Exendin-4 protects murine MIN6 pancreatic β-cells from interleukin-1β-induced apoptosis via the NF-κB pathway

Journal of Endocrinological Investigation

Volumn 36, Issue 10, 2013, Pages 803-811

  Liu, X H ^a   Wang, Y P ^a   Wang, L X ^a   Chen, Z ^a   Liu, X Y ^a   Liu, L B ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

cell apoptosis; Exendin 4; Glucagon like peptide 1; Inducible nitric oxide synthase; Interleukin 1 ; Nuclear factor B

Indexed keywords

EXENDIN 4; HOE 33342; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LIPOCORTIN 5; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRITE; PYRROLIDINE DITHIOCARBAMATE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; IMMUNE RESPONSE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOKINES; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; INTERLEUKIN-1BETA; MICE; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDES; SIGNAL TRANSDUCTION; VENOMS;

EID: 84891693203     PISSN: 03914097     EISSN: 17208386     Source Type: Journal    
DOI: 10.3275/8938     Document Type: Article

References (51)

1. Lee SC, Pervaiz S. Apoptosis in the pathophysiology of diabetes mellitus. Int J Biochem Cell Biol 2007, 39: 497-504.
2. Tews D, Werner U, Eckel J. Enhanced protection against cytokine- and fatty acid-induced apoptosis in pancreatic beta cells by combined treatment with glucagon-like peptide-1 receptor agonists and insulin analogues. Horm Metab Res 2008, 40: 172-80.
3. Pan XD, Chen XC, Zhu YG, et al. Neuroprotective role of tripchlorolide on inflammatory neurotoxicity induced by lipopolysaccharide-activated microglia. Biochem Pharmacol 2008, 76: 362-72.
4. Wang LX, Wang YP, Chen Z, et al. Exendin-4 protects murine pancreatic beta-cells from dexamethasone-induced apoptosis through PKA and PI-3K signaling. Diabetes Res Clin Pract 2010, 90: 297-304.
5. Liu LB, Wang YP, Pan XD, Jiang SY, Chen Z. [Exendin-4 protected murine MIN6 pancreatic beta-cells from oxidative stress-induced apoptosis via down-regulation of NF-kappaB-iNOS-NO pathway]. Yao Xue Xue Bao 2008, 43: 690-4.
6. 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 2002, 110: 851-60.
7. Storling J, Binzer J, Andersson AK, et al. Nitric oxide contributes to cytokine-induced apoptosis in pancreatic beta cells via potentiation of JNK activity and inhibition of Akt. Diabetologia 2005, 48: 2039-50.
8. Zumsteg U, Frigerio S, Hollander GA. Nitric oxide production and Fas surface expression mediate two independent pathways of cytokine-induced murine beta-cell damage. Diabetes 2000, 49: 39-47.
9. Ortis F, Cardozo AK, Crispim D, Storling J, Mandrup-Poulsen T, Eizirik DL. Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-kappaB activation. Mol Endocrinol 2006, 20: 1867-79.
10. Makeeva N, Myers JW, Welsh N. Role of MKK3 and p38 MAPK in cytokine-induced death of insulin-producing cells. Biochem J 2006, 393: 129-39.
11. Abdelli S, Abderrahmani A, Hering BJ, Beckmann JS, Bonny C. The c-Jun N-terminal kinase JNK participates in cytokine- and isolation stress-induced rat pancreatic islet apoptosis. Diabetologia 2007, 50: 1660-9.
12. Perez-Arana G, Blandino-Rosano M, Prada-Oliveira A, Aguilar-Diosdado M, Segundo C. Decrease in {beta}-cell proliferation precedes apoptosis during diabetes development in bio-breeding/worcester rat: beneficial role of Exendin-4. Endocrinology 2010, 151: 2538-46.
13. Donath MY, Schumann DM, Faulenbach M, Ellingsgaard H, Perren A, Ehses JA. Islet inflammation in type 2 diabetes: from metabolic stress to therapy. Diabetes Care 2008, 31 (Suppl. 2): S161-4.
