XGenetically encoded chemical probes in cells reveal the binding path of urocortin-i to CRF class B GPCR

Cell

Volumn 155, Issue 6, 2013, Pages 1258-

  Coin, Irene ^a   Katritch, Vsevolod ^b   Sun, Tingting ^a   Xiang, Zheng ^a   Siu, Fai Yiu ^b   Beyermann, Michael ^c   Stevens, Raymond C ^b   Wang, Lei ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; P AZIDO PHENYLALANINE; P BENZOYL PHENYLALANINE; PHENYLALANINE DERIVATIVE; TRANSFER RNA; UNCLASSIFIED DRUG; UROCORTIN I; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CROSS LINKING REAGENT; UCN1 PROTEIN, HUMAN; UROCORTIN;

ARTICLE; BINDING KINETICS; BINDING SITE; CRYSTAL STRUCTURE; HUMAN; MAMMAL CELL; MOLECULAR MODEL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ULTRAVIOLET IRRADIATION; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CLICK CHEMISTRY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MOUSE; RAT; SEQUENCE ALIGNMENT; PROCEDURES;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; CLICK CHEMISTRY; CROSS-LINKING REAGENTS; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SEQUENCE ALIGNMENT; UROCORTINS;

EID: 84890023965     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.11.008     Document Type: Article

References (59)

