Allosteric modulation of muscarinic acetylcholine receptors

Current Neuropharmacology

Volumn 5, Issue 3, 2007, Pages 157-167

  Gregory, Karen J ^a   Sexton, Patrick M ^a   Christopoulos, Arthur ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Acetylcholine; Allosteric interaction; G protein coupled receptor; Molecular modeling; Muscarinic acetylcholine receptor; Mutagenesis; Radioligand binding; Structure activity studies; Ternary complex model

Indexed keywords

1,6 HEXAMETHYLENEBIS[DIMETHYL(3 PHTHALIMIDOPROPYL)AMMONIUM BROMIDE]; 17ALPHA ETHYNYL 17BETA HYDROXY 5ALPHA ANDROSTANO[3,2 B]PYRIMIDO[1,2 A]BENZIMIDAZOLE; 4 [3 (4 BUTYLPIPERIDIN 1 YL) PROPYL] 7 FLUORO 4H BENZO[1,4]OXASIN 3 ONE; 4 N BUTYL 1 [4 (2 METHYLPHENYL) 4 OXO 1 BUTYL] PIPERIDINE; [4 [(3 CHLOROPHENYL)CARBAMOYLOXY] 2 BUTYNYL]TRIMETHYLAMMONIUM; AC 260584; AC 42; ACETYLCHOLINE; ALCURONIUM; BRUCINE; CARBACHOL; G PROTEIN COUPLED RECEPTOR; GALLAMINE; KT 5720; MUSCARINIC AGENT; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC M5 RECEPTOR; MUSCARINIC RECEPTOR; NORCLOZAPINE; OBIDOXIME; PILOCARPINE; RECEPTOR SUBTYPE; STAUROSPORINE; STRYCHNINE; TACRINE; TUBOCURARINE CHLORIDE; UNINDEXED DRUG; VINBURNINE; VINCAMINE;

ALLOSTERISM; BINDING AFFINITY; BINDING SITE; CENTRAL NERVOUS SYSTEM; CHO CELL; DRUG TARGETING; GUINEA PIG; HUMAN; LIGAND BINDING; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

EID: 45749136445     PISSN: 1570159X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157015907781695946     Document Type: Review

References (113)

1. Andersen, M.B., Fink-Jensen, A., Peacock, L., Gerlach, J., Bymaster, F., Lundbaek, J.A., Werge, T. (2003) The muscarinic M1/M4 receptor agonist xanomeline exhibits antipsychotic-like activity in Cebus apella monkeys. Neuropsychopharmacology, 28, 1168-1175.
2. Arunlakshana, O., Schild, H.O. (1959) Some quantitative uses of drug antagonists. Br. J. Pharmacol. Chemother., 14, 48-58.
3. Avlani, V., May, L.T., Sexton, P.M., Christopoulos, A. (2004) Application of a kinetic model to the apparently complex behavior of negative and positive allosteric modulators of muscarinic acetylcholine receptors. J. Pharmacol. Exp. Ther., 308, 1062-1072.
4. Birdsall, N.J., Burgen, A.S., Hulme, E.C., Stockton, J.M., Zigmond, M.J. (1983) The effect of McN-A-343 on muscarinic receptors in the cerebral cortex and heart. Br. J. Pharmacol., 78, 257-259.
5. Birdsall, NJ., Farries, T., Gharagozloo, P., Kobayashi, S., Lazareno, S., Sugimoto, M. (1999) Subtype-selective positive cooperative interactions between brucine analogs and acetylcholine at muscarinic receptors: functional studies. Mol. Pharmacol., 55, 778-786.
6. Birdsall, N.J., Lazareno, S., (2005) Allosterism at muscarinic receptors: ligands and mechanisms. Mini Rev. Med. Chem., 5, 523-543.
7. Buckley, N.J., Bonner, T.I., Bunn, M.R. (1988) Localization of a family of muscarinic receptor mRNAs in rat brain. J. Neurosci., 8, 4646-4652.
8. Buller, S., Zlotos, D.P., Mohr, K., Ellis, J. (2002) Allostcric site on muscarinic acetylcholine receptors: a single amino acid in transmembrane region 7 is critical to the subtype selectivities of caracurine V derivatives and alkane-bisammonium ligands. Mol. Pharmacol., 61, 160-168.
