Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants

Free Radical Research

Volumn 37, Issue 11, 2003, Pages 1169-1180

  Kowluru, Renu A ^a   Koppolu, Prashant ^a   Chakrabarti, Subrata ^b   Chen, Shali ^b  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Antioxidants; Cell death; Diabetic retinopathy; Nuclear transcriptional factor; Oxidative stress

Indexed keywords

3 NITROTYROSINE; ACETYLCYSTEINE; ALLOXAN; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; BETA CAROTENE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID PEROXIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SELENIUM; TROLOX C;

ALLOXAN DIABETES MELLITUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; DIET SUPPLEMENTATION; DISEASE DURATION; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HISTOPATHOLOGY; HYPERGLYCEMIA; IN VIVO STUDY; MALE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PERICYTE; PROTEIN INDUCTION; RAT; RETINA; RETINA CAPILLARY;

ALPHA-TOCOPHEROL; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BETA CAROTENE; CHROMANS; CYSTEINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; GLUCOSE; LIPID PEROXIDES; MALE; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; RETINA; SELENIUM; TYROSINE;

ANIMALIA;

EID: 0142180047     PISSN: 10715762     EISSN: None     Source Type: Journal    
DOI: 10.1080/10715760310001604189     Document Type: Article

References (51)

1. Baynes, J.W. (1991) "Role of oxidative stress in development of complications in diabetes", Diabetes 40, 405-412.
2. Armstrong, D., Abdella, N., Salman, A., Miller, N., Rahman, E.A. and Bojancyzk, M. (1992) "Relationship of lipid peroxides to diabetic complications", J. Diabetes Complications 6, 116-122.
3. Kowluru, R.A., Kern, T.S. and Engerman, R.L. (1996) "Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system", Free Radic. Biol. Med. 22, 587-592.
4. Kowluru, R.A., Tang, J. and Kern, T.S. (2001) "Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy", Diabetes 50, 1938-1942.
5. Kowluru, R.A., Kern, T.S., Engerman, R.L. and Armstrong, D. (1996) "Abnormalities of retinal metabolism in diabetes or experimental galactosemia. III. Effects of antioxidants", Diabetes 45, 1233-1237.
6. Kowluru, R.A., Engerman, R.L. and Kern, T.S. (1999) "Abnormalities of retinal metabolism in diabetes or experimental galactosemia VI. Comparison of retinal and cerebral cortex metabolism, and effects of antioxidant therapy", Free Radic. Biol. Med. 26, 371-378.
7. Obrosova, I.G., Fathallah, L. and Greene, D.A. (2000) "Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of DL-alpha-lipoic acid", Eur. J. Pharmacol. 398, 139-146.
8. Heath, H., Rutter, A.C. and Beck, T.C. (1962) "Changes in the ascorbic acid and glutathione content of the retinae and adrenals from alloxan-cliabetic rats", Vision Res. 2, 431-437.
9. Kern, T.S., Kowluru, R. and Engerman, R.L. (1994) "Abnormalities of retinal metabolism in diabetes or galactosemia, ATPases and glutathione", Invest. Ophthalmol. Vis. Sci. 35, 2962-2967.
10. Szabo, M.E., Haines, D., Garay, E., Chiavaroli, C., Farine, J.C., Hannaert, P., Berta, A. and Garay, R.P. (2001) "Antioxidant properties of calcium dobesilate in ischemic/reperfused diabetic rat retina", Eur. J. Pharmacol. 428, 277-286.
11. Li, W., Yanoff, M., Jian, B. and He, Z. (1999) "Altered mRNA levels of antioxidant enzymes in pre-apoptotic pericytes from human diabetic retinas", Cell. Mol. Biol. 45, 59-66.
12. Mizutani, M., Kern, T.S. and Lorenzi, M. (1996) "Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy", J. Clin. Investig. 97, 2883-2890.
13. Kern, T.S., Tang, J., Mizutani, M., Kowluru, R., Nagraj, R. and Lorenzi, M. (2000) "Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia", Invest. Ophthal. Vis. Sci. 41, 3972-3978.
