Antioxidants N-acetyl-L-cysteine and manganese(III)tetrakis (4-benzoic acid)porphyrin do not prevent β-cell dysfunction in rat islets cultured in high glucose for 1 wk

American Journal of Physiology - Endocrinology and Metabolism

Volumn 291, Issue 1, 2006, Pages

  Khaldi, M Z ^a   Elouil, H ^a   Guiot, Y ^a   Henquin, J C ^a   Jonas, J C ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Cytosolic calcium concentration; Heme oxygenase 1; Insulin secretion; Mitochondrial membrane potential; Oxidative stress; Pancreatic cell; Superoxide dismutase mimetic

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; GLUCOSE; HOMEODOMAIN PROTEIN; HYDROGEN PEROXIDE; INSULIN; MANGANESE SUPEROXIDE DISMUTASE; MANGANESE(III) TETRAKIS(4 BENZOIC ACID)PORPHYRIN; PORPHYRIN DERIVATIVE; SCAVENGER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL PROTECTION; CELL STRUCTURE; CONTROLLED STUDY; DNA CONTENT; DRUG EFFECT; GLUCOSE INTAKE; INSULIN RELEASE; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STIMULUS SECRETION COUPLING;

ACETYLCYSTEINE; ANIMALS; CALCIUM; FREE RADICAL SCAVENGERS; GLUCOSE; HEME OXYGENASE-1; HISTOCYTOCHEMISTRY; HYDROGEN PEROXIDE; INSULIN; INSULIN-SECRETING CELLS; MALE; MEMBRANE POTENTIALS; METALLOPORPHYRINS; MICROSCOPY, PHASE-CONTRAST; PROINSULIN; PROTEIN PRECURSORS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 33745839806     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00145.2005     Document Type: Article

References (64)