9. Caulfield, M.P. (1993) Muscarinic receptors - characterization, coupling and function. Pharmacol. Ther., 58, 319-379.
10. Choo, L.K., Mitchelson, F., Vong, Y.M. (1985) The interaction of McN-A-343 with pirenzepine and other selective muscarine receptor antagonists at a prejunctional muscarine receptor. Naunyn Schmiedebergs Arch. Pharmacol., 328, 430-438.
11. Christopoulos, A. (2000) Quantification of allosteric interactions at G protein-coupled Receptors using radioligand binding assays, in Current Protocols In Pharmacology. Enna, S.J. (ed.), Wiley and Sons, NY. pp. 1.22.21-21.22.40.
12. Christopoulos, A. (2002) Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nat. Rev. Drug Discov., 1, 198-210.
13. Christopoulos, A. (2007) Muscarinic acetylcholine receptors in the central nervous system: structure, function, and pharmacology, in exploring the vertebrate central cholinergic nervous system. Karczmar, A.G. Springer, NY, pp. 163-208.
14. Christopoulos, A., Lanzafame, A., Mitchelson, F. (1998) Allosteric interactions at muscarinic cholinoceptors. Clin. Exp. Pharmacol. Physiol., 25, 185-194.
15. Christopoulos, A., Loiacono, R., Mitchelson, F. (1993) Binding of the muscarine receptor antagonist heptane-1,7-bis(dimethyl-3′-phthamidopropyl)ammonium bromide at cholinoceptor sites. Eur. J. Pharmacol., 246, 1-8.
16. Christopoulos, A., Mitchelson, F. (1994) Assessment of the allosteric interactions of the bisquatemary heptane-1,7-bis(dimethyl-3′-phthalimidopropyl)ammonium bromide at M1 and M2 muscarine receptors. Mol. Pharmacol., 46, 105-114.
17. Christopoulos, A., Mitchelson, F. (1997) Pharmacologioal analysis of the mode of interaction of McN-A-343 at atrial muscarinic M2 receptors. Eur. J. Pharmacol., 339, 153-156.
18. Christopoulos, A., Sormam, J.L., Mitchelson, F., El-Fakahany, E.E. (1999) Characterization of the subtype selectivity of the allosteric modulator heptane-1,7-bis-(dimediyl-3′-phthalimidopropyl) ammonium bromide (C7/3-phth) at cloned muscarinic acetylcholine receptors. Biochem. Pharmacol., 57, 171-179.
19. Clark, A.L., Mitchelson, F. (1976) The inhibitory effect of gallamine on muscarinic receptors. Br. J. Pharmacol., 58, 323-331.
20. Cummings, J.L. (2000) Cholinesterase inhibitors: A new class of psychotropic compounds. Am. J. Psychiatry, 157, 4-15.
21. Disingrini, T., Muth, M., Dallanoce, C., Barocelli, E., Bertoni, S., Kellershohn, K., Mohr, K., De Amici, M., Holzgrabe, U. (2006) Design, synthesis, and action of oxotremorine-related hybrid-type allosteric, modulators of muscarinic acetylcholine receptors. J. Med. Chem., 49, 366-372.
22. Dunlap, J., Brown, J.H. (1983) Heterogeneity of binding sites on cardiac muscarinic receptors induced by the neuromuscular blocking agents gallamine and pencuronium. Mol. Pharmacol., 24, 15-22.
23. Duttaroy, A., Gomeza, J., Gan, J.W., Siddiqui, N., Basile, A.S., Harman, W.D., Smith, P.L., Felder, C.C., Levey, A.I., Wess, J. (2002) Evaluation of muscarinic agonist-induced analgesia in muscarinic acetylcholine receptor knockout mice. Mol. Pharmacol., 62, 1084-1093.
24. Ehlert, F.J. (1988) Estimation of the affinities of allosteric ligands using radioligand binding and pharmacological null methods. Mol. Pharmacol., 33, 187-194.
25. Ellis, J., Huyler, J., Brann, M.R. (1991) Allosteric regulation of cloned m1-m5 muscarinic receptor subtypes. Biochem. Pharmacol., 42, 1927-1932.
26. Ellis, J., Seidenberg, M. (1992) Two allosteric modulators interact at a common site on cardiac muscarinic receptors. Mol. Pharmacol., 42, 638-641.