1. R.A. Abagyan, A. Orry, E. Raush, L. Budagyan, and M. Totrov ICM Manual 2012 MolSoft LLC La Jolla, CA
2. I. Assil-Kishawi, and A.B. Abou-Samra Sauvagine cross-links to the second extracellular loop of the corticotropin-releasing factor type 1 receptor J. Biol. Chem. 277 2002 32558 32561
3. I. Assil-Kishawi, T.A. Samra, D.F. Mierke, and A.B. Abou-Samra 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
4. M. Beyermann, S. Rothemund, N. Heinrich, K. Fechner, J. Furkert, M. Dathe, R. Winter, E. Krause, and M. Bienert A role for a helical connector between two receptor binding sites of a long-chain peptide hormone J. Biol. Chem. 275 2000 5702 5709
5. M. Beyermann, N. Heinrich, K. Fechner, J. Furkert, W. Zhang, O. Kraetke, M. Bienert, and H. Berger Achieving signalling selectivity of ligands for the corticotropin-releasing factor type 1 receptor by modifying the agonist's signalling domain Br. J. Pharmacol. 151 2007 851 859
6. I. Coin, M.H. Perrin, W.W. Vale, and L. Wang Photo-cross-linkers incorporated into G-protein-coupled receptors in mammalian cells: a ligand comparison Angew. Chem. Int. Ed. Engl. 50 2011 8077 8081
7. M. Dong, P.C. Lam, D.I. Pinon, K. Hosohata, A. Orry, P.M. Sexton, R. Abagyan, and L.J. Miller Molecular basis of secretin docking to its intact receptor using multiple photolabile probes distributed throughout the pharmacophore J. Biol. Chem. 286 2011 23888 23899
8. M. Dong, X. Xu, A.M. Ball, J.A. Makhoul, P.C. Lam, D.I. Pinon, A. Orry, P.M. Sexton, R. Abagyan, and L.J. Miller 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
9. C.R. Grace, M.H. Perrin, J.P. Cantle, W.W. Vale, J.E. Rivier, and R. Riek Common and divergent structural features of a series of corticotropin releasing factor-related peptides J. Am. Chem. Soc. 129 2007 16102 16114
10. C.R. Grace, M.H. Perrin, J. Gulyas, J.E. Rivier, W.W. Vale, and R. Riek 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
11. A. Grunbeck, T. Huber, R. Abrol, B. Trzaskowski, W.A. Goddard 3rd, and T.P. Sakmar Genetically encoded photo-cross-linkers map the binding site of an allosteric drug on a G protein-coupled receptor ACS Chem. Biol. 7 2012 967 972
12. J. Gulyas, C. Rivier, M. Perrin, S.C. Koerber, S. Sutton, A. Corrigan, S.L. Lahrichi, A.G. Craig, W. Vale, and J. Rivier Potent, structurally constrained agonists and competitive antagonists of corticotropin-releasing factor Proc. Natl. Acad. Sci. USA 92 1995 10575 10579
13. C.F. Hemley, A. McCluskey, and P.A. Keller Corticotropin releasing hormone - a GPCR drug target Curr. Drug Targets 8 2007 105 115
14. S.R. Hoare, B.T. Brown, M.A. Santos, S. Malany, S.F. Betz, and D.E. Grigoriadis Single amino acid residue determinants of non-peptide antagonist binding to the corticotropin-releasing factor1 (CRF1) receptor Biochem. Pharmacol. 72 2006 244 255
15. K. Hollenstein, J. Kean, A. Bortolato, R.K. Cheng, A.S. Doré, A. Jazayeri, R.M. Cooke, M. Weir, and F.H. Marshall Structure of class B GPCR corticotropin-releasing factor receptor 1 Nature 499 2013 438 443
16. V. Katritch, V. Cherezov, and R.C. Stevens Structure-function of the G protein-coupled receptor superfamily Annu. Rev. Pharmacol. Toxicol. 53 2013 531 556
17. W.D. Kornreich, R. Galyean, J.F. Hernandez, A.G. Craig, C.J. Donaldson, G. Yamamoto, C. Rivier, W. Vale, and J. Rivier Alanine series of ovine corticotropin releasing factor (oCRF): a structure-activity relationship study J. Med. Chem. 35 1992 1870 1876
18. O. Kraetke, B. Holeran, H. Berger, E. Escher, M. Bienert, and M. Beyermann Photoaffinity cross-linking of the corticotropin-releasing factor receptor type 1 with photoreactive urocortin analogues Biochemistry 44 2005 15569 15577
19. L.J. Miller, Q. Chen, P.C. Lam, D.I. Pinon, P.M. Sexton, R. Abagyan, and M. Dong 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
20. P. Monaghan, B.E. Thomas, I. Woznica, A. Wittelsberger, D.F. Mierke, and M. Rosenblatt Mapping peptide hormone-receptor interactions using a disulfide-trapping approach Biochemistry 47 2008 5889 5895