1. Baynes JW and Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48: 1-9, 1999.
2. Benhamou PY, Moriscot C, Richard MJ, Beatrix O, Badet L, Pattou F, Kerr-Conte J, Chroboczek J, Lemarchand P, and Halimi S. Adenovirus-mediated catalase gene transfer reduces oxidant stress in human, porcine and rat pancreatic islets. Diabetologia 41: 1093-1100, 1998.
3. Bindokas VP, Kuznetsov A, Sreenan S, Polonsky KS, Roe MW, and Philipson LH. Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 278: 9796-9801, 2003.
4. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
5. Brownlee M. A radical explanation for glucose-induced beta cell dysfunction. J Clin Invest 112: 1788-1790, 2003.
6. Day BJ, Fridovich I, and Crapo JD. Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch Biochem Biophys 347: 256-262, 1997.
7. Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329: 977-986, 1993.
8. Eizirik DL, Welsh N, and Hellerstrom C. Predominance of stimulatory effects of interleukin-1-β on isolated human pancreatic islets. J Clin Endocrinol Metab 76: 399-403, 1993.
9. Elbirt KK and Bonkovsky HL. Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 111: 438-447, 1999.
10. Elouil H, Cardozo AK, Eizirik DL, Henquin JC, and Jonas JC. 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, 2005.
11. Evans JL, Goldfine ID, Maddux BA, and Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes 52: 1-8, 2003.
12. Fridlyand LE and Philipson LH. Does the glucose-dependent insulin secretion mechanism itself cause oxidative stress in pancreatic β-cells? Diabetes 53: 1942-1948, 2004.
13. Gorogawa S, Kajimoto Y, Umayahara Y, Kaneto H, Watada H, Kuroda A, Kawamori D, Yasuda T, Matsuhisa M, Yamasaki Y, and Hori M. Probucol preserves pancreatic β-cell function through reduction of oxidative stress in type 2 diabetes. Diabetes Res Clin Pract 57: 1-10, 2002.
14. Green K, Brand MD, and Murphy MP. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 53, Suppl 1: S110-S118, 2004.
15. Gurgul E, Lortz S, Tiedge M, Jorns A, and Lenzen S. Mitochondrial catalase overexpression protects insulin-producing cells against toxicity of reactive oxygen species and proinflammatory cytokines. Diabetes 53: 2271-2280, 2004.
16. Heding LG. Determination of total serum insulin (IRI) in insulin-treated diabetic patients. Diabetologia 8: 260-266, 1972.
17. Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, Hiai H, Seino Y, and Yamada Y. Hyperglycemia causes oxidative stress in pancreatic β-cells of GK rats, a model of type 2 diabetes. Diabetes 48: 927-932, 1999.
18. Ihara Y, Yamada Y, Toyokuni S, Miyawaki K, Ban N, Adachi T, Kuroe A, Iwakura T, Kubota A, Hiai H, and Seino Y. Antioxidant α-tocopherol ameliorates glycemic control of GK rats, a model of type 2 diabetes. FEBS Lett 473: 24-26, 2000.
19. Jonas JC, Guiot Y, Rahier J, and Henquin JC. Haeme-oxygenase 1 expression in rat pancreatic β-cells is stimulated by supraphysiological glucose concentrations and by cyclic AMP. Diabetologia 46: 1234-1244, 2003.
20. Jonas JC, Sharma A, Hasenkamp W, Ilkova H, Patane G, Laybutt R, Bonner-Weir S, and Weir GC. Chronic hyperglycemia triggers loss of pancreatic β cell differentiation in an animal model of diabetes. J Biol Chem 274: 14112-14121, 1999.
21. Kaiser N, Leibowitz G, and Nesher R. Glucotoxicity and β-cell failure in type 2 diabetes mellitus. J Pediatr Endocrinol Metab 16: 5-22, 2003.
22. Kaneto H, Fujii J, Myint T, Miyazawa N, Islam KN, Kawasaki Y, Suzuki K, Nakamura M, Tatsumi H, Yamasaki Y, and Taniguchi N. Reducing sugars trigger oxidative modification and apoptosis in pancreatic β-cells by provoking oxidative stress through the glycation reaction. Biochem J 320: 855-863, 1996.
23. Kaneto H, Kajimoto Y, Miyagawa J, Matsuoka T, Fujitani Y, Umayahara Y, Hanafusa T, Matsuzawa Y, Yamasaki Y, and Hori M. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic β-cells against glucose toxicity. Diabetes 48: 2398-2406, 1999.
24. Kaneto H, Xu G, Song KH, Suzuma K, Bonner-Weir S, Sharma A, and Weir GC. Activation of the hexosamine pathway leads to deterioration of pancreatic β-cell function through the induction of oxidative stress. J Biol Chem 276: 31099-31104, 2001.
25. Khaldi MZ, Guiot Y, Gilon P, Henquin JC, and Jonas JC. Increased glucose sensitivity of both triggering and amplifying pathways of insulin secretion in rat islets cultured for one week in high glucose. Am J Physiol Endocrinol Metab 287: E207-E217, 2004.
26. Kjorholt C, Akerfeldt MC, Biden TJ, and Laybutt DR. Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of β-cell differentiation and secretory function in the db/db mouse model of diabetes. Diabetes 54: 2755-2763, 2005.
27. Kosaka K, Kuzuya T, Akanuma Y, and Hagura R. Increase in insulin response after treatment of overt maturity-onset diabetes is independent of the mode of treatment. Diabetologia 18: 23-28, 1980.
28. Koya D and King GL. Protein kinase C activation and the development of diabetic complications. Diabetes 47: 859-866, 1998.
29. 2 with stimulus-secretion coupling in mouse pancreatic β-cells. J Physiol 514: 471-481, 1999.
30. Labarca C and Paigen K. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102: 344-352, 1980.
31. Laybutt DR, Kaneto H, Hasenkamp W, Grey S, Jonas JC, Sgroi DC, Groff A, Ferran C, Bonner-Weir S, Sharma A, and Weir GC. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to β-cell survival during chronic hyperglycemia. Diabetes 51: 413-423, 2002.
32. Ling Z, Kiekens R, Mahler T, Schuit FC, Pipeleers-Marichal M, Sener A, Kloppel G, Malaisse WJ, and Pipeleers DG. Effects of chronically elevated glucose levels on the functional properties of rat pancreatic β-cells. Diabetes 45: 1774-1782, 1996.
