Structure of the full-length glucagon class B G-protein-coupled receptor

Nature

Volumn 546, Issue 7657, 2017, Pages 259-264

  Zhang, Haonan ^a,b   Qiao, Anna ^a,b   Yang, Dehua ^a   Yang, Linlin ^c   Dai, Antao ^a   De Graaf, Chris ^d   Reedtz Runge, Steffen ^e   Dharmarajan, Venkatasubramanian ^f   Zhang, Hui ^a,b   Han, Gye Won ^g   Grant, Thomas D ^h   Sierra, Raymond G ⁱ   Weierstall, Uwe ^j   Nelson, Garrett ^j   Liu, Wei ^j   Wu, Yanhong ^a,b,k   Ma, Limin ^a   Cai, Xiaoqing ^a   Lin, Guangyao ^a,b,k   Wu, Xiaoai ^l   Geng, Zhi ^m   Dong, Yuhui ^m   Song, Gaojie ^k   Griffin, Patrick R ^f   Lau, Jesper ^e   Cherezov, Vadim ^g   Yang, Huaiyu ^a   Hanson, Michael A ⁿ   Stevens, Raymond C ^k   Zhao, Qiang ^a,b   Jiang, Hualiang ^a   Wang, Ming Wei ^a,k,o   Wu, Beili ^a,b,k   more..

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c ZHENGZHOU UNIVERSITY   (China)

^d AMSTERDAM INSTITUTE FOR MOLECULES   (Netherlands)

^e NOVO NORDISK A S   (Denmark)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^h UNIVERSITY AT BUFFALO   (United States)

ⁱ SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^j ARIZONA STATE UNIVERSITY   (United States)

^k SHANGHAITECH UNIVERSITY   (China)

^l SIBS Novo Nordisk Translational Research Centre for PreDiabetes   (China)

^m INSTITUTE OF HIGH ENERGY PHYSICS   (China)

ⁿ GPCR Consortium   (United States)

^o FUDAN UNIVERSITY   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; G PROTEIN COUPLED RECEPTOR; GLUCAGON RECEPTOR; BENZAMIDE DERIVATIVE; CARBANILAMIDE DERIVATIVE; CROSS LINKING REAGENT; LIGAND; NNC0640;

CRYSTAL STRUCTURE; DEUTERIUM; DIABETES; HOMEOSTASIS; HOMINID; HYDROGEN; LIGAND; MEMBRANE; PROTEIN;

ALPHA HELIX; ANTIGEN BINDING; ARTICLE; BETA SHEET; CROSS LINKING; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DISULFIDE BOND; LIGAND BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; AGONISTS; ALLOSTERIC SITE; CELL MEMBRANE; CHEMISTRY; CLASSIFICATION; DRUG EFFECTS; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN STABILITY; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC SITE; BENZAMIDES; CELL MEMBRANE; CROSS-LINKING REAGENTS; CRYSTALLOGRAPHY, X-RAY; DEUTERIUM EXCHANGE MEASUREMENT; DISULFIDES; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PHENYLUREA COMPOUNDS; PROTEIN DOMAINS; PROTEIN STABILITY; RECEPTORS, GLUCAGON;

EID: 85020450107     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22363     Document Type: Article

References (44)