14. Heimberg H, Heremans Y, Jobin C, et al. Inhibition of cytokine-induced NF-kappaB activation by adenovirus-mediated expression of a NF-kappaB super-repressor prevents beta-cell apoptosis. Diabetes 2001, 50: 2219-24.
15. Giannoukakis N, Rudert WA, Trucco M, Robbins PD. Protection of human islets from the effects of interleukin-1beta by adenoviral gene transfer of an Ikappa B repressor. J Biol Chem 2000, 275: 36509-13.
16. Nauck MA, Heimesaat MM, Behle K, et al. Effects of glucagon-like peptide 1 on counterregulatory hormone responses, cognitive functions, and insulin secretion during hyperinsulinemic, stepped hypoglycemic clamp experiments in healthy volunteers. J Clin Endocrinol Metab 2002, 87: 1239-46.
17. Gutzwiller JP, Goke B, Drewe J, et al. Glucagon-like peptide-1: a potent regulator of food intake in humans. Gut 1999, 44: 81-6.
18. Komatsu R, Matsuyama T, Namba M, et al. Glucagonostatic and insulinotropic action of glucagonlike peptide I-(7-36)-amide. Diabetes 1989, 38: 902-5.
19. Tang-Christensen M, Larsen PJ, Thulesen J, Romer J, Vrang N. The proglucagon-derived peptide, glucagon-like peptide-2, is a neurotransmitter involved in the regulation of food intake. Nat Med 2000, 6: 802-7.
20. Blandino-Rosano M, Perez-Arana G, Mellado-Gil JM, Segundo C, Aguilar-Diosdado M. Anti-proliferative effect of pro-inflammatory cytokines in cultured beta cells is associated with extracellular signal-regulated kinase 1/2 pathway inhibition: protective role of glucagon-like peptide-1. J Mol Endocrinol 2008, 41: 35-44.
21. Wang Q, Li L, Xu E, Wong V, Rhodes C, Brubaker PL. Glucagon-like peptide-1 regulates proliferation and apoptosis via activation of protein kinase B in pancreatic INS-1 beta cells. Diabetologia 2004, 47: 478-87.
22. Li L, El-Kholy W, Rhodes CJ, Brubaker PL. Glucagon-like peptide-1 protects beta cells from cytokine-induced apoptosis and necrosis: role of protein kinase B. Diabetologia 2005, 48: 1339-49.
23. Hui H, Nourparvar A, Zhao X, Perfetti R. Glucagon-like peptide-1 inhibits apoptosis of insulin-secreting cells via a cyclic 5′-adenosine monophosphate-dependent protein kinase A- and a phosphatidylinositol 3-kinase-dependent pathway. Endocrinology 2003, 144: 1444-55.
24. Kwon G, Pappan KL, Marshall CA, Schaffer JE, McDaniel ML. cAMP dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem 2004, 279: 8938-45.
25. Ferdaoussi M, Abdelli S, Yang JY, et al. Exendin-4 protects beta-cells from interleukin-1 beta-induced apoptosis by interfering with the c-Jun NH2-terminal kinase pathway. Diabetes 2008, 57: 1205-15.
26. Tourrel C, Bailbe D, Meile MJ, Kergoat M, Portha B. Glucagon-like peptide-1 and exendin-4 stimulate beta-cell neogenesis in streptozotocin-treated newborn rats resulting in persistently improved glucose homeostasis at adult age. Diabetes 2001, 50: 1562-70.
27. Watts VL, Motley ED. Role of protease-activated receptor-1 in endothelial nitric oxide synthase-Thr495 phosphorylation. Exp Biol Med (Maywood) 2009, 234: 132-9.
28. Pan XD, Zhu YG, Lin N, et al. Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer's disease. Mol Neurodegener 2011, 6: 45.
29. Bredt DS, Snyder SH. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 1994, 63: 175-95.
30. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med 1996, 20: 463-6.
31. Tiedge M, Lortz S, Drinkgern J, Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997, 46: 1733-42.
32. Corbett JA, McDaniel ML. Does nitric oxide mediate autoimmune destruction of beta-cells? Possible therapeutic interventions in IDDM. Diabetes 1992, 41: 897-903.
