Peroxisome-generated hydrogen peroxide as important mediator of lipotoxicity in insulin-producing cells

Diabetes

Volumn 60, Issue 1, 2011, Pages 200-208

  Elsner, Matthias ^a   Gehrmann, Wiebke ^a   Lenzen, Sigurd ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; FATTY ACID; HYDROGEN PEROXIDE; INSULIN; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY ACID OXIDATION; LIPOTOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALS; CELL CULTURE TECHNIQUES; CELL SURVIVAL; DNA PRIMERS; EXTRACELLULAR MATRIX; FLUORESCEINS; HEP G2 CELLS; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; LENTIVIRUS; MALE; OXIDATIVE STRESS; PEROXISOMES; POLYMERASE CHAIN REACTION; RATS; RATS, INBRED LEW; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 78751513443     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1401     Document Type: Article

References (50)

1. Boden G: Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 1997;46:3-10
2. DeFronzo RA: Lilly lecture 1987. The triumvirate: β-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 1988;37:667-687
3. Carpentier A, Mittelman SD, Lamarche B, Bergman RN, Giacca A, Lewis GF. Acute enhancement of insulin secretion by FFA in humans is lost with prolonged FFA elevation. Am J Physiol 1999;276:E1055-E1066
4. Kashyap S, Belfort R, Gastaldelli A, Pratipanawatr T, Berria R, Pratipanawatr W, Bajaj M, Mandarino L, DeFronzo R, Cusi K. A sustained increase in plasma free fatty acids impairs insulin secretion in nondiabetic subjects genetically predisposed to develop type 2 diabetes. Diabetes 2003;52:2461-2474
5. Paolisso G, Gambardella A, Amato L, Tortoriello R, D'Amore A, Varricchio M, D'Onofrio F. Opposite effects of short- and long-term fatty acid infusion on insulin secretion in healthy subjects. Diabetologia 1995;38:1295-1299
6. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
7. Clark A, Wells CA, Buley ID, Cruickshank JK, Vanhegan RI, Matthews DR, Cooper GJ, Holman RR, Turner RC. Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes. Diabetes Res 1988;9:151-159
8. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic β-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008;10(Suppl 4):32-42
9. Gordon ES. Non-esterified fatty acids in the blood of obese and lean subjects. Am J Clin Nutrition 1960;8:740-747
10. Poitout V, Robertson RP. Minireview: Secondary β-cell failure in type 2 diabetes-a convergence of glucotoxicity and lipotoxicity. Endocrinology 2002;143:339-342
11. Zhou YP, Grill VE. Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 1994;93:870-876
12. Azevedo-Martins AK, Monteiro AP, Lima CL, Lenzen S, Curi R. Fatty acid-induced toxicity and neutral lipid accumulation in insulin-producing RINm5F cells. Toxicol In Vitro 2006;20:1106-1113
13. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001;50:1771-1777
14. Cnop M. Fatty acids and glucolipotoxicity in the pathogenesis of type 2 diabetes. Biochem Soc Trans 2008;36:348-352
15. Newsholme P, Keane D, Welters HJ, Morgan NG. Life and death decisions of the pancreatic β-cell: the role of fatty acids. Clin Sci (Lond) 2007;112: 27-42
16. Cnop M, Igoillo-Esteve M, Cunha DA, Ladriere L, Eizirik DL. An update on lipotoxic endoplasmic reticulum stress in pancreatic β-cells. Biochem Soc Trans 2008;36:909-915
17. Cunha DA, Hekerman P, Ladriere L, Bazarra-Castro A, Ortis F, Wakeham MC, Moore F, Rasschaert J, Cardozo AK, Bellomo E, Overbergh L, Mathieu C, Lupi R, Hai T, Herchuelz A, Marchetti P, Rutter GA, Eizirik DL, Cnop M. Initiation and execution of lipotoxic ER stress in pancreatic β-cells. J Cell Sci 2008;121:2308-2318
18. Lai E, Bikopoulos G, Wheeler MB, Rozakis-Adcock M, Volchuk A. Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic β-cells. Am J Physiol Endocrinol Metab 2008;294:E540-E550
19. Berne C. The metabolism of lipids in mouse pancreatic islets. The oxidation of fatty acids and ketone bodies. Biochem J 1975;152:661-666
20. Lenzen S, Panten U. 2-oxocarboxylic acids and function of pancreatic islets in obese-hyperglycaemic mice. Insulin secretion in relation to 45Ca uptake and metabolism. Biochem J 1980;186:135-144
21. Panten U, Lenzen S. Alterations in energy metabolism of secretory cells. In The Energetics of Secretion Responses. Boca Raton, FL, CRC Press, 1988
