Effects of resveratrol on biomarkers of oxidative stress and on the activity of delta aminolevulinic acid dehydratase in liver and kidney of streptozotocin-induced diabetic rats

Biochimie

Volumn 94, Issue 2, 2012, Pages 374-383

  Schmatz, Roberta ^a   Perreira, Luciane Belmonte ^a   Stefanello, Naiara ^a   Mazzanti, Cinthia ^a   Spanevello, Roselia ^a,c   Gutierres, Jessié ^a   Bagatini, Margarete ^b   Martins, Caroline Curry ^a   Abdalla, Fátima Husein ^a   Daci Da Silva Serres, Jonas ^a   Zanini, Daniela ^a   Vieira, Juliano Marchi ^a   Cardoso, Andréia MacHado ^a   Schetinger, Maria Rosa ^a   Morsch, Vera Maria ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b UNIVERSIDADE FEDERAL DA FRONTEIRA SUL   (Brazil)

^c FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

Author keywords

Aminolevulinic acid dehydratase; Diabetes; Liver; Oxidative stress; Resveratrol

Indexed keywords

ALANINE AMINOTRANSFERASE; ASCORBIC ACID; ASPARTATE AMINOTRANSFERASE; CATALASE; CHOLESTEROL; CREATININE; GAMMA GLUTAMYLTRANSFERASE; PORPHOBILINOGEN SYNTHASE; RESVERATROL; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL; UREA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD LEVEL; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DRUG EFFECT; ENZYME ACTIVITY; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; KIDNEY; LIPID PEROXIDATION; LIVER; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; STREPTOZOCIN DIABETES; TREATMENT DURATION; TRIACYLGLYCEROL BLOOD LEVEL; UREA BLOOD LEVEL;

ALANINE TRANSAMINASE; ANIMALS; ANTIOXIDANTS; ASPARTATE AMINOTRANSFERASES; BIOLOGICAL MARKERS; CATALASE; DIABETES MELLITUS, EXPERIMENTAL; GAMMA-GLUTAMYLTRANSFERASE; KIDNEY; LIPID PEROXIDATION; LIVER; MALE; OXIDATIVE STRESS; PORPHOBILINOGEN SYNTHASE; RATS; RATS, WISTAR; STILBENES; STREPTOZOCIN; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

ANIMALIA; RATTUS;

EID: 84855848324     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.08.005     Document Type: Article

References (90)

