GLP-1 receptor activation improves β cell function and survival following induction of endoplasmic reticulum stress

Bagdade, 1967, The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects, J. Clin. Invest., 46, 1549, 10.1172/JCI105646 Blais, 2004, Activating transcription factor 4 is translationally regulated by hypoxic stress, Mol. Cell. Biol., 24, 7469, 10.1128/MCB.24.17.7469-7482.2004 Buchanan, 2002, Preservation of pancreatic beta-cell function and prevention of type 2 diabetes by pharmacological treatment of insulin resistance in high-risk hispanic women, Diabetes, 51, 2796, 10.2337/diabetes.51.9.2796 Buse, 2004, Effects of exenatide (exendin-4) on glycemic control over 30 weeks in sulfonylurea-treated patients with type 2 diabetes, Diabetes Care, 27, 2628, 10.2337/diacare.27.11.2628 Buteau, 1999, Glucagon-like peptide-1 promotes DNA synthesis, activates phosphatidylinositol 3-kinase and increases transcription factor pancreatic and duodenal homeobox gene 1 (PDX-1) DNA binding activity in beta (INS-1)-cells, Diabetologia, 42, 856, 10.1007/s001250051238 Buteau, 2001, Protein kinase Czeta activation mediates glucagon-like peptide-1-induced pancreatic beta-cell proliferation, Diabetes, 50, 2237, 10.2337/diabetes.50.10.2237 Buteau, 2004, Glucagon-like peptide-1 prevents beta cell glucolipotoxicity, Diabetologia, 47, 806, 10.1007/s00125-004-1379-6 Butler, 2003, Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes, Diabetes, 52, 102, 10.2337/diabetes.52.1.102 Campos, 1996, Identification of protein phosphatase-1-binding proteins by microcystin-biotin affinity chromatography, J. Biol. Chem., 271, 28478, 10.1074/jbc.271.45.28478 Chomczynski, 1987, Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem., 162, 156, 10.1016/0003-2697(87)90021-2 Degn, 2004, One week's treatment with the long-acting glucagon-like peptide 1 derivative liraglutide (NN2211) markedly improves 24-h glycemia and alpha- and beta-cell function and reduces endogenous glucose release in patients with type 2 diabetes, Diabetes, 53, 1187, 10.2337/diabetes.53.5.1187 Delepine, 2000, EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome, Nat. Genet., 25, 406, 10.1038/78085 Drucker, 2003, Glucagon-like peptide-1 and the islet beta-cell: augmentation of cell proliferation and inhibition of apoptosis, Endocrinology, 144, 5145, 10.1210/en.2003-1147 Drucker, 2006, The biology of incretin hormones, Cell Metab, 3, 153, 10.1016/j.cmet.2006.01.004 Drucker, 1987, Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line, Proc. Natl. Acad. Sci. USA, 84, 3434, 10.1073/pnas.84.10.3434 Efanova, 1998, Glucose and tolbutamide induce apoptosis in pancreatic beta-cells. A process dependent on intracellular Ca2+ concentration, J. Biol. Chem., 273, 33501, 10.1074/jbc.273.50.33501 Farilla, 2002, Glucagon-like Peptide-1 promotes islet cell growth and inhibits apoptosis in zucker diabetic rats, Endocrinology, 143, 4397, 10.1210/en.2002-220405 Farilla, 2003, Glucagon-like peptide 1 inhibits cell apoptosis and improves glucose responsiveness of freshly isolated human islets, Endocrinology, 144, 5149, 10.1210/en.2003-0323 Fonseca, 2005, WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells, J. Biol. Chem., 280, 39609, 10.1074/jbc.M507426200 Garcia, 1976, Biosynthesis of proinsulin and insulin in newborn rat pancreas. Interaction of glucose, cyclic AMP, somatostatin, and sulfonylureas on the (3H) leucine incorporation into immunoreactive insulin, J. Clin. Invest., 57, 230, 10.1172/JCI108264 Gomez, 2004, Glucose-stimulated protein synthesis in pancreatic beta-cells parallels an increase in the availability of the translational ternary complex (eIF2-GTP.Met-tRNAi) and the dephosphorylation of eIF2 alpha, J. Biol. Chem., 279, 53937, 10.1074/jbc.M408682200 Harding, 1999, Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase, Nature, 397, 271, 10.1038/16729 Harding, 2000, Regulated translation initiation controls stress-induced gene expression in mammalian cells, Mol. Cell, 6, 1099, 10.1016/S1097-2765(00)00108-8 Harding, 2000, Perk is essential for translational regulation and cell survival during the unfolded protein response, Mol. Cell, 5, 897, 10.1016/S1097-2765(00)80330-5 Harding, 2001, Diabetes mellitus and exocrine pancreatic dysfunction in perk−/− mice reveals a role for