Reactive oxygen species stimulate insulin secretion in rat pancreatic islets: Studies using mono-oleoyl-glycerol

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Saadeh, Marylana ^a   Ferrante, Thomas C ^a   Kane, Ada ^a   Shirihai, Orian ^a   Corkey, Barbara E ^a   Deeney, Jude T ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM); COENZYME A; DIACYLGLYCEROL KINASE; DIAZOXIDE; GLYCEROL; GLYCEROL OLEATE; INSULIN; LONG CHAIN COENZYME A; LONG CHAIN FATTY ACID COENZYME A LIGASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OLEIC ACID; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RESVERATROL; UNCLASSIFIED DRUG; 3 [2 [4 (4,4' DIFLUOROBENZHYDRYLIDENE)PIPERIDINO]ETHYL] 2,3 DIHYDRO 2 THIOXO 4(1H) QUINAZOLINONE; ACYL COENZYME A; ACYLGLYCEROL; CALCIUM; FATTY ACID; GLUCOSE; PIPERIDINE DERIVATIVE; QUINAZOLINONE DERIVATIVE; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOTRANSFORMATION; CALCIUM CELL LEVEL; CELL CLONE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF HORMONE METABOLISM; DRUG MECHANISM; DRUG TARGETING; ENZYME INHIBITION; GLUCOSE STIMULATED INSULIN SECRETION; INSULIN HYPERSECRETION; INSULIN RELEASE; LIPID METABOLISM; MALE; NONHUMAN; OXIDATION REDUCTION STATE; OXYGEN CONSUMPTION; PANCREAS ISLET BETA CELL; RAT; SIGNAL TRANSDUCTION; ANIMAL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; OXIDATION REDUCTION REACTION; PANCREAS ISLET; SECRETION; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

RATTUS;

3-HYDROXYBUTYRIC ACID; ACYL COENZYME A; ANIMALS; CALCIUM; CELL LINE, TUMOR; DIACYLGLYCEROL KINASE; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS; GLUCOSE; GLYCERIDES; GLYCEROL; INSULIN; ISLETS OF LANGERHANS; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PIPERIDINES; QUINAZOLINONES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; STILBENES;

EID: 84855827249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030200     Document Type: Article

References (56)