21. S.M. Nielsen, L.Z. Nielsen, S.A. Hjorth, M.H. Perrin, and W.W. Vale Constitutive activation of tethered-peptide/corticotropin-releasing factor receptor chimeras Proc. Natl. Acad. Sci. USA 97 2000 10277 10281
22. K. Pal, K. Swaminathan, H.E. Xu, and A.A. Pioszak Structural basis for hormone recognition by the Human CRFR2α G protein-coupled receptor J. Biol. Chem. 285 2010 40351 40361
23. K. Pal, K. Melcher, and H.E. Xu Structure and mechanism for recognition of peptide hormones by Class B G-protein-coupled receptors Acta Pharmacol. Sin. 33 2012 300 311
24. C. Parthier, S. Reedtz-Runge, R. Rudolph, and M.T. Stubbs Passing the baton in class B GPCRs: peptide hormone activation via helix induction? Trends Biochem. Sci. 34 2009 303 310
25. V.I. Pham, and P.M. Sexton Photoaffinity scanning in the mapping of the peptide receptor interface of class II G protein-coupled receptors J. Pept. Sci. 10 2004 179 203
26. A.A. Pioszak, N.R. Parker, K. Suino-Powell, and H.E. Xu Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1 J. Biol. Chem. 283 2008 32900 32912
27. J. Rivier, J. Spiess, and W. Vale Characterization of rat hypothalamic corticotropin-releasing factor Proc. Natl. Acad. Sci. USA 80 1983 4851 4855
28. J. Rivier, C. Rivier, and W. Vale Synthetic competitive antagonists of corticotropin-releasing factor: effect on ACTH secretion in the rat Science 224 1984 889 891
29. J. Rivier, S.L. Lahrichi, J. Gulyas, J. Erchegyi, S.C. Koerber, A.G. Craig, A. Corrigan, C. Rivier, and W. Vale Minimal-size, constrained corticotropin-releasing factor agonists with i-(i+3) Glu-Lys and Lys-Glu bridges J. Med. Chem. 41 1998 2614 2620
30. C. Romier, J.M. Bernassau, C. Cambillau, and H. Darbon Solution structure of human corticotropin releasing factor by 1H NMR and distance geometry with restrained molecular dynamics Protein Eng. 6 1993 149 156
31. K. Sakamoto, A. Hayashi, A. Sakamoto, D. Kiga, H. Nakayama, A. Soma, T. Kobayashi, M. Kitabatake, K. Takio, and K. Saito Site-specific incorporation of an unnatural amino acid into proteins in mammalian cells Nucleic Acids Res. 30 2002 4692 4699
32. F.Y. Siu, M. He, C. de Graaf, G.W. Han, D. Yang, Z. Zhang, C. Zhou, Q. Xu, D. Wacker, and J.S. Joseph Structure of the human glucagon class B G-protein-coupled receptor Nature 499 2013 444 449
33. J.K. Takimoto, K.L. Adams, Z. Xiang, and L. Wang Improving orthogonal tRNA-synthetase recognition for efficient unnatural amino acid incorporation and application in mammalian cells Mol. Biosyst. 5 2009 931 934
34. J. Vaughan, C. Donaldson, J. Bittencourt, M.H. Perrin, K. Lewis, S. Sutton, R. Chan, A.V. Turnbull, D. Lovejoy, and C. Rivier Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor Nature 378 1995 287 292
35. W.Y. Wang, J.K. Takimoto, G.V. Louie, T.J. Baiga, J.P. Noel, K.F. Lee, P.A. Slesinger, and L. Wang Genetically encoding unnatural amino acids for cellular and neuronal studies Nat. Neurosci. 10 2007 1063 1072
36. J.F. White, N. Noinaj, Y. Shibata, J. Love, B. Kloss, F. Xu, J. Gvozdenovic-Jeremic, P. Shah, J. Shiloach, C.G. Tate, and R. Grisshammer Structure of the agonist-bound neurotensin receptor Nature 490 2012 508 513
37. A. Wittelsberger, M. Corich, B.E. Thomas, B.K. Lee, A. Barazza, P. Czodrowski, D.F. Mierke, M. Chorev, and M. Rosenblatt The mid-region of parathyroid hormone (1-34) serves as a functional docking domain in receptor activation Biochemistry 45 2006 2027 2034
38. D. Wootten, J. Simms, L.J. Miller, A. Christopoulos, and P.M. Sexton Polar transmembrane interactions drive formation of ligand-specific and signal pathway-biased family B G protein-coupled receptor conformations Proc. Natl. Acad. Sci. USA 110 2013 5211 5216
39. B. Wu, E.Y. Chien, C.D. Mol, G. Fenalti, W. Liu, V. Katritch, R. Abagyan, A. Brooun, P. Wells, and F.C. Bi Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071
40. Z. Xiang, H. Ren, Y.S. Hu, I. Coin, J. Wei, H. Cang, and L. Wang Adding an unnatural covalent bond to proteins through proximity-enhanced bioreactivity Nat. Methods 10 2013 885 888