33. Ling Z and Pipeleers DG. Prolonged exposure of human β cells to elevated glucose levels results in sustained cellular activation leading to a loss of glucose regulation. J Clin Invest 98: 2805-2812, 1996.
34. Maechler P, Jornot L, and Wollheim CB. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic β cells. J Biol Chem 274: 27905-27913, 1999.
35. Martens GA, Cai Y, Hinke S, Stange G, Van de CM, and Pipeleers D. Glucose suppresses superoxide generation in metabolically responsive pancreatic beta cells. J Biol Chem 280: 20389-20396, 2005.
36. Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, Crapo JD, and Wallace DC. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18: 159-163, 1998.
37. Moore PC, Ugas MA, Hagman DK, Parazzoli SD, and Poitout V. Evidence against the involvement of oxidative stress in fatty acid inhibition of insulin secretion. Diabetes 53: 2610-2616, 2004.
38. Nakazaki M, Kakei M, Yaekura K, Koriyama N, Morimitsu S, Ichinari K, Yada T, and Tei C. Diverse effects of hydrogen peroxide on cytosolic Ca2+ homeostasis in rat pancreatic beta-cells. Cell Struct Funct 25: 187-193, 2000.
39. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, and Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000.
40. Otterbein LE and Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 279: L1029-L1037, 2000.
41. Piro S, Anello M, Di Pietro C, Lizzio MN, Patane G, Rabuazzo AM, Vigneri R, Purrello M, and Purrello F. Chronic exposure to free fatty acids or high glucose induces apoptosis in rat pancreatic islets: possible role of oxidative stress. Metabolism 51: 1340-1347, 2002.
42. Poitout V and Robertson RP. Minireview: Secondary β-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 143: 339-342, 2002.
43. Prasad KM, Thimmalapura PR, Woode EA, and Nadler JL. Evidence that increased 12-lipoxygenase expression impairs pancreatic β cell function and viability. Biochem Biophys Res Commun 308: 427-432, 2003.
44. Rasilainen S, Nieminen JM, Levonen AL, Otonkoski T, and Lapatto R. Dose-dependent cysteine-mediated protection of insulin-producing cells from damage by hydrogen peroxide. Biochem Pharmacol 63: 1297-1304, 2002.
45. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet β cells in diabetes. J Biol Chem 279: 42351-42354, 2004.
46. Robertson RP, Harmon J, Tran PO, Tanaka Y, and Takahashi H. Glucose toxicity in β-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 52: 581-587, 2003.
47. Sakai K, Matsumoto K, Nishikawa T, Suefuji M, Nakamaru K, Hirashima Y, Kawashima J, Shirotani T, Ichinose K, Brownlee M, and Araki E. Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic β-cells. Biochem Biophys Res Commun 300: 216-222, 2003.
48. Sakuraba H, Mizukami H, Yagihashi N, Wada R, Hanyu C, and Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 45: 85-96, 2002.
49. Sharma A, Olson LK, Robertson RP, and Stein R. The reduction of insulin gene transcription in HIT-T15 beta cells chronically exposed to high glucose concentration is associated with the loss of RIPE3b1 and STF-1 transcription factor expression. Mol Endocrinol 9: 1127-1134, 1995.
50. Spitaler MM and Graier WF. Vascular targets of redox signalling in diabetes mellitus. Diabetologia 45: 476-494, 2002.
51. Tajiri Y and Grill VE. Interactions between vitamin E and glucose on B-cell functions in the rat: an in vivo and in vitro study. Pancreas 18: 274-281, 1999.
52. Takahashi H, Tran PO, LeRoy E, Harmon JS, Tanaka Y, and Robertson RP. D-Glyceraldehyde causes production of intracellular peroxide in pancreatic islets, oxidative stress, and defective beta cell function via non-mitochondrial pathways. J Biol Chem 279: 37316-37323, 2004.
53. Tanaka Y, Gleason CE, Tran PO, Harmon JS, and Robertson RP. Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci USA 96: 10857-10862, 1999.
54. Tanaka Y, Tran PO, Harmon J, and Robertson RP. A role for glutathione peroxidase in protecting pancreatic β cells against oxidative stress in a model of glucose toxicity. Proc Natl Acad Sci USA 99: 12363-12368, 2002.
55. Tiedge M, Lortz S, Drinkgern J, and Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 46: 1733-1742, 1997.
56. Tokuyama Y, Sturis J, DePaoli AM, Takeda J, Stoffel M, Tang J, Sun X, Polonsky KS, and Bell GI. Evolution of β-cell dysfunction in the male Zucker diabetic fatty rat. Diabetes 44: 1447-1457, 1995.
57. Tomlinson DR. Mitogen-activated protein kinases as glucose transducers for diabetic complications. Diabetologia 42: 1271-1281, 1999.
58. Turner RC. The UK Prospective Diabetes Study. A review. Diabetes Care 21, Suppl 3: C35-C38, 1998.
59. UK Prospective Diabetes Study Group. UK prospective diabetes study 16 Overview of 6 years' therapy of type II diabetes: a progressive disease. Diabetes 44: 1249-1258, 1995.
60. Uchiyama K, Naito Y, Hasegawa G, Nakamura N, Takahashi J, and Yoshikawa T. Astaxanthin protects beta-cells against glucose toxicity in diabetic db/db mice. Redox Rep 7: 290-293, 2002.
61. Vincent AM, Russell JW, Low P, and Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25: 612-628, 2004.
62. Weir GC, Laybutt DR, Kaneto H, Bonner-Weir S, and Sharma A. β-cell adaptation and decompensation during the progression of diabetes. Diabetes 50, Suppl 1: S154-S159, 2001.
63. Wiernsperger NF. Oxidative stress as a therapeutic target in diabetes: revisiting the controversy. Diabetes Metab 29: 579-585, 2003.
64. Zangen DH, Bonner-Weir S, Lee CH, Latimer JB, Miller CP, Habener JF, and Weir GC. Reduced insulin, GLUT2, and IDX-1 in beta-cells after partial pancreatectomy. Diabetes 46: 258-264, 1997.