1. American Diabetes Association Diagnosis and classification of diabetes mellitus Diabetes Care 33 2010 62 69
2. A.C. Maritim, R.A. Sandres, and J.B. Watkins Diabetes, oxidative stress, and antioxidants: a review J. Biochem. Mol. Toxicol. 17 2003 24 39
3. F. Giacco, and M. Brownlee Oxidative stress and diabetic complications Circ. Res. 107 9 2010 1058 1070
4. M.J. Stevens Redox-based mechanisms in diabetes Antioxid. Redox Signal. 7 2005 1483 1485 (Pubitemid 41767983)
5. J.L. Rains, and S.K. Jain Oxidative stress, insulin signaling, and diabetes Free Radic. Biol. Med. 50 2011 567 575
6. M. Brownlee A radical explanation for glucose-induced beta cell dysfunction J. Clin. Invest. 112 2003 1788 1790 (Pubitemid 38063700)
7. P.S. Gill, and C.S. Wilcox NADPH oxidases in the kidney Antioxid. Redox Signal. 8 2006 1597 1607 (Pubitemid 44726334)
8. J. Shao, L. Qiao, R.C. Janssen, M. Pagliassotti, and J.E. Friedman Chronic hyperglycemia enhances PEPCK gene expression and hepatocellular glucose production via elevated liver activating protein/liver inhibitory protein ratio Diabetes 54 2005 976 984 (Pubitemid 40446311)
9. B. Halliwell, and J.M.C. Gutterdige Free Radicals in Biology and Medicine 1999 Oxford University Press Oxford
10. A.F. Fidan, and Y. Dündar The effects of Yucca schidigera and Quillaja saponaria on DNA damage, protein oxidation, lipid peroxidation, and some biochemical parameters in streptozotocin-induced diabetic rats J. Diabet. Complications 22 2008 348 356
11. A. Likidlilid, N. Patchanans, T. Peerapatdit, and C. Sriratanasathavorn Lipid peroxidation and antioxidant enzyme activities in erythrocytes of type 2 diabetic patients J. Med. Assoc. Thai. 93 2010 682 693
12. N.F. Wiernsperger Oxidative stress as a therapeutic target in diabetes: revisiting the controversy Diabet. Med. 29 2003 579 585 (Pubitemid 38082159)
13. S. Sassa ALAD porphyria Semin. Liver Dis. 18 1998 95 101 (Pubitemid 28133448)
14. D. Shemim 5-Aminolevulinic acid dehydratase: structure, function, and mechanism Phil. Trans. R. Soc. Lond. B 273 1976 109 115
15. C.W. Nogueira, F.A. Soares, P.C. Nascimento, D. Muller, and J.B.T. Rocha 2,3-Dimercaptopropane-1-sulfonic acid and meso-2,3-dimercaptosuccinic acid increase mercury and cadmium-induced inhibition of delta-aminolevulinate dehydratase Toxicology 184 2003 85 95 (Pubitemid 36009291)
16. B. Fernández-Cuartero, J.L. Rebollar, A. Batlle, and E.R. de Salamanca Delta aminolevulinate dehydratase (ALA-D) activity in human and experimental diabetes mellitus Int. J. Biochem. Cell Biol. 31 1999 479 488 (Pubitemid 29112908)
17. K. Bhooshan, P. Syed, and I. Rizvi Plant polyphenols as dietary antioxidants in human health and disease Oxid. Med. Cell. Longev. 2 2009 270 278
18. Z. Francine, M. Marques, A. Markus, and B.J. Morris Resveratrol: cellular actions of a potent natural chemical that confers a diversity of health benefits Int. J. Biochem. Cell Biol. 41 2009 2125 2128
19. K.B. Pandey, and S.I. Rizvi Anti-oxidative action of resveratrol: implications for human health Arabian J. Chem. 4 2011 293 298
20. S.M. Lee, H. Yang, D.M. Tartar, B. Gao, X. Luo, S.Q. Ye, H. Zaghouani, and D. Fang Prevention and treatment of diabetes with resveratrol in a non-obese mouse model of type 1 diabetes Diabetologia 54 2011 1136 1146