41. M. Alken, C. Rutz, R. Kochl, U. Donalies, M. Oueslati, J. Furkert, D. Wietfeld, R. Hermosilla, A. Scholz, and M. Beyermann The signal peptide of the rat corticotropin-releasing factor receptor 1 promotes receptor expression but is not essential for establishing a functional receptor Biochem. J. 390 2005 455 464
42. Y.A. Arnautova, R.A. Abagyan, and M. Totrov Development of a new physics-based internal coordinate mechanics force field and its application to protein loop modeling Proteins 79 2011 477 498
43. J.C. Bittencourt, J. Vaughan, C. Arias, R.A. Rissman, W.W. Vale, and P.E. Sawchenko Urocortin expression in rat brain: evidence against a pervasive relationship of urocortin-containing projections with targets bearing type 2 CRF receptors J. Comp. Neurol. 415 1999 285 312
44. E. Ceraudo, S. Murail, Y.V. Tan, J.J. Lacapère, J.M. Neumann, A. Couvineau, and M. Laburthe 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
45. E. Ceraudo, R. Hierso, Y.V. Tan, S. Murail, C. Rouyer-Fessard, P. Nicole, J.C. Robert, N. Jamin, J.M. Neumann, and P. Robberecht 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
46. P. Di Tommaso, S. Moretti, I. Xenarios, M. Orobitg, A. Montanyola, J.M. Chang, J.F. Taly, and C. Notredame T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension Nucleic Acids Res. 39 2011 W13 W17
47. M. Dong, D.I. Pinon, R.F. Cox, and L.J. Miller Molecular approximation between a residue in the amino-terminal region of calcitonin and the third extracellular loop of the class B G protein-coupled calcitonin receptor J. Biol. Chem. 279 2004 31177 31182
48. R.C. Gensure, T.J. Gardella, and H. Jüppner Parathyroid hormone and parathyroid hormone-related peptide, and their receptors Biochem. Biophys. Res. Commun. 328 2005 666 678
49. K. Gkountelias, T. Tselios, M. Venihaki, G. Deraos, I. Lazaridis, O. Rassouli, A. Gravanis, and G. Liapakis Alanine scanning mutagenesis of the second extracellular loop of type 1 corticotropin-releasing factor receptor revealed residues critical for peptide binding Mol. Pharmacol. 75 2009 793 800
50. P. Gouet, E. Courcelle, D.I. Stuart, and F. Métoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308
51. G.R. Kunkel, R.L. Maser, J.P. Calvet, and T. Pederson U6 small nuclear RNA is transcribed by RNA polymerase III Proc. Natl. Acad. Sci. USA 83 1986 8575 8579
52. C.W. Liaw, D.E. Grigoriadis, M.T. Lorang, E.B. De Souza, and R.A. Maki Localization of agonist- and antagonist-binding domains of human corticotropin-releasing factor receptors Mol. Endocrinol. 11 1997 2048 2053
53. C.W. Liaw, D.E. Grigoriadis, T.W. Lovenberg, E.B. De Souza, and R.A. Maki Localization of ligand-binding domains of human corticotropin-releasing factor receptor: a chimeric receptor approach Mol. Endocrinol. 11 1997 980 985
54. L.J. Miller, M. Dong, and K.G. Harikumar Ligand binding and activation of the secretin receptor, a prototypic family B G protein-coupled receptor Br. J. Pharmacol. 166 2012 18 26
55. V. Pham, M. Dong, J.D. Wade, L.J. Miller, C.J. Morton, H.L. Ng, M.W. Parker, and P.M. Sexton Insights into interactions between the α-helical region of the salmon calcitonin antagonists and the human calcitonin receptor using photoaffinity labeling J. Biol. Chem. 280 2005 28610 28622
56. S. Sydow, A. Flaccus, A. Fischer, and J. Spiess The role of the fourth extracellular domain of the rat corticotropin-releasing factor receptor type 1 in ligand binding Eur. J. Biochem. 259 1999 55 62
57. Y.V. Tan, A. Couvineau, S. Murail, E. Ceraudo, J.M. Neumann, J.J. Lacapère, and M. Laburthe Peptide agonist docking in the N-terminal ectodomain of a class II G protein-coupled receptor, the VPAC1 receptor. Photoaffinity, NMR, and molecular modeling J. Biol. Chem. 281 2006 12792 12798
58. J.M. Turner, J. Graziano, G. Spraggon, and P.G. Schultz Structural characterization of a p-acetylphenylalanyl aminoacyl-tRNA synthetase J. Am. Chem. Soc. 127 2005 14976 14977
59. D. Wietfeld, N. Heinrich, J. Furkert, K. Fechner, M. Beyermann, M. Bienert, and H. Berger Regulation of the coupling to different G proteins of rat corticotropin-releasing factor receptor type 1 in human embryonic kidney 293 cells J. Biol. Chem. 279 2004 38386 38394