Quantification of ligand bias for clinically relevant b2-adrenergic receptor ligands: Implications for drug taxonomy s

Molecular Pharmacology

Volumn 85, Issue 3, 2014, Pages 492-509

  Van Der Westhuizen, Emma T ^a,b   Breton, Billy ^a   Christopoulos, Arthur ^b   Bouvier, Michel ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL LINE; CYCLIC AMP; DRUG DISCOVERY; ENDOCYTOSIS; HEK293 CELLS; HUMANS; LIGANDS; MAP KINASE SIGNALING SYSTEM; PHARMACEUTICAL PREPARATIONS; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION;

EID: 84894090269     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.088880     Document Type: Article

References (57)

1. Azzi M, Charest PG, Angers S, Rousseau G, Kohout T, Bouvier M, and Piñeyro G (2003) Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc Natl Acad Sci USA 100:11406-11411.
2. Baker JG (2010) The selectivity of beta-adrenoceptor agonists at human beta1-, beta2-and beta3-adrenoceptors. Br J Pharmacol 160:1048-1061.
3. Baker JG (2005) The selectivity of beta-adrenoceptor antagonists at the human beta1, beta2 and beta3 adrenoceptors. Br J Pharmacol 144:317-322.
4. Baker JG, Hall IP, and Hill SJ (2003) Agonist and inverse agonist actions of betablockers at the human beta 2-adrenoceptor provide evidence for agonist-directed signaling. Mol Pharmacol 64:1357-1369.
5. Baker JG, Hill SJ, and Summers RJ (2011) Evolution of b-blockers: From anti-anginal drugs to ligand-directed signalling. Trends Pharmacol Sci 32:227-234.
6. Black JW and Leff P (1983) Operational models of pharmacological agonism. Proc R Soc Lond B Biol Sci 220:141-162.
7. Black JW, Leff P, Shankley NP, and Wood J (1985) An operational model of pharmacological agonism: The effect of E/[A] curve shape on agonist dissociation constant estimation. Br J Pharmacol 84:561-571.
8. Castle W, Fuller R, Hall J, and Palmer J (1993) Serevent nationwide surveillance study: Comparison of salmeterol with salbutamol in asthmatic patients who require regular bronchodilator treatment. BMJ 306:1034-1037.
9. Chidiac P, Hebert TE, Valiquette M, Dennis M, and BouvierM (1994) Inverse agonist activity of beta-adrenergic antagonists. Mol Pharmacol 45:490-499.
10. Cruickshank JM (1993) The xamoterol experience in the treatment of heart failure. Am J Cardiol 71:61C-64C.
11. Daaka Y, Luttrell LM, and Lefkowitz RJ (1997) Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390: 88-91.
12. Daaka Y, Luttrell LM, Ahn S, Della Rocca GJ, Ferguson SS, Caron MG, and Lefkowitz RJ (1998) Essential role for G protein-coupled receptor endocytosis in the activation of mitogen-activated protein kinase. J Biol Chem 273:685-688.
13. Del Carmine R, Ambrosio C, Sbraccia M, Cotecchia S, Ijzerman AP, and Costa T (2002) Mutations inducing divergent shifts of constitutive activity reveal different modes of binding among catecholamine analogues to the beta(2)-adrenergic receptor. Br J Pharmacol 135:1715-1722.
14. Dittman AH, Weber JP, Hinds TR, Choi EJ, Migeon JC, Nathanson NM, and Storm DR (1994) A novel mechanism for coupling of m4 muscarinic acetylcholine receptors to calmodulin-sensitive adenylyl cyclases: Crossover from G protein-coupled inhibition to stimulation. Biochemistry 33:943-951.
15. Drake MT, Violin JD, Whalen EJ, Wisler JW, Shenoy SK, and Lefkowitz RJ (2008) beta-arrestin-biased agonism at the beta2-adrenergic receptor. J Biol Chem 283: 5669-5676.
16. Ehlert FJ (2008) On the analysis of ligand-directed signaling at G protein-coupled receptors. Naunyn Schmiedebergs Arch Pharmacol 377:549-577.
17. Eichhorn EJ and Young JB (2001) Optimizing the use of beta-blockers in the effective treatment and management of heart failure: A case study approach. Am J Med 110 (Suppl 5A):11S-20S.
