Glucose-Dependent Insulinotropic Peptide Stimulates Glucagon-Like Peptide 1 Production by Pancreatic Islets via Interleukin 6, Produced by α Cells

Gastroenterology

Volumn 151, Issue 1, 2016, Pages 165-179

  Timper, Katharina ^a   Dalmas, Elise ^a   Dror, Erez ^a   Rütti, Sabine ^b   Thienel, Constanze ^a   Sauter, Nadine S ^a   Bouzakri, Karim ^b   Bédat, Benoit ^c   Pattou, Francois ^d   Kerr Conte, Julie ^d   Böni Schnetzler, Marianne ^a   Donath, Marc Y ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d UNIV LILLE   (France)

Author keywords

Hormones; Immune Regulation; Incretin; Mouse Model

Indexed keywords

ADENOSINE PHOSPHATE; ADENYLATE CYCLASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DAPAGLIFLOZIN; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; SODIUM GLUCOSE COTRANSPORTER 2; GLUCOSE BLOOD LEVEL; INSULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETOGENESIS; DIET INDUCED OBESITY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE AMPLIFICATION; GENE EXPRESSION; GLUCAGON RELEASE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INSULIN BLOOD LEVEL; INSULIN RELEASE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DIABETES MELLITUS, EXPERIMENTAL; METABOLISM; SECRETION (PROCESS);

ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON-LIKE PEPTIDE 1; GLUCAGON-SECRETING CELLS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; INTERLEUKIN-6; MICE; MICE, INBRED C57BL;

EID: 84990057324     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2016.03.003     Document Type: Article

References (44)

