Reactive oxygen species-mediated pancreatic β-cell death is regulated by interactions between stress-activated protein kinases, p38 and c-jun N-terminal kinase, and mitogen-activated protein kinase phosphatases

Endocrinology

Volumn 149, Issue 4, 2008, Pages 1654-1665

  Hou, Ni ^a   Torii, Seiji ^a   Saito, Naoya ^a   Hosaka, Masahiro ^a   Takeuchi, Toshiyuki ^a  

^a GUNMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; BENZOIC ACID DERIVATIVE; CYTOKINE; GLUCOSE; MANGANESE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; REACTIVE OXYGEN METABOLITE; SCAVENGER; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TETRAKIS(4 BENZOIC ACID)PORPHYRIN MANGANESE; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OXIDATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; APOPTOSIS; CELLS, CULTURED; DUAL SPECIFICITY PHOSPHATASE 1; INSULIN-SECRETING CELLS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES;

EID: 41549115946     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-0988     Document Type: Article

References (49)

1. Robertson RP, Harmon J, Tran PO, Poitout V 2004 β-Cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 53(Suppl 1):S119-S124
2. Evans JL, Goldfine ID, Maddux BA, Grodsky GM 2003 Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes 52:1-8
3. Tabatabaie T, Vasquez-Weldon A, Moore DR, Kotake Y 2003 Free radicals and the pathogenesis of type 1 diabetes: β-cell cytokine-mediated free radical generation via cyclooxygenase-2. Diabetes 52:1994-1999
4. Robertson RP 2004 Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 279:42351-42354
5. Wang J, Cao Y, Chen Y, Chen Y, Gardner P, Steiner DF 2006 Pancreatic β cells lack a low glucose and O2-inducible mitochondrial protein that augments cell survival. Proc Natl Acad Sci USA 103:10636-10641
6. Li X, Chen H, Epstein PN 2006 Metallothionein and catalase sensitize to diabetes in nonobese diabetic mice: reactive oxygen species may have a protective role in pancreatic β-cells. Diabetes 55:1592-1604
7. Rösen P, Nawroth PP, King G, Möller W, Tritschler HJ, Packer L 2001 The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 17:189-212
8. Martens GA, Cai Y, Hinke S, Stangé G, Van de Casteele M, Pipeleers D 2005 Glucose suppresses superoxide generation in metabolically responsive pancreatic β cells. J Biol Chem 280:20389-20396
9. Robertson RP, Harmon JS 2006 Diabetes, glucose toxicity, and oxidative stress: a case of double jeopardy for the pancreatic islet β cell. Free Radic Biol Med 41:177-184
10. Morgan D, Oliveira-Emilio HR, Keane D, Hirata AE, Santos da Rocha M, Bordin S, Curi R, Newsholme P, Carpinelli AR 2007 Glucose, palmitate and pro-inflammatory cytokines modulate production and activity of a phagocyte-like NADPH oxidase in rat pancreatic islets and a clonal β cell line. Diabetologia 50:359-369
11. Kaelin Jr WG 2005 ROS: really involved in oxygen sensing. Cell Metab 1:357-358
12. Guzy RD, Schumacker PT 2006 Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91:807-819
13. Mandrup-Poulsen T 2001 β-Cell apoptosis: stimuli and signaling. Diabetes 50(Suppl 1):S58-S63
14. Harper SJ, LoGrasso P 2001 Signalling for survival and death in neurones: the role of stress-activated kinases, JNK and p38. Cell Signal 13:299-310
15. McCubrey JA, Lahair MM, Franklin RA 2006 Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8:1775-1789
16. Kaneto H, Matsuoka TA, Nakatani Y, Kawamori D, Miyatsuka T, Matsuhisa M, Yamasaki Y 2005 Oxidative stress, ER stress, and the JNK pathway in type 2 diabetes. J Mol Med 83:429-439
17. Shen HM, Liu ZG 2006 JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic Biol Med 40: 928-939
18. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H 1998 Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17:2596-2606
19. Liu Y, Min W 2002 Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ Res 90:1259-1266
20. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M 2005 Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120:649-661
21. Ehses JA, Casilla VR, Doty T, Pospisilik JA, Winter KD, Demuth HU, Pederson RA, McIntosh CH 2003 Glucose-dependent insulinotropic polypeptide promotes β-(INS-1) cell survival via cyclic adenosine monophosphate- mediated caspase-3 inhibition and regulation of p38 mitogen-activated protein kinase. Endocrinology 144:4433-4445
22. Dickinson RJ, Keyse SM 2006 Diverse physiological functions for dual-specificity MAP kinase phosphatases. J Cell Sci 119:4607-4615
23. Fiscella M, Zhang H, Fan S, Sakaguchi K, Shen S, Mercer WE, Vande Woude GF, O'Connor PM, Appella E 1997 Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci USA 94:6048-6053
