Structure and mechanism for recognition of peptide hormones by Class B G-protein-coupled receptors

Acta Pharmacologica Sinica

Volumn 33, Issue 3, 2012, Pages 300-311

  Pal, Kuntal ^a   Melcher, Karsten ^a   Xu, H Eric ^a,b  

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

calcitonin; crystal structure; G protein coupled receptor (GPCR); glucagons; parathyroid hormone

Indexed keywords

CALCITONIN; CORTICOTROPIN RELEASING FACTOR; EXENDIN 4; G PROTEIN COUPLED RECEPTOR; GLUCAGON; LIRAGLUTIDE; PARATHYROID HORMONE; PARATHYROID HORMONE[1-34]; PEPTIDE HORMONE; PRAMLINTIDE; RECOMBINANT PARATHYROID HORMONE; SALCATONIN; SMYLIN; TEDUGLUTIDE; TELCAGEPANT; TESAMORELIN; UNCLASSIFIED DRUG;

ARTICLE; DEVELOPMENT; DIABETES MELLITUS; DRUG INDICATION; DRUG TARGETING; HORMONE BINDING; HORMONE RECEPTOR INTERACTION; HORMONE STRUCTURE; HUMAN; METABOLIC REGULATION; OSTEOPOROSIS; PROTEIN DOMAIN; PROTEIN FAMILY; RECEPTOR AFFINITY; SKELETON; STRESS;

AMINO ACID SEQUENCE; HUMANS; LIGANDS; MOLECULAR SEQUENCE DATA; PEPTIDE HORMONES; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, G-PROTEIN-COUPLED; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84863274700     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2011.170     Document Type: Article

References (76)

1. Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB. The G-proteincoupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003; 63: 1256-72. (Pubitemid 36627220)
2. Foord SM, Bonner TI, Neubig RR, Rosser EM, Pin JP, Davenport AP, et al. International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacol Rev 2005; 57: 279-88. (Pubitemid 41043887)
3. Harmar AJ. Family-B G-protein-coupled receptors. Genome Biol 2001; 2; REVIEWS3013.
4. Lagerstrom MC, Schioth HB. Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat Rev Drug Discov 2008; 7: 339-57.
5. Grace CR, Perrin MH, DiGruccio MR, Miller CL, Rivier JE, Vale WW, 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 2004; 101: 12836-41. (Pubitemid 39167545)
6. Grace CR, Perrin MH, Gulyas J, Digruccio MR, Cantle JP, Rivier JE, 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 2007; 104: 4858-63. (Pubitemid 47186141)
7. Parthier C, Kleinschmidt M, Neumann P, Rudolph R, Manhart S, Schlenzig D, et al. Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor. Proc Natl Acad Sci U S A 2007; 104: 13942-7. (Pubitemid 350003317)
8. Sun C, Song D, Davis-Taber RA, Barrett LW, Scott VE, Richardson PL, 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 2007; 104: 7875-80. (Pubitemid 47185844)
9. Runge S, Thogersen H, Madsen K, Lau J, Rudolph R. Crystal structure of the ligand-bound glucagon-like peptide-1 receptor extracellular domain. J Biol Chem 2008; 283: 11340-7.
10. Pioszak AA, Xu HE. Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc Natl Acad Sci U S A 2008; 105: 5034-9. (Pubitemid 351738505)
11. Pioszak AA, Parker NR, Suino-Powell K, Xu HE. Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1. J Biol Chem 2008; 283: 32900-12.
12. Pioszak AA, Parker NR, Gardella TJ, Xu HE. Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides. J Biol Chem 2009; 284: 28382-91.
13. Grace CR, Perrin MH, Gulyas J, Rivier JE, Vale WW, Riek R. 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 2010; 285: 38580-9.
14. Pal K, Swaminathan K, Xu HE, Pioszak AA. Structural basis for hormone recognition by the Human CRFR2{alpha} G protein-coupled receptor. J Biol Chem 2010; 285: 40351-61.
15. ter Haar E, Koth CM, Abdul-Manan N, Swenson L, Coll JT, Lippke JA, et al. Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure 2010; 18: 1083-93.
16. Kumar S, Pioszak A, Zhang C, Swaminathan K, Xu HE. Crystal structure of the PAC1R extracellular domain unifies a consensus fold for hormone recognition by class B G-protein coupled receptors. PLoS One 2011; 6: e19682.
17. Horvath K, Stefanatos G, Sokolski KN, Wachtel R, Nabors L, Tildon JT. Improved social and language skills after secretin administration in patients with autistic spectrum disorders. J Assoc Acad Minor Phys 1998; 9: 9-15.
18. Bale TL, Vale WW. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 2004; 44: 525-57. (Pubitemid 38263852)
19. Hao Z, Huang Y, Cleman J, Jovin IS, Vale WW, Bale TL, et al. Urocortin2 inhibits tumor growth via effects on vascularization and cell proliferation. Proc Natl Acad Sci U S A 2008; 105: 3939-44. (Pubitemid 351723503)
20. Poole KE, Reeve J. Parathyroid hormone -a bone anabolic and catabolic agent. Curr Opin Pharmacol 2005; 5: 612-7. (Pubitemid 41614461)
21. Dobolyi A, Palkovits M, Usdin TB. The TIP39-PTH2 receptor system: unique peptidergic cell groups in the brainstem and their interactions with central regulatory mechanisms. Prog Neurobiol 2010; 90: 29-59.
22. Yamada Y. Gastric inhibitory polypeptide (GIP) receptor. Nippon Rinsho 1997; 55: 512-6.
23. Nauck MA, Baller B, Meier JJ. Gastric inhibitory polypeptide and glucagon-like peptide-1 in the pathogenesis of type 2 diabetes. Diabetes 2004; 53: S190-6. (Pubitemid 39564543)
24. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 2000; 52: 269-324. (Pubitemid 30368434)
25. Sexton PM, Morfis M, Tilakaratne N, Hay DL, Udawela M, Christopoulos G, et al. Complexing receptor pharmacology: modulation of family B G protein-coupled receptor function by RAMPs. Ann N Y Acad Sci 2006; 1070: 90-104. (Pubitemid 44126627)
26. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased betacell mass and improved glucose tolerance in diabetic rats. Diabetes 1999; 48: 2270-6. (Pubitemid 30395416)
27. Sasaki K, Dockerill S, Adamiak DA, Tickle IJ, Blundell T. X-ray analysis of glucagon and its relationship to receptor binding. Nature 1975; 257: 751-7.
28. Grace CR, Perrin MH, Cantle JP, Vale WW, Rivier JE, Riek R. Common and divergent structural features of a series of corticotropin releasing factor-related peptides. J Am Chem Soc 2007; 129: 16102-14.
29. Venneti KC, Hewage CM. Conformational and molecular interaction studies of glucagon-like peptide-2 with its N-terminal extracellular receptor domain. FEBS Lett 2011; 585: 346-52.