1. Lagerström, M. C., Schiöth, H. B. Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7, 339-357 (2008).
2. Hollenstein, K., et al. Insights into the structure of class B GPCRs. Trends Pharmacol. Sci. 35, 12-22 (2014).
3. Finan, B., et al. Chemical hybridization of glucagon and thyroid hormone optimizes therapeutic impact for metabolic disease. Cell 167, 843-857.e14 (2016).
4. Longuet, C., et al. The glucagon receptor is required for the adaptive metabolic response to fasting. Cell Metab. 8, 359-371 (2008).
5. 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).
6. Koth, C. M., et al. Molecular basis for negative regulation of the glucagon receptor. Proc. Natl Acad. Sci. USA 109, 14393-14398 (2012).
7. Yang, L., et al. Conformational states of the full-length glucagon receptor. Nat. Commun. 6, 7859 (2015).
8. Siu, F. Y., et al. Structure of the human glucagon class B G-protein-coupled receptor. Nature 499, 444-449 (2013).
9. Jazayeri, A., et al. Extra-helical binding site of a glucagon receptor antagonist. Nature 533, 274-277 (2016).
10. Hollenstein, K., et al. Structure of class B GPCR corticotropin-releasing factor receptor 1. Nature 499, 438-443 (2013).
11. Song, G., et al. Human GLP-1 receptor transmembrane domain structure in complex with allosteric modulators. Nature http://dx.doi.org/10.1038/nature22378 (2017).
12. 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).
13. 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).
14. Ballesteros, J., Weinstein, H. In Methods in Neuroscience Vol. 25 (ed, Sealfon, S.) 366-428 (Elsevier, 1995).
15. Wootten, D., Simms, J., Miller, L. J., Christopoulos, A., Sexton, P. M. 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, 5211-5216 (2013).
16. Mann, R., Wigglesworth, M. J., Donnelly, D. Ligand-receptor interactions at the parathyroid hormone receptors: Subtype binding selectivity is mediated via an interaction between residue 23 on the ligand and residue 41 on the receptor. Mol. Pharmacol. 74, 605-613 (2008).
17. Unson, C. G., et al. Roles of specific extracellular domains of the glucagon receptor in ligand binding and signaling. Biochemistry 41, 11795-11803 (2002).
18. 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).
19. Byrne, E. F., et al. Structural basis of Smoothened regulation by its extracellular domains. Nature 535, 517-522 (2016).
20. Laskowski, R. A., Swindells, M. B. LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786 (2011).
21. Caffrey, M., Cherezov, V. Crystallizing membrane proteins using lipidic mesophases. Nat. Protocols 4, 706-731 (2009).
22. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
23. Liu, W., Ishchenko, A., Cherezov, V. Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography. Nat. Protocols 9, 2123-2134 (2014).
24. Weierstall, U., et al. Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography. Nat. Commun. 5, 3309 (2014).
25. Liang, M., et al. The Coherent X-ray Imaging instrument at the Linac Coherent Light Source. J. Synchrotron Radiat. 22, 514-519 (2015).
26. Siewert, F., et al. Ultra-precise characterization of LCLS hard X-ray focusing mirrors by high resolution slope measuring deflectometry. Opt. Express 20, 4525-4536 (2012).
27. White, T. A., et al. Crystallographic data processing for free-electron laser sources. Acta Crystallogr. D Biol. Crystallogr. 69, 1231-1240 (2013).
28. White, T. A., et al. CrystFEL: A software suite for snapshot serial crystallography. J. Appl. Crystallogr. 45, 335-341 (2012).
29. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., Leslie, A. G. iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281 (2011).
30. Duisenberg, A. J. M. Indexing in single-crystal diffractometry with an obstinate list of reflections. J. Appl. Crystallogr. 25, 92-96 (1992).
31. Afonine, P. V., et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012).
32. McCoy, A. J., et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
33. Murshudov, G. N., Vagin, A. A., Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
34. Smart, O. S., et al. Exploiting structure similarity in refinement: Automated NCS and target-structure restraints in BUSTER. Acta Crystallogr. D Biol. Crystallogr. 68, 368-380 (2012).
35. Emsley, P., Lohkamp, B., Scott, W. G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
36. 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).
37. Pronk, S., et al. GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29, 845-854 (2013).
38. 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).
39. Bussi, G., Donadio, D., Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
40. Parrinello, M., Rahman, A. Polymorphic transitions in single-crystals-a new molecular dynamics method. J. Appl. Phys. 52, 7182-7190 (1981).
41. Miyamoto, S., Kollman, P. A. Settle-an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem. 13, 952-962 (1992).
42. Hess, B., Bekker, H., Berendsen, H. J. C., Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472 (1997).
43. Essmann, U., et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593 (1995).
44. Chen, V. B., et al. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).