Transmembrane α-helix 2 and 7 are important for small molecule-mediated activation of the GLP-1 receptor

Pharmacology

Volumn 88, Issue 5-6, 2011, Pages 340-348

  Rye Underwood, Christina ^a,c   Møller Knudsen, Sanne ^a   Schjellerup Wulff, Birgitte ^a   Bräuner Osborne, Hans ^b   Lau, Jesper ^a   Knudsen, Lotte Bjerre ^a   Peters, Günther H ^c   Reedtz Runge, Steffen ^a  

^a NOVO NORDISK A S   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

cAMP; G protein coupled receptor; Mutagenesis; Small molecule agonist

Indexed keywords

CHIMERIC PROTEIN; CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON RECEPTOR; MEMBRANE PROTEIN;

ALPHA HELIX; ARTICLE; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL;

CYCLIC AMP; GLUCAGON; GLUCAGON-LIKE PEPTIDE 1; HEK293 CELLS; HUMANS; LIGANDS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, GLUCAGON;

EID: 82355171998     PISSN: 00317012     EISSN: 14230313     Source Type: Journal    
DOI: 10.1159/000334338     Document Type: Article

References (44)

1. Holst JJ, Ørskov C, Nielsen OV, Schwartz TW: Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Lett 1987; 211: 169-174. (Pubitemid 17049446)
2. Thorens B, Porret A, Bühler L, Deng SP, Morel P, Widmann C: Cloning and functional expression of the human islet GLP-1 receptor: Demonstration that exendin-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes 1993; 42: 1678-1682. (Pubitemid 23318127)
3. Weir GC, Mojsov S, Hendrick GK, Habener JF: Glucagonlike peptide I (7-37) actions on endocrine pancreas. Diabetes 1989; 38: 338-342. (Pubitemid 19071474)
4. Knudsen LB, Nielsen PF, Huusfeldt PO, Johansen NL, Madsen K, Pedersen FZ, Thøgersen H, Wilken M, Agersø H: Potent derivatives of glucagon-like peptide-1 with pharmacokinetic properties suitable for once daily administration. J Med Chem 2000; 43: 1664-1669. (Pubitemid 30304999)
5. Madsbad S, Schmitz O, Ranstam J, Jakobsen G, Matthews DR, International Study Group: Improved glycemic control with no weight increase in patients with type 2 diabetes after once-daily treatment with the long-acting glucagon-like peptide 1 analog liraglutide (NN2211): A 12-week, double-blind, randomized, controlled trial. Diabetes care 2004; 27: 1335-1342. (Pubitemid 38679980)
6. Fredriksson R, Lagerström MC, Lundin LG, Schiöth HB: The G-protein-coupled receptors in the human genome form five main families: Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003; 63: 1256-1272. (Pubitemid 36627220)
7. Parthier C, Kleinschmidt M, Neumann P, Rudolph R, Manhart S, Schlenzig D, Fanghänel J, Rahfeld JU, Demuth HU, Stubbs MT: Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor. Proc Natl Acad Sci USA 2007; 104: 13942-13947. (Pubitemid 350003317)
8. Pioszak AA, Xu HE: Molecular recognition of parathyroid hormone by its G proteincoupled receptor. Proc Natl Acad Sci USA 2008; 105: 5034-5039. (Pubitemid 351738505)
9. Pioszak AA, Parker NR, Suino-Powell K, Xu HE: Molecular recognition of corticotrophin releasing factor by its G-protein-coupled receptor CRFR1. J Biol Chem 2008; 283: 32900-32912.
10. Runge S, Thøgersen H, Madsen K, Lau J, Rudolph R: Crystal structure of the ligandbound glucagon-like peptide-1 receptor extracellular domain. J Biol Chem 2008; 283: 11340-11347.
11. Sun C, Song D, vis-Taber RA, Barrett LW, Scott VE, Richardson PL, Pereda-Lopez A, Uchic ME, Solomon LR, Lake MR, Walter KA, Hajduk PJ, Olejniczak ET: Solution structure and mutational analysis of pituitary adenylate cyclase-activating polypeptide binding to the extracellular domain of PAC1-RS. Proc Natl Acad Sci USA 2007; 104: 7875-7880. (Pubitemid 47185844)
12. Underwood CR, Garibay P, Knudsen LB, Hastrup S, Peters GH, Rudolph R, Reedtz- Runge S: Crystal structure of glucagon-like peptide-1 in complex with the extracellular domain of the glucagon-like peptide-1 receptor. J Biol Chem 2010; 285: 723-730.
