Antagonism between Saturated and Unsaturated Fatty Acids in ROS Mediated Lipotoxicity in Rat Insulin-Producing Cells

Cellular Physiology and Biochemistry

Volumn 36, Issue 3, 2015, Pages 852-865

  Gehrmann, Wiebke ^a   Würdemann, Wiebke ^a   Plötz, Thomas ^a   Jörns, Anne ^a   Lenzen, Sigurd ^a   Elsner, Matthias ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Hydrogen peroxide; Lipotoxicity; Oleic acid; Oxidative stress; Palmitic acid; Peroxisome; Type 2 diabetes mellitus

Indexed keywords

CARBON; FAT DROPLET; HYDROGEN PEROXIDE; HYPER PROTEIN; OLEIC ACID; PALMITIC ACID; PROTEIN; REACTIVE OXYGEN METABOLITE; SATURATED FATTY ACID; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CASPASE ASSAY; CELL ORGANELLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG ANTAGONISM; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; FLUORESCENCE; LIPOTOXICITY; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RINM5F CELL LINE; SENSOR; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOASSAY; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; LEWIS RAT; MALE; METABOLISM; PRIMARY CELL CULTURE;

ANIMALS; BIOLOGICAL ASSAY; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; HYDROGEN PEROXIDE; INSULIN-SECRETING CELLS; LIPID DROPLETS; MALE; OLEIC ACID; PALMITIC ACID; PEROXISOMES; PRIMARY CELL CULTURE; RATS; RATS, INBRED LEW;

EID: 84930515860     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000430261     Document Type: Article

References (55)

