Functional consequences of glucagon-like peptide-1 receptor cross-talk and trafficking

Journal of Biological Chemistry

Volumn 290, Issue 2, 2015, Pages 1233-1243

  Roed, Sarah Noerklit ^a   No, Anne Cathrine ^b   Wismann, Pernille ^a   Iversen, Helle ^a   Bräuner Osborne, Hans ^b   Knudsen, Sanne Moeller ^a   Waldhoer, Maria ^a  

^a NOVO NORDISK A S   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; PEPTIDES; RECYCLING; SIGNALING; SYSTEM THEORY;

DIFFERENTIAL PROPERTIES; DOMINANT NEGATIVE; GLUCAGON-LIKE PEPTIDE-1; MECHANISTIC LINK; PANCREATIC ISLET; RECEPTOR TRAFFICKING; SIGNALING PATHWAYS; STRUCTURAL SIMILARITY;

CROSSTALK;

BETA ARRESTIN 2; DYNAMIN; G PROTEIN COUPLED RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE DEPENDENT INSULINOTROPIC POLYPEPTIDE RECEPTOR; HORMONE RECEPTOR; UNCLASSIFIED DRUG; DYNAMIN I; GASTRIC INHIBITORY POLYPEPTIDE; GLP1R PROTEIN, HUMAN; GLUCAGON; GLUCAGON RECEPTOR; INCRETIN; LIGAND; SEVEN-TRANSMEMBRANE G-PROTEIN-COUPLED RECEPTOR;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; INTERNALIZATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET; PATHOLOGY;

DIABETES MELLITUS, TYPE 2; DYNAMIN I; GASTRIC INHIBITORY POLYPEPTIDE; GENE EXPRESSION REGULATION; GLUCAGON; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; HEK293 CELLS; HUMANS; INCRETINS; ISLETS OF LANGERHANS; LIGANDS; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION;

EID: 84920885272     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.592436     Document Type: Article

References (40)