13. Hoare SR: Mechanisms of peptide and nonpeptide ligand binding to class B G-protein coupled receptors. Drug Discov Today 2005; 10: 417-427. (Pubitemid 40450272)
14. Di PE, De NP, Moguilevsky N, Petry H, Bollen A, Waelbroeck M, Robberecht P: Contribution of the second transmembrane helix of the secretin receptor to the positioning of secretin. FEBS Lett 1998; 424: 207-210. (Pubitemid 28135315)
15. Perret J, Van CM, Langer I, Vertongen P, Gregoire F, Robberecht P, Waelbroeck M: Mutational analysis of the glucagon receptor: Similarities with the vasoactive intestinal peptide (VIP)/pituitary adenylate cyclase-Activating peptide (PACAP)/secretin receptors for recognition of the ligand's third residue. Biochem J 2002; 362: 389-394. (Pubitemid 34214481)
16. Solano RM, Langer I, Perret J, Vertongen P, Juarranz MG, Robberecht P, Waelbroeck M: Two basic residues of the h-VPAC1 receptor second transmembrane helix are essential for ligand binding and signal transduction. J Biol Chem 2001; 276: 1084-1088. (Pubitemid 32098012)
17. Turner PR, Bambino T, Nissenson RA: Mutations of neighboring polar residues on the second transmembrane helix disrupt signaling by the parathyroid hormone receptor. Mol Endocrinol 1996; 10: 132-139. (Pubitemid 26042545)
18. Gardella TJ, Luck MD, Fan MH, Lee C: Transmembrane residues of the parathyroid hormone (PTH)/PTH-related peptide receptor that specifically affect binding and signaling by agonist ligands. J Biol Chem 1996; 271: 12820-12825. (Pubitemid 26175855)
19. Rölz C, Pellegrini M, Mierke DF: Molecular characterization of the receptor-ligand complex for parathyroid hormone. Biochemistry 1999; 38: 6397-6405.
20. Chugunov AO, Simms J, Poyner DR, Dehouck Y, Rooman M, Gilis D, Langer I: Evidence that interaction between conserved residues in transmembrane helices 2, 3, and 7 are crucial for human VPAC1 receptor activation. Mol Pharmacol 2010; 78: 394-401.
21. Gaudin P, Maoret JJ, Couvineau A, Rouyer- Fessard C, Laburthe M: Constitutive activation of the human vasoactive intestinal peptide 1 receptor, a member of the new class II family of G protein-coupled receptors. J Biol Chem 1998; 273: 4990-4996. (Pubitemid 28108654)
22. Hjorth SA, Ørskov C, Schwartz TW: Constitutive activity of glucagon receptor mutants. Mol Endocrinol 1998; 12: 78-86. (Pubitemid 28124781)
23. Schipani E, Jensen GS, Pincus J, Nissenson RA, Gardella TJ, Jüppner H: Constitutive activation of the cyclic adenosine 3 ,5α- monophosphate signaling pathway by parathyroid hormone (PTH)/PTH-related peptide receptors mutated at the two loci for Jansen's metaphyseal chondrodysplasia. Mol Endocrinol 1997; 11: 851-858. (Pubitemid 27241778)
24. Schipani E, Langman C, Hunzelman J, Le- Merrer M, Loke KY, Dillon MJ, Silve C, Jüppner H: A novel parathyroid hormone (PTH)/PTHrelated peptide receptor mutation in Jansen's metaphyseal chondrodysplasia. J Clin Endocrinol Metab 1999; 84: 3052-3057. (Pubitemid 30646922)
25. Turner PR, Mefford S, Bambino T, Nissenson RA: Transmembrane residues together with the amino terminus limit the response of the parathyroid hormone (PTH) 2 receptor to PTH-related peptide. J Biol Chem 1998; 273: 3830-3837. (Pubitemid 28103237)
26. Cascieri MA, Koch GE, Ber E, Sadowski SJ, Louizides D, de Laszlo SE, Hacker C, Hagmann WK, MacCoss M, Chicchi GG, Vicario PP: Characterization of a novel, non-peptidyl antagonist of the human glucagon receptor. J Biol Chem 1999; 274: 8694-8697. (Pubitemid 29164665)
27. Chen D, Liao J, Li N, Zhou C, Liu Q, Wang G, Zhang R, Zhang S, Lin L, Chen K, Xie X, Nan F, Young AA, Wang MW: A nonpeptidic agonist of glucagon-like peptide 1 receptors with efficacy in diabetic db/db mice. Proc Natl Acad Sci USA 2007; 104: 943-948. (Pubitemid 46154716)