27. Ellis, J., Seidenberg, M. (1999) Competitive and allosteric interactions of 6-chloro-5, 10-dhydro-5-[(1-methyl-4-piperidinyl)acetyl]-11H-di benzo[b,e][1, 4]diazepine-11-one hydrochloride (UH-AH 37) at muscarinic receptors, via distinct epitopes. Biochem. Pharmacol., 57, 181-186.
28. Ellis, J., Seidenberg, M. (2000) Interactions of alcuronium, TMB-8, and other allosteric ligands with muscarinic acetylcholine receptors: studies with chimeric receptors. Mol. Pharmacol., 58, 1451-1460.
29. Ellis, J., Seidenberg, M., Brann, M.R. (1993) Use of chimeric muscarinic receptors to investigate epitopes involved in allosteric interactions. Mol. Pharmacol., 44, 583-588.
30. Feuerstein, T.J., Lehmann, J., Sauermann, W., van Velthoven, V., Jackisch, R. (1992) The autoinhibitory feedback control of acetylcholine release in human neocortex tissue. Brain Res., 572, 64-71.
31. Flyan, D.D., Ferrari-DiLeo, G., Levey, A.I., Mash, D.C. (1995) Differential alterations in muscarinic receptor subtypes in Alzheimer's disease: implications for cholinergic-based therapies. Life Sci., 56, 869-876.
32. Flynn, D.D., Mash, D.C. (1989) Multiple in vitro interactions with and differential in vivo regulation of muscarinic receptor subtypes by tetrahydroaminoacridine. J. Pharmacol. Exp. Ther., 250, 573-581.
33. Gaddum, J. (1936) The quantitative effects of antagonistic drugs. J. Physiol. (Lond.), 99, 7P-9P.
34. Gautam, D., Gavrilova, O., Jeon, J., Pack, S., Jou, W., Cui, Y., Li, J.H., Wess, J. (2006) Beneficial metabolic effects of M3 muscarinic acetylcholine receptor deficiency. Cell Metab., 4, 363-375.
35. Gharagozloo, P., Lazareno, S., Miyauchi, M., Popham, A., Birdsall, N.J. (2002) Substituted pentacyclic carbazolones as novel muscarinic allosteric agents: synthesis and structure-affinity and cooperativity relationships. J. Med. Chem., 45, 1259-1274.
36. Gilsbach, R., Grossmuller, M., Alptuzun, V., Erciyas, E., Trankle, C., Holzgrabe, U., Mohr, K. (2003) Cooperative intemboas at M2 muscarinic acetylcholine receptors: structure/activity relationships in stepwise shortened bispyridinium- and bis(ammonio)alkane-type allosteric modulators. Neurochem. Res., 28, 667-673.
37. Gnagey, A.L., Seidenberg, M., Ellis, J. (1999) Site-directed mutagenesis reveals two epitopes involved in the subtype selectivity of the allosteric interactions of gallamine at muscarinic acetylcholine receptors. Mol. Pharmacol., 56, 1245-1253.
38. Hall, D.A. (2000) Modeling the functional effects of allosteric modulators at pharmacological receptors: An extension of the two-state model of receptor activation. Mol. Pharmacol., 58, 1412-1423.
39. Hejnova, L., Tucek S., El-Fakahany, E.E. (1995) Positive and negative allosteric interactions on muscarinic receptors. Eur. J. Pharmacol. Mol. Pharmacol., 291, 427-430.
40. Hilf, G., Jakobs, K.H. (1992) Activation of solubilized G-proteins by muscarinic acetylcholine receptors. Cell Signal, 4, 787-794.
41. Hopkins, A.L., Groom, C.R. (2002) The druggable genome. Nat. Rev. Drug Discov., 1, 727-730.
42. Huang, X.P., Prilla, S., Mohr, K., Ellis, J. (2005) 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(ammoniym)alkane-type hexamethylene-bis-[dimethyl-(3-phthalimidopropyl)ammonium]dibromide. Mol. Pharmacol., 68, 769-778.
43. Jakubik, J., Bacakova, L., el-Fakahany, E.E., Tucek, S. (1995) Subtype selectivity of the positive allosteric action of alcuronium, at cloned M1-M5 muscarinic acetylcholine receptors. J. Pharmacol. Exp. Ther., 274, 1077-1083.
44. Jakubik, J., Bacakova, L., El-Fakahany, E.E., Tucek, S. (1997) Positive cooperativity of acetylcholine and other agonists with allosteric ligands on muscarinic acetylcholine receptors. Mol. Pharmacol., 52, 172-179.
