Conformational states of the full-length glucagon receptor

Nature Communications

Volumn 6, Issue , 2015, Pages 1-13

  Yang, Linlin ^a   Yang, Dehua ^a   De Graaf, Chris ^b   Moeller, Arne ^c   West, Graham M ^d   Dharmarajan, Venkatasubramanian ^d   Wang, Chong ^c   Siu, Fai Y ^c   Song, Gaojie ^e   Reedtz Runge, Steffen ^f   Pascal, Bruce D ^d   Wu, Beili ^a   Potter, Clinton S ^c   Zhou, Hu ^a   Griffin, Patrick R ^d   Carragher, Bridget ^c   Yang, Huaiyu ^a   Wang, Ming Wei ^a   Stevens, Raymond C ^c,e,g   Jiang, Hualiang ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b AMSTERDAM INSTITUTE FOR MOLECULES   (Netherlands)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e SHANGHAITECH UNIVERSITY   (China)

^f NOVO NORDISK A S   (Denmark)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; G PROTEIN COUPLED RECEPTOR; GLUCAGON RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 23; UNCLASSIFIED DRUG; GLUCAGON; LIGAND; PROTEIN BINDING;

DEUTERIUM; HORMONE; HYDROGEN; LIGAND; MEMBRANE; PEPTIDE; PROTEIN; SIGNALING; STABILIZATION;

ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DISULFIDE BOND; ELECTRON MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HYDROGEN BOND; LIGAND BINDING; LIQUID CHROMATOGRAPHY; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN STABILITY; TANDEM MASS SPECTROMETRY; ANIMAL; CHEMISTRY; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SF9 CELL LINE; ULTRASTRUCTURE;

ANIMALS; CHROMATOGRAPHY, LIQUID; DEUTERIUM EXCHANGE MEASUREMENT; DISULFIDES; GLUCAGON; HUMANS; LIGANDS; MICROSCOPY, ELECTRON; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUCAGON; SF9 CELLS; TANDEM MASS SPECTROMETRY;

EID: 84938517765     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8859     Document Type: Article

References (70)