28. Dong M, Cox RF, Miller LJ: Juxtamembranous region of the amino terminus of the family B G protein-coupled calcitonin receptor plays a critical role in small-molecule agonist action. J Biol Chem 2009; 284: 21839-21847.
29. Katayama T, Furuya M, Yamaichi K, Konishi K, Sugiura N, Murafuji H, Magota K, Saito M, Tanaka S, Oikawa S: Discovery of a nonpeptide small molecule that selectively mimics the biological actions of calcitonin. Biochim Biophys Acta 2001; 1526: 183-190. (Pubitemid 32452254)
30. Knudsen LB, Kiel D, Teng M, Behrens C, Bhumralkar D, Kodra JT, Holst JJ, Jeppesen CB, Johnson MD, de Jong JC, Jorgensen AS, Kercher T, Kostrowicki J, Madsen P, Olesen PH, Petersen JS, Poulsen F, Sidelmann UG, Sturis J, Truesdale L, May J, Lau J: Smallmolecule agonists for the glucagon-like peptide 1 receptor. Proc Natl Acad Sci USA 2007; 104: 937-942. (Pubitemid 46154715)
31. Liaw CW, Grigoriadis DE, Lorang MT, De Souza EB, Maki RA: Localization of agonistand antagonist-binding domains of human corticotropin-releasing factor receptors. Mol Endocrinol 1997; 11: 2048-2053. (Pubitemid 27524887)
32. Tibaduiza EC, Chen C, Beinborn M: A small molecule ligand of the glucagon-like peptide 1 receptor targets its amino-terminal hormone binding domain. J Biol Chem 2001; 276: 37787-37793.
33. ter-Haar E, Koth CM, bdul-Manan N, Swenson L, Coll JT, Lippke JA, Lepre CA, Garcia Guzman M, Moore JM: Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure 2010; 18: 1083-1093.
34. Sloop KW, Willard FS, Brenner MB, Ficorilli J, Valasek K, Showalter AD, Farb TB, Cao JX, Cox AL, Michael MD, Gutierrez-Sanfeliciano SM, Tebbe MJ, Coghlan MJ: Novel small molecule glucagon-like peptide-1 receptor agonist stimulates insulin secretion in rodents and from human islets. Diabetes 2010; 59: 3099-3107.
35. Lin F, Wang RX: Molecular modeling of the three-dimensional structure of GLP-1R and its interactions with several agonists. J Mol Model 2009; 15: 53-65.
36. Lok S, Kuijper JL, Jelinek LJ, et al: The human glucagon receptor encoding gene: Structure, cDNA sequence and chromosomal localization. Gene 1994; 140: 203-209. (Pubitemid 24115231)
37. Thorens B: Expression cloning of the pancreatic beta cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc Natl Acad Sci USA 1992; 89: 8641-8645.
38. Runge S, Wulff BS, Madsen K, Bräuner-Osborne H, Knudsen LB: Different domains of the glucagon and glucagon-like peptide-1 receptors provide the critical determinants of ligand selectivity. Br J Pharmacol 2003; 138: 787-794. (Pubitemid 36390634)
39. Frimurer TM, Bywater RP: Structure of the integral membrane domain of the GLP1 receptor. Proteins 1999; 35: 375-386. (Pubitemid 29264834)
40. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, Stevens RC: High-resolution crystal structure of an engineered human beta2-adrenergic G protein- coupled receptor. Science 2007; 318: 1258-1265. (Pubitemid 350172884)
41. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Yao XJ, Weis WI, Stevens RC, Kobilka BK: GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 2007; 318: 1266-1273. (Pubitemid 350172885)
42. Thomas BE, Woznica I, Mierke DF, Wittelsberger A, Rosenblatt M: Conformational changes in the parathyroid hormone receptor associated with activation by agonist. Mol Endocrinol 2008; 22: 1154-1162. (Pubitemid 351629615)
43. Runge S, Gram C, Bräuner-Osborne H, Madsen K, Knudsen LB, Wulff BS: Three distinct epitopes on the extracellular face of the glucagon receptor determine specificity for the glucagon amino terminus. J Biol Chem 2003; 278: 28005-28010. (Pubitemid 36899996)
44. Coopman K, Wallis R, Robb G, Brown AJH, Wilkinson GF, Timms D, Willars GB: Residues within the transmembrane domain of the glucagon-like peptide-1 receptor involved in ligand binding and receptor activation: Modelling the ligand-bound receptor. Mol Endocrinol 2011; 25: 1804-1818.