Molecular mechanism of an antagonistic antibody against glucose-dependent insulinotropic polypeptide receptor

References

• Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology. 2007;132:2131–12. doi:https://doi.org/10.1053/j.gastro.2007.03.054.
   PubMed Web of Science ®Google Scholar
• Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 2013;17:819–37. doi:https://doi.org/10.1016/j.cmet.2013.04.008.
   PubMed Web of Science ®Google Scholar
• Ahren B. The future of incretin-based therapy: novel avenues–novel targets. Diabetes Obes Metab. 2011;13(Suppl 1):158–66. doi:https://doi.org/10.1111/dom.2011.13.issue-s1.
   PubMed Web of Science ®Google Scholar
• Irwin N, Flatt PR. Evidence for beneficial effects of compromised gastric inhibitory polypeptide action in obesity-related diabetes and possible therapeutic implications. Diabetologia. 2009;52:1724–31. doi:https://doi.org/10.1007/s00125-009-1422-8.
   Google Scholar
• Kieffer TJ, McIntosh CH, Pederson RA. Degradation of glucose-dependent insulinotropic polypeptide and truncated glucagon-like peptide 1 in vitro and in vivo by dipeptidyl peptidase IV. Endocrinology. 1995;136:3585–96. doi:https://doi.org/10.1210/endo.136.8.7628397.
   PubMed Web of Science ®Google Scholar
• Usdin TB, Mezey E, DC B, Brownstein MJ, Bonner TI. Gastric inhibitory polypeptide receptor, a member of the secretin-vasoactive intestinal peptide receptor family, is widely distributed in peripheral organs and the brain. Endocrinology. 1993;133:2861–70. doi:https://doi.org/10.1210/endo.133.6.8243312.
   PubMed Web of Science ®Google Scholar
• Beck B, Max JP. Direct metabolic effects of gastric inhibitory polypeptide (GIP): dissociation at physiological levels of effects on insulin-stimulated fatty acid and glucose incorporation in rat adipose tissue. Diabetologia. 1986;29:68. doi:https://doi.org/10.1007/BF02427284.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Nian C, McIntosh CH. Activation of lipoprotein lipase by glucose-dependent insulinotropic polypeptide in adipocytes. A role for a protein kinase B, LKB1, and AMP-activated protein kinase cascade. J Biol Chem. 2007;282:8557–67. doi:https://doi.org/10.1074/jbc.M609088200.
   PubMed Web of Science ®Google Scholar
• Getty-Kaushik L, Song DH, Boylan MO, Corkey BE, MM W. Glucose-dependent insulinotropic polypeptide modulates adipocyte lipolysis and reesterification. Obesity (Silver Spring). 2006;14:1124–31. doi:https://doi.org/10.1038/oby.2006.129.
   PubMed Web of Science ®Google Scholar
• Chia CW, Carlson OD, Kim W, Shin YK, Charles CP, Kim HS, Melvin DL, Egan JM. Exogenous glucose-dependent insulinotropic polypeptide worsens post prandial hyperglycemia in type 2 diabetes. Diabetes. 2009;58:1342–49.
   PubMed Web of Science ®Google Scholar
• Meier JJ, Gallwitz B, Siepmann N, Holst JJ, Deacon CF, Schmidt WE, Nauck MA. Gastric inhibitory polypeptide (GIP) dose-dependently stimulates glucagon secretion in healthy human subjects at euglycaemia. Diabetologia. 2003;46:798–801. doi:https://doi.org/10.1007/s00125-003-1103-y.
   PubMed Web of Science ®Google Scholar
• Christensen M, Vedtofte L, Holst JJ, Vilsboll T, Knop FK. Glucose-dependent insulinotropic polypeptide: a bifunctional glucose-dependent regulator of glucagon and insulin secretion in humans. Diabetes. 2011;60:3103–09. doi:https://doi.org/10.2337/db11-0979.
   PubMed Web of Science ®Google Scholar
• Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Lango Allen H, Lindgren CM, Luan J, Magi R, et al. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet. 2010;42:937–48. doi:https://doi.org/10.1038/ng.686.
   PubMed Web of Science ®Google Scholar
• Okada Y, Kubo M, Ohmiya H, Takahashi A, Kumasaka N, Hosono N, Maeda S, Wen W, Dorajoo R, Go MJ, et al. Common variants at CDKAL1 and KLF9 are associated with body mass index in east Asian populations. Nat Genet. 2012;44:302–06. doi:https://doi.org/10.1038/ng.1086.
   PubMed Web of Science ®Google Scholar
• Wen W, Cho YS, Zheng W, Dorajoo R, Kato N, Qi L, Chen CH, Delahanty RJ, Okada Y, Tabara Y, et al. Meta-analysis identifies common variants associated with body mass index in east Asians. Nat Genet. 2012;44:307–11. doi:https://doi.org/10.1038/ng.1087.
   PubMed Web of Science ®Google Scholar
• Berndt SI, Gustafsson S, Magi R, Ganna A, Wheeler E, Feitosa MF, Justice AE, Monda KL, Croteau-Chonka DC, Day FR, et al. Genome-wide meta-analysis identifies 11 new loci for anthropometric traits and provides insights into genetic architecture. Nat Genet. 2013;45:501–12. doi:https://doi.org/10.1038/ng.2606.