45. Jakubik J., Bacakova, L., Lisa, V., el-Fakahany, E.E., Tucek, S. (1996) Activation of muscarinic acetylcholine receptors via their allosteric binding sites. Proc. Natl. Acad. Sci. USA, 93, 8705-8709.
46. Jakubik, J., Haga, T., Tucek, S. (1998) Effects of an agonist, allosteric modulator, and antagonist on guanosine-gamma-[35S]thiotriphosphate binding to liposomes with varying muscarinic receptor/Go protein stoichiometry. Mol. Pharmacol., 54, 899-906.
47. Jakabik, J., Krejci, A., Dolezal, V. (2005) Asparagine, valine, and threonine in the third extracellular loop of muscarinic receptor have essential roles in the positive cooperativity of strychine-like allosteric modulators. J. Pharmacol. Exp. Ther., 313, 688-696.
48. Johren, K., Holtje, H.D. (2002) A model of the human M2 muscarinic acetylcholine receptor. J. Comput. Aided Mol. Des., 16, 795-801.
49. Kenakin, T. (2005) New concepts in drug discovery: collateral efficacy and permissive antagonism. Nat. Rev. Drug Discov., 4, 919-927.
50. Kiefer-Day, J.S., Campbell, H.E., Towles, J., el-Fakahany, E.E. (1991) Muscarinic subtype selectivity of tetrahydroaminoacridine: possible relationship to its capricious efficacy. Eur. J. Pharmacol., 203, 421-423.
51. Kostenis, E., Botero Cid, H.M., Holzgrabe, Y., Mohr, K. (1996) Evidence for a multiple binding mode of bispyridinium-type allosteric modulators of muscarinic receptors. Eur. J. Pharmacol., 314, 385-392.
52. Kostenis, E., Mohr, K. (1996) Two-point kinetic experiments to quantify allosteric effects on radioligand dissociation. Trends Pharmacol. Sci., 17, 280-283.
53. Krejci, A., Tucek, S. (2001) 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., 60, 761-767.
54. Langmead, C.J., Fry, V.A., Forbes, I.T., Branch, C.L., Christopoulos, A., Wood, M.D., Herden, H.J. (2006) Probing the molecular mechanism of interaction between 4-n-butyl-1-[4-(2-methylphenyl)4-oxo-1-butyl]-piperidine (AC-42) and the muscarinic M(1) receptor: direct pharmacological evidence that AC-42 is an allosteric agonist. Mol. Pharmacol., 69, 236-246.
55. Lanzafame, A., Christopoulos, A., Mitchelson, F. (1996) Interactions of agonists with an allosteric antagonist at muscarinic acetylcholine M2 receptors. Eur. J. Pharmacol., 316, 27-32.
56. Lanzafame, A., Christopoulos, A., Mitchelson, F. (1997) Three allosteric modulators act at a common site, distinct from that of competitive antagonists, at muscarinic acetylcholine M2 receptors. J. Pharmacol. Exp. Ther., 282, 278-285.
57. Lanzafame, A., Christopoulos, A., Mitchelson, F. (2001) The allosteric interaction of otenzepad (AF-DX 116) at muscarinic M2 receptors in guinea pig atria. Eur. J. Pharmacol., 416, 235-244.
58. Lanzafame, A.A., Christopoulos, A., Mitchelson, F. (2003) Cellular signaling mechanisms for muscarinic acetylcholine receptors. Recept. Channels, 9, 241-260.
59. Lanzafame, A.A., Sexton, P.M., Christopoulos, A. (2006) Interaction studies of multiple binding sites on m4 muscarinic acetylcholine receptors. Mol. Pharmacol., 70, 736-746.
60. Lazareno, S., Birdsall, N. (1995) Detection, quantitation, and verification of allosteric interactions of agents with labeled and unlabeled liganda at G protein-coupled receptors: interactions of strychnine and acetylcholine at muscarinic receptors. Mol. Pharmacol., 48, 362-378.
61. Lazareno, S., Dolezal, V., Popham, A., Birdsall, N.J. (2004) Thiochrome enhances acetylcholine affinity at muscarinic M4 receptors: receptor subtype selectivity via cooperativity rather than affinity. Mol. Pharmacol., 65, 257-266.
