Xanthine oxidase-induced oxidative stress causes activation of NF-κB and inflammation in the liver of type I diabetic rats

Free Radical Biology and Medicine

Volumn 49, Issue 2, 2010, Pages 171-177

  Romagnoli, Marco ^b   Gomez Cabrera, Mari Carmen ^a   Perrelli, Maria Giulia ^c   Biasi, Fiorella ^c   Pallardó, Federico V ^a   Sastre, Juan ^a   Poli, Giuseppe ^c   Viña, Jose ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSIDAD CATÓLICA DE VALENCIA SAN VICENTE MÁRTIR   (Spain)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Allopurinol; Diabetic complications; Free radicals; Interleukin 1 ; Interleukin 6

Indexed keywords

ALLOPURINOL; CYTOKINE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TRANSCRIPTION FACTOR RELA; XANTHINE OXIDASE;

ALLOXAN DIABETES MELLITUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; GLUCOSURIA; HEPATITIS; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE STRESS; POLYURIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; STREPTOZOCIN DIABETES; TRANSCRIPTION INITIATION;

ALLOPURINOL; ALLOXAN; ANIMALS; CELL MOVEMENT; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; INFLAMMATION MEDIATORS; LIVER; MALE; NEUTROPHILS; NF-KAPPA B; OXIDATIVE STRESS; POLYURIA; RATS; RATS, WISTAR; STREPTOZOCIN; TRANSCRIPTIONAL ACTIVATION; XANTHINE OXIDASE;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 77953538684     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.03.024     Document Type: Article

References (47)

