Insights into the structure of class B GPCRs

Trends in Pharmacological Sciences

Volumn 35, Issue 1, 2014, Pages 12-22

  Hollenstein, Kaspar ^a   De Graaf, Chris ^b   Bortolato, Andrea ^a   Wang, Ming Wei ^c   Marshall, Fiona H ^a   Stevens, Raymond C ^d  

^a Heptares Therapeutics Ltd   (United Kingdom)

^b AMSTERDAM INSTITUTE FOR MOLECULES   (Netherlands)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

class B G protein coupled receptor (GPCR); corticotropin releasing factor receptor 1 (CRF1); crystal structure; glucagon receptor (GCGR); ligand binding

Indexed keywords

ALBIGLUTIDE; ALD 403; AMYLIN RECEPTOR; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; DULAGLUTIDE; ELCATONIN; ELSIGLUTIDE; EXENDIN 4; G PROTEIN COUPLED RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; LIRAGLUTIDE; LIXISENATIDE; LY 2409021; LY 2951742; PARATHYROID HORMONE[1-34]; PRAMLINTIDE; RIMEGEPANT; SALCATONIN; SECRETIN; TEDUGLUTIDE; TELCAGEPANT; TESAMORELIN; TT 401; TTP 054; UBROGEPANT; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERUCERFONT; ZP 2929;

AMINO ACID SEQUENCE; BINDING SITE; CRYSTAL STRUCTURE; DRUG MECHANISM; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

EID: 84891633786     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2013.11.001     Document Type: Review

References (70)