1. Holst, J. J. (2007) The physiology of glucagon-like peptide 1. Physiol. Rev. 87, 1409-1439
2. Holst, J. J., and Deacon, C. F. (2007) New horizons in diabetes therapy. Immunol. Endocr. Metab. Agents Med. Chem. 7, 49-55
3. Mayo, K. E., Miller, L. J., Bataille, D., Dalle, S., Göke, B., Thorens, B., and Drucker, D. J. (2003) International Union of Pharmacology. XXXV. The glucagon receptor family. Pharmacol. Rev. 55, 167-194
4. Doyle, M. E., and Egan, J. M. (2007) Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol. Ther. 113, 546-593
5. Montrose-Rafizadeh, C., Avdonin, P., Garant, M. J., Rodgers, B. D., Kole, S., Yang, H., Levine, M. A., Schwindinger, W., and Bernier, M. (1999) Pancreatic glucagon-like peptide-1 receptor couples to multiple G proteins and activates mitogen-activated protein kinase pathways in Chinese hamster ovary cells. Endocrinology 140, 1132-1140
6. Quoyer, J., Longuet, C., Broca, C., Linck, N., Costes, S., Varin, E., Bockaert, J., Bertrand, G., and Dalle, S. (2010) GLP-1 mediates antiapoptotic effect by phosphorylating Bad through a β-arrestin 1-mediated ERK1/2 activation in pancreatic β-cells. J. Biol. Chem. 285, 1989-2002
7. Hanyaloglu, A. C., and von Zastrow, M. (2008) Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48, 537-568
8. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24
9. Chini, B., and Parenti, M. (2004) G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J. Mol. Endocrinol. 32, 325-338
10. Irannejad, R., Tomshine, J. C., Tomshine, J. R., Chevalier, M., Mahoney, J. P., Steyaert, J., Rasmussen, S. G., Sunahara, R. K., El-Samad, H., Huang, B., and von Zastrow, M. (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534-538
11. Calebiro, D., Nikolaev, V. O., Gagliani, M. C., de Filippis, T., Dees, C., Tacchetti, C., Persani, L., and Lohse, M. J. (2009). Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol. 7, e1000172
12. Ferrandon, S., Feinstein, T. N., Castro, M., Wang, B., Bouley, R., Potts, J. T., Gardella, T. J., and Vilardaga, J. P. (2009) Sustained cyclicAMPproduction by parathyroid hormone receptor endocytosis. Nat. Chem. Biol. 5, 734-742
13. Roed, S. N., Wismann, P., Underwood, C. R., Kulahin, N., Iversen, H., Cappelen, K. A., Schäffer, L., Lehtonen, J., Hecksher-Soerensen, J., Secher, A., Mathiesen, J. M., Bräuner-Osborne, H., Whistler, J. L., Knudsen, S. M., and Waldhoer, M. (2014) Real-time trafficking and signaling of the gluca-gon-like peptide-1 receptor. Mol. Cell. Endocrinol. 382, 938-949
14. Widmann, C., Dolci, W., and Thorens, B. (1995) Agonist-induced internalization and recycling of the glucagon-like peptide-1 receptor in transfected fibroblasts and in insulinomas. Biochem. J. 310, 203-214
15. Harikumar, K. G., Morfis, M. M., Sexton, P. M., and Miller, L. J. (2008) Pattern of intra-family hetero-oligomerization involving the G-proteincoupled secretin receptor. J. Mol. Neurosci. 36, 279-285
16. Schelshorn, D., Joly, F., Mutel, S., Hampe, C., Breton, B., Mutel, V., and Lütjens, R. (2012) Lateral allosterism in the glucagon receptor family: GLP-1 induces GPCR heteromer formation. Mol. Pharmacol. 81, 309-318
17. Whitaker, G. M., Lynn, F. C., McIntosh, C. H., and Accili, E. A. (2012) Regulation of GIP and GLP1 receptor cell surface expression by N-glycosylation and receptor heteromerization. PLoS ONE 7, e32675
18. Roed, S. N., Orgaard, A., Jorgensen, R., and De Meyts, P. (2012) Receptor oligomerization in family B1 of G-protein-coupled receptors: focus on BRET investigations and the link between GPCR oligomerization and binding cooperativity. Front. Endocrinol. 3, 62
19. Jorgensen, R., Norklit Roed, S., Heding, A., and Elling, C. E. (2011) Beta-arrestin-2 as a competitor for GRK2 interaction with the GLP-1 receptor upon receptor activation. Pharmacology 88, 174-181
20. DeBlasi, A., O'Reilly, K., and Motulsky, H. J. (1989) Calculating receptor number from binding experiments using same compound as radioligand and competitor. Trends Pharmacol. Sci. 10, 227-229
21. Jordan, B. A., Trapaidze, N., Gomes, I., Nivarthi, R., and Devi, L. A. (2001) Oligomerization of opioid receptors with β2-adrenergic receptors: a role in trafficking and mitogen-activated protein kinase activation. Proc. Natl. Acad. Sci. U.S.A. 98, 343-348