translational control in secretory cell survival, Mol. Cell, 7, 1153, 10.1016/S1097-2765(01)00264-7 Harding, 2002, Transcriptional and translational control in the Mammalian unfolded protein response, Annu. Rev. Cell Dev. Biol., 18, 575, 10.1146/annurev.cellbio.18.011402.160624 Hohmeier, 2000, Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion, Diabetes, 49, 424, 10.2337/diabetes.49.3.424 Holz, 2004, Epac: a new cAMP-binding protein in support of glucagon-like peptide-1 receptor-mediated signal transduction in the pancreatic beta-cell, Diabetes, 53, 5, 10.2337/diabetes.53.1.5 Hoorens, 1996, Glucose promotes survival of rat pancreatic beta cells by activating synthesis of proteins which suppress a constitutive apoptotic program, J. Clin. Invest., 98, 1568, 10.1172/JCI118950 Hosokawa, 1996, Mechanism of impaired glucose-potentiated insulin secretion in diabetic 90% pancreatectomy rats. Study using glucagonlike peptide-1 (7–37), J. Clin. Invest., 97, 180, 10.1172/JCI118387 Inoue, 1998, A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome), Nat. Genet., 20, 143, 10.1038/2441 Iwawaki, 2004, A transgenic mouse model for monitoring endoplasmic reticulum stress, Nat. Med., 10, 98, 10.1038/nm970 Jhala, 2003, cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2, Genes Dev., 17, 1575, 10.1101/gad.1097103 Jiang, 2004, Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response, Mol. Cell. Biol., 24, 1365, 10.1128/MCB.24.3.1365-1377.2004 Kaneto, 2005, Oxidative stress, ER stress, and the JNK pathway in type 2 diabetes, J. Mol. Med., 83, 429, 10.1007/s00109-005-0640-x Kaufman, 2002, The unfolded protein response in nutrient sensing and differentiation, Nat. Rev. Mol. Cell Biol., 3, 411, 10.1038/nrm829 Kharroubi, 2004, Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress, Endocrinology, 145, 5087, 10.1210/en.2004-0478 Kim, 2003, Development and characterization of a glucagon-like peptide 1-albumin conjugate: the ability to activate the glucagon-like peptide 1 receptor in vivo, Diabetes, 52, 751, 10.2337/diabetes.52.3.751 Kimmerling, 1976, Locating the site(s) of insulin resistance in patients with nonketotic diabetes mellitus, Diabetes, 25, 673, 10.2337/diab.25.8.673 Koehler, 2005, The HeLa cell glucagon-like peptide-2 receptor is coupled to regulation of apoptosis and ERK1/2 activation through divergent signaling pathways, Mol. Endocrinol., 19, 459, 10.1210/me.2004-0196 Lassot, 2001, ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase, Mol. Cell. Biol., 21, 2192, 10.1128/MCB.21.6.2192-2202.2001 Laybutt, 2002, Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycemia, Diabetes, 51, 413, 10.2337/diabetes.51.2.413 Li, 2003, Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis, J. Biol. Chem., 278, 471, 10.1074/jbc.M209423200 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)), Methods, 25, 402, 10.1006/meth.2001.1262 Lowell, 2005, Mitochondrial dysfunction and type 2 diabetes, Science, 307, 384, 10.1126/science.1104343 Lu, 2004, Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response, J. Cell Biol., 167, 27, 10.1083/jcb.200408003 Ma, 2002, Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response, J. Mol. Biol., 318, 1351, 10.1016/S0022-2836(02)00234-6 Ma, 2003, Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress, J. Biol. Chem., 278, 34864, 10.1074/jbc.M301107200 Maedler, 2005, Sulfonylurea induced beta-cell apoptosis in cultured human islets, J. Clin. Endocrinol. Metab., 90, 501, 10.1210/jc.2004-0699 Marciniak, 2004, CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum, Genes Dev., 18, 3066, 10.1101/gad.1250704 Miyazaki, 1990, Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms, Endocrinology, 127, 126, 10.1210/endo-127-1-126 Novoa, 2001, Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha, J. Cell Biol., 153, 1011, 10.1083/jcb.153.5.1011 Novoa, 2003, Stress-induced gene expression requires programmed recovery from translational repression, EMBO J., 22, 1180, 10.1093/emboj/cdg112 Ovalle, 2004, Effect of rosiglitazone versus insulin on the pancreatic beta-cell function of subjects with type 2 diabetes, Diabetes Care, 27, 2585, 10.2337/diacare.27.11.2585 Oyadomari, 2004, Roles of CHOP/GADD153 in endoplasmic reticulum stress, Cell Death Differ., 11, 381, 10.1038/sj.cdd.4401373 Ozcan, 