33. Wadt KA, Larsen CM, Andersen HU, Nielsen K, Karlsen AE, Mandrup-Poulsen T. Ciliary neurotrophic factor potentiates the beta-cell inhibitory effect of IL-1beta in rat pancreatic islets associated with increased nitric oxide synthesis and increased expression of inducible nitric oxide synthase. Diabetes 1998, 47: 1602-8.
34. Dunger A, Schroder D, Augstein P, et al. Impact of metabolic activity of beta cells on cytokine-induced damage and recovery of rat pancreatic islets. Acta Diabetol 1995, 32: 217-24.
35. Sarkar SA, Kutlu B, Velmurugan K, et al. Cytokine-mediated induction of anti-apoptotic genes that are linked to nuclear factor kappa-B (NF-kappaB) signalling in human islets and in a mouse beta cell line. Diabetologia 2009, 52: 1092-101.
36. Eizirik DL, Flodstrom M, Karlsen AE, Welsh N. The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic beta cells. Diabetologia 1996, 39: 875-90.
37. Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005; 54 (Suppl 2): S97-107.
38. Hoeldtke RD, Bryner KD, McNeill DR, Warehime SS, Van Dyke K, Hobbs G. Oxidative stress and insulin requirements in patients with recent-onset type 1 diabetes. J Clin Endocrinol Metab 2003, 88: 1624-8.
39. Stassi G, De Maria R, Trucco G, et al. Nitric oxide primes pancreatic beta cells for Fas-mediated destruction in insulin-dependent diabetes mellitus. J Exp Med 1997, 186: 1193-200.
40. Xie Q, Nathan C. The high-output nitric oxide pathway: role and regulation. J Leukoc Biol 1994, 56: 576-82.
41. Xia Y, Roman LJ, Masters BS, Zweier JL. Inducible nitric-oxide synthase generates superoxide from the reductase domain. J Biol Chem 1998, 273: 22635-9.
42. Eberhardt W, Pluss C, Hummel R, Pfeilschifter J. Molecular mechanisms of inducible nitric oxide synthase gene expression by IL-1beta and cAMP in rat mesangial cells. J Immunol 1998, 160: 4961-9.
43. Baeuerle PA, Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 1988, 242: 540-6.
44. Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, Baeuerle PA. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. Embo J 1995, 14: 2876-83.
45. Salehi A, Meidute Abaraviciene S, Jimenez-Feltstrom J, Ostenson CG, Efendic S, Lundquist I. Excessive islet NO generation in type 2 diabetic GK rats coincides with abnormal hormone secretion and is counteracted by GLP-1. PLOS One 2008, 3: e2165.
46. Kim EK, Kwon KB, Lee JH, et al. Inhibition of cytokine-mediated nitric oxide synthase expression in rat insulinoma cells by scoparone. Biol Pharm Bull 2007, 30: 242-6.
47. Cunha DA, Ladrière L, Ortis F, et al. Glucagon-like peptide-1 agonists protect pancreatic beta-cells from lipotoxic endoplasmic reticulum stress through upregulation of Bip and JunB. Diabetes 2009, 58: 2851-62.
48. Chen J, Couto FM, Minn AH, Shalev A. Exenatide inhibits beta-cell apoptosis by decreasing thioredoxin-interacting protein. Biochem Biophys Res Commun 2006, 346: 1067-74.
49. Fan R, Li X, Gu X, Chan JC, Xu G. Exendin-4 protects pancreatic beta cells from human islet amyloid polypeptide-induced cell damage: potential involvement of AKT and mitochondria biogenesis. Diabetes Obes Metab 2010, 12: 815-24.
50. Natalicchio A, De Stefano F, Orlando MR, et al. Exendin-4 prevents c-Jun N-terminal protein kinase activation by tumor necrosis factor-alpha (TNF alpha) and inhibits INF alpha-induced apoptosis in insulin-secreting cells. Endocrinology 2010, 151: 2019-29.
51. Ehses JA, Casilla VR, 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 2003, 144: 4433-45.