New insight into active muscarinic receptors with the novel radioagonist [3H]iperoxo

Biochemical Pharmacology

Volumn 90, Issue 3, 2014, Pages 307-319

  Schrage, Ramona ^a   Holze, Janine ^a   Klöckner, Jessica ^b   Balkow, Aileen ^a   Klause, Anne S ^a   Schmitz, Anna Lena ^a   De Amici, Marco ^c   Kostenis, Evi ^a   Tränkle, Christian ^a   Holzgrabe, Ulrike ^b   Mohr, Klaus ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Allosteric modulation; G protein coupled receptor; Iperoxo; Muscarinic acetylcholine receptor; Superagonism

Indexed keywords

ACETYLCHOLINE H 3; IPEROXO H 3; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M2 RECEPTOR AGONIST; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC M5 RECEPTOR; MUSCARINIC RECEPTOR; NUCLEOTIDE DERIVATIVE; OXOTREMORINE M H 3; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING KINETICS; BINDING SITE; CHO CELL LINE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ISOTOPE LABELING; MEMBRANE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL;

W84 (3-(1,3-DIOXOISOINDOL-2-YL)PROPYL-[6-[3-(1,3-DIOXOISOINDOL-2-YL)PROPYL-DIMETHYLAZANIUMYL]HEXYL]-DIMETHYLAZANIUM); ACETYLCHOLINE; ALLOSTERIC MODULATION; ATROPINE; CHOLERA TOXIN (CTX); G PROTEIN-COUPLED RECEPTOR; GUANOSINE TRIPHOSPHATE (GTP); IPEROXO; MUSCARINIC ACETYLCHOLINE RECEPTOR; N-METHYLSCOPOLAMINE (NMS); PERTUSSIS TOXIN (PTX); PILOCARPINE; SUPERAGONISM; [(3)H]IPEROXO;

ALLOSTERIC REGULATION; ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETULUS; DRUG INVERSE AGONISM; DRUG STABILITY; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; ISOXAZOLES; KINETICS; LIGANDS; MODELS, BIOLOGICAL; MUSCARINIC AGONISTS; N-METHYLSCOPOLAMINE; PROTEIN CONFORMATION; QUATERNARY AMMONIUM COMPOUNDS; RADIOLIGAND ASSAY; RECEPTOR, MUSCARINIC M2; RECEPTOR, MUSCARINIC M4; RECEPTORS, MUSCARINIC; RECOMBINANT PROTEINS; TRITIUM;

EID: 84903900447     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.05.012     Document Type: Article

References (52)