1. Lagerstrom, M. C. & Schioth, H. B. Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug. Discov. 7, 339-357 (2008).
2. Mirzadegan, T., Benko, G., Filipek, S. & Palczewski, K. Sequence analyses of G-protein-coupled receptors: similarities to rhodopsin. Biochemistry 42, 2759-2767 (2003).
3. Venkatakrishnan, A. J. et al. Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194 (2013).
4. Siu, F. Y. et al. Structure of the human glucagon class B G-protein-coupled receptor. Nature 499, 444-449 (2013).
5. Wu, H. et al. Structure of a class C GPCR metabotropic glutamate receptor 1 bound to an allosteric modulator. Science 344, 58-64 (2014).
6. Wang, C. et al. Structure of the human smoothened receptor bound to an antitumour agent. Nature 497, 338-343 (2013).
7. Katritch, V., Cherezov, V. & Stevens, R. C. Structure-function of the G proteincoupled receptor superfamily. Annu. Rev. Pharmacol. 53, 531-556 (2013).
8. Pin, J. P., Galvez, T. & Prezeau, L. Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol. Ther. 98, 325-354 (2003).
9. Janda, C. Y., Waghray, D., Levin, A. M., Thomas, C. & Garcia, K. C. Structural basis of Wnt recognition by Frizzled. Science 337, 59-64 (2012).
10. Parthier, C., Reedtz-Runge, S., Rudolph, R. & Stubbs, M. T. Passing the baton in class B GPCRs: peptide hormone activation via helix induction? Trends Biochem. Sci. 34, 303-310 (2009).
11. Hollenstein, K. et al. Insights into the structure of class B GPCRs. Trends Pharmacol. Sci. 35, 12-22 (2014).
12. Pal, K., Melcher, K. & Xu, H. E. Structure and mechanism for recognition of peptide hormones by Class B G-protein-coupled receptors. Acta Pharmacol. Sin. 33, 300-311 (2012).
13. Rivier, J., Rivier, C. & Vale, W. Synthetic competitive antagonists of corticotropin-releasing factor - effect on ACTH-secretion in the rat. Science 224, 889-891 (1984).
14. Ahn, J. M., Medeiros, M., Trivedi, D. & Hruby, V. J. Development of potent truncated glucagon antagonists. J. Med. Chem. 44, 1372-1379 (2001).
15. Hinke, S. A. et al. Identification of a bioactive domain in the amino-terminus of glucose-dependent insulinotropic polypeptide (GIP). Biochim. Biophys. Acta 1547, 143-155 (2001).
16. Donnelly, D. The structure and function of the glucagon-like peptide-1 receptor and its ligands. Br. J. Pharmacol. 166, 27-41 (2012).
17. Unson, C. G., Gurzenda, E. M. & Merrifield, R. B. Biological-activities of Des- His1[Glu9]Glucagon amide, a glucagon antagonist. Peptides 10, 1171-1177 (1989).
18. Pioszak, A. A., Parker, N. R., Suino-Powell, K. & Xu, H. E. Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1. J. Biol. Chem. 283, 32900-32912 (2008).
19. Underwood, C. 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. 285, 723-730 (2010).
20. Pioszak, A. A., Parker, N. R., Gardella, T. J. & Xu, H. E. Structural basis for parathyroid hormone-related protein binding to the parathyroid hormone receptor and design of conformation-selective peptides. J. Biol. Chem. 284, 28382-28391 (2009).
21. Grace, C. R. 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. USA 101, 12836-12841 (2004).
22. 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. 283, 11340-11347 (2008).
23. Pioszak, A. A. & Xu, H. E. Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc. Natl Acad. Sci. USA 105, 5034-5039 (2008).
24. ter Haar, E. et al. Crystal structure of the ectodomain complex of the CGRP receptor, a class-B GPCR, reveals the site of drug antagonism. Structure 18, 1083-1093 (2010).
25. Kumar, S., Pioszak, A., Zhang, C., Swaminathan, K. & Xu, H. E. Crystal structure of the PAC1R extracellular domain unifies a consensus fold for hormone recognition by class B G-protein coupled receptors. PLoS ONE 6, e19682 (2011).
26. Grace, C. R. et al. Structure of the N-terminal domain of a type B1 G proteincoupled receptor in complex with a peptide ligand. Proc. Natl Acad. Sci. USA 104, 4858-4863 (2007).
27. Parthier, C. et al. Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor. Proc. Natl Acad. Sci. USA 104, 13942-13947 (2007).
28. Sun, C. 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. USA 104, 7875-7880 (2007).
29. Hollenstein, K. et al. Structure of class B GPCR corticotropin-releasing factor receptor 1. Nature 499, 438-443 (2013).
30. Koth, C. M. et al. Molecular basis for negative regulation of the glucagon receptor. Proc. Natl Acad. Sci. USA 109, 14393-14398 (2012).
31. Inooka, H. et al. Conformation of a peptide ligand bound to its G-protein coupled receptor. Nat. Struct. Biol. 8, 161-165 (2001).
32. Runge, S. et al. Three distinct epitopes on the extracellular face of the glucagon receptor determine specificity for the glucagon amino terminus. J. Biol. Chem. 278, 28005-28010 (2003).
33. Unson, C. G. et al. Roles of specific extracellular domains of the glucagon receptor in ligand binding and signaling. Biochemistry 41, 11795-11803 (2002).
34. Roberts, D. J., Vertongen, P. & Waelbroeck, M. Analysis of the glucagon receptor first extracellular loop by the substituted cysteine accessibility method. Peptides 32, 1593-1599 (2011).