1. M.C. Lagerstrom et al. Structural diversity of G protein-coupled receptors and significance for drug discovery Nat. Rev. Drug Discov. 7 2008 339 357
2. S.R. Hoare Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein-coupled receptors Drug Discov. Today 10 2005 417 427 (Pubitemid 40450272)
3. C. de Graaf et al. Structure-based discovery of allosteric modulators of two related class B G-protein-coupled receptors ChemMedChem 6 2011 2159 2169
4. K. Pal et al. Structure and mechanism for recognition of peptide hormones by Class B G-protein-coupled receptors Acta Pharmacol. Sin. 33 2012 300 311
5. J.K. Archbold et al. Structural insights into RAMP modification of secretin family G protein-coupled receptors: implications for drug development Trends Pharmacol. Sci. 32 2011 591 600
6. C. Parthier et al. Passing the baton in class B GPCRs: peptide hormone activation via helix induction? Trends Biochem. Sci. 34 2009 303 310
7. V. Katritch et al. Structure-function of the G protein-coupled receptor superfamily Annu. Rev. Pharmacol. Toxicol. 53 2013 531 556
8. A.J. Venkatakrishnan et al. Molecular signatures of G-protein-coupled receptors Nature 494 2013 185 194
9. M. Congreve et al. The use of GPCR structures in drug design Adv. Pharmacol. 62 2011 1 36
10. K. Hollenstein et al. Structure of class B GPCR corticotropin-releasing factor receptor 1 Nature 499 2013 438 443
11. F.Y. Siu et al. Structure of the human glucagon class B G-protein-coupled receptor Nature 499 2013 444 449
12. N. Robertson et al. The properties of thermostabilised G protein-coupled receptors (StaRs) and their use in drug discovery Neuropharmacology 60 2011 36 44
13. Y.L. Chen et al. 2-aryloxy-4-alkylaminopyridines: discovery of novel corticotropin-releasing factor 1 antagonists J. Med. Chem. 51 2008 1385 1392 (Pubitemid 351480399)
14. D. Wootten et al. Polar transmembrane interactions drive formation of ligand-specific and signal pathway-biased family B G protein-coupled receptor conformations Proc. Natl. Acad. Sci. U.S.A. 110 2013 5211 5216
15. E. Schipani et al. Constitutive activation of the cyclic adenosine 3′,5′-monophosphate signaling pathway by parathyroid hormone (PTH)/PTH-related peptide receptors mutated at the two loci for Jansen's metaphyseal chondrodysplasia Mol. Endocrinol. 11 1997 851 858 (Pubitemid 27241778)
16. S.A. Hjorth et al. Constitutive activity of glucagon receptor mutants Mol. Endocrinol. 12 1998 78 86 (Pubitemid 28124781)
17. S.G. Rasmussen et al. Crystal structure of the beta2 adrenergic receptor-Gs protein complex Nature 477 2011 549 555
18. C. Sun et al. Solution structure and mutational analysis of pituitary adenylate cyclase-activating polypeptide binding to the extracellular domain of PAC1-RS Proc. Natl. Acad. Sci. U.S.A. 104 2007 7875 7880 (Pubitemid 47185844)
19. S. Kumar et al. Crystal structure of the PAC1R extracellular domain unifies a consensus fold for hormone recognition by class B G-protein coupled receptors PLoS ONE 6 2011 e19682
20. J. Rivier et al. Synthetic competitive antagonists of corticotropin-releasing factor: effect on ACTH secretion in the rat Science 224 1984 889 891 (Pubitemid 14102465)
21. D. Donnelly The structure and function of the glucagon-like peptide-1 receptor and its ligands Br. J. Pharmacol. 166 2012 27 41
22. T.J. Gardella et al. Molecular properties of the PTH/PTHrP receptor Trends Endocrinol. Metab. 12 2001 210 217 (Pubitemid 33714207)
23. C.S. Walker et al. Regulation of signal transduction by calcitonin gene-related peptide receptors Trends Pharmacol. Sci. 31 2010 476 483
24. E. ter Haar et al. Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism Structure 18 2010 1083 1093
25. L.J. Miller et al. Refinement of glucagon-like peptide 1 docking to its intact receptor using mid-region photolabile probes and molecular modeling J. Biol. Chem. 286 2011 15895 15907
26. K. Coopman et al. 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. 25 2011 1804 1818
27. J.M. Neumann et al. Class-B GPCR activation: is ligand helix-capping the key? Trends Biochem. Sci. 33 2008 314 319
28. H. Inooka et al. Conformation of a peptide ligand bound to its G-protein coupled receptor Nat. Struct. Biol. 8 2001 161 165 (Pubitemid 32116070)
29. J. Perret et al. 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. 362 2002 389 394 (Pubitemid 34214481)
30. S. Runge et al. Three distinct epitopes on the extracellular face of the glucagon receptor determine specificity for the glucagon amino terminus J. Biol. Chem. 278 2003 28005 28010 (Pubitemid 36899996)
31. C.G. Unson et al. Roles of specific extracellular domains of the glucagon receptor in ligand binding and signaling Biochemistry 41 2002 11795 11803
32. D.J. Roberts et al. Analysis of the glucagon receptor first extracellular loop by the substituted cysteine accessibility method Peptides 32 2011 1593 1599
33. M. Prevost et al. Mutational and cysteine scanning analysis of the glucagon receptor N-terminal domain J. Biol. Chem. 285 2010 30951 30958
34. C.M. Koth et al. Molecular basis for negative regulation of the glucagon receptor Proc. Natl. Acad. Sci. U.S.A. 109 2012 14393 14398
35. M.A. Cascieri et al. Characterization of a novel, non-peptidyl antagonist of the human glucagon receptor J. Biol. Chem. 274 1999 8694 8697 (Pubitemid 29164665)
36. V.J. Hruby et al. Conformational considerations in the design of glucagon agonists and antagonists: examination using synthetic analogs Biopolymers 25 Suppl. 1986 S135 S155
37. C.G. Unson et al. Glucagon antagonists: contribution to binding and activity of the amino-terminal sequence 1-5, position 12, and the putative alpha-helical segment 19-27 J. Biol. Chem. 264 1989 789 794 (Pubitemid 19038054)
38. J.M. Ahn et al. Development of potent truncated glucagon antagonists J. Med. Chem. 44 2001 1372 1379