1. 1 Svendsen, B., Holst, J.J., Regulation of gut hormone secretion. Studies using isolated perfused intestines. Peptides 77 (2016), 47–53.
2. 2 Rouille, Y., Kantengwa, S., Irminger, J.C., et al. Role of the prohormone convertase PC3 in the processing of proglucagon to glucagon-like peptide 1. J Biol Chem 272 (1997), 32810–32816.
3. 3 Rouille, Y., Martin, S., Steiner, D.F., Differential processing of proglucagon by the subtilisin-like prohormone convertases PC2 and PC3 to generate either glucagon or glucagon-like peptide. J Biol Chem 270 (1995), 26488–26496.
4. 4 Marchetti, P., Lupi, R., Bugliani, M., et al. A local glucagon-like peptide 1 (GLP-1) system in human pancreatic islets. Diabetologia 55 (2012), 3262–3272.
5. 5 Ellingsgaard, H., Hauselmann, I., Schuler, B., et al. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and alpha cells. Nat Med 17 (2011), 1481–1489.
6. 6 Baggio, L.L., Drucker, D.J., Biology of incretins: GLP-1 and GIP. Gastroenterology 132 (2007), 2131–2157.
7. 7 Ehses, J.A., Casilla, V.R., Doty, T., et al. Glucose-dependent insulinotropic polypeptide promotes beta-(INS-1) cell survival via cyclic adenosine monophosphate-mediated caspase-3 inhibition and regulation of p38 mitogen-activated protein kinase. Endocrinology 144 (2003), 4433–4445.
8. 8 Li, Y., Hansotia, T., Yusta, B., et al. Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J Biol Chem 278 (2003), 471–478.
9. 9 Seino, Y., Yabe, D., Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1: incretin actions beyond the pancreas. J Diabetes Investig 4 (2013), 108–130.
10. 10 Moens, K., Heimberg, H., Flamez, D., et al. Expression and functional activity of glucagon, glucagon-like peptide I, and glucose-dependent insulinotropic peptide receptors in rat pancreatic islet cells. Diabetes 45 (1996), 257–261.
11. 11 Fujita, Y., Wideman, R.D., Asadi, A., et al. Glucose-dependent insulinotropic polypeptide is expressed in pancreatic islet alpha-cells and promotes insulin secretion. Gastroenterology 138 (2010), 1966–1975.
12. 12 Holst, J.J., Christensen, M., Lund, A., et al. Regulation of glucagon secretion by incretins. Diabetes Obes Metab 13:Suppl 1 (2011), 89–94.
13. 13 De Marinis, Y.Z., Salehi, A., Ward, C.E., Zhang, Q., et al. GLP-1 inhibits and adrenaline stimulates glucagon release by differential modulation of N- and L-type Ca2+ channel-dependent exocytosis. Cell Metab 11 (2010), 543–553.
14. 14 Roberge, J.N., Brubaker, P.L., Regulation of intestinal proglucagon-derived peptide secretion by glucose-dependent insulinotropic peptide in a novel enteroendocrine loop. Endocrinology 133 (1993), 233–240.
15. 15 Hansen, L., Holst, J.J., The effects of duodenal peptides on glucagon-like peptide-1 secretion from the ileum. A duodeno–ileal loop?. Regul Pept 110 (2002), 39–45.
16. 16 Vilsboll, T., Knop, F.K., Krarup, T., et al. The pathophysiology of diabetes involves a defective amplification of the late-phase insulin response to glucose by glucose-dependent insulinotropic polypeptide-regardless of etiology and phenotype. J Clin Endocrinol Metab 88 (2003), 4897–4903.
17. 17 Vilsboll, T., Krarup, T., Madsbad, S., et al. Defective amplification of the late phase insulin response to glucose by GIP in obese type II diabetic patients. Diabetologia 45 (2002), 1111–1119.
18. 18 Nauck, M.A., Heimesaat, M.M., Orskov, C., et al. Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest 91 (1993), 301–307.
19. 19 Chia, C.W., Carlson, O.D., Kim, W., et al. Exogenous glucose-dependent insulinotropic polypeptide worsens post prandial hyperglycemia in type 2 diabetes. Diabetes 58 (2009), 1342–1349.
20. 20 Mentis, N., Vardarli, I., Kothe, L.D., et al. GIP does not potentiate the antidiabetic effects of GLP-1 in hyperglycemic patients with type 2 diabetes. Diabetes 60 (2011), 1270–1276.
21. 21 Donath, M.Y., Dalmas, E., Sauter, N.S., et al. Inflammation in obesity and diabetes: islet dysfunction and therapeutic opportunity. Cell Metab 17 (2013), 860–872.
22. 22 Donath, M.Y., Shoelson, S.E., Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11 (2011), 98–107.
23. 23 Donath, M.Y., Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov 13 (2014), 465–476.
24. 24 Timper, K., Grisouard, J., Sauter, N.S., et al. Glucose-dependent insulinotropic polypeptide induces cytokine expression, lipolysis, and insulin resistance in human adipocytes. Am J Physiol Endocrinol Metab 304 (2013), E1–E13.