21. J.A. Baur, and D.A. Sinclair Therapeutic potential of resveratrol: the in vivo evidence Nat. Rev. Drug Discov. 5 6 2006 493 506 (Pubitemid 44136961)
22. P. Saiko, A. Szakmary, W. Jaeger, and T. Szekeres Resveratrol and its analogs: defense against cancer, coronary disease and neurodegenerative maladies or just a fad? Mutat. Res. Rev. 658 2008 68 94 (Pubitemid 351172881)
23. K. Szkudelska, and T. Szkudelski Resveratrol, obesity and diabetes Eur. J. Pharmacol. 635 2010 1 8
24. K.B. Pandey, and S.I. Rizvi Protective effect of resveratrol on formation of membrane protein carbonyls and lipid peroxidation in erythrocytes subjected to oxidative stress Appl. Physiol. Nutr. Metab. 34 2009 1093 1097
25. R. Schmatz, C.M. Mazzanti, R. Spanevello, N. Stefanello, J. Gutierres, M. Corrêa, M.M. da Rosa, M.A. Rubin, M.R.C. Schetinger, and V.M. Morsch Resveratrol prevents memory deficits and the increase in acetylcholinesterase activity in streptozotocin-induced diabetic rats Eur. J. Pharmacol. 610 2009 42 48
26. R. Schmatz, M.R.C. Schetinger, R.M. Spanevello, C.M. Mazzanti, N. Stefanello, P.A. Maldonado, J. Gutierres, and V.M. Morsch Effects of resveratrol on nucleotide degrading enzymes in streptozotocin-induced diabetic rats Life Sci. 84 2009 345 350
27. R. Schmatz, C.M. Mazzanti, R. Spanevello, N. Stefanello, J. Gutierres, P.A. Maldonado, M. Correa, and V.M. Morsch Ectonucleotidase and acetylcholinesterase activities in synaptosomes from the cerebral cortex of streptozotocin-induced diabetic rats and treated with resveratrol Brain Res. Bull. 80 2009 371 376
28. M.E. Juan, M.P. Vinardell, and J.M. Planas The daily oral administration of high doses of trans-resveratrol to rats for 28 days is not harmful J. Nutr. 132 2002 257 260 (Pubitemid 34135604)
29. V. Tiwari, and K.l Chopra Resveratrol prevents alcohol-induced cognitive deficits and brain damage by blocking inflammatory signaling and cell death cascade in neonatal rat brain J. Neurochem. 117 2011 678 690
30. E.S. Lee, M.O. Shin, and S. Yoon Resveratrol inhibits dimethylnitrosamine-induced hepatic fibrosis in rats Arch. Pharm. Res. 33 2010 925 932
31. E.H. Siemann, and L.L. Creasy Concentration of the phytoalexin resveratrol in wine Am. J. Enol. Viticult. 43 1992 49 52
32. D.M. Goldberg, E. Ng, J. Yan, A. Karumanchiri, G.J. Soleas, and E.P. Diamandis Regional differences in resveratrol isomer concentrations of wines from various cultivars J. Wine Res. 7 1996 13 24 (Pubitemid 126068530)
33. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358 (Pubitemid 9194347)
34. 2 solutions in the UV) Anal. Biochem. 49 1972 474 478
35. H.P. Misra, and I. Fridovich The role of superoxide anion in the autoxidation of epinephrine and simple assay for superoxide dismutase J. Biol. Chem. 247 1972 3170 3175
36. M.C. Jacques-Silva, C.W. Nogueira, L.C. Broch, E.M.M. Flores, and J.B.T. Rocha Diphenyl diselenide and ascorbic changes deposition of selenium and ascorbic acid in liver and brain of mice Pharmacolol. Toxicol. 88 2001 119 125 (Pubitemid 32174036)
37. G.L. Ellman Tissue sulphydryl groups Arch. Biochem. Biophys. 82 1959 70 77
38. S. Sassa δ-Aminolevulinic acid dehydratase assay Enzyme 28 1982 133 145
39. M.M. Bradford A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
40. K.K. Wu, and Y. Huan Streptozotocin-Induced diabetic models in mice and rats Curr. Protoc. Pharmacol. 40 2008 1 5