1. D.M. Rosenbaum, S.G. Rasmussen, and B.K. Kobilka The structure and function of G-protein-coupled receptors Nature 459 2009 356 363
2. M.C. Lagerström, and H.B. Schiöth Structural diversity of G protein-coupled receptors and significance for drug discovery Nat Rev Drug Discov 7 2008 339 357
3. W.M. Oldham, and H.E. Hamm Heterotrimeric G protein activation by G-protein-coupled receptors Nat Rev Mol Cell Biol 9 2008 60 71
4. J. Wess Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications Annu Rev Pharmacol Toxicol 44 2004 423 450 (Pubitemid 38263848)
5. R. Fredriksson, M.C. Lagerström, L. Lundin, and H.B. Schiöth The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints Mol Pharmacol 63 2003 1256 1272 (Pubitemid 36627220)
6. J. Wess, R.M. Eglen, and D. Gautam Muscarinic acetylcholine receptors: mutant mice provide new insights for drug development Nat Rev Drug Discov 6 2007 721 733 (Pubitemid 47342315)
7. A.C. Kruse, D.R. Weiss, M. Rossi, J. Hu, K. Hu, and K. Eitel et al. Muscarinic receptors as model targets and antitargets for structure-based ligand discovery Mol Pharmacol 84 2013 528 540
8. P.J. Conn, C.K. Jones, and C.W. Lindsley Subtype-selective allosteric modulators of muscarinic receptors for the treatment of CNS disorders Trends Pharmacol Sci 30 2009 148 155
9. C. Dallanoce, P. Conti, M. De Amici, C. De Micheli, E. Barocelli, and M. Chiavarini et al. Synthesis and functional characterization of novel derivatives related to oxotremorine and oxotremorine-M Bioorg Med Chem 7 1999 1539 1547 (Pubitemid 29347120)
10. J. Kloeckner, J. Schmitz, and U. Holzgrabe Convergent, short synthesis of the muscarinic superagonist iperoxo Tetrahedron Lett 51 2010 3470 3472 Available from: URL: http://www.sciencedirect.com/science/article/pii/ S0040403910007665
11. R. Schrage, W.K. Seemann, J. Klöckner, C. Dallanoce, K. Racké, and E. Kostenis et al. Agonists with supraphysiological efficacy at the muscarinic M 2 ACh receptor Br J Pharmacol 169 2013 357 370
12. K. Haga, A.C. Kruse, H. Asada, T. Yurugi-Kobayashi, M. Shiroishi, and C. Zhang et al. Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist Nature 482 2012 547 551
13. A.C. Kruse, A.M. Ring, A. Manglik, J. Hu, K. Hu, and K. Eitel et al. Activation and allosteric modulation of a muscarinic acetylcholine receptor Nature 504 2013 101 106
14. S.B. Daval, E. Kellenberger, D. Bonnet, V. Utard, J. Galzi, and B. Ilien Exploration of the orthosteric/allosteric interface in human M1 muscarinic receptors by bitopic fluorescent ligands Mol Pharmacol 84 2013 71 85
15. M. Grossmüller, J. Antony, C. Tränkle, U. Holzgrabe, and K. Mohr Allosteric site in M2 acetylcholine receptors: evidence for a major conformational change upon binding of an orthosteric agonist instead of an antagonist Naunyn-Schmied Arch Pharmacol 372 2006 267 276 (Pubitemid 43123954)
16. A. Gnagey, and J. Ellis Allosteric regulation of the binding of [3H]acetylcholine to m2 muscarinic receptors Biochem Pharmacol 52 1996 1767 1775 (Pubitemid 26407993)
17. A.C. Kruse, J. Hu, A.C. Pan, D.H. Arlow, D.M. Rosenbaum, and E. Rosemond et al. Structure and dynamics of the M3 muscarinic acetylcholine receptor Nature 482 2012 552 556
18. A. De Lean, J.M. Stadel, and R.J. Lefkowitz A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled beta-adrenergic receptor J Biol Chem 255 1980 7108 7117 (Pubitemid 11232874)
19. T.P. Kenakin Biased signalling and allosteric machines: new vistas and challenges for drug discovery Br J Pharmacol 165 2012 1659 1669
20. H. Lüllmann, F.K. Ohnesorge, G.C. Schauwecker, and O. Wassermann Inhibition of the actions of carbachol and DFP on guinea pig isolated atria by alkane-bis-ammonium compounds Eur J Pharmacol 6 1969 241 247
21. A.L. Clark, and F. Mitchelson The inhibitory effect of gallamine on muscarinic receptors Br J Pharmacol 58 1976 323 331
22. J.M. Stockton, N.J. Birdsall, A.S. Burgen, and E.C. Hulme Modification of the binding properties of muscarinic receptors by gallamine Mol Pharmacol 23 1983 551 557 (Pubitemid 13089769)
23. S. Prilla, J. Schrobang, J. Ellis, H. Höltje, and K. Mohr 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 70 2006 181 193
24. R.O. Dror, H.F. Green, C. Valant, D.W. Borhani, J.R. Valcourt, and A.C. Pan et al. Structural basis for modulation of a G-protein-coupled receptor by allosteric drugs Nature 503 2013 295 299
25. A. Bock, N. Merten, R. Schrage, C. Dallanoce, J. Bätz, and J. Klöckner et al. The allosteric vestibule of a seven transmembrane helical receptor controls G-protein coupling Nat Commun 3 2012 1044
26. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
27. J. Antony, K. Kellershohn, M. Mohr-Andrä, A. Kebig, S. Prilla, and M. Muth et al. Dualsteric GPCR targeting: a novel route to binding and signaling pathway selectivity FASEB J 23 2009 442 450