25. 25 Suzuki, T., Imai, J., Yamada, T., et al. Interleukin-6 enhances glucose-stimulated insulin secretion from pancreatic beta-cells: potential involvement of the PLC-IP3-dependent pathway. Diabetes 60 (2011), 537–547.
26. 26 Ellingsgaard, H., Ehses, J.A., Hammar, E.B., et al. Interleukin-6 regulates pancreatic alpha-cell mass expansion. Proc Natl Acad Sci U S A 105 (2008), 13163–13168.
27. 27 Ehses, J.A., Perren, A., Eppler, E., et al. Increased number of islet-associated macrophages in type 2 diabetes. Diabetes 56 (2007), 2356–2370.
28. 28 Parnaud, G., Bosco, D., Berney, T., et al. Proliferation of sorted human and rat beta cells. Diabetologia 51 (2008), 91–100.
29. 29 Boni-Schnetzler, M., Thorne, J., Parnaud, G., et al. Increased interleukin (IL)-1beta messenger ribonucleic acid expression in beta -cells of individuals with type 2 diabetes and regulation of IL-1beta in human islets by glucose and autostimulation. J Clin Endocrinol Metab 93 (2008), 4065–4074.
30. 30 Malaisse, W.J., Garcia-Morales, P., Dufrane, S.P., et al. Forskolin-induced activation of adenylate cyclase, cyclic adenosine monophosphate production and insulin release in rat pancreatic islets. Endocrinology 115 (1984), 2015–2020.
31. 31 Bonner, C., Kerr-Conte, J., Gmyr, V., et al. Inhibition of the glucose transporter SGLT2 with dapagliflozin in pancreatic alpha cells triggers glucagon secretion. Nat Med 21 (2015), 512–517.
32. 32 Christensen, M., Vedtofte, L., Holst, J.J., et al. Glucose-dependent insulinotropic polypeptide: a bifunctional glucose-dependent regulator of glucagon and insulin secretion in humans. Diabetes 60 (2011), 3103–3109.
33. 33 Malmgren, S., Ahren, B., DPP-4 inhibition contributes to the prevention of hypoglycaemia through a GIP-glucagon counterregulatory axis in mice. Diabetologia 58 (2015), 1091–1099.
34. 34 Wang, J., Cao, Y., Steiner, D.F., Regulation of proglucagon transcription by activated transcription factor (ATF) 3 and a novel isoform, ATF3b, through the cAMP-response element/ATF site of the proglucagon gene promoter. J Biol Chem 278 (2003), 32899–32904.
35. 35 Ferrannini, E., Muscelli, E., Frascerra, S., et al. Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients. J Clin Invest 124 (2014), 499–508.
36. 36 Hansen, A.M., Bodvarsdottir, T.B., Nordestgaard, D.N., et al. Upregulation of alpha cell glucagon-like peptide 1 (GLP-1) in Psammomys obesus–an adaptive response to hyperglycaemia?. Diabetologia 54 (2011), 1379–1387.
37. 37 Fernandez-Millan, E., de Toro-Martin, J., Lizarraga-Mollinedo, E., et al. Role of endogenous IL-6 in the neonatal expansion and functionality of Wistar rat pancreatic alpha cells. Diabetologia 56 (2013), 1098–1107.
38. 38 Pamir, N., Lynn, F.C., Buchan, A.M., et al. Glucose-dependent insulinotropic polypeptide receptor null mice exhibit compensatory changes in the enteroinsular axis. Am J Physiol Endocrinol Metab 284 (2003), E931–E939.
39. 39 Shirazi, R., Palsdottir, V., Collander, J., et al. Glucagon-like peptide 1 receptor induced suppression of food intake, and body weight is mediated by central IL-1 and IL-6. Proc Natl Acad Sci U S A 110 (2013), 16199–16204.
40. 40 Amland, P.F., Jorde, R., Burhol, P.G., et al. Effect of intravenously infused porcine GIP on serum insulin in obese and lean subjects studied with the hyperglycemic clamp technique. Scand J Gastroenterol 20 (1985), 309–314.
41. 41 Maedler, K., Sergeev, P., Ris, F., et al. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110 (2002), 851–860.
42. 42 Aaboe, K., Akram, S., Deacon, C.F., et al. Restoration of the insulinotropic effect of glucose-dependent insulinotropic polypeptide contributes to the antidiabetic effect of dipeptidyl peptidase-4 inhibitors. Diabetes Obes Metab 17 (2015), 74–81.
43. 43 Hojberg, P.V., Vilsboll, T., Rabol, R., et al. Four weeks of near-normalisation of blood glucose improves the insulin response to glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide in patients with type 2 diabetes. Diabetologia 52 (2009), 199–207.
44. 44 Timper, K., Seelig, E., Tsakiris, D.A., et al. Safety, pharmacokinetics, and preliminary efficacy of a specific anti-IL-1alpha therapeutic antibody (MABp1) in patients with type 2 diabetes mellitus. J Diabetes Complications 29 (2015), 955–960.