30. Runge S, Gram C, Brauner-Osborne H, Madsen K, Knudsen LB, Wulff BS. Three distinct epitopes on the extracellular face of the glucagons receptor determine specificity for the glucagon amino terminus. J Biol Chem 2003; 278: 28005-10. (Pubitemid 36899996)
31. Runge S, Wulff BS, Madsen K, Brauner-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: 787-94. (Pubitemid 36390634)
32. Bergwitz C, Gardella TJ, Flannery MR, Potts JT Jr, Kronenberg HM, Goldring SR, et al. Full activation of chimeric receptors by hybrids between parathyroid hormone and calcitonin. Evidence for a common pattern of ligand-receptor interaction. J Biol Chem 1996; 271: 26469-72. (Pubitemid 26359042)
33. Stroop SD, Kuestner RE, Serwold TF, Chen L, Moore EE. Chimeric human calcitonin and glucagon receptors reveal two dissociable calcitonin interaction sites. Biochemistry 1995; 34: 1050-7.
34. Holtmann MH, Hadac EM, Miller LJ. Critical contributions of aminoterminal extracellular domains in agonist binding and activation of secretin and vasoactive intestinal polypeptide receptors. Studies of chimeric receptors. J Biol Chem 1995; 270: 14394-8.
35. Laburthe M, Couvineau A, Marie JC. VPAC receptors for VIP and PACAP. Receptors Channels 2002; 8: 137-53.
36. Beyermann M, Rothemund S, Heinrich N, Fechner K, Furkert J, Dathe M, et al. A role for a helical connector between two receptor binding sites of a long-chain peptide hormone. J Biol Chem 2000; 275: 5702-9. (Pubitemid 30115211)
37. Norman DG, Barlow PN, Baron M, Day AJ, Sim RB, Campbell ID. Three-dimensional structure of a complement control protein module in solution. J Mol Biol 1991; 219: 717-25. (Pubitemid 121003544)
38. Parthier C, Reedtz-Runge S, Rudolph R, Stubbs MT. Passing the baton in class B GPCRs: peptide hormone activation via helix induction? Trends Biochem Sci 2009; 34: 303-10.
39. Pioszak AA, Harikumar KG, Parker NR, Miller LJ, Xu HE. Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation. J Biol Chem 2010; 285: 12435-44.
40. Gurevich VV, Gurevich EV. How and why do GPCRs dimerize? Trends Pharmacol Sci 2008; 29: 234-40.
41. Pin JP, Kniazeff J, Liu J, Binet V, Goudet C, Rondard P, et al. Allosteric functioning of dimeric class C G-protein-coupled receptors. FEBS J 2005; 272: 2947-55. (Pubitemid 40904683)
42. Fotiadis D, Jastrzebska B, Philippsen A, Muller DJ, Palczewski K, Engel A. Structure of the rhodopsin dimer: a working model for G-proteincoupled receptors. Curr Opin Struct Biol 2006; 16: 252-9.
43. Fung JJ, Deupi X, Pardo L, Yao XJ, Velez-Ruiz GA, Devree BT, et al. Ligand-regulated oligomerization of beta(2)-adrenoceptors in a model lipid bilayer. EMBO J 2009; 28: 3315-28.
44. Hern JA, Baig AH, Mashanov GI, Birdsall B, Corrie JE, Lazareno S, et al. Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc Natl Acad Sci U S A 2010; 107: 2693-8.
45. Harikumar KG, Pinon DI, Miller LJ. Transmembrane segment IV contributes a functionally important interface for oligomerization of the Class II G protein-coupled secretin receptor. J Biol Chem 2007; 282: 30363-72. (Pubitemid 350035177)
46. Harikumar KG, Morfis MM, Sexton PM, Miller LJ. Pattern of intrafamily hetero-oligomerization involving the G-protein-coupled secretin receptor. J Mol Neurosci 2008; 36: 279-85.
47. Harikumar KG, Morfis MM, Lisenbee CS, Sexton PM, Miller LJ. Constitutive formation of oligomeric complexes between family B G protein-coupled vasoactive intestinal polypeptide and secretin receptors. Mol Pharmacol 2006; 69: 363-73. (Pubitemid 43048923)
48. Seck T, Baron R, Horne WC. The alternatively spliced deltae13 transcript of the rabbit calcitonin receptor dimerizes with the C1a isoform and inhibits its surface expression. J Biol Chem 2003; 278: 23085-93. (Pubitemid 36830374)
49. Kraetke O, Wiesner B, Eichhorst J, Furkert J, Bienert M, Beyermann M. Dimerization of corticotropin-releasing factor receptor type 1 is not coupled to ligand binding. J Recept Signal Transduct Res 2005; 25: 251-76. (Pubitemid 43068279)
50. Maurel D, Comps-Agrar L, Brock C, Rives ML, Bourrier E, Ayoub MA, et al. Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat Methods 2008; 5: 561-7. (Pubitemid 351761765)
51. Mesleh MF, Shirley WA, Heise CE, Ling N, Maki RA, Laura RP. NMR structural characterization of a minimal peptide antagonist bound to the extracellular domain of the corticotropin-releasing factor1 receptor. J Biol Chem 2007; 282: 6338-46. (Pubitemid 47100882)
52. Inooka H, Ohtaki T, Kitahara O, Ikegami T, Endo S, Kitada C, et al. Conformation of a peptide ligand bound to its G-protein coupled receptor. Nat Struct Biol 2001; 8: 161-5. (Pubitemid 32116070)
53. Neumann JM, Couvineau A, Murail S, Lacapere JJ, Jamin N, Laburthe M. Class-B GPCR activation: is ligand helix-capping the key? Trends Biochem Sci 2008; 33: 314-9.
54. Shimizu N, Guo J, Gardella TJ. Parathyroid hormone (PTH)-(1-14) and -(1-11) analogs conformationally constrained by alphaaminoisobutyric acid mediate full agonist responses via the juxtamembrane region of the PTH-1 receptor. J Biol Chem 2001; 276: 49003-12.
55. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, Donaldson C, et al. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci U S A 2001; 98: 7570-5. (Pubitemid 32567989)
56. Usdin TB, Hoare SR, Wang T, Mezey E, Kowalak JA. TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus. Nat Neurosci 1999; 2: 941-3. (Pubitemid 30599554)
57. Hoare SR, Clark JA, Usdin TB. Molecular determinants of tuberoinfundibular peptide of 39 residues (TIP39) selectivity for the parathyroid hormone-2 (PTH2) receptor. N-terminal truncation of TIP39 reverses PTH2 receptor/PTH1 receptor binding selectivity. J Biol Chem 2000; 275: 27274-83.
58. Abraham-Nordling M, Persson B, Nordling E. Model of the complex of Parathyroid hormone-2 receptor and Tuberoinfundibular peptide of 39 residues. BMC Res Notes 2010; 3: 270.
59. Grammatopoulos DK, Randeva HS, Levine MA, Katsanou ES, Hillhouse EW. Urocortin, but not corticotropin-releasing hormone (CRH), activates the mitogen-activated protein kinase signal transduction pathway in human pregnant myometrium: an effect mediated via R1alpha and R2beta CRH receptor subtypes and stimulation of Gqproteins. Mol endocrinol 2000; 14: 2076-91.
60. Brar BK, Chen A, Perrin MH, Vale W. Specificity and regulation of extracellularly regulated kinase1/2 phosphorylation through corticotropin- releasing factor (CRF) receptors 1 and 2beta by the CRF/ urocortin family of peptides. Endocrinology 2004; 145: 1718-29. (Pubitemid 38402380)
61. Lefkowitz RJ, Shenoy SK. Transduction of receptor signals by betaarrestins. Science 2005; 308: 512-7.
62. Gesty-Palmer D, Chen M, Reiter E, Ahn S, Nelson CD, Wang S, et al. Distinct beta-arrestin-and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J Biol Chem 2006; 281: 10856-64. (Pubitemid 43855508)
63. Gesty-Palmer D, Flannery P, Yuan L, Corsino L, Spurney R, Lefkowitz RJ, et al. A beta-arrestin-biased agonist of the parathyroid hormone receptor (PTH1R) promotes bone formation independent of G protein activation. Sci transl med 2009; 1: 1ra1.
64. Hoare SR. Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein-coupled receptors. Drug Discov Today 2005; 10: 417-27. (Pubitemid 40450272)
65. Poyner DR, Sexton PM, Marshall I, Smith DM, Quirion R, Born W, et al. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 2002; 54: 233-46. (Pubitemid 34575714)
66. Kusano S, Kukimoto-Niino M, Akasaka R, Toyama M, Terada T, Shirouzu M, et al. Crystal structure of the human receptor activitymodifying protein 1 extracellular domain. Protein Sci 2008; 17: 1907-14.
67. Dangoor D, Biondi B, Gobbo M, Vachutinski Y, Fridkin M, Gozes I, et al. Novel glycosylated VIP analogs: synthesis, biological activity, and metabolic stability. J Pept Sci 2008; 14: 321-8. (Pubitemid 351385424)
68. Knudsen LB, Nielsen PF, Huusfeldt PO, Johansen NL, Madsen K, Pedersen FZ, et al. Potent derivatives of glucagon-like peptide-1 with pharmacokinetic properties suitable for once daily administration. J Med Chem 2000; 43: 1664-9. (Pubitemid 30304999)
69. Langer I, Gregoire F, Nachtergael I, De Neef P, Ver tongen P, Robberecht P. Hexanoylation of a VPAC2 receptor-preferring ligand markedly increased its selectivity and potency. Peptides 2004; 25: 275-8. (Pubitemid 38520058)
70. Xiao Q, Giguere J, Parisien M, Jeng W, St-Pierre SA, Brubaker PL, et al. Biological activities of glucagon-like peptide-1 analogues in vitro and in vivo. Biochemistry 2001; 40: 2860-9. (Pubitemid 32198288)
71. Spyroulias GA, Papazacharias S, Pairas G, Cordopatis P. Monitoring the structural consequences of Phe12 ? D-Phe and Leu15 ? Aib substitution in human/rat corticotropin releasing hormone. Implications for design of CRH antagonists. Eur J Biochem 2002; 269: 6009-19. (Pubitemid 35461814)
72. Gault VA, Kerr BD, Irwin N, Flatt PR. C-terminal mini-PEGylation of glucose-dependent insulinotropic polypeptide exhibits metabolic stability and improved glucose homeostasis in dietary-induced diabetes. Biochem Pharmacol 2008; 75: 2325-33.
73. Gallwitz B. The evolving place of incretin-based therapies in type 2 diabetes. Pediatr Nephrol 2010; 25: 1207-17.
74. Teichman SL, Neale A, Lawrence B, Gagnon C, Castaigne JP, Frohman LA. Prolonged stimulation of growth hormone (GH) and insulin-like growth factor I secretion by CJC-1295, a long-acting analog of GHreleasing hormone, in healthy adults. J Clin Endocrinol Metab 2006; 91: 799-805. (Pubitemid 43357742)
75. Chunxiao W, Jingjing L, Yire X, Min D, Zhaohui W, Gaofu Q, et al. Study on preparation and activity of a novel recombinant human parathyroid hormone(1-34) analog with N-terminal Pro-Pro extension. Regul Pept 2007; 141: 35-43. (Pubitemid 46482694)
76. Underwood CR, Garibay P, Knudsen LB, Hastrup S, Peters GH, Rudolph R, 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 2010; 285: 723-30.