22. Schonfeld P, Wojtczak L. Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic Biol Med 2008;45:231-241
23. Lenzen S. Oxidative stress: the vulnerable β-cell. Biochem Soc Trans 2008;36:343-347
24. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. New York, Oxford University Press, 2007
25. El-Assaad W, Buteau J, Peyot ML, Nolan C, Roduit R, Hardy S, Joly E, Dbaibo G, Rosenberg L, Prentki M. Saturated fatty acids synergize with elevated glucose to cause pancreatic β-cell death. Endocrinology 2003;144: 4154-4163
26. Hellemans K, Kerckhofs K, Hannaert JC, Martens G, Van Veldhoven P, Pipeleers D. Peroxisome proliferator-activated receptor alpha-retinoid X receptor agonists induce β-cell protection against palmitate toxicity. FEBS J 2007;274:6094-6105
27. Kunau WH, Dommes V, Schulz H. β-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog Lipid Res 1995;34:267-342
28. Dansen TB, Wirtz KW. The peroxisome in oxidative stress. IUBMB Life 2001;51:223-230
29. 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;20:463-466
30. Tiedge M, Lortz S, Drinkgern J, Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulinproducing cells. Diabetes 1997;46:1733-1742
31. Asfari M, Janjic D, Meda P, Li G, Halban PA, Wollheim CB. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 1992;130:167-178
32. Lortz S, Gurgul-Convey E, Lenzen S, Tiedge M. Importance of mitochondrial superoxide dismutase expression in insulin-producing cells for the toxicity of reactive oxygen species and proinflammatory cytokines. Diabetologia 2005;48:1541-1548
33. Gurgul E, Lortz S, Tiedge M, Jorns A, Lenzen S. Mitochondrial catalase overexpression protects insulin-producing cells against toxicity of reactive oxygen species and proinflammatory cytokines. Diabetes 2004;53:2271-2280
34. Claiborne A. Catalase activity. In CRC Handbook of Methods for Oxygen Radical Research. Greenwald RA, Ed. Boca Raton, FL, CRC Press, 1985, p. 283-284
35. Cornu M, Modi H, Kawamori D, Kulkarni RN, Joffraud M, Thorens B. Glucagon-like peptide-1 (GLP-1) increases β-cell glucose competence and proliferation by translational induction of insulin-like growth factor-1 receptor (IGF-1R) expression. J Biol Chem 2010;285:10538-10545
36. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63
37. Darzynkiewicz Z, Bruno S, Del Bino G, Gorczyca W, Hotz MA, Lassota P, Traganos F. Features of apoptotic cells measured by flow cytometry. Cytometry 1992;13:795-808
38. Rosenkranz AR, Schmaldienst S, Stuhlmeier KM, Chen W, Knapp W, Zlabinger GJ. A microplate assay for the detection of oxidative products using 2′,7′-dichlorofluorescin-diacetate. J Immunol Methods 1992;156: 39-45
39. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 2006;3:281-286
40. de Hoop MJ, Ab G. Import of proteins into peroxisomes and other microbodies. Biochem J 1992;286(Pt 3):657-669
41. Subramani S. Protein import into peroxisomes and biogenesis of the organelle. Annu Rev Cell Biol 1993;9:445-478
42. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998;72:9873-9880
43. Sastry L, Johnson T, Hobson MJ, Smucker B, Cornetta K. Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods. Gene Ther 2002;9:1155-1162
44. Wanders RJ, Waterham HR. Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 2006;75:295-332
45. Reddy JK, Mannaerts GP. Peroxisomal lipid metabolism. Annu Rev Nutr 1994;14:343-370
46. Akesson B, Lundquist I. Nitric oxide and hydroperoxide affect islet hormone release and Ca(2) efflux. Endocrine 1999;11:99-107
47. Maechler P, Jornot L, Wollheim CB. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic β cells. J Biol Chem 1999;274:27905-27913
48. Morgan D, Oliveira-Emilio HR, Keane D, Hirata AE, Santos da Rocha M, Bordin S, Curi R, Newsholme P, Carpinelli AR. 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 2007;50:359-369
49. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M, Sano H, Utsumi H, Nawata H. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000;49:1939-1945
50. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC. Palmitate increases superoxide production through mitochondrial electron transport chain and NADPH oxidase activity in skeletal muscle cells. J Cell Physiol 2008;216:796-804