1. Marban SL, DeLoia JA, Gearhart JD, (1989) Hyperinsulinemia in transgenic mice carrying multiple copies of the human insulin gene. Dev Genet 10: 356-364.
2. Cusin I, Terrettaz J, Rohner-Jeanrenaud F, Jeanrenaud B, (1990) Metabolic consequences of hyperinsulinaemia imposed on normal rats on glucose handling by white adipose tissue, muscles and liver. Biochem J 267: 99-103.
3. Rizza RA, Mandarino LJ, Genest J, Baker BA, Gerich JE, (1985) Production of insulin resistance by hyperinsulinaemia in man. Diabetologia 28: 70-75.
4. Segall L, Lameloise N, Assimacopoulos-Jeannet F, Roche E, Corkey P, et al. (1999) Lipid rather than glucose metabolism is implicated in altered insulin secretion caused by oleate in INS-1 cells. Am J Physiol 277: E521-528.
5. Yaney GC, Corkey BE, (2003) Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 46: 1297-1312.
6. Stein DT, Esser V, Stevenson BE, Lane KE, Whiteside JH, et al. (1996) Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J Clin Invest 97: 2728-2735.
7. Poitout V, Robertson RP, (2008) Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 29: 351-366.
8. El-Assaad W, Buteau J, Peyot ML, Nolan C, Roduit R, et al. (2003) Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 144: 4154-4163.
9. McGarry JD, Dobbins RL, (1999) Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42: 128-138.
10. Warnotte C, Nenquin M, Henquin JC, (1999) Unbound rather than total concentration and saturation rather than unsaturation determine the potency of fatty acids on insulin secretion. Mol Cell Endocrinol 153: 147-153.
11. Gravena C, Mathias PC, Ashcroft SJ, (2002) Acute effects of fatty acids on insulin secretion from rat and human islets of Langerhans. J Endocrinol 173: 73-80.
12. Las G, Mayorek N, Dickstein K, Bar-Tana J, (2006) Modulation of insulin secretion by fatty acyl analogs. Diabetes 55: 3478-3485.
13. Zhou YP, Grill VE, (1994) 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 93: 870-876.
14. Prentki M, Corkey BE, (1996) Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45: 273-283.
15. Di Marzo V, (2008) The endocannabinoid system in obesity and type 2 diabetes. Diabetologia 51: 1356-1367.
16. Hayes KC, (2001) Synthetic and modified glycerides: effects on plasma lipids. Curr Opin Lipidol 12: 55-60.
17. Zawalich WS, Zawalich KC, (1990) Influence of monooleoylglycerol on islet cell phosphoinositide hydrolysis and insulin secretion. Mol Cell Endocrinol 68: 129-136.
18. Zawalich WS, Zawalich KC, Rasmussen H, (1989) The effect of monooleoylglycerol on insulin secretion from isolated perifused rat islets. Diabetologia 32: 360-364.
19. Dobbins RL, Chester MW, Daniels MB, McGarry JD, Stein DT, (1998) Circulating fatty acids are essential for efficient glucose-stimulated insulin secretion after prolonged fasting in humans. Diabetes 47: 1613-1618.
20. Dobbins RL, Chester MW, Stevenson BE, Daniels MB, Stein DT, et al. (1998) A fatty acid-dependent step is critically important for both glucose- and non-glucose-stimulated insulin secretion. J Clin Invest 101: 2370-2376.
21. Heart E, Corkey RF, Wikstrom JD, Shirihai OS, Corkey BE, (2006) Glucose-dependent increase in mitochondrial membrane potential, but not cytoplasmic calcium, correlates with insulin secretion in single islet cells. Am J Physiol Endocrinol Metab 290: E143-148.
22. + channel-dependent and-independent glucose-stimulated insulin secretion. Diabetes 49: 424-430.
23. Cunningham BA, Deeney JT, Bliss CR, Corkey BE, Tornheim K, (1996) Glucose-induced oscillatory insulin secretion in perifused rat pancreatic islets and clonal beta-cells (HIT). Am J Physiol 271: E702-710.
24. 2+-dependent translocation of protein kinase C and glucose-induced insulin release. J Biol Chem 271: 18154-18160.
25. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, et al. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3: 281-286.
26. Rasband WS, Image J. U. S. National Institutes of Health, Bethesda, Maryland, USA,http://imagej.nih.gov/ij/index.html.
27. 2+, NAD(P)H and membrane potential changes in pancreatic beta-cells by methyl succinate: comparison with glucose. Biochem J 403: 197-205.
28. Corkey BE, (1988) Analysis of acyl-coenzyme A esters in biological samples. Methods Enzymol 166: 55-70.
29. Peyot ML, Nolan CJ, Soni K, Joly E, Lussier R, et al. (2004) Hormone-sensitive lipase has a role in lipid signaling for insulin secretion but is nonessential for the incretin action of glucagon-like peptide 1. Diabetes 53: 1733-1742.
30. Prentki M, Segall L, Roche E, Thumelin S, Brun T, et al. (1998) [Gluco-lipotoxicity and gene expression in the pancreatic beta cell]. Journ Annu Diabetol Hotel Dieu pp. 17-27.
