Xiang, Y.; Rodriguez, A.L.; Shirey, J.K.; Brady, A.E.; Nalywajko, T.; Luo, Q.; Austin, C.A.; Williams, M.B.; Kim, K.; Williams, R.; Orton, D.; Brown, H.A.; Lindsley, C.W.; Weaver, C.D.; Conn, P.J. Discovery and characterization of novel allosteric potentiators of M1 muscarinic receptors reveals multiple modes of activity. Mol. Pharmacol. 2009, 75, 577-588.
77. Bridges, T.M.; Marlo, J.E.; Niswender, C.M.; Jones, C.K.; Jadhav, S.B.; Gentry, P.R.; Plumley, H.C.; Weaver, C.D.; Conn, P.J.; Lindsley, C.W. Discovery of the first highly M5-preferring muscarinic acetylcholine receptor ligand, an M5 positive allosteric modulator derived from a series of 5-trifluoromethoxy N-benzyl isatins. J. Med. Chem. 2009, 52, 3445-3448.
78. Shirey, J.K.; Xiang, Z.; Orton, D.; Brady, A.E.; Johnson, K.A.; Williams, R.; Ayala, J.E.; Rodriguez, A.L.; Wess, J.; Weaver, D.; Niswender, C.M.; Conn, P.J. An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat. Chem. Biol. 2008, 4, 42-50.
79. Brady, A.E.; Jones, C.K.; Bridges, T.M.; Kennedy, J.P.; Thompson, A.D.; Heiman, J.U.; Breininger, M.L.; Gentry, P.R.; Yin, H.; Jadhav, S.B.; Shirey, J.K.; Conn, P.J.; Lindsley, C.W. Centrally Active Allosteric Potentiators of the M4 Muscarinic Acetylcholine Receptor Reverse Amphetamine- Induced Hyperlocomotor Activity in Rats. J. Pharm. Expert. Ther. 2008, 327, 941-953.
80. Chan, W.Y.; McKinzie, D.L.; Bose, S.; Mitchell, S.N.; Witkin, J.M.; Thompson, R.C.; Christopoulos, A.; Lazareno, S.; Birdsall, N.J.M.; Bymaster, F.P.; Felder, C.C. Allosteric modulation of the muscarinic M4 receptor as an approach to treating schizophrenia. Proc. Natl. Acad. Sci. USA 2008, 105, 10978-10983.
81. Nawaratne, V.; Leach, K.; Suratman, N.; Loiacono, R.E.; Felder, C.C.; Armbruster, B.N.; Roth, B.L.; Sexton, P.M.; Christopoulos, A. New insights into the function of M4 muscarinic acetylcholine receptors gained using a novel allosteric modulator and a DREADD (designer receptor exclusively activated by a designer drug). Mol. Pharmacol. 2008, 74, 1119-1131.
82. Nawaratne, V.; Leach, K.; Suratman, N.; Loiacono, R.E.; Felder, C.C.; Armbruster, B.N.; Roth, B.L.; Sexton, P.M.; Christopoulos, A. New insights into the function of M4 muscarinic acetylcholine receptors gained using a novel allosteric modulator and a DREADD (designer receptor exclusively activated by a designer drug). Mol. Pharmacol. 2008, 74, 1119-1131.
83. Jakubík, J.; Randáková, A.; El-Fakahany, E.E.; Doležal, V. Divergence of allosteric effects of rapacuronium on binding and function of muscarinic receptors. BMC Pharmacol. 2009, 9, 15.
84. Goudsouzian, N.G. Rapacuronium and bronchospasm. Anesthesiology 2001, 94, 727-728.
85. Jakubík, J.; Bacáková, L.; Lisá, V.; el-Fakahany, E.E.; Tuček, S. Activation of muscarinic acetylcholine receptors via their allosteric binding sites. Proc. Natl. Acad. Sci. USA 1996, 93, 8705-8709.
86. Sur, C.; Mallorga, P.J.; Wittmann, M.; Jacobson, M.A.; Pascarella, D.; Williams, J.B.; Brandish, P.E.; Pettibone, D.J.; Scolnick, E.M.; Conn, P.J. N-desmethylclozapine, an allosteric agonist at muscarinic 1 receptor, potentiates N-methyl-D-aspartate receptor activity. Proc. Natl. Acad. Sci. USA 2003, 100, 13674-13679.
87. Spalding, T.A.; Trotter, C.; Skjaerbaek, N.; Messier, T.L.; Currier, E.A.; Burstein, E.S.; Li, D.; Hacksell, U.; Brann, M.R. Discovery of an ectopic activation site on the M(1) muscarinic receptor. Mol. Pharmacol. 2002, 61, 1297-1302.
88. Bradley, S.R.; Lameh, J.; Ohrmund, L.; Son, T.; Bajpai, A.; Nguyen, D.; Friberg, M.; Burstein, E.S.; Spalding, T.A.; Ott, T.R.; Schiffer, H.H.; Tabatabaei, A.; McFarland, K.; Davis, R.E.; Bonhaus, D.W. AC-260584, an orally bioavailable M(1) muscarinic receptor allosteric agonist, improves cognitive performance in an animal model. Neuropharmacology 2009, 58, 365-373.
89. Spalding, T.A.; Ma, J.; Ott, T.R.; Friberg, M.; Bajpai, A.; Bradley, S.R.; Davis, R.E.; Brann, M.R.; Burstein, E.S. Structural requirements of transmembrane domain 3 for activation by the M1 muscarinic receptor agonists AC-42, AC-260584, clozapine, and N-desmethylclozapine, evidence for three distinct modes of receptor activation. Mol. Pharmacol. 2006, 70, 1974-1983.
90. Lebon, G.; Langmead, C.J.; Tehan, B.G.; Hulme, E.C. Mutagenic mapping suggests a novel binding mode for selective agonists of M1 muscarinic acetylcholine receptors. Mol. Pharmacol. 2009, 75, 331-341.
91. Thomas, R.L.; Langmead, C.J.; Wood, M.D.; Challiss, R.A.J. Contrasting effects of allosteric and orthosteric agonists on m1 muscarinic acetylcholine receptor internalization and down-regulation. J. Pharmacol. Exp. Ther. 2009, 331, 1086-1095.