Glucagon-like peptide-1: Modulator of β-cell dysfunction and death

Diabetes, Obesity and Metabolism

Volumn 15, Issue S3, 2013, Pages 185-192

  Rondas, D ^a   D'Hertog, W ^a   Overbergh, L ^a   Mathieu, C ^a  

^a Division of Experimental Medicine and Endocrinology   (Belgium)

Author keywords

GLP 1; Glucose stimulated insulin secretion; Incretin based therapies; Type 1 diabetes; Type 2 diabetes; cell mass

Indexed keywords

CARBOHYDRATE; CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON LIKE PEPTIDE 2; GLUCOSE; INCRETIN; LIPID; PROTEIN;

CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CELL TYPE; DECREASED APPETITE; ENDOCRINE CELL; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN BLOOD LEVEL; INSULIN RELEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; STOMACH EMPTYING;

GLP-1; GLUCOSE-STIMULATED INSULIN SECRETION; INCRETIN-BASED THERAPIES; TYPE 1 DIABETES; TYPE 2 DIABETES; Β-CELL MASS;

ANIMALS; CELL DEATH; DIABETES MELLITUS; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INSULIN-SECRETING CELLS;

EID: 84883527081     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12165     Document Type: Review

References (81)

1. Bayliss WM, Starling EH. The mechanism of pancreatic secretion. J Physiol 1902; 28: 325-353.
2. Moore B. On the treatment of diabetus mellitus by acid extract of duodenal mucous membrane. Biochem J 1906; 1: 28-38.
3. Zunz ELJ. Contributions à l'étude des variations physiologiques de la secretion interne du pancreas: relations entre les secretions externe et interne du pancreas. Arch Int Physiol Biochim 1929; 31: 20-44.
4. Labarre J, Still EU. Studies on the physiology of secretin. Am J Physiol 1930; 91: 649-653.
5. McIntyre N, Holdsworth CD, Turner DS. New interpretation of oral glucose tolerance. Lancet 1964; 2: 20-21.
6. Elrick H, Stimmler L, Hlad CJ Jr, Arai Y. Plasma insulin response to oral and intravenous glucose administration. J Clin Endocrinol Metab 1964; 24: 1076-1082.
7. Arnould Y, Bellens R, Franckson JR, Conard V. Insulin response and glucose-C14 disappearance rate during the glucose tolerance test in the unanesthetized dog. Metabolism 1963; 12: 1122-1131.
8. Dupre J, Ross SA, Watson D, Brown JC. Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J Clin Endocrinol Metab 1973; 37: 826-828.
9. Mojsov S, Weir GC, Habener JF. Insulinotropin: glucagon-like peptide I (7-37) co-encoded in the glucagon gene is a potent stimulator of insulin release in the perfused rat pancreas. J Clin Invest 1987; 79: 616-619.
10. Holst JJ, Orskov C, Nielsen OV, Schwartz TW. Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Lett 1987; 211: 169-174.
11. Kreymann B, Williams G, Ghatei MA, Bloom SR. Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet 1987; 2: 1300-1304.
12. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007; 132: 2131-2157.
13. Portha B, Tourrel-Cuzin C, Movassat J. Activation of the GLP-1 receptor signalling pathway: a relevant strategy to repair a deficient beta-cell mass. Exp Diabetes Res 2011; 2011: 376509.
14. Bell GI, Santerre RF, Mullenbach GT. Hamster preproglucagon contains the sequence of glucagon and two related peptides. Nature 1983; 302: 716-718.
15. Heinrich G, Gros P, Lund PK, Bentley RC, Habener JF. Pre-proglucagon messenger ribonucleic acid: nucleotide and encoded amino acid sequences of the rat pancreatic complementary deoxyribonucleic acid. Endocrinology 1984; 115: 2176-2181.
16. Lund PK, Goodman RH, Dee PC, Habener JF. Pancreatic preproglucagon cDNA contains two glucagon-related coding sequences arranged in tandem. Proc Natl Acad Sci U S A 1982; 79: 345-349.
17. Ghiglione M, Uttenthal LO, George SK, Bloom SR. How glucagon-like is glucagon-like peptide-1? Diabetologia 1984; 27: 599-600.
18. Drucker DJ, Mojsov S, Habener JF. Cell-specific post-translational processing of preproglucagon expressed from a metallothionein-glucagon fusion gene. J Biol Chem 1986; 261: 9637-9643.
