Control of the intracellular redox state by glucose participates in the insulin secretion mechanism

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Rebelato, Eduardo ^a   Abdulkader, Fernando ^a   Curi, Rui ^a   Carpinelli, Angelo Rafael ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CALCIUM ION; CATALASE; GLUCOSE; HYDROGEN PEROXIDE; INSULIN; PENTOSE PHOSPHATE; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT;

AGED; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FLUORESCENCE; GLUCOSE METABOLISM; INSULIN RELEASE; NONHUMAN; OXIDATION REDUCTION STATE; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PENTOSE PHOSPHATE CYCLE; RAT; ANIMAL; CYTOLOGY; DRUG EFFECT; INTRACELLULAR SPACE; METABOLISM; OXIDATION REDUCTION REACTION; SECRETION;

RATTUS;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; CALCIUM SIGNALING; CATALASE; FEMALE; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; INTRACELLULAR SPACE; OXIDATION-REDUCTION; PENTOSE PHOSPHATE PATHWAY; RATS; REACTIVE OXYGEN SPECIES;

EID: 80052327311     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024507     Document Type: Article

References (41)

1. Ashcroft FM, Harrison DE, Ashcroft SJ, (1984) Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 312: 446-448.
2. Carpinelli AR, Malaisse WJ, (1980) Regulation of 86Rb+ outflow from pancreatic islets III. Possible significance of ATP. J Endocrinol Invest 3: 365-370.
3. Ravier MA, Gilon P, Henquin JC, (1999) Oscillations of insulin secretion can be triggered by imposed oscillations of cytoplasmic Ca2+ or metabolism in normal mouse islets. Diabetes 48: 2374-2382.
4. Zhang Z, Liew CW, Handy DE, Zhang Y, Leopold JA, et al. (2010) High glucose inhibits glucose-6-phosphate dehydrogenase, leading to increased oxidative stress and beta-cell apoptosis. Faseb J 24: 1497-1505.
5. Lacraz G, Figeac F, Movassat J, Kassis N, Coulaud J, et al. (2009) Diabetic beta-cells can achieve self-protection against oxidative stress through an adaptive up-regulation of their antioxidant defenses. PLoS One 4: e6500.
6. Martens GA, Cai Y, Hinke S, Stange G, Van de Casteele M, et al. (2005) Glucose suppresses superoxide generation in metabolically responsive pancreatic beta cells. J Biol Chem 280: 20389-20396.
7. Leloup C, Tourrel-Cuzin C, Magnan C, Karaca M, Castel J, et al. (2009) Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion. Diabetes 58: 673-681.
8. 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.
9. Syed I, Kyathanahalli CN, Kowluru A, (2011) Phagocyte-like NADPH oxidase generates ROS in INS 832/13 cells and rat islets: role of protein prenylation. Am J Physiol Regul Integr Comp Physiol 300: R756-762.
10. Goldstein BJ, Mahadev K, Wu X, (2005) Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 54: 311-321.
11. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T, (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270: 296-299.
12. Gier B, Krippeit-Drews P, Sheiko T, Aguilar-Bryan L, Bryan J, et al. (2009) Suppression of KATP channel activity protects murine pancreatic beta cells against oxidative stress. J Clin Invest 119: 3246-3256.
13. Maechler P, Jornot L, Wollheim CB, (1999) Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J Biol Chem 274: 27905-27913.
14. Nakazaki M, Kakei M, Koriyama N, Tanaka H, (1995) Involvement of ATP-sensitive K+ channels in free radical-mediated inhibition of insulin secretion in rat pancreatic beta-cells. Diabetes 44: 878-883.
15. Rebelato E, Abdulkader F, Curi R, Carpinelli AR, (2009) Low doses of hydrogen peroxide impair glucose-stimulated insulin secretion via inhibition of glucose metabolism and intracellular calcium oscillations. Metabolism.
16. Bulteau AL, Ikeda-Saito M, Szweda LI, (2003) Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42: 14846-14855.
17. Chatham JC, Gilbert HF, Radda GK, (1989) The metabolic consequences of hydroperoxide perfusion on the isolated rat heart. Eur J Biochem 184: 657-662.