35. Prevost, M. et al. Mutational and cysteine scanning analysis of the glucagon receptor N-terminal domain. J. Biol. Chem. 285, 30951-30958 (2010).
36. Perret, J. 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, 389-394 (2002).
37. Preininger, A. M., Meiler, J. & Hamm, H. E. Conformational flexibility and structural dynamics in GPCR-mediated G protein activation: a perspective. J. Mol. Biol. 425, 2288-2298 (2013).
38. Lau, J. et al. New beta-alanine derivatives are orally available glucagon receptor antagonists. J. Med. Chem. 50, 113-128 (2007).
39. Unson, C. G., Wu, C. R., Fitzpatrick, K. J. & Merrifield, R. B. Multiple-site replacement analogs of glucagon - a molecular-basis for antagonist design. J. Biol. Chem. 269, 12548-12551 (1994).
40. West, G. M. et al. Ligand-dependent perturbation of the conformational ensemble for the GPCR beta(2) adrenergic receptor revealed by HDX. Structure. 19, 1424-1432 (2011).
41. Tirion, M. M. Large amplitude elastic motions in proteins from a singleparameter, atomic analysis. Phys. Rev. Lett. 77, 1905-1908 (1996).
42. Bahar, I., Atilgan, A. R. & Erman, B. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des. 2, 173-181 (1997).
43. Schurpf, T. & Springer, T. A. Regulation of integrin affinity on cell surfaces. EMBO J. 30, 4712-4727 (2011).
44. Trivedi, D. et al. Design and synthesis of conformationally constrained glucagon analogues. J. Med. Chem. 43, 1714-1722 (2000).
45. Coin, I. et al. Genetically encoded chemical probes in cells reveal the binding path of urocortin-I to CRF class B GPCR. Cell 155, 1258-1269 (2013).
46. Liaw, C. W., Grigoriadis, D. E., Lovenberg, T. W., DeSouza, E. B. & Maki, R. A. Localization of ligand-binding domains of human corticotropin-releasing factor receptor: a chimeric receptor approach. Mol. Endocrinol. 11, 980-985 (1997).
47. Assil-Kishawi, I., Samra, T. A., Mierke, D. F. & Abou-Samra, A. B. Residue 17 of sauvagine cross-links to the first transmembrane domain of corticotropinreleasing factor receptor 1 (CRFR1). J. Biol. Chem. 283, 35644-35651 (2008).
48. Miller, L. J. 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, 15895-15907 (2011).
49. Yaqub, T. 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, 547-558 (2010).
50. Dong, M. 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, 5092-5105 (2012).
51. Ceraudo, E. 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, 2060-2071 (2012).
52. Xiao, Q., Jeng, W. & Wheeler, M. B. Characterization of glucagon-like peptide- 1 receptor-binding determinants. J. Mol. Endocrinol. 25, 321-335 (2000).
53. Holtmann, M. H., Ganguli, S., Hadac, E. M., Dolu, V. & Miller, L. J. Multiple extracellular loop domains contribute critical determinants for agonist binding and activation of the secretin receptor. J. Biol. Chem. 271, 14944-14949 (1996).
54. Devigny, C. et al. Biomimetic screening of class B G protein-coupled receptors. J. Am. Chem. Soc. 133, 8927-8933 (2011).
55. Kufareva, I., Salanga, C. L. & Handel, T. M. Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies. Immunol. Cell Biol. 93, 372-383 (2015).
56. Qin, L. et al. Structural biology. Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine. Science 347, 1117-1122 (2015).
57. Burg, J. S. et al. Structural biology. Structural basis for chemokine recognition and activation of a viral G protein-coupled receptor. Science 347, 1113-1117 (2015).
58. Tao, H. C. et al. Engineered nanostructured beta-sheet peptides protect membrane proteins. Nat. Methods 10, 759-761 (2013).
59. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
60. Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95-102 (2009).
61. Voss, N. R., Yoshioka, C. K., Radermacher, M., Potter, C. S. & Carragher, B. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166, 205-213 (2009).
62. Scheres, S. H. W. et al. Maximum-likelihood multi-reference refinement for electron microscopy images. J. Mol. Biol. 348, 139-149 (2005).
63. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
64. Radermacher, M., Wagenknecht, T., Verschoor, A. & Frank, J. Threedimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc. 146, 113-136 (1987).
65. Pascal, B. D. et al. HDX workbench: software for the analysis of H/D exchange MS data. J. Am. Soc. Mass Spectrom. 23, 1512-1521 (2012).
66. Duc, N. M. et al. Effective application of bicelles for conformational analysis of g protein-coupled receptors by hydrogen/deuterium exchange mass spectrometry. J. Am. Soc. Mass Spectrom. 26, 808-817 (2015).
67. Yang, B. et al. Identification of cross-linked peptides from complex samples. Nat. Methods 9, 904-906 (2012).
68. Hess, B., Kutzner, C., van der Spoel, D. & Lindahl, E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447 (2008).
69. Klauda, J. B. et al. Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J. Phys. Chem. B 114, 7830-7843 (2010).
70. Suhre, K. & Sanejouand, Y. H. ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res. 32, W610-W614 (2004).