19. Mojsov S, Heinrich G, Wilson IB, Ravazzola M, Orci L, Habener JF. Preproglucagon gene expression in pancreas and intestine diversifies at the level of post-translational processing. J Biol Chem 1986; 261: 11880-11889.
20. Drucker DJ, Philippe J, Mojsov S, Chick WL, Habener JF. Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc Natl Acad Sci U S A 1987; 84: 3434-3438.
21. Suen CS, Burn P. The potential of incretin-based therapies in type 1 diabetes. Drug Discov Today 2012; 17: 89-95.
22. MacDonald PE, El-Kholy W, Riedel MJ, Salapatek AM, Light PE, Wheeler MB. The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes 2002; 51: S434-S442.
23. Nauck MA, Sauerwald A, Ritzel R, Holst JJ, Schmiegel W. Influence of glucagon-like peptide 1 on fasting glycemia in type 2 diabetic patients treated with insulin after sulfonylurea secondary failure. Diabetes Care 1998; 21: 1925-1931.
24. Hansen L, Deacon CF, Orskov C, Holst JJ. Glucagon-like peptide-1-(7-36)amide is transformed to glucagon-like peptide-1-(9-36)amide by dipeptidyl peptidase IV in the capillaries supplying the L cells of the porcine intestine. Endocrinology 1999; 140: 5356-5363.
25. Kim W, Egan JM. The role of incretins in glucose homeostasis and diabetes treatment. Pharmacol Rev 2008; 60: 470-512.
26. Deacon CF, Hughes TE, Holst JJ. Dipeptidyl peptidase IV inhibition potentiates the insulinotropic effect of glucagon-like peptide 1 in the anesthetized pig. Diabetes 1998; 47: 764-769.
27. Pederson RA, White HA, Schlenzig D, Pauly RP, McIntosh CH, Demuth HU. Improved glucose tolerance in Zucker fatty rats by oral administration of the dipeptidyl peptidase IV inhibitor isoleucine thiazolidide. Diabetes 1998; 47: 1253-1258.
28. Chu ZL, Jones RM, He H et al. A role for beta-cell-expressed G protein-coupled receptor 119 in glycemic control by enhancing glucose-dependent insulin release. Endocrinology 2007; 148: 2601-2609.
29. Chu ZL, Carroll C, Alfonso J et al. A role for intestinal endocrine cell-expressed g protein-coupled receptor 119 in glycemic control by enhancing glucagon-like Peptide-1 and glucose-dependent insulinotropic Peptide release. Endocrinology 2008; 149: 2038-2047.
30. Thorens B. Expression cloning of the pancreatic beta cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc Natl Acad Sci U S A 1992; 89: 8641-8645.
31. Thorens B, Porret A, Buhler L, Deng SP, Morel P, Widmann C. Cloning and functional expression of the human islet GLP-1 receptor. Demonstration that exendin-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes 1993; 42: 1678-1682.
32. Dillon JS, Tanizawa Y, Wheeler MB et al. Cloning and functional expression of the human glucagon-like peptide-1 (GLP-1) receptor. Endocrinology 1993; 133: 1907-1910.
33. Stoffel M, Espinosa R 3rd, Le Beau MM, Bell GI. Human glucagon-like peptide-1 receptor gene. Localization to chromosome band 6p21 by fluorescence in situ hybridization and linkage of a highly polymorphic simple tandem repeat DNA polymorphism to other markers on chromosome 6. Diabetes 1993; 42: 1215-1218.
34. Underwood CR, Garibay P, Knudsen LB 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 2010; 285: 723-730.
35. Al-Sabah S, Donnelly D. A model for receptor-peptide binding at the glucagon-like peptide-1 (GLP-1) receptor through the analysis of truncated ligands and receptors. Br J Pharmacol 2003; 140: 339-346.
36. Coopman K, Wallis R, Robb G et al. Residues within the transmembrane domain of the glucagon-like peptide-1 receptor involved in ligand binding and receptor activation: modelling the ligand-bound receptor. Mol Endocrinol 2011; 25: 1804-1818.
37. Miyawaki K, Yamada Y, Yano H et al. Glucose intolerance caused by a defect in the entero-insular axis: a study in gastric inhibitory polypeptide receptor knockout mice. Proc Natl Acad Sci U S A 1999; 96: 14843-14847.