22. Jorgensen, R., Kubale, V., Vrecl, M., Schwartz, T. W., and Elling, C. E. (2007) Oxyntomodulin differentially affects glucagon-like peptide-1 receptor β-arrestin recruitment and signaling through Gα J. Pharmacol. Exp. Ther. 322, 148-154
23. Moens, K., Heimberg, H., Flamez, D., Huypens, P., Quartier, E., Ling, Z., Pipeleers, D., Gremlich, S., Thorens, B., and Schuit, F. (1996) Expression and functional activity of glucagon, glucagon-like peptide I, and glucosedependent insulinotropic peptide receptors in rat pancreatic islet cells. Diabetes 45, 257-261
24. Gallwitz, B., Witt, M., Fölsch, U. R., Creutzfeldt, W., and Schmidt, W. E. (1993) Binding specificity and signal transduction of receptors for gluca-gon-like peptide-1(7-36)amide and gastric inhibitory polypeptide on RINm5F insulinoma cells. J. Mol. Endocrinol. 10, 259-268
25. Irannejad, R., and von Zastrow, M. (2014) GPCR signaling along the endocytic pathway. Curr. Opin. Cell Biol. 27, 109-116
26. Calebiro, D., Nikolaev, V. O., Persani, L., and Lohse, M. J. (2010) Signaling by internalized G-protein-coupled receptors. Trends Pharmacol. Sci. 31, 221-228
27. Syme, C. A., Zhang, L., and Bisello, A. (2006) Caveolin-1 regulates cellular trafficking and function of the glucagon-like peptide 1 receptor. Mol. Endocrinol. 20, 3400-3411
28. Harper, C. B., Popoff, M. R., McCluskey, A., Robinson, P. J., and Meunier, F. A. (2013) Targeting membrane trafficking in infection prophylaxis: dynamin inhibitors. Trends Cell Biol. 23, 90-101
29. Herskovits, J. S., Burgess, C. C., Obar, R. A., and Vallee, R. B. (1993) Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578
30. Buggy, J. J., Heurich, R. O., MacDougall, M., Kelley, K. A., Livingston, J. N., Yoo-Warren, H., and Rossomando, A. J. (1997) Role of the glucagon receptor COOH-terminal domain in glucagon-mediated signaling and receptor internalization. Diabetes 46, 1400-1405
31. Krilov, L., Nguyen, A., Miyazaki, T., Unson, C. G., Williams, R., Lee, N. H., Ceryak, S., and Bouscarel, B. (2011) Dual mode of glucagon receptor internalization: role of PKCα, GRKs andβ-arrestins. Exp. Cell Res. 317, 2981-2994
32. Merlen, C., Fabrega, S., Desbuquois, B., Unson, C. G., and Authier, F. (2006) Glucagon-mediated internalization of serine-phosphorylated glucagon receptor and Gsα in rat liver. FEBS Lett. 580, 5697-5704
33. Wheeler, M. B., Gelling, R. W., Hinke, S. A., Tu, B., Pederson, R. A., Lynn, F., Ehses, J., and McIntosh, C. H. (1999) Characterization of the carboxylterminal domain of the rat glucose-dependent insulinotropic polypeptide (GIP) receptor. A role for serines 426 and 427 in regulating the rate of internalization. J. Biol. Chem. 274, 24593-24601
34. van Rijn, R. M., Whistler, J. L., and Waldhoer, M. (2010) Opioid-receptor-heteromer-specific trafficking and pharmacology. Curr. Opin. Pharmacol. 10, 73-79
35. Kedees, M. H., Grigoryan, M., Guz, Y., and Teitelman, G. (2009) Differential expression of glucagon and glucagon-like peptide 1 receptors in mouse pancreatic alpha and beta cells in two models of alpha cell hyperplasia. Mol. Cell. Endocrinol. 311, 69-76
36. Moens, K., Flamez, D., Van Schravendijk, C., Ling, Z., Pipeleers, D., and Schuit, F. (1998) Dual glucagon recognition by pancreatic β-cells via glucagon and glucagon-like peptide 1 receptors. Diabetes 47, 66-72
37. Kieffer, T. J., Heller, R. S., Unson, C. G., Weir, G. C., and Habener, J. F. (1996) Distribution of glucagon receptors on hormone-specific endocrine cells of rat pancreatic islets. Endocrinology 137, 5119-5125
38. Gromada, J., Ding, W. G., Barg, S., Renström, E., and Rorsman, P. (1997) Multisite regulation of insulin secretion by cAMP-increasing agonists: evidence that glucagon-like peptide 1 and glucagon act via distinct receptors. Pflugers Arch. 434, 515-524
39. Kuna, R. S., Girada, S. B., Asalla, S., Vallentyne, J., Maddika, S., Patterson, J. T., Smiley, D. L., DiMarchi, R. D., and Mitra, P. (2013) Glucagon-like peptide-1 receptor-mediated endosomal cAMP generation promotes glu-cose-stimulated insulin secretion in pancreatic β-cells. Am. J. Physiol. Endocrinol. Metab. 305, E161-E170
40. Pamir, N., Lynn, F. C., Buchan, A. M., Ehses, J., Hinke, S. A., Pospisilik, J. A., Miyawaki, K., Yamada, Y., Seino, Y., McIntosh, C. H., and Pederson, R. A. (2003) Glucose-dependent insulinotropic polypeptide receptor null mice exhibit compensatory changes in the enteroinsular axis. Am. J. Physiol. Endocrinol. Metab. 284, E931-E939