Exogenous sod mimetic tempol ameliorates the early retinal changes reestablishing the redox status in diabetic hypertensive rats

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 8, 2010, Pages 4327-4336

  Rosales, Mariana A B ^a   Silva, Kamila C ^a   de Faria, José B Lopes ^a   de Faria, Jacqueline M Lopes ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; FIBRONECTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); SUPEROXIDE DISMUTASE; TEMPOL; 3 NITROTYROSINE; 3-NITROTYROSINE; AMINE OXIDE; DRUG DERIVATIVE; NEUROPROTECTIVE AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NOS2 PROTEIN, RAT; PEROXYNITROUS ACID; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC HYPERTENSION; DIABETIC RETINOPATHY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME SYNTHESIS; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RETINA; STREPTOZOCIN DIABETES; TREATMENT RESPONSE; ANIMAL; DRUG EFFECT; ENZYME IMMUNOASSAY; EXPERIMENTAL DIABETES MELLITUS; HYPERTENSION; MALE; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; SPIN LABELING; SPONTANEOUSLY HYPERTENSIVE RAT; WESTERN BLOTTING; WISTAR KYOTO RAT;

ANIMALS; BLOTTING, WESTERN; CYCLIC N-OXIDES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; FIBRONECTINS; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; HYPERTENSION; IMMUNOENZYME TECHNIQUES; MALE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXYNITROUS ACID; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SPIN LABELS; SUPEROXIDE DISMUTASE; TYROSINE;

EID: 77955858949     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4690     Document Type: Article

References (72)