18. Elster L, Elling C, and Heding A (2007) Bioluminescence resonance energy transfer as a screening assay: Focus on partial and inverse agonism. J Biomol Screen 12: 41-49.
19. Evans BA, Broxton N, Merlin J, Sato M, Hutchinson DS, Christopoulos A, and Summers RJ (2011) Quantification of functional selectivity at the human a(1A)-adrenoceptor. Mol Pharmacol 79:298-307.
20. Evans BA, Sato M, Sarwar M, Hutchinson DS, and Summers RJ (2010) Liganddirected signalling at beta-adrenoceptors. Br J Pharmacol 159:1022-1038.
21. Ferguson-Myrthil N (2012) Vasopressor use in adult patients. Cardiol Rev 20: 153-158.
22. Figueroa KW, Griffin MT, and Ehlert FJ (2009) Selectivity of agonists for the active state of M1 to M4 muscarinic receptor subtypes. J Pharmacol Exp Ther 328: 331-342.
23. Frielle T, Kobilka B, Lefkowitz RJ, and Caron MG (1988) Human beta 1-and beta 2-adrenergic receptors: Structurally and functionally related receptors derived from distinct genes. Trends Neurosci 11:321-324.
24. Galandrin S and Bouvier M (2006) Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol Pharmacol 70: 1575-1584.
25. Helfand M, Peterson K, and Dana T (2007) Drug class review on beta adrenergic blockers: Final report. Portland, OR: Oregon Health & Science University.
26. Hoffmann C, Leitz MR, Oberdorf-Maass S, Lohse MJ, and Klotz KN (2004) Comparative pharmacology of human beta-adrenergic receptor subtypes- characterization of stably transfected receptors in CHO cells. Naunyn Schmiedebergs Arch Pharmacol 369:151-159.
27. Illarionov BA, Frank LA, Illarionova VA, Bondar VS, Vysotski ES, and Blinks JR (2000) Recombinant obelin: Cloning and expression of cDNA purification, and characterization as a calcium indicator. Methods Enzymol 305:223-249.
28. Isogaya M, Sugimoto Y, Tanimura R, Tanaka R, Kikkawa H, Nagao T, and Kurose H (1999) Binding pockets of the beta(1)-and beta(2)-adrenergic receptors for subtypeselective agonists. Mol Pharmacol 56:875-885.
29. Javed U and Deedwania PC (2009) Beta-adrenergic blockers for chronic heart failure. Cardiol Rev 17:287-292.
30. Keiper M, Stope MB, Szatkowski D, Böhm A, Tysack K, Vom Dorp F, Saur O, Oude Weernink PA, and Evellin S et al. (2004) Epac-and Ca21-controlled activation of Ras and extracellular signal-regulated kinases by Gs-coupled receptors. J Biol Chem 279:46497-46508.
31. Kenakin T and Christopoulos A (2013) Signalling bias in new drug discovery: Detection, quantification and therapeutic impact. Nat Rev Drug Discov 12:205-216.
32. Kenakin T, Watson C, Muniz-Medina V, Christopoulos A, and Novick S (2012) A simple method for quantifying functional selectivity and agonist bias. ACS Chem Neurosci 3:193-203.
33. Liapakis G, Chan WC, Papadokostaki M, and Javitch JA (2004) Synergistic contributions of the functional groups of epinephrine to its affinity and efficacy at the beta2 adrenergic receptor. Mol Pharmacol 65:1181-1190.
34. McGraw DW, Almoosa KF, Paul RJ, Kobilka BK, and Liggett SB (2003) Antithetic regulation by b-adrenergic receptors of Gq receptor signaling via phospholipase C underlies the airway b-agonist paradox. J Clin Invest 112:619-626.
35. McLean-Tooke AP, Bethune CA, Fay AC, and Spickett GP (2003) Adrenaline in the treatment of anaphylaxis: What is the evidence? BMJ 327:1332-1335.
36. Moore RH, Millman EE, Godines V, Hanania NA, Tran TM, Peng H, Dickey BF, Knoll BJ, and Clark RB (2007) Salmeterol stimulation dissociates beta2-adrenergic receptor phosphorylation and internalization. Am J Respir Cell Mol Biol 36: 254-261.
37. Pauwels PJ, Gommeren W, Van Lommen G, Janssen PA, and Leysen JE (1988) The receptor binding profile of the new antihypertensive agent nebivolol and its stereoisomers compared with various beta-adrenergic blockers. Mol Pharmacol 34: 843-851.