62. Lazareno, S., Gharagozloo, P., Kuonen, D., Popham, A., Birdsall, N.J. (1998) Subtype-selective positive cooperative interactions between brucine analogues and acetylcholine at muscarinic receptors: radioligand binding studies. Mol. Pharmacol., 53, 573-589.
63. Lazareno, S., Popham, A., Birdsall, N.J. (2000) 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., 58, 194-207.
64. Lazareno, S., Popham, A., Birdsall, N.J. (2002) Analogs of WIN 62,577 define a second allosteric site on muscarinic receptors. Mol. Pharmacol., 62, 1492-1505.
65. Lee, N.H., el-Fakahany, E.E. (1988) Influence of ligand choice on the apparent binding profile of gallamine to cardiac muscarinic receptors. Identification of three main types of gallamine-muscarinic receptor interactions. J. Pharmacol. Exp. Ther., 246, 829-838.
66. Lee, N.H., el-Fakahany, E.E. (1991) Allosteric interactions at the m1, m2 and m3 muscarmic receptor subtypes. J. Pharmacol. Exp. Ther., 256, 468-479.
67. Leppik, R.A., Miller, R.C., Eck, M., Paquet, J.L. (1994) Role of acidic amino acids in the allosteric modulation by gallamine of antagonist binding at the m2 muscarmic acetylcholine receptor. Mol. Pharmacol., 45, 983-990.
68. Levey, A.I., Edmunds, S.M., Koliatsos, V., Wiley, R-G., Heilman, C.J. (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J. Neurosci., 15, 4077-4092.
69. Levey, A.I., Kitt, C.A., Simonds, W.F., Price, D.L., Brann, M.R. (1991) Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci., 11, 3218-3226.
70. Lullmann, H., Ohnesorge, F.K., Schauwecker, G.C., Wassermann, O. (1969) Inhibition of the actions of carbachol and DFP on guinea pig isolated atria by alkane-bis-ammonium compounds. Eur. J. Pharmacol., 6, 241-247.
71. Maa, A., Kostenis, E., Mohr, K. (1995) Potentiation by alcuronium of the antimuscarinic effect of N-methylscopolamine in guinea pig left atria. Eur. J. Pharmacol., 272, 103-106.
72. Maa, A., Mohr, K. (1996) Opposite effects of alcuronium, on agonist and on antagonist binding to muscarinic receptors. Eur. J. Pharmacol., 305, 231-234.
73. Matsui, H., Lazareno, S., Birdsall, N.J. (1995) Probing of the location of the allosteric site on m1 muscarinic receptors by site-directed mutagenesis. Mol. Pharmacol., 47, 88-98.
74. May, L.T., Leach, K., Sexton, P.M., Christopoulos, A. (2007) Allosteric modulation of g protein-coupled receptors. Annu. Rev. Pharmacol. Toxicol., 47, 1-51.
75. May, L.T., Lin, Y., Sexton, P.M., Christopoulos, A. (2005) Regulation of M2 muscarinic acetylcholine receptor expression and signaling by prolonged exposure to allosteric modulators. J. Pharmacol. Exp. Ther., 312, 382-390.
76. Miyakawa, T., Yamada, M., Duttaroy, A., Wess, J. (2001) Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J. Neurosci., 21, 5239-5250.
77. Mohr, K., Trankle, C., Holzgrabe, U. (2003) Strueture/activity relationships of M2 muscarmic allosteric modulators. Recept. Channels, 9, 229-240.
78. Motulsky, H.J., Mahan, L.C. (1984) The kinetics of competitive radioligand binding predicted by the law of mass action. Mol. Pharmacol., 25, 1-9.
79. Neubig, R.R., Spedding, M., Kenakin, T., Christopoulos, A. (2003) International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification. XXXVIII. Update on terms and symbols in quantitative pharmacology. Pharmacol. Rev., 55, 597-606.
80. Oki, T., Takagi, Y., Inagaki, S., Taketo, M.M., Manabe, T., Matsui, M., Yamada, S. (2005) Quantitative analysis of binding parameters of [3H]N-methylscopolamine in central nervous system of muscarinic acetylcholine receptor knockout mice. Brain Res. Mol. Brain Res., 133, 6-11.
81. Pearce, B.D., Potter, L.T. (1988) Effects of tetrahydroaminoacridine on M1 and M2 muscarine receptors. Neurosci Lett., 88, 281-285.