38. Xu G, Kaneto H, Laybutt DR et al. Downregulation of GLP-1 and GIP receptor expression by hyperglycemia: possible contribution to impaired incretin effects in diabetes. Diabetes 2007; 56: 1551-1558.
39. Kang ZF, Deng Y, Zhou Y et al. Pharmacological reduction of NEFA restores the efficacy of incretin-based therapies through GLP-1 receptor signalling in the beta cell in mouse models of diabetes. Diabetologia 2013; 56: 423-433.
40. Fonseca SG, Urano F, Weir GC, Gromada J, Burcin M. Wolfram syndrome 1 and adenylyl cyclase 8 interact at the plasma membrane to regulate insulin production and secretion. Nat Cell Biol 2012; 14: 1105-1112.
41. Cooper DM. Regulation and organization of adenylyl cyclases and cAMP. Biochem J 2003; 375: 517-529.
42. Song WJ, Seshadri M, Ashraf U et al. Snapin mediates incretin action and augments glucose-dependent insulin secretion. Cell Metab 2011; 13: 308-319.
43. Light PE, Manning Fox JE, Riedel MJ, Wheeler MB. Glucagon-like peptide-1 inhibits pancreatic ATP-sensitive potassium channels via a protein kinase A- and ADP-dependent mechanism. Mol Endocrinol 2002; 16: 2135-2144.
44. Beguin P, Nagashima K, Nishimura M, Gonoi T, Seino S. PKA-mediated phosphorylation of the human K(ATP) channel: separate roles of Kir6.2 and SUR1 subunit phosphorylation. EMBO J 1999; 18: 4722-4732.
45. Kang G, Leech CA, Chepurny OG, Coetzee WA, Holz GG. Role of the cAMP sensor Epac as a determinant of KATP channel ATP sensitivity in human pancreatic beta-cells and rat INS-1 cells. J Physiol 2008; 586: 1307-1319.
46. MacDonald PE, Wheeler MB. Voltage-dependent K(+) channels in pancreatic beta cells: role, regulation and potential as therapeutic targets. Diabetologia 2003; 46: 1046-1062.
47. Gromada J, Bokvist K, Ding WG, Holst JJ, Nielsen JH, Rorsman P. Glucagon-like peptide 1 (7-36) amide stimulates exocytosis in human pancreatic beta-cells by both proximal and distal regulatory steps in stimulus-secretion coupling. Diabetes 1998; 47: 57-65.
48. Salapatek AM, MacDonald PE, Gaisano HY, Wheeler MB. Mutations to the third cytoplasmic domain of the glucagon-like peptide 1 (GLP-1) receptor can functionally uncouple GLP-1-stimulated insulin secretion in HIT-T15 cells. Mol Endocrinol 1999; 13: 1305-1317.
49. Suga S, Kanno T, Nakano K, Takeo T, Dobashi Y, Wakui M. GLP-I(7-36) amide augments Ba2+ current through L-type Ca2+ channel of rat pancreatic beta-cell in a cAMP-dependent manner. Diabetes 1997; 46: 1755-1760.
50. Fraser ID, Tavalin SJ, Lester LB et al. A novel lipid-anchored A-kinase anchoring protein facilitates cAMP-responsive membrane events. EMBO J 1998; 17: 2261-2272.
51. Lester LB, Langeberg LK, Scott JD. Anchoring of protein kinase A facilitates hormone-mediated insulin secretion. Proc Natl Acad Sci U S A 1997; 94: 14942-14947.
52. Graves TK, Hinkle PM. Ca(2+)-induced Ca(2+) release in the pancreatic beta-cell: direct evidence of endoplasmic reticulum Ca(2+) release. Endocrinology 2003; 144: 3565-3574.
53. Kang G, Holz GG. Amplification of exocytosis by Ca2+-induced Ca2+ release in INS-1 pancreatic beta cells. J Physiol 2003; 546: 175-189.
54. Kang G, Chepurny OG, Rindler MJ et al. A cAMP and Ca2+ coincidence detector in support of Ca2+-induced Ca2+ release in mouse pancreatic beta cells. J Physiol 2005; 566: 173-188.
55. Bootman MD, Berridge MJ. The elemental principles of calcium signaling. Cell 1995; 83: 675-678.
56. Tsuboi T, da Silva XG, Holz GG, Jouaville LS, Thomas AP, Rutter GA. Glucagon-like peptide-1 mobilizes intracellular Ca2+ and stimulates mitochondrial ATP synthesis in pancreatic MIN6 beta-cells. Biochem J 2003; 369: 287-299.
57. Renstrom E, Eliasson L, Rorsman P. Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol 1997; 502: 105-118.
58. Eliasson L, Ma X, Renstrom E et al. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 2003; 121: 181-197.
59. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY. Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic beta-cells. Diabetes 2007; 56: 2579-2588.
60. Vikman J, Svensson H, Huang YC et al. Truncation of SNAP-25 reduces the stimulatory action of cAMP on rapid exocytosis in insulin-secreting cells. Am J Physiol Endocrinol Metab 2009; 297: E452-E461.
61. Dalle S, Quoyer J, Varin E, Costes S. Roles and regulation of the transcription factor CREB in pancreatic beta -cells. Curr Mol Pharmacol 2011; 4: 187-195.
62. Wang X, Cahill CM, Pineyro MA, Zhou J, Doyle ME, Egan JM. Glucagon-like peptide-1 regulates the beta cell transcription factor, PDX-1, in insulinoma cells. Endocrinology 1999; 140: 4904-4907.
63. Buteau J, Roduit R, Susini S, Prentki M. 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 1999; 42: 856-864.
64. Wang X, Zhou J, Doyle ME, Egan JM. 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 2001; 142: 1820-1827.
65. Knoch KP, Meisterfeld R, Kersting S et al. cAMP-dependent phosphorylation of PTB1 promotes the expression of insulin secretory granule proteins in beta cells. Cell Metab 2006; 3: 123-134.
66. Holz GGT, Kuhtreiber WM, Habener JF. Pancreatic beta-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1(7-37). Nature 1993; 361: 362-365.
67. Gillard P, Vandemeulebroucke E, Keymeulen B et al. Functional beta-cell mass and insulin sensitivity is decreased in insulin-independent pancreas-kidney recipients. Transplantation 2009; 87: 402-407.
68. Contreras JL, Bilbao G, Smyth CA et al. Cytoprotection of pancreatic islets before and soon after transplantation by gene transfer of the anti-apoptotic Bcl-2 gene. Transplantation 2001; 71: 1015-1023.
69. Garcia-Ocana A, Vasavada RC, Takane KK, Cebrian A, Lopez-Talavera JC, Stewart AF. Using beta-cell growth factors to enhance human pancreatic Islet transplantation. J Clin Endocrinol Metab 2001; 86: 984-988.
70. Velmurugan K, Balamurugan AN, Loganathan G, Ahmad A, Hering BJ, Pugazhenthi S. Antiapoptotic actions of exendin-4 against hypoxia and cytokines are augmented by CREB. Endocrinology 2012; 153: 1116-1128.
71. Buteau J, Foisy S, Rhodes CJ, Carpenter L, Biden TJ, Prentki M. Protein kinase Czeta activation mediates glucagon-like peptide-1-induced pancreatic beta-cell proliferation. Diabetes 2001; 50: 2237-2243.
72. Buteau J, Spatz ML, Accili D. Transcription factor FoxO1 mediates glucagon-like peptide-1 effects on pancreatic beta-cell mass. Diabetes 2006; 55: 1190-1196.
73. Gomez E, Pritchard C, Herbert TP. cAMP-dependent protein kinase and Ca2+ influx through L-type voltage-gated calcium channels mediate Raf-independent activation of extracellular regulated kinase in response to glucagon-like peptide-1 in pancreatic beta-cells. J Biol Chem 2002; 277: 48146-48151.
74. Drucker DJ. Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endocrinol 2003; 17: 161-171.
75. Rutti S, Sauter NS, Bouzakri K, Prazak R, Halban PA, Donath MY. In vitro proliferation of adult human beta-cells. PLoS One 2012; 7: e35801.
76. Zhou J, Wang X, Pineyro MA, Egan JM. Glucagon-like peptide 1 and exendin-4 convert pancreatic AR42J cells into glucagon- and insulin-producing cells. Diabetes 1999; 48: 2358-2366.
77. Hui H, Wright C, Perfetti R. Glucagon-like peptide 1 induces differentiation of islet duodenal homeobox-1-positive pancreatic ductal cells into insulin-secreting cells. Diabetes 2001; 50: 785-796.
78. Doyle ME, Egan JM. Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol Ther 2007; 113: 546-593.
79. Li Y, Hansotia T, Yusta B, Ris F, Halban PA, Drucker DJ. Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J Biol Chem 2003; 278: 471-478.
80. Buteau J, El-Assaad W, Rhodes CJ, Rosenberg L, Joly E, Prentki M. Glucagon-like peptide-1 prevents beta cell glucolipotoxicity. Diabetologia 2004; 47: 806-815.
81. Yusta B, Baggio LL, Estall JL et al. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006; 4: 391-406.