38. Pauwels PJ, Van Gompel P, and Leysen JE (1991) Human beta 1-and beta 2-adrenergic receptor binding and mediated accumulation of cAMP in transfected Chinese hamster ovary cells. Profile of nebivolol and known beta-adrenergic blockers. Biochem Pharmacol 42:1683-1689.
39. Peng H, Bond RA, and Knoll BJ (2011) The effects of acute and chronic nadolol treatment on b2AR signaling in HEK293 cells. Naunyn Schmiedebergs Arch Pharmacol 383:209-216.
40. Pönicke K, Heinroth-Hoffmann I, and Brodde OE (2002) Differential effects of bucindolol and carvedilol on noradenaline-induced hypertrophic response in ventricular cardiomyocytes of adult rats. J Pharmacol Exp Ther 301:71-76.
41. Ponsioen B, Zhao J, Riedl J, Zwartkruis F, van der Krogt G, Zaccolo M, Moolenaar WH, Bos JL, and Jalink K (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 5:1176-1180.
42. Rajagopal S, Ahn S, Rominger DH, Gowen-MacDonald W, Lam CM, Dewire SM, Violin JD, and Lefkowitz RJ (2011) Quantifying ligand bias at seventransmembrane receptors. Mol Pharmacol 80:367-377.
43. Ram CV (2010) Beta-blockers in hypertension. Am J Cardiol 106:1819-1825.
44. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VR, Sanishvili R, and Fischetti RF et al. (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450:383-387.
45. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, and Calinski D et al. (2011) Crystal structure of the b2 adrenergic receptor-Gs protein complex. Nature 477:549-555.
46. Reed SE, Staley EM, Mayginnes JP, Pintel DJ, and Tullis GE (2006) Transfection of mammalian cells using linear polyethylenimine is a simple and effective means of producing recombinant adeno-associated virus vectors. J Virol Methods 138:85-98.
47. Rovati GE and Nicosia S (1994) Lower efficacy: Interaction with an inhibitory receptor or partial agonism? Trends Pharmacol Sci 15:140-144.
48. Schmidt M, Evellin S, Weernink PA, von Dorp F, Rehmann H, Lomasney JW, and Jakobs KH (2001) A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 3:1020-1024.
49. Shenoy SK, Drake MT, Nelson CD, Houtz DA, Xiao K, Madabushi S, Reiter E, Premont RT, Lichtarge O, and Lefkowitz RJ (2006) beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J Biol Chem 281:1261-1273.
50. Tzingounis AV, von Zastrow M, and Yudowski GA (2010) b-blocker drugs mediate calcium signaling in native central nervous system neurons by b-arrestin-biased agonism. Proc Natl Acad Sci USA 107:21028-21033.
51. U'Prichard DC, Bylund DB, and Snyder SH (1978). (1/-2)-[3H]epinephrine and (-) [3H]dihydroalprenolol binding to beta1-and beta2-noradrenergic receptors in brain, heart, and lung membranes. J Biol Chem 253: 5090-5102.
52. Violin JD, DiPilato LM, Yildirim N, Elston TC, Zhang J, and Lefkowitz RJ (2008) beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J Biol Chem 283:2949-2961.
53. Violin JD, Soergel DG, Boerrigter G, Burnett JC, Jr, and Lark MW (2013) GPCR biased ligands as novel heart failure therapeutics. Trends Cardiovasc Med 23: 242-249.
54. Wacker D, Fenalti G, Brown MA, Katritch V, Abagyan R, Cherezov V, and Stevens RC (2010) Conserved binding mode of human beta2 adrenergic receptor inverse agonists and antagonist revealed by X-ray crystallography.J AmChemSoc 132:11443-11445.
55. Wisler JW, DeWire SM, Whalen EJ, Violin JD, Drake MT, Ahn S, Shenoy SK, and Lefkowitz RJ (2007) A unique mechanism of beta-blocker action: Carvedilol stimulates beta-arrestin signaling. Proc Natl Acad Sci USA 104:16657-16662.
56. Zhang ZS, Cheng HJ, Ukai T, Tachibana H, and Cheng CP (2001) Enhanced cardiac L-type calcium current response to b2-adrenergic stimulation in heart failure. J Pharmacol Exp Ther 298:188-196.
57. Zimmerman B, Beautrait A, Aguila B, Charles R, Escher E, Claing A, Bouvier M, and Laporte SA (2012) Differential b-arrestin-dependent conformational signaling and cellular responses revealed by angiotensin analogs. Sci Signal 5:ra33.