31. Bollheimer LC, Skelly RH, Chester MW, McGarry JD, Rhodes CJ, (1998) Chronic exposure to free fatty acids reduces pancreatic ß-cell insulin content by increasing basal insulin secretion that is not compensated for by a corresponding increase in proinsulin biosynthetic translation. J Clin Invest 101: 1094-1101.
32. McGarry JD, (2002) Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51: 7-18.
33. + channel by long chain acyl-CoA. A role in modulation of pancreatic beta-cell glucose sensitivity. J Biol Chem 271: 10623-10626.
34. Civelek VN, Deeney JT, Kubik K, Schultz V, Tornheim K, et al. (1996) Temporal sequence of metabolic and ionic events in glucose-stimulated clonal pancreatic beta-cells (HIT). Biochem J 315 (Pt 3): 1015-1019.
35. Kim JH, Lewin TM, Coleman RA, (2001) Expression and characterization of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J Biol Chem 276: 24667-24673.
36. Deeney JT, Gromada J, Hoy M, Olsen HL, Rhodes CJ, et al. (2000) Acute stimulation with long chain acyl-CoA enhances exocytosis in insulin-secreting cells (HIT T-15 and NMRI beta-cells). J Biol Chem 275: 9363-9368.
37. 2+, substrate and ADP. Biochem J 318 (Pt 2): 615-621.
38. Hoffman DL, Brookes PS, (2009) Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions. J Biol Chem 284: 16236-16245.
39. Pi J, Bai Y, Zhang Q, Wong V, Floering LM, et al. (2007) Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 56: 1783-1791.
40. Jayaram B, Syed I, Singh A, Subasinghe W, Kyathanahalli CN, et al. (2011) Isoprenylcysteine carboxyl methyltransferase facilitates glucose-induced Rac1 activation, ROS generation and insulin secretion in INS 832/13 beta-cells. Islets 3: 48-57.
41. Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M, (2006) Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 55 (Suppl 2): S16-23.
42. Noel RJ, Antinozzi PA, McGarry JD, Newgard CB, (1997) Engineering of glycerol-stimulated insulin secretion in islet beta cells. Differential metabolic fates of glucose and glycerol provide insight into mechanisms of stimulus-secretion coupling. J Biol Chem 272: 18621-18627.
43. Deeney JT, Prentki M, Corkey BE, (2000) Metabolic control of beta-cell function. Semin Cell Dev Biol 11: 267-275.
44. Branstrom R, Aspinwall CA, Valimaki S, Ostensson CG, Tibell A, et al. (2004) Long-chain CoA esters activate human pancreatic beta-cell KATP channels: potential role in Type 2 diabetes. Diabetologia 47: 277-283.
45. Branstrom R, Corkey BE, Berggren PO, Larsson O, (1997) Evidence for a unique long chain acyl-CoA ester binding site on the ATP-regulated potassium channel in mouse pancreatic beta cells. J Biol Chem 272: 17390-17394.
46. Branstrom R, Leibiger IB, Leibiger B, Corkey BE, Berggren PO, et al. (1998) Long chain coenzyme A esters activate the pore-forming subunit (Kir6. 2) of the ATP-regulated potassium channel. J Biol Chem 273: 31395-31400.
47. Gribble FM, Proks P, Corkey BE, Ashcroft FM, (1998) Mechanism of cloned ATP-sensitive potassium channel activation by oleoyl-CoA. J Biol Chem 273: 26383-26387.
48. 2+ handling by permeabilized clonal pancreatic beta-cells. J Biol Chem 267: 19840-19845.
49. Webster NJ, Searle GJ, Lam PP, Huang YC, Riedel MJ, et al. (2008) Elevation in intracellular long-chain acyl-coenzyme A esters lead to reduced beta-cell excitability via activation of adenosine 5′-triphosphate-sensitive potassium channels. Endocrinology 149: 3679-3687.
50. Hamming KS, Riedel MJ, Soliman D, Matemisz LC, Webster NJ, et al. (2008) Splice variant-dependent regulation of beta-cell sodium-calcium exchange by acyl-coenzyme As. Mol Endocrinol 22: 2293-2306.
51. McGarry JD, Foster DW, (1981) Importance of experimental conditions in evaluating the malonyl-CoA sensitivity of liver carnitine acyltransferase. Studies with fed and starved rats. Biochem J 200: 217-223.
52. Schonfeld P, Bohnensack R, (1991) Intramitochondrial fatty acid activation enhances control strength of adenine nucleotide translocase. Biomed Biochim Acta 50: 841-849.
53. Shrago E, (1978) The effect of long chain fatty acyl CoA esters on the adenine nucleotide translocase and myocardial metabolism. Life Sci 22: 1-5.
54. Kuwajima M, Foster DW, McGarry JD, (1988) Regulation of lipoprotein lipase in different rat tissues. Metabolism 37: 597-601.
55. Wang X, Li H, De Leo D, Guo W, Koshkin V, et al. (2004) Gene and protein kinase expression profiling of reactive oxygen species-associated lipotoxicity in the pancreatic beta-cell line MIN6. Diabetes 53: 129-140.
56. El-Assaad W, Joly E, Barbeau A, Sladek R, Buteau J, et al. (2010) Glucolipotoxicity alters lipid partitioning and causes mitochondrial dysfunction, cholesterol, and ceramide deposition and reactive oxygen species production in INS832/13 ß-cells. Endocrinology 151: 3061-3073.