1. Patz A, Smith RE. The ETDRS and Diabetes 2000. Ophthalmology. 1991;98:739-740.
2. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283-290.
3. Cunha-Vaz JG, Fonseca JR, Abreu JF, Ruas MA. Detection of early retinal changes in diabetes by vitreous fluorophotometry. Diabetes. 1979;28:16-19.
4. Dodson PM. Diabetic retinopathy: treatment and prevention. Diab Vasc Dis Res. 2007;4:S9-S11.
5. The UKPDS Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ. 1998;317: 703-713.
6. Danser AH, van den Dorpel MA, Deinum J, et al. Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy. J Clin Endocrinol Metab. 1989;68: 160-167.
7. Kawamura H, Kobayashi M, Li Q, et al. Effects of angiotensin II on the pericyte-containing microvasculature of the rat retina. J Physiol. 2004;561:671-683.
8. Moravski CJ, Kelly DJ, Cooper ME, et al. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension. 2000;36:1099-1104.
9. Silva KC, Rosales MA, Biswas SK, Lopes de Faria JB, Lopes de Faria JM. Diabetic retinal neurodegeneration is associated with mitochondrial oxidative stress and is improved by angiotensin receptor blocker in a model that combines hypertension and diabetes. Diabetes. 2009;58:1382-1390.
10. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol Cell Physiol. 1996;40:C1424-C1437.
11. Krishna MC, Russo A, Mitchell JB, Goldstein S, Dafni H, Samuni A. Do nitroxide antioxidants act as scavengers of O2+ or as SOD mimics? J Biol Chem. 1996;271:26026-26031.
12. Chen P, Guo AM, Edwards PA, Trick G, Scicli AG. Role of NADPH oxidase and ANG II in diabetes-induced retinal leukostasis. Am J Physiol Regul Integr Comp Physiol. 2007;293:R1619-R1629.
13. El-Remessy AB, Khalil IE, Matragoon S, et al. Neuroprotective effect of (_) Delta9-tetrahydrocannabinol and cannabidiol in N-methyl-D-aspartate-induced retinal neurotoxicity: involvement of peroxynitrite. Am J Pathol. 2003;163:1997-2008.
14. Shastri S, Gopalakrishnan V, Poduri R, Di Wang H. Tempol selectively attenuates angiotensin II evoked vasoconstrictor responses in spontaneously hypertensive rats. J Hypertens. 2002;20:1381-1391.
15. Kowluru RA, Tang J, Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia, VII: effect of long-term administration of antioxidants on the development of retinopathy. Diabetes. 2001;50:1938-1942.
16. Pinto CC, Silva KC, Biswas SK, Martins N, de Faria JB, de Faria JM. Arterial hypertension exacerbates oxidative stress in early diabetic retinopathy. Free Radic Res. 2007;41:1151-1158.
17. Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006;7:517-528.
18. Chiu J, Xu BY, Chen S, Feng B, Chakrabarti S. Oxidative stressinduced, poly (ADP-ribose) polymerase-dependent upregulation of ET-1 expression in chronic diabetic complications. Can J Physiol Pharmacol. 2008;86:365-372.
19. Xu B, Chiu J, Feng B, Chen S, Chakrabarti S. PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes. Diabetes Metab Res Rev. 2008; 24:404-412.
20. Garcia Soriano F, Virág L, Jagtap P, et al. Diabetic endothelial dysfunction: the role of poly(ADPribose) polymerase activation. Nat Med. 2001;7:108-113.
21. Zheng L, Szabó C, Kern TS. Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-+B. Diabetes. 2004;53:2960-2967.
22. Chiarugi A, Moskowitz MA. Poly(ADP-ribose) polymerase-1 activity promotes NF-_B-driven transcription and microglial activation: implication for neurodegenerative disorders. J Neurochem. 2003;85: 306-317.
23. Silva KC, Pinto CC, Biswas SK, Souza DS, de Faria JB, de Faria JM. Prevention of hypertension abrogates early inflammatory events in the retina of diabetic hypertensive rats. Exp Eye Res. 2007;85:123-129.
24. Drel VR, Xu W, Zhang J, et al. Poly (ADP-ribose) polymerase inhibition counteracts cataract formation and early retinal changes in streptozotocin-diabetic rats. Invest Ophthalmol Vis Sci. 2008; 50:1778-1790.
25. Silva KC, Pinto CC, Biswas SK, de Faria JB, de Faria JM. Hypertension increases retinal inflammation in experimental diabetes: a possible mechanism for aggravation of diabetic retinopathy by hypertension. Curr Eye Res. 2007;32:533-541.
26. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-isoprostaglandin F2. Hypertension. 1999;33:424-428.
27. Vaziri ND, Ding Y. Effect of lead on nitric oxide synthase expression in coronary endothelial cells: role of superoxide. Hypertension. 2001;37:223-226.
28. Bradford MM. A rapid and sensive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72:248-254.
29. Li Y, Zhu H, Kuppusamy P, Roubaud V, Zweier JL, Trush MA. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J Biol Chem. 1998;273:2015-2023.
30. Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882-888.
31. Yoshida Y, Yamagishi S, Matsui T, et al. Protective role of pigment epithelium-derived factor (PEDF) in early phase of experimental diabetic retinopathy. Diabetes Metab Res Rev. 2009;25:678-686.
32. Roy S, Lorenzi M. Early biosynthetic changes in the diabetic-like retinopathy of galactose-fed rats. Diabetologia. 1996;39:735-738.
33. Joussen AM, Doehmen S, Le ML, et al. TNF-alpha mediated apoptosis plays an important role in the development of early diabetic retinopathy and long-term histopathological alterations. Mol Vis. 2009;15:1418-1428.
34. Gardiner TA, Anderson HR, Stitt AW. Inhibition of advanced glycation end-products protects against retinal capillary basement membrane expansion during long-term diabetes. J Pathol. 2003; 201:328-333.
35. Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med. 2002;33:337-349.
36. Zheng L, Gong B, Hatala DA, Kern TS. Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes. Invest Ophthalmol Vis Sci. 2007;48:361-367.