2004, Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes, Science, 306, 457, 10.1126/science.1103160 Perfetti, 2000, Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats, Endocrinology, 141, 4600, 10.1210/endo.141.12.7806 Perseghin, 2003, Cellular mechanism of insulin resistance: potential links with inflammation, Int. J. Obes. Relat. Metab. Disord., 27, S6, 10.1038/sj.ijo.0802491 Pipeleers, 1985, A new in vitro model for the study of pancreatic A and B cells, Endocrinology, 117, 806, 10.1210/endo-117-3-806 Pipeleers, 1985, Interplay of nutrients and hormones in the regulation of glucagon release, Endocrinology, 117, 817, 10.1210/endo-117-3-817 Pipeleers, 1986, Pancreatic B cells possess defense mechanisms against cell-specific toxicity, Proc. Natl. Acad. Sci. USA, 83, 5267, 10.1073/pnas.83.14.5267 Rachman, 1996, Normalization of insulin responses to glucose by overnight infusion of glucagon-like peptide 1(7-36)amide in patients with NIDDM, Diabetes, 45, 1524, 10.2337/diab.45.11.1524 Rhodes, 2005, Type 2 diabetes-a matter of beta-cell life and death?, Science, 307, 380, 10.1126/science.1104345 Robertson, 2004, Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes, J. Biol. Chem., 279, 42351, 10.1074/jbc.R400019200 Ron, 2002, Translational control in the endoplasmic reticulum stress response, J. Clin. Invest., 110, 1383, 10.1172/JCI0216784 Rothman, 1995, Decreased muscle glucose transport/phosphorylation is an early defect in the pathogenesis of non-insulin-dependent diabetes mellitus, Proc. Natl. Acad. Sci. USA, 92, 983, 10.1073/pnas.92.4.983 Schatz, 1975, (Pro-) insulin biosynthesis and release of newly synthesized (pro-) insulin from isolated islets of rat pancreas in the presence of amino acids and sulphonylureas, Eur. J. Clin. Invest., 5, 477 Scheuner, 2001, Translational control is required for the unfolded protein response and in vivo glucose homeostasis, Mol. Cell, 7, 1165, 10.1016/S1097-2765(01)00265-9 Scheuner, 2005, Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis, Nat. Med., 11, 757, 10.1038/nm1259 Schuit, 1991, Measuring the balance between insulin synthesis and insulin release, Biochem. Biophys. Res. Commun., 178, 1182, 10.1016/0006-291X(91)91017-7 Shen, 2004, The unfolded protein response–a stress signaling pathway of the endoplasmic reticulum, J. Chem. Neuroanat., 28, 79, 10.1016/j.jchemneu.2004.02.006 Vattem, 2004, Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells, Proc. Natl. Acad. Sci. USA, 101, 11269, 10.1073/pnas.0400541101 Wang, 2002, Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice, Diabetologia, 45, 1263, 10.1007/s00125-002-0828-3 Wang, 1999, A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse, J. Clin. Invest., 103, 27, 10.1172/JCI4431 Wang, 1999, Glucagon-like peptide-1 regulates the beta cell transcription factor, PDX-1, in insulinoma cells, Endocrinology, 140, 4904, 10.1210/endo.140.10.7158 Wang, 2001, Glucagon-like peptide-1 causes pancreatic duodenal homeobox-1 protein translocation from the cytoplasm to the nucleus of pancreatic beta-cells by a cyclic adenosine monophosphate/protein kinase A-dependent mechanism, Endocrinology, 142, 1820, 10.1210/endo.142.5.8128 Wang, 2004, Glucagon-like peptide-1 regulates proliferation and apoptosis via activation of protein kinase B in pancreatic (INS-1) beta-cells, Diabetologia, 47, 478, 10.1007/s00125-004-1327-5 Wang, 2005, ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity, J. Cell Sci., 118, 3905, 10.1242/jcs.02513 Wek, 2006, Coping with stress: eIF2 kinases and translational control, Biochem. Soc. Trans., 34, 7, 10.1042/BST0340007 Wu, 2006, From acute ER stress to physiological roles of the unfolded protein response, Cell Death Differ., 13, 374, 10.1038/sj.cdd.4401840 Xu, 1999, Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats, Diabetes, 48, 2270, 10.2337/diabetes.48.12.2270 Yoshioka, 1997, A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice, Diabetes, 46, 887, 10.2337/diab.46.5.887 Yusta, 2000, Enteroendocrine localization of GLP-2 receptor expression, Gastroenterology, 119, 744, 10.1053/gast.2000.16489 Zander, 2002, Effect of 6-week course of glucagon-like peptide 1 on glycaemic control, insulin sensitivity, and beta-cell function in type 2 diabetes: a parallel-group study, Lancet, 359, 824, 10.1016/S0140-6736(02)07952-7