   PubMed Web of Science ®Google Scholar
• Miyawaki K, Yamada Y, Ban N, Ihara Y, Tsukiyama K, Zhou H, Fujimoto S, Oku A, Tsuda K, Toyokuni S, et al. Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat Med. 2002;8:738–42. doi:https://doi.org/10.1038/nm727.
   PubMed Web of Science ®Google Scholar
• PR F, Dorothy H Lecture. Gastric inhibitory polypeptide (GIP) revisited: a new therapeutic target for obesity-diabetes? Diabet Med. 2008;2008:759–64.
   Google Scholar
• Faivre E, Hamilton A, Holscher C. Effects of acute and chronic administration of GIP analogues on cognition, synaptic plasticity and neurogenesis in mice. Eur J Pharmacol. 2012;674:294–306. doi:https://doi.org/10.1016/j.ejphar.2011.11.007.
   PubMed Web of Science ®Google Scholar
• Hoare SR. Mechanisms of peptide and nonpeptide ligand binding to Class B G-protein-coupled receptors. Drug Discov Today. 2005;10:417–27. doi:https://doi.org/10.1016/S1359-6446(05)03370-2.
   PubMed Web of Science ®Google Scholar
• Culhane KJ, Liu Y, Cai Y, Yan EC. Transmembrane signal transduction by peptide hormones via family B G protein-coupled receptors. Front Pharmacol. 2015;6:264. doi:https://doi.org/10.3389/fphar.2015.00264.
   PubMed Web of Science ®Google Scholar
• Jazayeri A, Dore AS, Lamb D, Krishnamurthy H, Southall SM, Baig AH, Bortolato A, Koglin M, Robertson NJ, Errey JC, et al. Extra-helical binding site of a glucagon receptor antagonist. Nature. 2016;533:274–77. doi:https://doi.org/10.1038/nature17414.
   PubMed Web of Science ®Google Scholar
• Siu FY, He M, de Graaf C, Han GW, Yang D, Zhang Z, Zhou C, Xu Q, Wacker D, Joseph JS, et al. Structure of the human glucagon class B G-protein-coupled receptor. Nature. 2013;499:444–49. doi:https://doi.org/10.1038/nature12393.
   PubMed Web of Science ®Google Scholar
• Song G, Yang D, Wang Y, de Graaf C, Zhou Q, Jiang S, Liu K, Cai X, Dai A, Lin G, et al. Human GLP-1 receptor transmembrane domain structure in complex with allosteric modulators. Nature. 2017;546:312–15. doi:https://doi.org/10.1038/nature22378.
   PubMed Web of Science ®Google Scholar
• Liang YL, Khoshouei M, Radjainia M, Zhang Y, Glukhova A, Tarrasch J, Thal DM, Furness SGB, Christopoulos G, Coudrat T, et al. Phase-plate cryo-EM structure of a class B GPCR-G-protein complex. Nature. 2017;546:118–23. doi:https://doi.org/10.1038/nature22327.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sun B, Feng D, Hu H, Chu M, Qu Q, Tarrasch JT, Li S, Sun Kobilka T, Kobilka BK, et al. Cryo-EM structure of the activated GLP-1 receptor in complex with a G protein. Nature. 2017;546:248–53. doi:https://doi.org/10.1038/nature22394.
   PubMed Web of Science ®Google Scholar
• Zhang H, Qiao A, Yang D, Yang L, Dai A, de Graaf C, Reedtz-Runge S, Dharmarajan V, Zhang H, Han GW, et al. Structure of the full-length glucagon class B G-protein-coupled receptor. Nature. 2017;546:259–64. doi:https://doi.org/10.1038/nature22363.
   PubMed Web of Science ®Google Scholar
• Ravn P, Madhurantakam C, Kunze S, Matthews E, Priest C, O’Brien S, Collinson A, Papworth M, Fritsch-Fredin M, Jermutus L, et al. Structural and pharmacological characterization of novel potent and selective monoclonal antibody antagonists of glucose-dependent insulinotropic polypeptide receptor. J Biol Chem. 2013;288:19760–72. doi:https://doi.org/10.1074/jbc.M112.426288.
   PubMed Web of Science ®Google Scholar
• Mukund S, Shang Y, Clarke HJ, Madjidi A, Corn JE, Kates L, Kolumam G, Chiang V, Luis E, Murray J, et al. Inhibitory mechanism of an allosteric antibody targeting the glucagon receptor. J Biol Chem. 2013;288:36168–78. doi:https://doi.org/10.1074/jbc.M113.496984.
   PubMed Web of Science ®Google Scholar
• Hennen S, Kodra JT, Soroka V, Krogh BO, Wu X, Kaastrup P, Orskov C, Ronn SG, Schluckebier G, Barbateskovic S, et al. Structural insight into antibody-mediated antagonism of the Glucagon-like peptide-1 Receptor. Sci Rep. 2016;6:26236. doi:https://doi.org/10.1038/srep26236.