1. Roche HM, Phillips C, Gibney MJ: The metabolic syndrome: The crossroads of diet and genetics. Proc Nutr Soc 2005;64:371-377.
2. Sabin MA, De Hora M, Holly JM, Hunt LP, Ford AL, Williams SR, Baker JS, Retallick CJ, Crowne EC, Shield JP: Fasting nonesterified fatty acid profiles in childhood and their relationship with adiposity, insulin sensitivity, and lipid levels. Pediatrics 2007;120:1426-1433.
3. Unger RH: Lipotoxicity in the pathogenesis of obesity-dependent niddm. Genetic and clinical implications. Diabetes 1995;44:863-870.
4. Puzziferri N, Roshek TB, 3rd, Mayo HG, Gallagher R, Belle SH, Livingston EH: Long-term follow-up after bariatric surgery: A systematic review. Jama 2014;312:934-942.
5. Bergman RN, Ader M: Free fatty acids and pathogenesis of type 2 diabetes mellitus. Trends Endocrinol Metab 2000;11:351-356.
6. Boden G, Shulman GI: Free fatty acids in obesity and type 2 diabetes: Defining their role in the development of insulin resistance and beta-cell dysfunction. Eur J Clin Invest 2002;32 Suppl 3:14-23.
7. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC: Pancreatic beta-cell mass in european subjects with type 2 diabetes. Diabetes Obes Metab 2008;10 Suppl 4:32-42.
8. Dhayal S, Welters HJ, Morgan NG: Structural requirements for the cytoprotective actions of mono-unsaturated fatty acids in the pancreatic beta-cell line, brin-bd11. Br J Pharmacol 2008;153:1718-1727.
9. Elsner M, Gehrmann W, Lenzen S: Peroxisome-generated hydrogen peroxide as important mediator of lipotoxicity in insulin-producing cells. Diabetes 2011;60:200-208.
10. Yan W, Wang Y, Xiao Y, Wen J, Wu J, Du L, Cai W: Palmitate induces trb3 expression and promotes apoptosis in human liver cells. Cellular Physiology and Biochemistry 2014;33:823-834.
11. Nemcova-Furstova V, Balusikova K, Sramek J, James RF, Kovaf J: Caspase-2 and jnk activated by saturated fatty acids are not involved in apoptosis induction but modulate er stress in human pancreatic fj-cells. Cellular Physiology and Biochemistry 2013;31:277-289.
12. Kharroubi I, Ladriere L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL: Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: Role of nuclear factor-kappab and endoplasmic reticulum stress. Endocrinology 2004;145:5087-5096.
13. 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 beta-cells. Am J Physiol Endocrinol Metab 2008;294:E540-550.
14. Murphy MP: How mitochondria produce reactive oxygen species. Biochem J 2009;417:1-13.
15. Newsholme P, Haber EP, Hirabara SM, Rebelato EL, Procopio J, Morgan D, Oliveira-Emilio HC, Carpinelli AR, Curi R: Diabetes associated cell stress and dysfunction: Role of mitochondrial and non-mitochondrial ROS production and activity. J Physiol 2007;583:9-24.
16. Schonfeld P, Wojtczak L: Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic Biol Med 2008;45:231-241.
17. Lambertucci RH, Leandro CG, Vinolo MA, Nachbar RT, dos Reis Silveira L, Hirabara SM, Curi R, Pithon-Curi TC: The effects of palmitic acid on nitric oxide production by rat skeletal muscle: Mechanism via superoxide and inos activation. Cellular Physiology and Biochemistry 2012;30:1169-1180.
18. Newsholme P, Keane D, Welters HJ, Morgan NG: Life and death decisions of the pancreatic beta-cell: The role of fatty acids. Clin Sci (Lond) 2007;112:27-42.
19. Moffitt JH, Fielding BA, Evershed R, Berstan R, Currie JM, Clark A: Adverse physicochemical properties of tripalmitin in beta cells lead to morphological changes and lipotoxicity in vitro. Diabetologia 2005;48:1819-1829.
20. Eitel K, Staiger H, Brendel MD, Brandhorst D, Bretzel RG, Haring HU, Kellerer M: Different role of saturated and unsaturated fatty acids in beta-cell apoptosis. Biochem Biophys Res Commun 2002;299:853-856.
21. Welters HJ, Tadayyon M, Scarpello JH, Smith SA, Morgan NG: Mono-unsaturated fatty acids protect against beta-cell apoptosis induced by saturated fatty acids, serum withdrawal or cytokine exposure. FEBS Lett 2004;560:103-108.
22. Borg J, Klint C, Wierup N, Strom K, Larsson S, Sundler F, Lupi R, Marchetti P, Xu G, Kimmel A, Londos C, Holm C: Perilipin is present in islets of langerhans and protects against lipotoxicity when overexpressed in the beta-cell line ins-1. Endocrinology 2009;150:3049-3057.
23. Tiedge M, Lortz S, Drinkgern J, Lenzen S: Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997;46:1733-1742.
24. 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.
25. 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.
26. 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.
27. Mosmann T: Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
28. Naujok O, Francini F, Picton S, Bailey CJ, Lenzen S, Jorns A: Changes in gene expression and morphology of mouse embryonic stem cells on differentiation into insulin-producing cells in vitro and in vivo. Diabetes Metab Res Rev 2009;25:464-476.
29. 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.
30. de Hoop MJ, Ab G: Import of proteins into peroxisomes and other microbodies. Biochem J 1992;286:657-669.
31. Subramani S: Protein import into peroxisomes and biogenesis of the organelle. Annu Rev Cell Biol 1993;9:445-478.
32. Gehrmann W, Elsner M: A specific fluorescence probe for hydrogen peroxide detection in peroxisomes. Free Radic Res 2011;45:501-506.
33. 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.
34. 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.
35. Burke JP, Williams K, Gaskill SP, Hazuda HP, Haffner SM, Stern MP: Rapid rise in the incidence of type 2 diabetes from 1987 to 1996: Results from the san antonio heart study. Arch Intern Med 1999;159:1450-1456.
36. Hull RL, Kodama K, Utzschneider KM, Carr DB, Prigeon RL, Kahn SE: Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: Evidence for specificity of impaired beta cell adaptation. Diabetologia 2005;48:1350-1358.
37. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC: Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110.
38. 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.
39. Laaksonen DE, Lakka TA, Lakka HM, Nyyssonen K, Rissanen T, Niskanen LK, Salonen JT: Serum fatty acid composition predicts development of impaired fasting glycaemia and diabetes in middle-aged men. Diabet Med 2002;19:456-464.
40. Carlsson C, Borg LA, Welsh N: Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 1999;140:3422-3428.
41. Fransen M, Nordgren M, Wang B, Apanasets O: Role of peroxisomes in ROS/RNS-metabolism: Implications for human disease. Biochim Biophys Acta 2012;1822:1363-1373.
42. Dansen TB, Wirtz KW: The peroxisome in oxidative stress. IUBMB Life 2001;51:223-230.
43. Nordgren M, Fransen M: Peroxisomal metabolism and oxidative stress. Biochimie 2014;98:56-62.
44. 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.
45. Kunau WH, Dommes V, Schulz H: Beta-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: A century of continued progress. Prog Lipid Res 1995;34:267-342.
46. Wanders RJ, Waterham HR: Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 2006;75:295-332.
47. Van Veldhoven PP: Biochemistry and genetics of inherited disorders of peroxisomal fatty acid metabolism. J Lipid Res 2010;51:2863-2895.
48. Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK: Peroxisomal beta-oxidation-a metabolic pathway with multiple functions. Biochim Biophys Acta 2006;1763:1413-1426.
49. Halliwell B, Gutteridge JMC: Free radicals in biology and medicine, ed Fourth Edition. Oxford University Press, 2007.
50. Lenzen S: Oxidative stress: The vulnerable beta-cell. Biochem Soc Trans 2008;36:343-347.
51. Diakogiannaki E, Welters HJ, Morgan NG: Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J Endocrinol 2008;197:553-563.
52. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV Jr, Ory DS, Schaffer JE: Triglyceride accumulation protects against fatty acid-induced lipotoxicity. PNAS 2003;100:3077-3082.
53. Garbarino J, Padamsee M, Wilcox L, Oelkers PM, D'Ambrosio D, Ruggles KV, Ramsey N, Jabado O, Turkish A, Sturley SL: Sterol and diacylglycerol acyltransferase deficiency triggers fatty acid-mediated cell death. J Biol Chem 2009;284:30994-31005.
54. Parekh S, Anania FA: Abnormal lipid and glucose metabolism in obesity: Implications for nonalcoholic fatty liver disease. Gastroenterology 2007;132:2191-2207.
55. Kienesberger PC, Pulinilkunnil T, Nagendran J, Dyck JR: Myocardial triacylglycerol metabolism. J Mol Cell Cardiol 2013;55:101-110.