Investigating G protein signalling bias at the glucagon-like peptide-1 receptor in yeast

British Journal of Pharmacology

Volumn 171, Issue 15, 2014, Pages 3651-3665

  Weston, C ^a   Poyner, D ^b   Patel, V ^a   Dowell, S ^c   Ladds, G ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

diabetes; exenatide; G proteins; glucagon; glucagon like peptide 1 (GLP 1); GPCR; liraglutide; signal bias

Indexed keywords

GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHIMERA; CONTROLLED STUDY; FUNGAL STRAIN; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; YEAST; AGONISTS; GENETICS; HEK293 CELL LINE; METABOLISM; SACCHAROMYCES CEREVISIAE;

GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 84904546714     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12716     Document Type: Article

References (49)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, Peters JA, Harmar AJ, and CGTP Collaborators (2013). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
2. Anderson SL, Trujillo JM, (2010). Association of pancreatitis with glucagon-like peptide-1 agonist use. Ann Pharmacother 44: 904-909.
3. Baggio LL, Drucker DJ, (2007). Biology of Incretins: GLP-1 and GIP. Gastroenterology 32: 2131-2157.
4. 2A receptor 1. Br J Pharmacol 169: 988-998.
5. Black JW, Leff P, (1983). Operational models of pharmacological agonism. Proc R Soc Lond B Biol Sci 220: 141-162.
6. Bond M, Croft W, Tyson R, Bretschneider T, Davey J, Ladds G, (2013). Quantitative analysis of human ras localization and function in the fission yeast Schizosaccharomyces pombe. Yeast 30: 145-156.
7. Brown AJ, Dyos SL, Whiteway MS, White JH, Watson MAE, Marzioch M, etal. (2000). Functional coupling of mammalian receptors to the yeast mating pathway using novel yeast/mammalian G protein α-subunit chimeras. Yeast 16: 11-22.
8. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, etal. (2003). The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278: 11312-11319.
9. Butler AE, Campbell-Thompson M, Gurlo T, Dawson DW, Atkinson M, Butler PC, (2013). Marked expansion of exocrine and endocrine pancreas with incretin therapy in humans with increased exocrine pancreas dysplasia and the potential for glucagon-producing neuroendocrine tumors. Diabetes 62: 2595-2604.
10. Cho YM, Merchant CE, Kieffer TJ, (2012). Targeting the glucagon receptor family for diabetes and obesity therapy. Pharmacol Ther 135: 247-278.
11. Coopman K, Huang Y, Johnston N, Bradley SJ, Wilkinson GF, Willars GB, (2010). Comparative effects of the endogenous agonist glucagon-like peptide-1 (GLP-1)-(7-36) amide and the small-molecule ago-allosteric agent 'compound 2' at the GLP-1 receptor. J Pharmacol Exp Ther 334: 795-808.
12. Dohlman HG, Apaniesk D, Chen Y, Song J, Nusskern D, (1995). Inhibition of G-protein signaling by dominant gain-of-function mutations in Sst2p, a pheromone desensitization factor in Saccharomyces cerevisiae. Mol Cell Biol 15: 3635-3643.
13. Dowell SJ, Brown AJ, (2002). Yeast assays for G-protein-coupled receptors. Receptors Channels 8: 343-352.
14. Dowell SJ, Brown AJ, (2009). Yeast assays for G protein-coupled receptors. In: G Protein-Coupled Receptors in Drug Discovery. Humana Press: New York, pp. 213-229.
15. Figueroa KW, Griffin MT, Ehlert FJ, (2009). Selectivity of agonists for the active state of M1 to M4 muscarinic receptor subtypes. J Pharmacol Exp Ther 328: 331-342.
16. Franks AS, Lee PH, George CM, (2012). Pancreatitis: a potential complication of liraglutide? Ann Pharmacother 46: 1547-1553.
17. Gaddum JH, Hameed KA, Hathway DE, Stephens FF, (1955). Quantitative studies of antagonists for 5-hydroxytryptamine. Q J Exp Physiol Cogn Med Sci 40: 49-74.
18. Gietz RD, Schiestl RH, (2007). High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34.
19. Göke R, Fehmann HC, Linn T, Schmidt H, Krause M, Eng J, etal. (1993). Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta-cells. J Biol Chem 268: 19650-19655.
20. Hallbrink M, Holmqvist T, Olsson M, Ostenson CG, Efendic S, Langel U, (2001). Different domains in the third intracellular loop of the GLP-1 receptor are responsible for Galpha(s) and Galpha(i)/Galpha(o) activation. Biochim Biophys Acta 1546: 79-86.
21. Hoare SR, (2005). Mechanisms of peptide and nonpeptide ligand binding to class B G-protein-coupled receptors. Drug Discov Today 10: 417-427.
22. Holst JJ, Seino Y, (2009). GLP-1 receptor agonists: targeting both hyperglycaemia and disease processes in diabetes. Diabetes Res Clin Pract 85: 1-3.
23. Jorgensen R, Kubale V, Vrecl M, Schwartz TW, Elling CE, (2007). Oxyntomodulin differentially affects glucagon-like peptide-1 receptor β-arrestin recruitment and signaling through Gα. J Pharmacol Exp Ther 322: 148-154.
24. Kenakin TP, (1995). Agonist-receptor efficacy II: agonist trafficking of receptor signals. Trends Pharmacol Sci 16: 232-238.
25. Knudsen LB, Kiel D, Teng M, Behrens C, Bhumralkar D, Kodra JT, etal. (2007). Small-molecule agonists for the glucagon-like peptide 1 receptor. Proc Natl Acad Sci U S A 104: 937-942.