41. R. Rodrigo, A. Miranda, and L. Vergara Modulation of endogenous antioxidant system by wine polyphenols in human disease Clin. Chim. Acta 412 2011 410 424
42. J.S. Lee Effects of soy protein and genistein on blood glucose, antioxidant enzyme activities, and lipid profile in streptozotocin-induced diabetic rats Life Sci. 79 2006 1578 1584
43. P. Palsamy, and S. Subramanian Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic beta-cell dysfunction in streptozotocin-nicotinamide-induced diabetic rats J. Cell Physiol. 224 2010 423 432
44. G. Stark Functional consequences of membrane damage J. Membr. Biol. 205 2005 1 16
45. L.F. Dmitriev, and V.N. Titov Lipid peroxidation in relation to ageing and the role of endogenous aldehydes in diabetes and other age-related diseases Ageing Res. Rev. 9 2010 200 210
46. H.R. Yilmaz, E. Uz, N. Yucel, I. Altuntas, and N. Ozcelik Protective effect of caffeic acid phenethyl ester (CAPE) on lipid peroxidation and antioxidant enzymes in diabetic rat liver J. Biochem. Mol. Toxicol. 18 2004 234 238 (Pubitemid 39341509)
47. L. Jin, H.Y. Xue, L.J. Jin, S.Y. Li, and Y.P. Xu Antioxidant and pancreas-protective effect of aucubin on rats with streptozotocin-induced diabetes Eur. J. Pharmacol. 582 2008 162 167
48. S.A. Santini, G. Marra, and B. Giardina Defective antioxidant defenses and enhanced susceptibility to lipid peroxidation in uncomplicated IDDM Diabetes 46 1997 1853 1858 (Pubitemid 27456421)
49. M. Kinalski, A. Sledziewski, B. Telejko, W. Zarzycki, and I. Kinalska Lipid peroxidation and scavenging enzyme activity in streptozotocin-induced diabetes Acta Diabetol. 37 2000 179 183 (Pubitemid 32547532)
50. A.K. Saxena, P. Srivastava, R.K. Kale, and N.Z. Baquer Impaired antioxidant status in diabetic rat liver. Effect of vanadate Biochem. Pharmacol. 45 3 1993 539 554
51. P. Palsamy, S. Sivakumar, and S. Subramanian Resveratrol attenuates hyperglycemia mediated oxidative stress, proinflammatory cytokines and protects hepatocytes ultrastructure in streptozotocin-nicotinamide-induced experimental diabetic rats Chem. Biol. Interact. 186 2010 200 210
52. P. Palsamy, and S. Subramanian Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling Biochim. Biophys. Acta 1812 2011 719 731
53. A. Kumar, R.K. Kaundal, S. Iyer, and S.S. Sharma Effects of resveratrol on nerve functions, oxidative stress and DNA fragmentation in experimental diabetic neuropathy Life Sci. 80 2007 1236 1244 (Pubitemid 46329013)
54. O. Ates, S.R. Cayli, N. Yucel, E. Altinoz, A. Kocak, M.A. Durak, Y. Turkoz, and S. Yologlu Central nervous system protection by resveratrol in streptozotocin-induced diabetic rats J. Clin. Neurosci. 14 2007 256 260 (Pubitemid 46136016)
55. Z. Cao, and Y. Li Potent induction of cellular antioxidants and phase 2 enzymes by resveratrol in cardiomyocytes: protection against oxidative and electrophilic injury Eur. J. Pharmacol. 489 2004 39 48 (Pubitemid 38520069)
56. S.S. Leonard, C. Xia, B.H. Jiang, B. Stinefelt, H. Klandorf, G.K. Harris, and X. Shi Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses Biochem. Biophys. Res. Commun. 309 2003 1017 1026 (Pubitemid 37122632)
57. S. Bradamante, L. Barenghi, and A. Villa Cardiovascular protective effects of resveratrol Cardiovasc. Drug Rev. 22 2004 169 188 (Pubitemid 39391187)
