Glucose oxidase induces insulin resistance via influencing multiple targets in vitro and in vivo: The central role of oxidative stress

Biochimie

Volumn 94, Issue 8, 2012, Pages 1705-1717

  Wang, Xin ^a   Gu, Chunshan ^a   He, Wei ^a   Ye, Xiaolong ^a   Chen, Hongli ^a   Zhang, Xiaodi ^a   Hai, Chunxu ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Glucose oxidase; Insulin resistance; Oxidative stress; ROS

Indexed keywords

ACETYLCYSTEINE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; GLUCOSE; GLUCOSE OXIDASE; GLUCOSE REGULATED PROTEIN 78; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; RECOMBINANT HUMAN INSULIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; INTRAPERITONEAL GLUCOSE TOLERANCE TEST; INTRAPERITONEAL INSULIN TOLERANCE TEST; LIVER CELL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GLUCOSE OXIDASE; HEPATOCYTES; INSULIN RESISTANCE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

ANIMALIA; RATTUS;

EID: 84862846889     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.03.024     Document Type: Article

References (54)

1. S. Wild, G. Roglic, A. Green, R. Sicree, H. King, Global prevalence of diabetes: estimates for the year 2000 and projections for 2030, Diabetes Care 27 (2004) 1047-1053.
2. B. Fletcher, C. Lamendola, Insulin resistance syndrome, Journal of Cardiovascular Nursing 19 (2004) 339-345.
3. M.M. Elgebaly, V. Portik-Dobos, K. Sachidanandam, D. Rychly, D. Malcom, M.H. Johnson, et al., Differential effects of ETA and ETB receptor antagonism on oxidative stress in type 2 diabetes, Vascular Pharmacology 47 (2007) 125-130.
4. T. Nishikawa, D. Kukidome, K. Sonoda, K. Fujisawa, T. Matsuhisa, H. Motoshima, et al., Impact of mitochondrial ROS production in the pathogenesis of insulin resistance, Diabetes Research and Clinical Practice 77 (2007) S161-S164.
5. R. Ritchie, Evidence for a causal role of oxidative stress in the myocardial complications of insulin resistance, Heart Lung and Circulation 18 (2009) 11-18.
6. N. Houstis, E. Rosen, E. Lander, Reactive oxygen species have a causal role in multiple forms of insulin resistance, Nature 440 (2006) 944-948.
7. B. Demple, C. Amabile-Cuevas, Redox redux: the control of oxidative stress responses, Cell 67 (1991) 837-839.
8. E. Lonn, S. Yusuf, B. Hoogwerf, J. Pogue, Q. Yi, B. Zinman, et al., Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes: results of the HOPE study and MICRO-HOPE substudy, Diabetes Care 25 (2002) 1919-1927.
9. L. JeBailey, O. Wanono, W. Niu, J. Roessler, A. Rudich, A. Klip, Ceramide- and oxidant-induced insulin resistance involve loss of insulin-dependent Racactivation and actin remodeling in muscle cells, Diabetes 56 (2007) 394-403.
10. H. Sakoda, T. Ogihara, M. Anai, M. Funaki, K. Inukai, H. Katagiri, et al., Dexamethasone- induced insulin resistance in 3T3-L1 adipocytes is due to inhibition of glucose transport rather than insulin signal transduction, Diabetes 49 (2000) 1700-1708.
11. X. Wang, J.Z. Liu, J.X. Hu, H. Wu, Y.L. Li, H.L. Chen, et al., ROS-activated p38 MAPK/ERK-Akt cascade plays a central role in palmitic acid-stimulated hepatocyte proliferation, Free Radical Biology and Medicine 51 (2011) 539-551.
12. X. Wang, Z. Wang, J.Z. Liu, J.X. Hu, H.L. Chen, W.L. Li, et al., Double antioxidant activities of rosiglitazone against high glucose-induced oxidative stress in hepatocyte, Toxicol in Vitro 25 (2011) 839-847.
13. O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall, Protein measurement with Folin phenol reagent, Journal of Biological Chemistry 193 (1951) 265-275.
14. M.A. Birch-Machin, H.L. Briggs, A.A. Saborido, L.A. Bindoff, D.M. Turnbull, An evaluation of the measurement of the activities of complexes I-IV in the respiratory chain of human skeletal muscle mitochondria, Biochemical Medicine and Metabolic Biology 51 (1944) 35-42.
15. N. Matsuzawa-Nagata, T. Takamura, H. Ando, S. Nakamura, S. Kurita, H. Misu, et al., Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity, Metabolism 57 (2008) 1071-1077.