82. Potter, L.T., Ferrendelli, C.A., Hanchett, H.E., Hollifield, M.A., Lorenzi, M.V. (1989) Tetrahydroaminoacridine and other allosteric antagonists of hippocampal M1 muscarine receptors. Mol. Pharmacol., 35, 652-660.
83. Prilla, S., Schrobang, J., Ellis, J., Holtje, H.-D., Mohr, K. (2006) 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 cooperstivity. Mol. Pharmacol., 70, 181-193.
84. Proska, J., Tucek, S. (1994) Mechanisms of steric and cooperative actions of alcuronium on cardiac muscarinic acetylcholine receptors. Mol. Pharmacol, 45, 709-717.
85. Proska, J., Tucek, S. (1995) Competition between positive and negative allosteric effectors on muscarmic receptors. AOL Pharmacol., 48, 696-702.
86. Proska J., Turek, S. (1996) Positive allosteric action of ebumamonine on cardiac muscarinic acetylcholine receptors. Eur. J. Pharmmacol., 305, 201-205.
87. Roszkowski, A.P. (1961) An unusual type of sympathetic ganglionic stimulant. J. Pharmacol. Exp. Ther., 132, 156-170.
88. Rouse, S.T., Marino, M.J., Potter, L.T., Conn, P.J., Levey, A.I. (1999) Muscarinic receptor subtypes involved in hipocampal circuits. Life Sci., 64, 501-509.
89. Schroter, A., Trankle, C., Mohr, K. (2000) Modes of allosteric interactions with free and [3H]N-methylscopolemine-occupied muscarinic M2 receptors as deduced from buffer-dependent potency shifts. Naunyn Schmiedebergs Arch. Pharmacol., 362, 512-519.
90. Schwartz, T.W., Holst, B. (2006) Ago-allosteric modulation and other types of allostery in dimeric 7TM receptors. J. Recept. Signal. Transduct. Res., 26, 107-128.
91. Shannon, H.E., Hart, J.C., Bymaster, F.P., Calligaro, D.O., DeLapp, N.W., Mitch, C.H., Ward, J.S., Fink-Jensen, A., Sauerberg, P., Jeppesen, L., Shear-down, MJ., Swedberg, M.D. (1999) Muscarinic receptor agoniists like dopamine receptor antagonist antipsychotics, inhibit conditioned avoidance response in rats. J Pharmacol. Exp. Ther., 290, 901-907.
92. Spalding, T.A., Ma, J.N., Ott, T.R., Friberg, M., Bajpai, A., Bradley, S.R., Davis, R.E., Brann, M.R., Burstein, E.S. (2006) 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 dictinct modes of receptor activation. Mol. Pharmacol., 70, 1974-1983.
93. Spalding, T.A., Trotter, C., Skjaerbaek, N. Messier, T.L., Currier, E.A., Burstein, E.S., Li, D. Hacksell, U., Brann, M.R. (2002). Discovery of an actopic activation site on the M(1) muscarinic receptor. Mol. Pharmacol., 61, 1297-1302.
94. Stockon, J.M., Birdsall, N.J., Burgen, A.S. Hulme, E.C. (1983) Modification of the binding properties of muscarinic receptors by gallamine. Mol. Pharmacol., 23, 551-557.
95. Sur, J.B., 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. (2003) N-desmethylclozapine, an allosteric agonist at muscarinic 1 receptor, potentiates N-methlyl-D-aspartate receptor activity. Proc. Natl. Acad. Sci. USA, 100, 13674-13679.
96. Trankle, C., Dittmann, A., Schulz, U., Weyand, O., Buller, S., Johren, K., Heller, E., Birdsall, N.J., Holzgrabe, U., Ellis, J., Holtje, H.D., Mohr, K. (2005) Atypical muscarinic allosteric modulation: cooperativity between mudulators and their atypical binding topology in muscarinic M2 and M27M5 chimeric receptors. Mol. Pharmacol., 68, 1597-1610.
97. Trankle, C., Mies-Klomfass, E., Cid, M.H., Holzgrabe, U., Mohr, K. (1998) Identification of a [3H]Ligand for the common allosteric site of muscarinic acetylcholine M2 receptors. Mol. Pharmacol., 54, 139-145.
98. Trankle, C., Mohr, K. (1997) Divergent modes of action among cationic allosteric modulators of muscarinic M2 receptors. Mol. Pharmacol., 51, 674-682.