58. Y.J. Cai, J.G. Fang, L.P. Ma, L. Yang, and Z.L. Liu Inhibition of free radical-induced peroxidation of rat liver microsomes by resveratrol and its analogues Biochim. Biophys. Acta 1637 2003 31 38 (Pubitemid 36071593)
59. M. Lüpez-Velez, F. Martínez-Martínez, and C. Del Valle-Ribes The study of phenolic compounds as natural antioxidants in wine Crit. Rev. Food Sci. Nutr. 43 2003 233 244 (Pubitemid 38552301)
60. D. Delmas, B. Jannin, and N. Latruffe Resveratrol: preventing properties against vascular alterations and ageing Mol. Nutr. Food Res. 49 2005 377 395 (Pubitemid 40780387)
61. L. Belguendouz, L. Fremont, and M.T. Gozzelino Interaction of trans resveratrol with plasma lipoproteins Biochem. Pharmacol. 55 1998 811 816 (Pubitemid 28319644)
62. W. Stahl, and H. Sies Antioxidant defense: vitamins E and C and carotenoids Diabetes 46 1997 14 18
63. P. Arulselvan, and S.P. Subramanian Beneficial effects of Murraya koenigii leaves on antioxidant defense system and ultra structural changes of pancreatic β-cells in experimental diabetes in rats Chem. Biol. Interact. 165 2007 155 164 (Pubitemid 46072799)
64. I.J. Kade, V.C. Borges, L. Savegnago, E.O. Ibukun, G. Zeni, C.W. Nogueira, and J.B. Rocha Effect of oral administration of diphenyl diselenide on antioxidant status, and activity of delta aminolevulinic acid dehydratase and isoforms of lactate dehydrogenase, in streptozotocin-induced diabetic rats Cell Biol. Toxicol. 25 2009 415 424
65. A. Sharma, S. Kharb, S.N. Chugh, R. Kakkar, and G.P. Singh Effect of glycemic control and vitamin E supplementation on total glutathione content in non-insulin-dependent diabetes mellitus Ann. Nutr. Metab. 44 2000 11 13 (Pubitemid 30326263)
66. X. Li, Z.C. Qu, and J.M. May GSH is required to recycle ascorbic acid in cultured liver cell lines Antioxid. Redox Signal. 3 2001 1089 1097 (Pubitemid 34027364)
67. D.M. Townsend, K.D. Tew, and H. Tapiero The importance of glutathione in human disease Biomed. Pharmacother. 57 2003 145 155 (Pubitemid 36740460)
68. V.B. Brito, V. Folmer, J.C. Soares, I.D. Silveira, and J.B. Rocha Long-term sucrose and glucose consumption decreases the delta-aminolevulinate dehydratase activity in mice Nutrition 23 2007 818 826 (Pubitemid 47532393)
69. E.J. Bechara Oxidative stress in acute intermittent porphyria and lead poisoning may be triggered by 5-aminolevulinic acid Braz. J. Med. Biol. Res. 29 1996 841 851 (Pubitemid 26245828)
70. J.B. Souza, J.B. Rocha, C.W. Nogueira, V.C. Borges, R.R. Kaizer, V.M. Morsch, V.L. Dressler, A.F. Martins, E.M. Flores, and M.R. Schetinger Delta-aminolevulinate dehydratase (delta-ALA-D) activity in diabetes and hypothyroidism Clin. Biochem. 40 2007 321 325
71. F.A. Caballero, E.N. Gerez, C.F. Polo, E.S. Vazquez, and A.M.C. Batlle Reducing sugars trigger d aminolevulinate dehydratase inactivation:evidence of in vitro aspirin prevention Gen. Pharmacol. 31 1998 441 445 (Pubitemid 28398873)
72. V. Folmer, J.C. Soares, D. Gabriel, and J.B.T. Rocha A high fat diet inhibits deltaaminolevulinate dehydratase and increases lipid peroxidation in mice (Musmusculus) J. Nutr. 133 2003 2165 2170 (Pubitemid 36841533)
73. D.W. Molander, F. Wroblewski, and J.S. Ladue Serum glutamic oxalacetic transaminase as an index of hepatocellular integrity J. Lab. Clin. Med. 46 1955 831 839
74. H. Elizabeth, and M.D. Harris Elevated liver function tests in type 2 diabetes Clin. Diabetes 23 2005 115 119