37. Le Page C, Sanceau J, Drapier JC, Wietzerbin J. Inhibitors of ADP-ribosylation impair inducible nitric oxide synthase gene transcription through inhibition of NFB activation. Biochem Biophys Res Commun. 1998;243:451-457.
38. Lewis GP, Matsumoto B, Fisher SK. Changes in the organization and expression of cytoskeletal proteins during retinal degeneration induced by retinal detachment. Invest Ophthalmol Vis Sci. 1995;36:2404-2416.
39. Wang L, Cioffi GA, Cull G, Dong J, Fortune B. Immunohistologic evidence for retinal glial cell changes in human glaucoma. Invest Ophthalmol Vis Sci. 2002;43:1088-1094.
40. Mizutani M, Gerhardinger C, Lorenzi M. Muller cell changes in human diabetic retinopathy. Diabetes. 1998;47:445-449.
41. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes: the Penn State Retina Research Group. Invest Ophthalmol Vis Sci. 2000;41:3561-3568.
42. Lewis GP, Fisher SK. Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int Rev Cytol. 2003; 230:263-290.
43. Stone J, Dreher Z. Relationship between astrocytes, ganglion cells and vasculature of the retina. J Comp Neurol. 1987;255:35-49.
44. Stone J, Itin A, Alon T, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci. 1995;15:4738-4747.
45. Amin RH, Frank RN, Kennedy A, Eliott D, Puklin JE, Abrams GW. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 1997;38:36-47.
46. Tretiach M, Madigan MC, Wen L, Gillies MC. Effect of Muller cell co-culture on in vitro permeability of bovine retinal vascular endothelium in normoxic and hypoxic conditions. Neurosci Lett. 2005;378:160-165.
47. Antonetti DA, Lieth E, Barber AJ, Gardner TW. Molecular mechanisms of vascular permeability in diabetic retinopathy. Semin Ophthalmol. 1999;14:240-248.
48. Lorenzi M, Gerhardinger C. Early cellular and molecular changes induced by diabetes in the retina. Diabetologia. 2001;44:791-804.
49. Cai J, Boulton M. The pathogenesis of diabetic retinopathy: old concepts and new questions. Eye. 2002;16:242-260.
50. Roy S, Sato T, Paryani G, Kao R. Downregulation of fibronectin overexpression reduces basement membrane thickening and vascular lesions in retinas of galactose-fed rats. Diabetes. 2003;52: 1229-1234.
51. Oshitari T, Polewski P, Chadda M, Li AF, Sato T, Roy S. Effect of combined antisense oligonucleotides against high-glucose- and diabetes-induced overexpression of extracellular matrix components and increased vascular permeability. Diabetes. 2006;55:86-92.
52. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-820.
53. Kowluru RA, Chan PS. Oxidative stress and diabetic retinopathy. Exp Diabetes Res. 2007;2007:43603.
54. Kowluru RA, Odenbach S. Effect of long-term administration of-lipoic acid on retinal capillary cell death and the development of retinopathy in diabetic rats. Diabetes. 2004;53:3233-3238.
55. Johnsen-Soriano S, Garcia-Pous M, Arnal E, et al. Early lipoic acid intake protects retina of diabetic mice. Free Radic Res. 2008;42: 613-617.
56. Kowluru RA, Kern TS, Engerman RL. Abnormalities of retinal metabolism in diabetes or experimental galactosemia, IV: antioxidant defense system. Free Radic Biol Med. 1997;22:587-592.
57. Mustata GT, Rosca M, Biemel KM, et al. Paradoxical effects of green tea (Camellia sinensis) and antioxidant vitamins in diabetic rats: improved retinopathy and renal mitochondrial defects but deterioration of collagen matrix glycoxidation and cross-linking. Diabetes. 2005;54:517-526.
58. Kowluru RA, Kowluru V, Xiong Y, Ho YS. Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Radic Biol Med. 2006; 41:1187-1190.
59. Chambon P, Weill JD, Mandel P. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizingnuclear enzyme. Biochem Biophys Res Commun. 1963;11:39-43.
60. Zhang J, Dawson VL, Dawson T, Snyder SH. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science. 1994; 263:687-689.
61. Kaur C, Foulds WS, Ling EA. Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog Retin Eye Res. 2008;27:622-647.
62. Yu SW, Andrabi SA, Wang H, et al. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA. 2006;103:18314-18319.
63. Zhang Y, Park TS, Gidday JM. Hypoxic preconditioning protects human brain endothelium from ischemic apoptosis by Aktdependent survivin activation. Am J Physiol Heart Circ Physiol. 2007;292:H2573-H2581.
64. Li WG, Zhang XY, Wu YJ, Gao MT, Zheng RL. The relationship between structure and antioxidative activity of piperidine nitroxides. J Pharm Pharmacol. 2006;58:941-949.
65. Wilcox CS, Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev. 2008;60:418-469.
66. Matsumoto K, Krishna MC, Mitchell JB. Novel pharmacokinetic measurement using electron paramagnetic resonance spectroscopy and simulation of in vivo decay of various nitroxyl spin probes in mouse blood. J Pharmacol Exp Ther. 2004;310:1076-1083.
67. An J, Hsie AW. Effects of an inhibitor and a mimic of superoxide dismutase on bleomycin mutagenesis in Chinese hamster ovary cells. Mutat Res. 1992;270:167-175.
68. Mitchell JB, Samuni A, Krishna MC, et al. Biologically active metalindependent superoxide dismutase mimics. Biochemistry. 1990; 29:2802-2807.
69. Samuni A, Winkelsberg D, Pinson A, Hahn SM, Mitchell JB, Russo A. Nitroxide stable radicals protect beating cardiomyocytes against oxidative damage. J Clin Invest. 1991;87:1526-1530.
70. Du Y, Smith MA, Miller CM, Kern TS. Diabetes induced nitrative stress in the retina, and correction by aminoguanidine. J Neurochem. 2002;80:771-779.
71. Abu El-Asrar AM, Desmet S, Meersschaert A, Dralands L, Missotten L, Geboes K. Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol. 2001;4:551-556.
72. Hernández C, Lecube A, Segura RM, Sararols L, Simó R. Nitric oxide and vascular endothelial growth factor concentrations are increased but not related in vitreous fluid of patients with proliferative diabetic retinopathy. Diabet Med. 2002;19:655-660.