14. Kowluru, R.A. and Koppolu, P. (2002) "Diabetes-induced activation of Caspase-3 in retina: Effect of antioxidant therapy", Free Radic. Res. 36, 933-999.
15. Lenardo, M.J. and Baltimore, D. (1998) "NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control", Cell 58, 227-229.
16. Baeuerle, P.A. (1991) "The inducible transcription activator NF-kappa B: regulation by distinct protein subunits", Biochim. Biophys. Acta 1072, 63-80.
17. Rahman, I. and MacNee, W. (2000) "Regulation of redox glutathione levels and genes transcription in lung inflammation: therpeutic approaches", Free Radic. Biol. Med. 28, 1405-1420.
18. Anderson, M.T., Staal, F.J., Gitler, C. and Herzenberg, L.A. (1994) "Separation of oxidant-initiated and redox-regulated steps in the NF-kappa B signal transduction pathway", Proc. Natl Acad. Sci. USA 22, 11527-11531.
19. Du, X., Stocklauser-Farber, K. and Rosen, P. (1999) "Generation of reactive oxygen intermediates, activation of NF-kappaB, and induction of apoptosis in human endothelial cells by glucose: role of nitric oxide synthase?", Free Radic. Biol. Med. 27, 752-763.
20. Hammes, H.P., Hoerauf, H., Alt, A., Schleicher, E., Clausen, J.T., Bretzel, R.G. and Laqua, H. (1999) "N(epsilon) (carboxymethyl) lysin and the AGE receptor RAGE colocalize in age-related macular degeneration", Invest. Ophthalmol. Vis. Sci. 40, 1855-1859.
21. Joussen, A.M., Huang, S., Poulaki, V, Camphausen, K., Beecken, W.D., Kirchhof, B. and Adamis, A.P. (2001) "In vivo retinal gene expression in early diabetes", Invest. Ophthalmol. Vis. Sci. 42, 3047-3057.
22. Schreck, R., Rieber, R and Baeuerle, P.A. (1991) "Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1", EMBO J. 10, 2247-2258.
23. Romeo, G., Liu, W., Asnaghi, V., Kern, T.S. and Lorenzi, M. (2002) "Activation of nuclear factor-kappa B induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes", Diabetes 51, 2241-2248.
24. Zhou, D., Brown, S.A., Yu, T., Chen, G., Barve, S., Kang, B.C. and Thompson, J.S. (1999) "A high dose of ionizing radiation induces tissue-specific activation of nuclear factor-kappaB in vivo", Radiat. Res. 151, 703-709.
25. Chen, S., Khan, Z.A., Cukiernik, M. and Chakrabarti, S. (2003) "Differential activation of NF-kappa B and AP-1 in increased fibronectin synthesis in target organs of diabetic complications", Am. J. Physiol. Endocrinol. Metab. 284, E1089-E1097.
26. Kowluru, R.A. (2003) "Effect of re-institution of good metabolic control on retinal oxidative stress and nitrative stress in diabetic rats", Diabetes 52, 818-823.
27. Shibuki, H., Katai, N., Yodoi, J., Uchida, K. and Yoshimura, N. (2000) "Lipid peroxidation and peroxynitrite in retinal ischemia-reperfusion injury", Invest. Ophthalmol. Vis. Sci. 41, 3607-3614.
28. Kowluru, R.A. (2001) "Diabetes-induced elevations in retinal oxidative stress, protein kinase C and nitric oxide are interrelated", Acta Diabetologica 38, 179-185.
29. Du, Y., Smith, M.A., Miller, C.M. and Kern, T.S. (2002) "Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine", J. Neurochem. 80, 771-779.
30. Kennedy, A., Frank, R.N., Sotolongo, L.B., Das, A. and Zhang, N.L. (1990) "Proliferative response and macromolecular synthesis by ocular cells cultured on extracellular matrix materials", Curr. Eye Res., 307-322.
31. Lin, Y.Z., Yao, S.Y., Veach, R.A., Torgerson, T.R. and Hawiger, J. (1995) "Inhibition of nuclear translocation of transcription factor NF-kappa B by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence", J. Biol. Chem. 270, 14225-14228.
32. Bradford, M.M. (1974) "A rapid and sensitive method for the quantitation of microgram quantities of protein", Anal. Biochem. 72, 248-258.