24. Keyse SM, Emslie EA 1992 Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase. Nature 359:644-647
25. Franklin CC, Kraft AS 1997 Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells. J Biol Chem 272:16917-16923
26. Wu JJ, Bennett AM 2005 Essential role for mitogen-activated protein (MAP) kinase phosphatase-1 in stress-responsive MAP kinase and cell survival signaling. J Biol Chem 280:16461-16466
27. Wu JJ, Roth RJ, Anderson EJ, Hong EG, Lee MK, Choi CS, Neufer PD, Shulman GI, Kim JK, Bennett AM 2006 Mice lacking MAP kinase phosphatase-1 have enhanced MAP kinase activity and resistance to diet-induced obesity. Cell Metab 4:61-73
28. Tonks NK 2006 Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7:833-846
29. Zhang B, Hosaka M, Sawada Y, Torii S, Mizutani S, Ogata M, Izumi T, Takeuchi T 2003 Parathyroid hormone-related protein induces insulin expression through activation of MAP kinase-specific phosphatase-1 that dephosphorylates c-Jun NH2-terminal kinase in pancreatic β-cells. Diabetes 52: 2720-2730
30. Mendelson KG, Contois LR, Tevosian SG, Davis RJ, Paulson KE 1996 Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc Natl Acad Sci USA 93:12908-12913
31. Zhou JY, Liu Y, Wu GS 2006 The role of mitogen-activated protein kinase phosphatase-1 in oxidative damage-induced cell death. Cancer Res 66:4888-4894
32. Maechler P, Jornot L, Wollheim CB 1999 Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic β cells. J Biol Chem 274:27905-27913
33. Kaneto H, Xu G, Fujii N, Kim S, Bonner-Weir S, Weir GC 2002 Involvement of c-Jun N-terminal kinase in oxidative stress-mediated suppression of insulin gene expression. J Biol Chem 277:30010-30018
34. Elouil H, Cardozo AK, Eizirik DL, Henquin JC, Jonas JC 2005 High glucose and hydrogen peroxide increase c-Myc and haeme-oxygenase 1 mRNA levels in rat pancreatic islets without activating NFκB. Diabetologia 48:496-505
35. 2-induced MIN6N8a cell death. Eur J Pharmacol 547:1-9
36. Clark SA, Chick WL 1990 Islet cell culture in defined serum-free medium. Endocrinology 126:1895-1903
37. Ling Z, Hannaert JC, Pipeleers D 1994 Effect of nutrients, hormones and serum on survival of rat islet β cells in culture. Diabetologia 37:15-21
38. Hoorens A, Van de Casteele M, Kloppel G, Pipeleers D 1996 Glucose promotes survival of rat pancreatic β cells by activating synthesis of proteins which suppress a constitutive apoptotic program. J Clin Invest 98:1568-1574
39. Kayo T, Sawada Y, Suzuki Y, Suda M, Tanaka S, Konda Y, Miyazaki J, Takeuchi T 1996 Proprotein-processing endoprotease furin decreases regulated secretory pathway-specific proteins in the pancreatic β cell line MIN6. J Biol Chem 271:10731-10737
40. Merglen A, Theander S, Rubi B, Chaffard G, Wollheim CB, Maechler P 2004 Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 145:667-678
41. Aihara M, Sugawara K, Torii S, Hosaka M, Kurihara H, Saito N, Takeuchi T 2004 Angiogenic endothelium-specific nestin expression is enhanced by the first intron of the nestin gene. Lab Invest 84:1581-1592
42. Johnson JD, Bernal-Mizrachi E, Alejandro EU, Han Z, Kalynyak TB, Li H, Beith JL, Gross J, Warnock GL, Townsend RR, Permutt MA, Polonsky KS 2006 Insulin protects islets from apoptosis via Pdx1 and specific changes in the human islet proteome. Proc Natl Acad Sci USA 103:19575-19580
43. Robertson RP, Harmon J, Tran PO, Tanaka Y, Takahashi H 2003 Glucose toxicity in β-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 52:581-587
44. Kim WH, Lee JW, Gao B, Jung MH 2005 Synergistic activation of JNK/SAPK induced by TNF-α and IFN-γ-: apoptosis of pancreatic β-cells via the p53 and ROS pathway. Cell Signal 17:1516-1532
45. Matsuda T, Omori K, Vuong T, Pascual M, Valiente L, Ferreri K, Todorov I, Kuroda Y, Smith CV, Kandeel F, Mullen Y 2005 Inhibition of p38 pathway suppresses human islet production of pro-inflammatory cytokines and improves islet graft function. Am J Transplant 5:484-493
46. Van de Casteele M, Kefas BA, Cai Y, Heimberg H, Scott DK, Henquin JC, Pipeleers D, Jonas JC 2003 Prolonged culture in low glucose induces apoptosis of rat pancreatic β-cells through induction of c-myc. Biochem Biophys Res Commun 312:937-944
47. Cai Y, Martens GA, Hinke SA, Heimberg H, Pipeleers D, Van de Casteele M 2007 Increased oxygen radical formation and mitochondrial dysfunction mediate β cell apoptosis under conditions of AMP-activated protein kinase stimulation. Free Radic Biol Med 42:64-78
48. Vandenabeele P, VandenBerghe T, Festjens N 2006 Caspase inhibitors promote alternative cell death pathways. Sci STKE 2006:pe44
49. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G 2007 Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14:1237-1243