39. C.R. Underwood et al. Crystal structure of glucagon-like peptide-1 in complex with the extracellular domain of the glucagon-like peptide-1 receptor J. Biol. Chem. 285 2010 723 730
40. S.K. Mathi et al. Scanning of the glucagon-like peptide-1 receptor localizes G protein-activating determinants primarily to the N terminus of the third intracellular loop Mol. Endocrinol. 11 1997 424 432 (Pubitemid 27147010)
41. Q. Xiao et al. Characterization of glucagon-like peptide-1 receptor-binding determinants J. Mol. Endocrinol. 25 2000 321 335 (Pubitemid 32059305)
42. C. Koole et al. Second extracellular loop of human glucagon-like peptide-1 receptor (GLP-1R) has a critical role in GLP-1 peptide binding and receptor activation J. Biol. Chem. 287 2012 3642 3658
43. C.C. Tseng et al. A point mutation in the glucose-dependent insulinotropic peptide receptor confers constitutive activity Biochem. Biophys. Res. Commun. 232 1997 96 100
44. T. Yaqub et al. Identification of determinants of glucose-dependent insulinotropic polypeptide receptor that interact with N-terminal biologically active region of the natural ligand Mol. Pharmacol. 77 2010 547 558
45. E. Di Paolo et al. Mutations of aromatic residues in the first transmembrane helix impair signalling by the secretin receptor Receptors Channels 6 1999 309 315 (Pubitemid 29329025)
46. E. Di Paolo et al. Contribution of the second transmembrane helix of the secretin receptor to the positioning of secretin FEBS Lett. 424 1998 207 210 (Pubitemid 28135315)
47. M. Dong et al. Mapping spatial approximations between the amino terminus of secretin and each of the extracellular loops of its receptor using cysteine trapping FASEB J. 26 2012 5092 5105
48. R.M. Solano et al. Two basic residues of the h-VPAC1 receptor second transmembrane helix are essential for ligand binding and signal transduction J. Biol. Chem. 276 2001 1084 1088 (Pubitemid 32098012)
49. E. Ceraudo et al. Spatial proximity between the VPAC1 receptor and the amino terminus of agonist and antagonist peptides reveals distinct sites of interaction FASEB J. 26 2012 2060 2071
50. R.C. Gensure et al. Identification of a contact site for residue 19 of parathyroid hormone (PTH) and PTH-related protein analogs in transmembrane domain two of the type 1 PTH receptor Mol. Endocrinol. 17 2003 2647 2658 (Pubitemid 37542225)
51. C.R. Grace et al. NMR structure and peptide hormone binding site of the first extracellular domain of a type B1 G protein-coupled receptor Proc. Natl. Acad. Sci. U.S.A. 101 2004 12836 12841 (Pubitemid 39167545)
52. C.W. Liaw et al. Localization of ligand-binding domains of human corticotropin-releasing factor receptor: a chimeric receptor approach Mol. Endocrinol. 11 1997 980 985 (Pubitemid 27241790)
53. S.R. Hoare et al. Single amino acid residue determinants of non-peptide antagonist binding to the corticotropin-releasing factor1 (CRF1) receptor Biochem. Pharmacol. 72 2006 244 255 (Pubitemid 43850430)
54. I. Assil-Kishawi et al. Residue 17 of sauvagine cross-links to the first transmembrane domain of corticotropin-releasing factor receptor 1 (CRFR1) J. Biol. Chem. 283 2008 35644 35651
55. S.A. Hinke et al. Identification of a bioactive domain in the amino-terminus of glucose-dependent insulinotropic polypeptide (GIP) Biochim. Biophys. Acta 1547 2001 143 155 (Pubitemid 32441571)
56. C.G. Unson et al. Biological activities of des-His1[Glu9]glucagon amide, a glucagon antagonist Peptides 10 1989 1171 1177 (Pubitemid 20037265)
57. B. Wu et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071
58. T. Shimamura et al. Structure of the human histamine H1 receptor complex with doxepin Nature 475 2011 65 70
59. J.S. Mason et al. New insights from structural biology into the druggability of G protein-coupled receptors Trends Pharmacol. Sci. 33 2012 249 260
60. A.A. Pioszak et al. Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1 J. Biol. Chem. 283 2008 32900 32912
61. C.R. Grace et al. NMR structure of the first extracellular domain of corticotropin-releasing factor receptor 1 (ECD1-CRF-R1) complexed with a high affinity agonist J. Biol. Chem. 285 2010 38580 38589
62. C.R. Grace et al. Structure of the N-terminal domain of a type B1 G protein-coupled receptor in complex with a peptide ligand Proc. Natl. Acad. Sci. U.S.A. 104 2007 4858 4863 (Pubitemid 47186141)
63. C. Parthier et al. Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor Proc. Natl. Acad. Sci. U.S.A. 104 2007 13942 13947 (Pubitemid 350003317)
64. A.A. Pioszak et al. Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation J. Biol. Chem. 285 2010 12435 12444
65. A.A. Pioszak et al. Molecular recognition of parathyroid hormone by its G protein-coupled receptor Proc. Natl. Acad. Sci. U.S.A. 105 2008 5034 5039 (Pubitemid 351738505)
66. A.A. Pioszak et al. Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides J. Biol. Chem. 284 2009 28382 28391
67. S. Runge et al. Crystal structure of the ligand-bound glucagon-like peptide-1 receptor extracellular domain J. Biol. Chem. 283 2008 11340 11347
68. M. Dong et al. Spatial approximation between the amino terminus of a peptide agonist and the top of the sixth transmembrane segment of the secretin receptor J. Biol. Chem. 279 2004 2894 2903 (Pubitemid 38114281)
69. E. Ceraudo et al. The vasoactive intestinal peptide (VIP) alpha-Helix up to C terminus interacts with the N-terminal ectodomain of the human VIP/Pituitary adenylate cyclase-activating peptide 1 receptor: photoaffinity, molecular modeling, and dynamics Mol. Endocrinol. 22 2008 147 155
70. J.A. Ballesteros et al. Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors S.C. Sealfon, Methods in Neurosciences Vol. 25 1995 Academic Press 366 428