28. Y. Cheng, and W.H. Prusoff Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction Biochem Pharmacol 22 1973 3099 3108
29. A. De Blasi, K. O'Reilly, and H.J. Motulsky Calculating receptor number from binding experiments using same compound as radioligand and competitor Trends Pharmacol Sci 10 1989 227 229 (Pubitemid 19146394)
30. A. Christopoulos, and E.E. El-Fakahany Qualitative and quantitative assessment of relative agonist efficacy Biochem Pharmacol 58 1999 735 748 (Pubitemid 29329522)
31. C. Valant, K.J. Gregory, N.E. Hall, P.J. Scammells, M.J. Lew, and P.M. Sexton et al. A novel mechanism of G protein-coupled receptor functional selectivity: muscarinic partial agonist McN-A-343 as a bitopic orthosteric/allosteric ligand J Biol Chem 283 2008 29312 29321
32. M.R. Tota, and M.I. Schimerlik Partial agonist effects on the interaction between the atrial muscarinic receptor and the inhibitory guanine nucleotide-binding protein in a reconstituted system Mol Pharmacol 37 1990 996 1004 (Pubitemid 20219915)
33. R. Mistry, M.R. Dowling, and R.A. Challiss An investigation of whether agonist-selective receptor conformations occur with respect to M2 and M4 muscarinic acetylcholine receptor signalling via Gi/o and Gs proteins Br J Pharmacol 144 2005 566 575 (Pubitemid 40349464)
34. M.T. Griffin, K.W. Figueroa, S. Liller, and F.J. Ehlert Estimation of agonist activity at G protein-coupled receptors: analysis of M2 muscarinic receptor signaling through Gi/o,Gs, and G15 J Pharmacol Exp Ther 321 2007 1193 1207 (Pubitemid 46762694)
35. P. Michal, E.E. El-Fakahany, and V. Dolezal Muscarinic M2 receptors directly activate Gq/11 and Gs G-proteins J Pharmacol Exp Ther 320 2007 607 614
36. P.G. Strange Agonist binding, agonist affinity and agonist efficacy at G protein-coupled receptors Br J Pharmacol 153 2008 1353 1363 (Pubitemid 351492449)
37. X. Deupi, and B. Kobilka Activation of G protein-coupled receptors Adv Protein Chem 74 2007 137 166 (Pubitemid 47369749)
38. P. Scheerer, J.H. Park, P.W. Hildebrand, Y.J. Kim, N. Krauß, and H. Choe et al. Crystal structure of opsin in its G-protein-interacting conformation Nature 455 2008 497 502
39. S.G. Rasmussen, B.T. DeVree, Y. Zou, A.C. Kruse, K.Y. Chung, and T.S. Kobilka et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex Nature 477 2011 549 555
40. N.J. Birdsall, A.S. Burgen, and E.C. Hulme The binding of agonists to brain muscarinic receptors Mol Pharmacol 14 1978 723 736 (Pubitemid 9026476)
41. M. Gillard, M. Waelbroeck, and J. Christophe Muscarinic receptor heterogeneity in rat central nervous system. II. Brain receptors labeled by [3H]oxotremorine-M correspond to heterogeneous M2 receptors with very high affinity for agonists Mol Pharmacol 32 1987 100 108 (Pubitemid 17112321)
42. A. Nesterov, M. Hong, C. Hertel, P. Jiao, L. Brownell, and E. Cannon Screening a plant extract library for inhibitors of cholecystokinin receptor CCK1 pathways J Biomol Screen 15 2010 518 527
43. S. Hennen, H. Wang, L. Peters, N. Merten, K. Simon, and A. Spinrath et al. Decoding signaling and function of the orphan G protein-coupled receptor GPR17 with a small-molecule agonist Sci Signal 6 2013 ra93
44. N.J. Birdsall, S. Lazareno, A. Popham, and J. Saldanha Multiple allosteric sites on muscarinic receptors Life Sci 68 2001 2517 2524 (Pubitemid 32455690)
45. M.C. Peeters, L.E. Wisse, A. Dinaj, B. Vroling, G. Vriend, and A.P. I.Jzerman The role of the second and third extracellular loops of the adenosine A1 receptor in activation and allosteric modulation Biochem Pharmacol 84 2012 76 87
46. B.F. Seibt, A.C. Schiedel, D. Thimm, S. Hinz, F.F. Sherbiny, and C.E. Müller The second extracellular loop of GPCRs determines subtype-selectivity and controls efficacy as evidenced by loop exchange study at A2 adenosine receptors Biochem Pharmacol 85 2013 1317 1329
47. J.R. Lane, E. Klaasse, J. Lin, J. van Bruchem, M.W. Beukers, and A.P. I.Jzerman Characterization of [3H]LUF5834: A novel non-ribose high-affinity agonist radioligand for the adenosine A1 receptor Biochem Pharmacol 80 2010 1180 1189
48. T. Kenakin Inverse, protean, and ligand-selective agonism: matters of receptor conformation FASEB J 15 2001 598 611 (Pubitemid 32245978)
49. A.K. Shukla, A. Manglik, A.C. Kruse, K. Xiao, R.I. Reis, and W. Tseng et al. Structure of active β-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide Nature 497 2013 137 141
50. K.J. Gregory, P.M. Sexton, A.B. Tobin, and A. Christopoulos Stimulus bias provides evidence for conformational constraints in the structure of a G protein-coupled receptor J Biol Chem 287 2012 37066 37077
51. T. Kenakin, and L.J. Miller Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery Pharmacol Rev 62 2010 265 304
52. A.M. Ring, A. Manglik, A.C. Kruse, M.D. Enos, W.I. Weis, and K.C. Garcia et al. Adrenaline-activated structure of β2-adrenoceptor stabilized by an engineered nanobody Nature 502 2013 575 579