16. M.K. Reimer, B. Ahren, Altered beta-cell distribution of pdx-1 and GLUT-2 after a short-term challenge with a high-fat diet in C57BL/6J mice, Diabetes 51 (2002) 138-143.
17. C.K. Tan, N. Leuenberger, M.J. Tan, Y.W. Yan, Y. Chen, R. Kambadur, et al., Smad3 deficiency in mice protects against insulin resistance and obesity induced by a high-fat diet, Diabetes 60 (2011) 464-476.
18. J.L. Evans, I.D. Goldfine, B.A. Maddux, G.M. Grodsky, Are oxidative stress-activated signaling pathways mediators of insulin resistance and B-cell dysfunction, Diabetes 52 (2003) 1-8.
19. A. Bloch-Damti, N. Bashan, Proposed mechanisms for the induction of insulin resistance by oxidative stress, Antioxidant Redox Signaling 7 (2005) 1553-1567.
20. A. Rudich, A. Tirosh, R. Potashnik, R. Hemi, H. Kanety, N. Bashan, Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes, Diabetes 47 (1998) 1562-1569.
21. B. Maddux, W. See, J. Lawrence Jr., A. Goldfine, I. Goldfine, J. Evans, Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolar concentrations of alpha-lipoic acid, Diabetes 50 (2001) 404-410.
22. A. Blair, E. Hajduch, G. Litherland, H. Hundal, Regulation of glucose transport and glycogen synthesis in L6 muscle cells during oxidative stress. Evidence for cross-talk between the insulin and SAPK2/p38 mitogen-activated protein kinase signaling pathways, Journal of Biological Chemistry 274 (1999) 36293-36299.
23. J. Kim, V. Saengsirisuwan, J. Sloniger, M. Teachey, E. Henriksen, Stimulation of muscle glucose transport by an oxidant stress: roles of insulin signaling and p38 MAP kinase, Free Radical Biology and Medicine 41 (2006) 818-824.
24. L. Groop, R. Bonadonna, S. DelPrato, K. Ratheiser, K. Zyck, E. Ferrannini, Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance, Journal of Clinical Investigation 84 (1989) 205-213.
25. S.P. Choukema, J.F. Gautiera, How to measure hepatic insulin resistance? Diabetes and Metabolism 34 (2008) 664-673.
26. M. Abdul-Ghani, C. Jenkinson, D. Richardson, D. Tripathy, R. DeFronzo, Insulin secretion and action in subjects with impaired fasting glucose and impaired glucose tolerance: results from the Veterans Administration Genetic Epidemiology Study, Diabetes 55 (2006) 1430-1435.
27. J. Nakae, B.C. Park, D. Accili, Insulin stimulates phosphorylation of the fork-head transcription factor FKHR on serine 253 through a Wortmannin-sensitive pathway, Journal of Biological Chemistry 274 (1999) 15982-15985.
28. T. Li, H. Ma, Y.J. Park, Y. Lee, S. Strom, D.D. Moore, et al., Forkhead box transcription factor O1 inhibits cholesterol 7[alpha]-hydroxylase in human hepatocytes and in high fat diet-fed mice, Biochimica et Biophysica Acta (BBA) e Molecular and Cell Biology of Lipids 1791 (2009) 991-996.
29. D. Schmoll, K.S. Walker, D.R. Alessi, R. Grempler, A. Burchell, S. Guo, et al., Regulation of glucose-6-phosphatase gene expression by protein kinase B alpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and -independent effects of insulin on promoter activity, Journal of Biological Chemistry 275 (2000) 36324-36333.
30. R.K. Hall, T. Yamasaki, T. Kucera, M. Waltner-Law, R.O. Brien, D.K. Granner, Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factorbinding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins, Journal of Biological Chemistry 275 (2000) 30169-30175.
31. T.B. Dansen, FOXO transcription factors: key players in redox signaling, Antioxidants and Redox Signaling 14 (2011) 559-561.
32. J.R. Woodgett, Molecular cloning and expression of glycogen synthase kinase-3/factor A, EMBO Journal 9 (1990) 2431-2438.
33. G. Cline, K. Johnson, W. Regittnig, P. Perret, E. Tozzo, L. Xiao, et al., Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats, Diabetes 51 (2002) 2903-2910.
34. E. Henriksen, B. Dokken, Role of glycogen synthase kinase-3 in insulin resistance and type 2 diabetes, Current Drug Targets 7 (2006) 1435-1442.