1. Oberley L.W. Free radicals and diabetes. Free Radic. Biol. Med. 1988, 5:113-124.
2. Baynes J.W. Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40:405-412.
3. Sagara M., Satoh J., Wada R., Yagihashi S., Takahashi K., Fukuzawa M., Muto G., Muto Y., Toyota T. Inhibition of development of peripheral neuropathy in streptozotocin-induced diabetic rats with N-acetylcysteine. Diabetologia 1996, 39:263-269.
4. Giugliano D., Ceriello A., Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care 1996, 19:257-267.
5. Desco M.C., Asensi M., Marquez R., Martinez-Valls J., Vento M., Pallardo F.V., Sastre J., Vina J. Xanthine oxidase is involved in free radical production in type 1 diabetes: protection by allopurinol. Diabetes 2002, 51:1118-1124.
6. Matsumoto S., Koshiishi I., Inoguchi T., Nawata H., Utsumi H. Confirmation of superoxide generation via xanthine oxidase in streptozotocin-induced diabetic mice. Free Radic. Res. 2003, 37:767-772.
7. Kabe Y., Ando K., Hirao S., Yoshida M., Handa H. Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid. Redox Signal. 2005, 7:395-403.
8. Arkan M.C., Hevener A.L., Greten F.R., Maeda S., Li Z.W., Long J.M., Wynshaw-Boris A., Poli G., Olefsky J., Karin M. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 2005, 11:191-198.
9. El-Serag H.B., Everhart J.E. Diabetes increases the risk of acute hepatic failure. Gastroenterology 2002, 122:1822-1828.
10. El-Serag H.B., Tran T., Everhart J.E. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 2004, 126:460-468.
11. El-Serag H.B., Richardson P.A., Everhart J.E. The role of diabetes in hepatocellular carcinoma: a case-control study among United States Veterans. Am. J. Gastroenterol. 2001, 96:2462-2467.
12. Reid A.E. Nonalcoholic steatohepatitis. Gastroenterology 2001, 121:710-723.
13. Dixon J.B., Bhathal P.S., O'Brien P.E. Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology 2001, 121:91-100.
14. Asensi M., Sastre J., Pallardo F.V., Garcia de la Asuncion J., Estrela J.M., Vina J. A high-performance liquid chromatography method for measurement of oxidized glutathione in biological samples. Anal. Biochem. 1994, 217:323-328.
15. Young S.H.Y., Knight J.A., Hopfer S.M., Zaharia O., Leach C.N., Sunderman F.W. Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin. Chem. 1987, 33:214-220.
16. Beckman J.S., Parks D.A., Pearson J.D., Marshall P.A., Freeman B.A. A sensitive fluorometric assay for measuring xanthine dehydrogenase and oxidase in tissues. Free Radic. Biol. Med. 1989, 6:607-615.
17. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
18. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
19. Hollander J., Fiebig R., Gore M., Ookawara T., Ohno H., Ji L.L. Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch. 2001, 442:426-434.
20. Newfry G.A., Jones K.J. Differential effects of facial nerve transection on heat shock protein 70 expression in the developing and adult hamster facial nucleus. Metab. Brain Dis. 1998, 13:253-257.
21. Smolka M.B., Zoppi C.C., Alves A.A., Silveira L.R., Marangoni S., Pereira-Da-Silva L., Novello J.C., Macedo D.V. HSP72 as a complementary protection against oxidative stress induced by exercise in the soleus muscle of rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 279:R1539-1545.
22. Matheu A., Maraver A., Klatt P., Flores I., Garcia-Cao I., Borras C., Flores J.M., Vina J., Blasco M.A., Serrano M. Delayed ageing through damage protection by the Arf/p53 pathway. Nature 2007, 448:375-379.
23. Moloney W.C., McPherson K., Fliegelman L. Esterase activity in leukocytes demonstrated by the use of naphthol AS-D chloroacetate substrate. J. Histochem. Cytochem. 1960, 8:200-207.
24. Niedowicz D.M., Daleke D.L. The role of oxidative stress in diabetic complications. Cell Biochem. Biophys. 2005, 43:289-330.
25. Eckel R.H., Wassef M., Chait A., Sobel B., Barrett E., King G., Lopes-Virella M., Reusch J., Ruderman N., Steiner G., Vlassara H. Prevention Conference VI: Diabetes and Cardiovascular Disease: Writing Group II: pathogenesis of atherosclerosis in diabetes. Circulation 2002, 105:e138-143.
26. Armstrong D., al-Awadi F. Lipid peroxidation and retinopathy in streptozotocin-induced diabetes. Free Radic. Biol. Med. 1991, 11:433-436.
27. Hofmann M.A., Schiekofer S., Isermann B., Kanitz M., Henkels M., Joswig M., Treusch A., Morcos M., Weiss T., Borcea V., Abdel Khalek A.K., Amiral J., Tritschler H., Ritz E., Wahl P., Ziegler R., Bierhaus A., Nawroth P.P. Peripheral blood mononuclear cells isolated from patients with diabetic nephropathy show increased activation of the oxidative-stress sensitive transcription factor NF-kappaB. Diabetologia 1999, 42:222-232.
28. Wellen K.E., Hotamisligil G.S. Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 115:1111-1119.
29. Boden G., She P., Mozzoli M., Cheung P., Gumireddy K., Reddy P., Xiang X., Luo Z., Ruderman N. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappaB pathway in rat liver. Diabetes 2005, 54:3458-3465.
30. Ceriello A., dello Russo P., Amstad P., Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 1996, 45:471-477.
31. Jain S.K., McVie R., Jaramillo J.J., Chen Y. Hyperketonemia (acetoacetate) increases the oxidizability of LDL + VLDL in Type-I diabetic patients. Free Radic. Biol. Med. 1998, 24:175-181.
32. Hunt J.V., Smith C.C., Wolff S.P. Autoxidative glycosylation and possible involvement of peroxides and free radicals in LDL modification by glucose. Diabetes 1990, 39:1420-1424.
33. Satoh M., Fujimoto S., Haruna Y., Arakawa S., Horike H., Komai N., Sasaki T., Tsujioka K., Makino H., Kashihara N. NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy. Am. J. Physiol. Renal Physiol. 2005, 288:F1144-1152.
34. Cai H., Harrison D.G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 2000, 87:840-844.
35. Inoguchi T., Li P., Umeda F., Yu H.Y., 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.
36. Galbusera C., Orth P., Fedida D., Spector T. Superoxide radical production by allopurinol and xanthine oxidase. Biochem. Pharmacol. 2006, 71:1747-1752.
37. Gomez-Cabrera M.C., Pallardo F.V., Sastre J., Vina J., Garcia-del-Moral L. Allopurinol and markers of muscle damage among participants in the Tour de France. Jama 2003, 289:2503-2504.
38. Siebenlist U., Franzoso G., Brown K. Structure, regulation and function of NF-kappa B. Annu. Rev. Cell Biol. 1994, 10:405-455.
39. Iwasaki Y., Kambayashi M., Asai M., Yoshida M., Nigawara T., Hashimoto K. High glucose alone, as well as in combination with proinflammatory cytokines, stimulates nuclear factor kappa-B-mediated transcription in hepatocytes in vitro. J. Diabet. Complications 2007, 21:56-62.
40. Bi Y., Sun W.P., Chen X., Li M., Liang H., Cai M.Y., Zhu Y.H., He X.Y., Xu F., Weng J.P. Effect of early insulin therapy on nuclear factor kappaB and cytokine gene expressions in the liver and skeletal muscle of high-fat diet, streptozotocin-treated diabetic rats. Acta Diabetol. 2008, 45:167-178.
41. Allen R.G., Tresini M. Oxidative stress and gene regulation. Free Radic. Biol. Med. 2000, 28:463-499.
42. Prabhakar S.S. Role of nitric oxide in diabetic nephropathy. Semin. Nephrol. 2004, 24:333-344.
43. Ali S., Diwakar G., Pawa S., Siddiqui M.R., Abdin M.Z., Ahmad F.J., Jain S.K. Xanthine oxidase-derived reactive oxygen metabolites contribute to liver necrosis: protection by 4-hydroxypyrazolo[3, 4-d]pyrimidine. Biochim. Biophys. Acta 2001, 1536:21-30.
44. Kono H., Rusyn I., Bradford B.U., Connor H.D., Mason R.P., Thurman R.G. Allopurinol prevents early alcohol-induced liver injury in rats. J. Pharmacol. Exp. Ther. 2000, 293:296-303.
45. McCord J.M. Oxygen-derived free radicals in postischemic tissue injury. N. Engl. J. Med. 1985, 312:159-163.
46. Inkster M.E., Cotter M.A., Cameron N.E. Treatment with the xanthine oxidase inhibitor, allopurinol, improves nerve and vascular function in diabetic rats. Eur. J. Pharmacol. 2007, 561:63-71.
47. Vincent A.M., Stevens M.J., Backus C., McLean L.L., Feldman E.L. Cell culture modeling to test therapies against hyperglycemia-mediated oxidative stress and injury. Antioxid. Redox Signal. 2005, 7:1494-1506.