26. Koole C, Wootten D, Simms J, Valant C, Sridhar R, Woodman OL, etal. (2010). Allosteric ligands of the glucagon-like peptide 1 receptor (GLP-1R) differentially modulate endogenous and exogenous peptide responses in a pathway-selective manner: implications for drug screening. Mol Pharmacol 78: 456-465.
27. Ladds G, Davey J, (2000). Sxa2 is a serine carboxypeptidase that degrades extracellular P-factor in the fission yeast Schizosaccharomyces pombe. Mol Microbiol 36: 377-390.
28. Ladds G, Davis K, Hillhouse EW, Davey J, (2003). Modified yeast cells to investigate the coupling of G protein-coupled receptors to specific G proteins. Mol Microbiol 47: 781-792.
29. Ladds G, Goddard A, Davey J, (2005a). Functional analysis of heterologous GPCR signalling pathways in yeast. Trends Biotechnol 23: 367-373.
30. Ladds G, Davis K, Das A, Davey J, (2005b). A constitutively active GPCR retains its G protein specificity and the ability to form dimers. Mol Microbiol 55: 482-497.
31. McIntyre N, Holdsworth CD, Turner DS, (1964). New interpretation of oral glucose tolerance. Lancet 2: 20-21.
32. Mentlein R, Gallwitz B, Schmidt WE, (1993). Dipeptidyl-peptidase IV hydrolyses gastric inhibitory polypeptide, glucagon-like peptide-1(7-36)amide, peptide histidine methionine and is responsible for their degradation in human serum. Eur J Biochem 214: 829-835.
33. Miret JJ, Rakhilina L, Silverman L, Oehlen B, (2002). Functional expression of heteromeric calcitonin gene-related peptide and adrenomedullin receptors in yeast. J Biol Chem 27: 6881-6887.
34. Montrose-Rafizadeh C, Avdonin P, Garant MJ, Rodgers BD, Kole S, Yang H, etal. (1999). Pancreatic glucagon-like peptide-1 receptor couples to multiple G proteins and activates mitogen-activated protein kinase pathways in Chinese hamster ovary cells. Endocrinology 140: 1132-1140.
35. Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, Sherwin R, etal. (2009). Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 32: 193-203.
36. Nauck MA, (2011). Incretin-based therapies for type 2 diabetes mellitus: properties, functions, and clinical implications. Am J Med 124: S3-S18.
37. Pabreja K, Mohd MA, Koole C, Wootten D, Furness SGB, (2014). Molecular mechanisms underlying physiological and receptor pleiotropic effects mediated by GLP-1R activation. Br J Pharmacol 171: 1114-1128.
38. Poyner DR, Andrew DP, Brown D, Bose C, Hanley MR, (1992). Pharmacological characterization of a receptor for calcitonin gene-related peptide on rat, L6 myocytes. Br J Pharmacol 105: 441-447.
39. Quddusi S, Vahl TP, Hanson K, Prigeon RL, D'Alessio DA, (2003). Differential effects of acute and extended infusions of glucagon-like peptide-1 on first- and second-phase insulin secretion in diabetic and nondiabetic humans. Diabetes Care 26: 791-798.
40. Rajagopal S, Ahn S, Rominger DH, Gowen-MacDonald W, Lam CM, DeWire SM, etal. (2011). Quantifying ligand bias at seven-transmembrane receptors. Mol Pharmacol 80: 367-377.
41. Schepp W, Schmidtler J, Dehne K, Schusdziarra V, Classen M, (1992). Pertussis toxin-sensitive and pertussis toxin-insensitive inhibition of parietal cell response to GLP-1 and histamine. Am J Physiol Gastrointest Liver Physiol 262: G660-G668.
42. Schepp W, Dehne K, Riedel T, Schmidtler J, Schaffer K, Classen M, (1996). Oxyntomodulin: a cAMP-dependent stimulus of rat parietal cell function via the receptor for glucagon-like peptide-1 (7-36) NH2. Digestion 57: 398-405.
43. Scott DA, Boye KS, Timlin L, Clark JF, Best JH, (2013). A network meta-analysis to compare glycaemic control in patients with type 2 diabetes treated with exenatide once weekly or liraglutide once daily in comparison with insulin glargine, exenatide twice daily or placebo. Diabetes Obes Metab 15: 213-223.
44. Seino S, (2012). Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea. Diabetologia 55: 2096-2108.
45. Singh S, Chang H-Y, Richards TM, Weiner JP, Clark JM, Degal JB, (2013). Glucagon-like peptide-1-based therapies and risk of hospitalization for acute pancreatitis in type 2 diabetes mellitus: a population-based matched case-control study. JAMA Intern Med 172: 534-540.
46. Sloop KW, Willard FS, Brenner MB, Ficorilli J, Valasek K, Showalter AD, etal. (2010). Novel small molecule glucagon-like peptide-1 receptor agonist stimulates insulin secretion in rodents and from human islets. Diabetes 59: 3099-3107.
47. 1 receptor agonist and antagonist pharmacology using Saccharomyces cerevisiae: implications for ligand screening and functional selectivity. J Pharmacol Exp Ther 331: 271-286.
48. Wootten D, Savage EE, Valant C, May LT, Sloop KW, Ficorilli J, etal. (2012). Allosteric modulation of endogenous metabolites as an avenue for drug discovery. Mol Pharmacol 82: 281-290.
49. Wynne K, Park AJ, Small CJ, Patterson M, Ellis SM, Murphy KG, etal. (2005). Subcutaneous oxyntomodulin reduces body weight in overweight and obese subjects a double-blind, randomized, controlled trial. Diabetes 54: 2390-2395.