33. Bursell, S.E., Clermont, A.C., Aiello, L.P., Aiello, L.M., Schlossman, D.K., Feener, E.P., Laffel, L. and King, G.L. (1999) "High-dose vitamin E supplementation normalizes retinal blood flow and creatinine clearance in patients with type 1 diabetes", Diabetes Care 22, 1245-1251.
34. Di Leo, M.A., Ghirlanda, G., Gentiloni Silveri, N., Giardina, B., Franconi, F. and Santini, S.A. (2003) "Potential therapeutic effect of antioxidants in experimental diabetic retina: a comparison between chronic taurine and vitamin E plus selenium supplementations", Free Radic. Res. 37, 323-330.
35. Stitt, A., Gardiner, T.A., Anderson, N.L., Canning, P., Frizzell, N., Duffy, N., Boyle, C., Januszewski, A.S., Chachich, M., Baynes, J.W. and Thorpe, S.R. (2002) "The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes", Diabetes 51, 2826-2832.
36. Robison, W.G., Jacot, J.L., Katz, ML. and Glover, J.P. (2000) "Retinal vascular changes induced by the oxidative stress of alpha-tocopherol deficiency contrasted with diabetic microangiopathy", J. Ocul. Pharmacol. Ther. 16, 109-120.
37. Wang, S.Y. and Lin, H.S. (2000) "Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage", J. Agric. Food Chem. 48, 140-146.
38. Van Zandwijk, N. (1995) "N-acetylcysteine for lung cancer prevention", Chest 10, 1437-1441.
39. Sies, H. and Arteel, G.E. (2000) "Interaction of peroxynitrite with selenoproteins and glutathione peroxidase mimics", Free Radic. Biol. Med. 8, 1451-1455.
40. Panasenko, O.M., Sharov, V.S., Briviba, K. and Sies, H. (2000) "Interaction of peroxynitrite with carotenoids in human low density lipoproteins", Arch. Biochem. Biophys. 373, 302-305.
41. Knudsen, C.A., Tappel, A.L. and North, J.A. (1996) "Multiple antioxidants protect against heme protein and lipid oxidation in kidney tissue", Free Radic. Biol. Med. 20, 165-173.
42. Koya, D., Li, K., Ishii, H., Kanoh, H. and King, G.L. (1997) "Prevention of glomerular dysfunction in diabetic rats by treatment with d-alpha tocopherol", J. Am. Soc. Nephrol. 8, 426-435.
43. Yanagihara, Y., Basaki, Y., Kajiwara, K. and Ikizawa, K. (1997) "A thiol antioxidant regulates IgE isotype switching by inhibiting activation of nuclear factor-kappaB", J. Allergy Clin. Immunol. 100, S33-S38.
44. Griscavage, J.M., Wilk, S. and Ignarro, L.J. (1996) "Inhibitors of the proteasome pathway interfere with induction of nitric oxide synthase in macrophages by blocking activation of transcription factor NF-kappa B", Proc. Natl Acad. Sci. USA 93, 3308-3312.
45. Takeda, M., Mori, F., Yoshida, A., Takamiya, A., Nakagomi, S., Sato, E. and Kiyama, H. (2001) "Constitutive nitric oxide synthase is associated with retinal vascular permeability in early diabetic rats", Diabetologia 44, 1043-1050.
46. Beckman, J.S. and Koppenol, W.H. (1996) "Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly", Am. J. Physiol. 271, C1424-C1437.
47. Diabetes Control and Complications Trial Research Group(1998) "Early worsening of diabetic retinopathy in the diabetes control and complication trial", Arch. Ophthalm. 116, 874-886.
48. Kowluru, R.A. and Abbas, S.N. (2003) "Diabetes-induced mitochondrial dysfunction in the retina", Invest. Ophthalmol. Vis. Sci., in press.
49. Kuhnel, F., Zender, L., Paul, Y., Tietze, M.K., Trautwein, C., Manns, M. and Kubicka, S. (2000) "NFkappaB mediates apoptosis through transcriptional activation of Fas (CD95) in adenoviral hepatitis", J. Biol. Chem. 275, 6421-6427.
50. Cooper, M.E. (2001) "Interaction of metabolic and haemodynamic factors in mediating experimental diabetic nephropathy", Diabetologia 44, 1957-1972.
51. Awazu, M., Ishikura, K., Hida, M. and Hoshiya, M. (1999) "Mechanisms of mitogen-activated protein kinase activation in experimental diabetes", J. Am. Soc. Nephrol. 10, 738-745.