18. Krippeit-Drews P, Kramer C, Welker S, Lang F, Ammon HP, et al. (1999) Interference of H2O2 with stimulus-secretion coupling in mouse pancreatic beta-cells. J Physiol 514 (Pt 2): 471-481.
19. Ammon HP, Grimm A, Lutz S, Wagner-Teschner D, Handel M, et al. (1980) Islet glutathione and insulin release. Diabetes 29: 830-834.
20. MacDonald MJ, (1995) Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J Biol Chem 270: 20051-20058.
21. Verspohl EJ, Handel M, Ammon HP, (1979) Pentosephosphate shunt activity of rat pancreatic islets: its dependence on glucose concentration. Endocrinology 105: 1269-1274.
22. Tian WN, Braunstein LD, Apse K, Pang J, Rose M, et al. (1999) Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am J Physiol 276: C1121-1131.
23. Tian WN, Braunstein LD, Pang J, Stuhlmeier KM, Xi QC, et al. (1998) Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J Biol Chem 273: 10609-10617.
24. Larrabee MG, (1989) The pentose cycle (hexose monophosphate shunt). Rigorous evaluation of limits to the flux from glucose using 14CO2 data, with applications to peripheral ganglia of chicken embryos. J Biol Chem 264: 15875-15879.
25. Larrabee MG, (1990) Evaluation of the pentose phosphate pathway from 14CO2 data. Fallibility of a classic equation when applied to non-homogeneous tissues. Biochem J 272: 127-132.
26. Morgan D, Oliveira-Emilio HR, Keane D, Hirata AE, Santos da Rocha M, et al. (2007) Glucose, palmitate and pro-inflammatory cytokines modulate production and activity of a phagocyte-like NADPH oxidase in rat pancreatic islets and a clonal beta cell line. Diabetologia 50: 359-369.
27. Oliveira HR, Curi R, Carpinelli AR, (1999) Glucose induces an acute increase of superoxide dismutase activity in incubated rat pancreatic islets. Am J Physiol 276: C507-510.
28. Ivarsson R, Quintens R, Dejonghe S, Tsukamoto K, in 't Veld P, et al. (2005) Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54: 2132-2142.
29. Tiedge M, Lortz S, Drinkgern J, Lenzen S, (1997) Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 46: 1733-1742.
30. Martens GA, Van de Casteele M, (2007) Glycemic control of apoptosis in the pancreatic beta cell: danger of extremes? Antioxid Redox Signal 9: 309-317.
31. Malaisse WJ, Hutton JC, Kawazu S, Herchuelz A, Valverde I, et al. (1979) The stimulus-secretion coupling of glucose-induced insulin release. XXXV. The links between metabolic and cationic events. Diabetologia 16: 331-341.
32. Zhang Q, Galvanovskis J, Abdulkader F, Partridge CJ, Gopel SO, et al. (2008) Cell coupling in mouse pancreatic beta-cells measured in intact islets of Langerhans. Philos Transact A Math Phys Eng Sci 366: 3503-3523.
33. Reinbothe TM, Ivarsson R, Li DQ, Niazi O, Jing X, et al. (2009) Glutaredoxin-1 mediates NADPH-dependent stimulation of calcium-dependent insulin secretion. Mol Endocrinol 23: 893-900.
34. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL, (2006) Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47: 74-80.
35. Barg S, Ma X, Eliasson L, Galvanovskis J, Gopel SO, et al. (2001) Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic B cells. Biophys J 81: 3308-3323.
36. Eliasson L, Abdulkader F, Braun M, Galvanovskis J, Hoppa MB, et al. (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J Physiol 586: 3313-3324.
37. Lacy PE, Kostianovsky M, (1967) Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 16: 35-39.
38. Bindokas VP, Kuznetsov A, Sreenan S, Polonsky KS, Roe MW, et al. (2003) Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 278: 9796-9801.
39. Morgan D, Rebelato E, Abdulkader F, Graciano MF, Oliveira-Emilio HR, et al. (2009) Association of NAD(P)H oxidase with glucose-induced insulin secretion by pancreatic beta-cells. Endocrinology 150: 2197-2201.
40. Robinson JP, Bruner LH, Bassoe CF, Hudson JL, Ward PA, et al. (1988) Measurement of intracellular fluorescence of human monocytes relative to oxidative metabolism. J Leukoc Biol 43: 304-310.
41. Quesada I, Nadal A, Soria B, (1999) Different effects of tolbutamide and diazoxide in alpha, beta-, and delta-cells within intact islets of Langerhans. Diabetes 48: 2390-2397.