35. E. Henriksen, M. Teachey, Short-term in vitro inhibition of glycogen synthase kinase-3 potentiates insulin signaling in skeletal muscle of Zucker diabetic fatty rats, Metabolism 56 (2007) 931-938.
36. B. Dokken, J. Sloniger, E. Henriksen, Acute selective glycogen synthase kinase-3 inhibition enhances insulin signaling in prediabetic insulin-resistant rat skeletal muscle, American Journal of Physiology e Endocrinology and Metabolism 288 (2005) -1188e-1194.
37. Y. Guan, Y. Zhang, M.D. Breyer, The role of PPARs in the transcriptional control of cellular processes, Drug News and Perspectives 15 (2002) 147-154.
38. J.Hirosumi,G. Tuncman, L. Chang, C.Z.Görgün, K.T.Uysal, K.Maeda, et al.,A central role for JNK in obesity and insulin resistance, Nature 420 (2002) 333-336.
39. H. Guo, W. Ling, Q. Wang, C. Liu, Y. Hu, M. Xia, Cyanidin 3-glucoside protects 3T3-L1 adipocytes against H2O2- or TNF-alpha-induced insulin resistance by inhibiting c-Jun NH2-terminal kinase activation, Biochemical Pharmacology 75 (2008) 1393-1401.
40. X. Wang, Y.L. Li, H. Wu, J.Z. Liu, J.X. Hu, N. Liao, et al., Antidiabetic effect of oleanolic acid: a promising use of a traditional pharmacological agent, Phytotherapy Research (2011). doi:10.1002/ptr.3385.
41. Z. Liu, W. Cao, p38 mitogen-activated protein kinase: a critical node linking insulin resistance and cardiovascular diseases in type 2 diabetes mellitus, Endocrine Metabolic and Immune Disorders e Drug Targets 9 (2009) 38-46.
42. X. Wang, X.L. Ye, R. Liu, H.L. Chen, H. Bai, X. Liang, et al., Antioxidant activities of oleanolic acid in vitro: possible role of Nrf2 and MAP kinases, Chemico-Biological Interactions 184 (2010) 328-337.
43. J. Dong, K.K. Sulik, S.Y. Chen, Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo: implications for the prevention of fetal alcohol spectrum disorders, Antioxidants and Redox Signaling 10 (2008) 2023-2033.
44. L. Favreau, C. Pickett, The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines, Journal of Biological Chemistry 270 (1995) 24468-24474.
45. D. Galloway, D. Blake, L. McLellan, Regulation of gamma-glutamylcysteine synthetase regulatory subunit (GLCLR) gene expression: identification of the major transcriptional start site in HT29 cells, Biochimica et Biophysica Acta 1446 (1999) 47-56.
46. K. Hintze, A. Keck, J. Finley, E. Jeffery, Induction of hepatic thioredoxin reductase activity by sulforaphane, both in Hepa1c1c7 cells and in male Fisher 344 rats, The Journal of Nutritional Biochemistry 14 (2003) 173-179.
47. T. Ishii, K. Itoh, H. Sato, S. Bannai, Oxidative stress-inducible proteins in macrophages, Free Radical Research 31 (1999) 351-355.
48. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements, Biochemical and Biophysical Research Communications 236 (1997) 313-322.
49. T. Nguyen, P. Sherratt, C. Pickett, Regulatory mechanisms controlling gene expression mediated by the antioxidant response element, The Annual Review of Pharmacology and Toxicology 43 (2003) 233-260.
50. T. Rushmore, C. Pickett, Transcriptional regulation of the rat glutathione Stransferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants, Journal of Biological Chemistry 265 (1990) 14648-14653.
51. B. Wang, G. Williamson, Detection of a nuclear protein which binds specifically to the antioxidant responsive element (ARE) of the human NAD(P) H: quinone oxidoreductase gene, Biochimica et Biophysica Acta 1219 (1994) 645-652.
52. H. Zhu, K. Itoh, M. Yamamoto, J.L. Zweier, Y. Li, Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury, FEBS Letters 579 (2005) 3029-3036.
53. H.S. Zhang, S.Q. Wang, Nrf2 is involved in the effect of tanshinone IIA on intracellular redox status in human aortic smooth muscle cells, Biochemical Pharmacology 73 (2007) 1358-1366.
54. T.A. Beyer, S. Werner, The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver, Cell Cycle 7 (2008) 874-878.