   PubMed Web of Science ®Google Scholar
• Kaneko K, Fu Y, Lin HY, Cordonier EL, Mo Q, Gao Y, Yao T, Naylor J, Howard V, Saito K, et al. Gut-derived GIP activates central Rap1 to impair neural leptin sensitivity during overnutrition. J Clin Invest. 2019;130:3786–3791. doi:https://doi.org/10.1172/JCI126107.
   Google Scholar
• Killion EA, Wang J, Yie J, Shi SD, Bates D, Min X, Komorowski R, Hager T, Deng L, Atangan L, et al. Anti-obesity effects of GIPR antagonists alone and in combination with GLP-1R agonists in preclinical models. Sci Transl Med. 2018;10(472). pii: eaat3392. doi: https://doi.org/10.1126/scitranslmed.aat3392.
   Google Scholar
• Parthier C, Kleinschmidt M, Neumann P, Rudolph R, Manhart S, Schlenzig D, Fanghanel J, Rahfeld JU, Demuth HU, Stubbs MT. Crystal structure of the incretin-bound extracellular domain of a G protein-coupled receptor. Proc Natl Acad Sci U S A. 2007;104:13942–47. doi:https://doi.org/10.1073/pnas.0706404104.
   PubMed Web of Science ®Google Scholar
• 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. doi:https://doi.org/10.1016/j.tibs.2009.02.004.
   PubMed Web of Science ®Google Scholar
• Jones IR, Owens DR, Moody AJ, Luzio SD, Morris T, Hayes TM. The effects of glucose-dependent insulinotropic polypeptide infused at physiological concentrations in normal subjects and type 2 (non-insulin-dependent) diabetic patients on glucose tolerance and B-cell secretion. Diabetologia. 1987;30:707–12. doi:https://doi.org/10.1007/BF00296993.
   PubMed Web of Science ®Google Scholar
• Dong M, Pinon DI, Cox RF, Miller LJ. 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. 2004;279:31177–82. doi:https://doi.org/10.1074/jbc.M404113200.
   PubMed Web of Science ®Google Scholar
• Koth CM, Murray JM, Mukund S, Madjidi A, Minn A, Clarke HJ, Wong T, Chiang V, Luis E, Estevez A, et al. Molecular basis for negative regulation of the glucagon receptor. Proc Natl Acad Sci U S A. 2012;109:14393–98. doi:https://doi.org/10.1073/pnas.1206734109.
   PubMed Web of Science ®Google Scholar
• Zhang H, Qiao A, Yang L, Van Eps N, Frederiksen KS, Yang D, Dai A, Cai X, Zhang H, Yi C, et al. Structure of the glucagon receptor in complex with a glucagon analogue. Nature. 2018;553:106–10. doi:https://doi.org/10.1038/nature25153.
   PubMed Web of Science ®Google Scholar
• Yang Y, Heffernan R, Paliwal K, Lyons J, Dehzangi A, Sharma A, Wang J, Sattar A, Zhou Y. SPIDER2: A Package to Predict Secondary Structure, Accessible Surface Area, and Main-Chain Torsional Angles by Deep Neural Networks. Methods Mol Biol. 2017;1484:55–63.
   PubMedGoogle Scholar
• Finan B, Ma T, Ottaway N, Muller TD, Habegger KM, Heppner KM, Kirchner H, Holland J, Hembree J, Raver C, et al. Unimolecular dual incretins maximize metabolic benefits in rodents, monkeys, and humans. Sci Transl Med. 2013;5:209ra151. doi:https://doi.org/10.1126/scitranslmed.3007218.
   PubMed Web of Science ®Google Scholar
• Frias JP, Nauck MA, Van J, Kutner ME, Cui X, Benson C, Urva S, Gimeno RE, Milicevic Z, Robins D, et al. Efficacy and safety of LY3298176, a novel dual GIP and GLP-1 receptor agonist, in patients with type 2 diabetes: a randomised, placebo-controlled and active comparator-controlled phase 2 trial. Lancet. 2018;392:2180–93. doi:https://doi.org/10.1016/S0140-6736(18)32260-8.
   PubMed Web of Science ®Google Scholar
• Mage MG. Preparation of Fab fragments from IgGs of different animal species. Methods Enzymol. 1980;70:142–50.
   PubMedGoogle Scholar
• McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, LC S, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658–74. doi:https://doi.org/10.1107/S0021889807021206.
   PubMed Web of Science ®Google Scholar
• Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60:2126–32. doi:https://doi.org/10.1107/S0907444904019158.
   PubMed Web of Science ®Google Scholar
• Murshudov GN, AA V, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53:240–55. doi:https://doi.org/10.1107/S0907444996012255.
   PubMed Web of Science ®Google Scholar
• CCP4. (Collaborative Computational Project N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 1994;50:760–63. doi:https://doi.org/10.1107/S0907444994003112.
   PubMed Web of Science ®Google Scholar
• Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66:213–21. doi:https://doi.org/10.1107/S0907444909052925.
   PubMed Web of Science ®Google Scholar