99. Trankle, C., Weyand, O., Schroter, A., Mohr, K. (1999) Using a radioalloster to test predictions of the cooperativity model for gallamine binding to the allosteric site of muscarinic acetylcholine M(2) receptors. Mol. Pharmacol., 56, 962-965.
100. Trankle, C., Weyand, O., Voigtlander, U., Mynett, A., Lazareno, S., Birdsall, N.J., Mohr, K. (2003) Interactions of orthosteric and allosteric ligands with [3H]dimethyl-W84 at the common allosteric site of muscarinic M2 receptors. Mol. Pharmacol., 64, 180-190.
101. Tucek, S., Musilkova, J., Nedoma, J., Proska, J., Shelkovnikov, S., Vorlicek, J. (1990) Positive cooperativity in the binding of alcuronium and N-methylscopolamine to muscarinic acetylcholine receptors. Mol. Pharmacol., 38, 674-680.
102. Urban, J.D., Clarke, W.P., von Zastrow, M., Nichols, D.E., Kobilka, B., Weinstein, H., Javitch, J.A., Roth, B.L., Christopoulos, A., Sexton, P.M., Miller, K.J., Spedding, M., Mailman, R.B. (2007) Functional selectivity and classical concepts of quantitative pharmacology. J. Pharmacol. Exp. Ther., 320, 1-13.
103. Vilaro, M.T., Palacios, J.M., Mengod, G. (1990) Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci. Lett., 114, 154-159.
104. Voigtlander, U., Johren, K., Mohr, M., Raasch, A., Trankle, C., Buller, S., Ellis, J., Holtje, H.D., Mohr, K. (2003) 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-occupied receptors. Mol. Pharmacol., 64, 21-31.
105. Waelbroeck, M. (1994) Identification of drugs competing with d-tubocurarine for an allosteric site on cardiac muscarinic receptors. Mol. Pharmacol., 46, 685-692.
106. Waelbroeck, M., Robberecht, P., De Neef, P., Christophe, J. (1988) Effects of d-tubocurarine on rat cardiac muscarinic receptors: a comparison with gallamine. J. Recept. Res., 8, 787-808.
107. Weiner, D.M., Levey, A.I., Brann, M.R. (1990) Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc. Natl. Acad. Sci. USA, 87, 7050-7054.
108. Yamada, M., Lamping, K.G., Duttaroy, A., Zhang, W., Cui, Y., Bymaster, F.P., McKinzie, D.L., Felder, C.C., Deng, C.X., Faraci, F.M., Wess, J. (2001) Cholinergic dilation of cerebral blood vessels is abolished in M(5) muscarinic acetylcholine receptor knockout mice. Proc. Natl. Acad. Sci. US4, 98, 14096-14101.
109. Yamada, M., Miyakawa, T., Duttaroy, A., Yamanaka, A., Moriguchi, T., Makita, R., Ogawa, M., Chou, C.J., Xia, B., Crawley, J.N., Felder, C.C., Deng, C.X., Wess, J. (2001) Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature, 410, 207-212.
110. Yasuda, R.P., Ciesla, W., Flores, L.R., Wall, S.J., Li, M., Satkus, S.A., Weisstein, J.S., Spagnola, B.V., Wolfe, B.B. (1993) Development of antisera selective for m4 and m5 muscarinic cholinergic receptors: distribution of m4 and m5 receptors in rat brain. Mol. Pharmacol., 43, 149-157.
111. Yeomans, J., Forster, G., Blaha, C. (2001) M5 muscarinic receptors are needed for slow activation of dopamine neurons and for rewarding brain stimulation. Life Sci., 68, 2449-2456.
112. Zahn, K., Eckstein, N., Trankle, C., Sadee, W., Mohr, K (2002) Allosteric, modulation of muscarinic receptor signaling: alcuronium-induced conversion of pilocarpine from an agonist into an antagonist. J. Pharmacol. Exp. Ther., 301, 720-728.
113. Zhang, H.M., Chen, SK, Matsui, M., Gautam, D., Wess, J., Pan, H.L. (2006) Opposing functions of spinal M2, M3, and M4 receptor subtypes in regulation of GABAergic inputs to dorsal horn neurons revealed by muscarinic receptor knockout mice. Mol. Pharmacol., 69, 1048-1055.