75. F.M. El-Demerdash, M.I. Yousef, and N.I. El-Naga Biochemical study on the hypoglycemic effects of onion and garlic in alloxan-induced diabetic rats Food Chem. Toxicol. 43 2005 57 63 (Pubitemid 39575733)
76. A.A. Fernandes, E.L. Novelli, K. Okoshi, M.P. Okoshi, B.P. Di Muzio, J.F. Guimarães, and A.J. Fernandes Influence of rutin treatment on biochemical alterations in experimental diabetes Biomed. Pharmacother. 64 2010 214 219
77. K.H. Janbaz, S.A. Saeed, and A.H. Gilani Studies on the protective effects of caffeic acid and quercetin on chemical-induced hepatotoxicity in rodents Phytomedicine 11 2004 424 430 (Pubitemid 38980523)
78. T. de Jesus Soares, R.A. Volpini, H.D. Francescato, R.S. Costa, C.G. da Silva, and T.M. Coimbra Effects of resveratrol on glycerol-induced renal injury Life Sci. 81 2007 647 656 (Pubitemid 47268017)
79. S. Sharma, M. Anjaneyulu, S.K. Kulkarni, and K. Chopra Resveratrol, a polyphenolic phytoalexin, attenuates diabetic nephropathy in rats Pharmacology 76 2006 69 75 (Pubitemid 43131538)
80. S. Hassan-Khabbar, C.H. Cottart, D. Wendum, F. Vibert, J.P. Clot, J.F. Savouret, M. Conti, and V. Nivet-Antoine Postischemic treatment by trans-resveratrol in rat liver ischemia-reperfusion: a possible strategy in liver surgery Liver Transpl. 14 2008 451 459 (Pubitemid 351524400)
81. W. Gadacha, M. Ben-Attia, D. Bonnefont-Rousselot, E. Aouani, N. Ghanem-Boughanmi, and Y. Touitou Resveratrol opposite effects on rat tissue lipoperoxidation: pro-oxidant during day-time and antioxidant at night Redox Rep. 14 2009 154 158
82. C.A. de la Lastra, and I. Villegas Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications Biochem. Soc. Trans. 35 2007 1156 1160 (Pubitemid 350206449)
83. S. Mukherjee, J.I. Dudley, and D.K. Das Dose-Dependency of resveratrol in providing health benefits Dose Response 8 2010 478 500
84. F.Z. Marques, and B.J. Morris Commentary on resveratrol and hormesis: resveratrol-a hormetic marvel in waiting? Hum. Exp. Toxicol. 29 2010 1026 1028
85. P. Pushparaj, C.H. Tan, and B.K.H. Tan Effects of Averrhoa bilimbi leaf extract on blood glucose and lipids in streptozotocin-diabetic rats J. Ethnopharmacol. 72 2000 69 76
86. S.V. Penumathsa, M. Thirunavukkarasu, S. Koneru, B. Juhasz, L. Zhan, and R. Pant Statin and resveratrol in combination induces cardioprotection against myocardial infarction in hypercholesterolemic rat J. Mol. Cell. Cardiol. 42 2007 508 516 (Pubitemid 46349117)
87. I.J. Cho, J.Y. Ahn, S. Kim, M.S. Choi, and T.Y. Ha Resveratrol attenuates the expression of HMG-CoA reductase mRNA in hamsters Biochem. Biophys. Res. Commun. 367 2008 190 194
88. J.N. Feige, M. Lagouge, and C. Canto Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation Cell Metab. 8 2008 347 358
89. M. Stefani, M.A. Markus, R.C. Lin, M. Pinese, I.W. Dawes, and B.J. Morris The effect of resveratrol on a cell model of human aging Ann. N.Y. Acad. Sci. 1114 2007 407 418 (Pubitemid 350070370)
90. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, K. Lewis, P.J. Pistell, S. Poosala, K.G. Becker, O. Boss, D. Gwinn, M. Wang, S. Ramaswamy, K.W. Fishbein, R.G. Spencer, E.G. Lakatta, D. Le Couteur, R.J. Shaw, P. Navas, P. Puigserver, D.K. Ingram, and R. de Cabo D.A.Sinclair, resveratrol improves health and survival of mice on a high-calorie diet Nature 16 2006 337 342 (Pubitemid 44764104)