Cellular and Molecular Neurobiology

, Volume 33, Issue 8, pp 1123–1133 | Cite as

Effect of Chronic Treatment with Conventional and Organic Purple Grape Juices (Vitis labrusca) on Rats Fed with High-Fat Diet

  • Marcia Gilceane Cardozo
  • Niara Medeiros
  • Denise dos Santos Lacerda
  • Daniela Campos de Almeida
  • João Antônio Pegas Henriques
  • Caroline Dani
  • Cláudia Funchal
Original Research

Abstract

Serra Gaucha is described as the most important wine region of Brazil. Regarding cultivars widespread in the Serra Gaucha, about 90 % of the area is occupied by vines of Vitis labrusca that is the most important specie used in grape juice production. The objective of this study was to investigate the antioxidant and neuroprotective effect of chronic intake of purple grape juice (organic and conventional) from Bordo variety (V. labrusca) on oxidative stress in different brain regions of rats supplemented with high-fat diet (HFD) for 3 months. A total of 40 male rats were randomly divided into 4 groups. Group 1 received a standard diet and water, group 2 HFD and water, group 3 HFD and conventional grape juice (CGJ), and group 4 HFD and organic grape juice (OGJ). All groups had free access to food and drink and after 3 months of treatment the rats were euthanized by decapitation and the cerebral cortex, hippocampus and cerebellum isolated and homogenized on ice for oxidative stress analysis. We observed that the consumption of calories in HFD and control groups, were higher than the groups supplemented with HFD and grape juices and that HFD diet group gain more weight than the other animals. Our results also demonstrated that HDF enhanced lipid peroxidation (TBARS) and protein damage (carbonyl) in cerebral cortex and hippocampus, reduced the non-enzymatic antioxidants defenses (sulfhydryl) in cerebral cortex and cerebellum, reduced catalase and superoxide dismutase activities in all brain tissues and enhanced nitric oxide production in all cerebral tissues. CGJ and OGJ were able to ameliorate these oxidative alterations, being OGJ more effective in this protection. Therefore, grape juices could be useful in the treatment of some neurodegenerative diseases associated with oxidative damage.

Keywords

Antioxidants Grapes Vitis labrusca High-fat diet 

References

  1. Abeywardena MY, Leifert WR (2008) Cardioprotective actions of grape polyphenols. Nutr. Res. 28:729–737PubMedCrossRefGoogle Scholar
  2. Aebi H (1984) Catalase in vitro. Method Enzymol. 105:121–126CrossRefGoogle Scholar
  3. Aksenov MY, Markesberry WR (2001) Change in thiol content and expression of glutathione redox system gene in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett 302:141–145PubMedCrossRefGoogle Scholar
  4. Amin K, Kamel H, Eltawab M (2011) The relation of high fat diet, metabolic disturbances and brain oxidative dysfunction: modulation by hydroxy citric acid. Lipids Health Dis. 10:74PubMedCrossRefGoogle Scholar
  5. AOAC (Association Official Agriculture Chemistry) (1998) Official methods of analysis of AOAC international, 16, 4th edn. AOAC, ArlingtonGoogle Scholar
  6. Balu M, Snageetha P, Murali G, Pannneerselvam C (2005) Age-related oxidative protein damage in central nervous system of rats: modulatory role of grape seed extract. Int J Dev Neurosci 23:501–507PubMedCrossRefGoogle Scholar
  7. Banas SM, Rouch C, Kassis N, Markaki EM, Gerozissis K (2009) A dietary fat excess alters metabolic and neuroendocrine responses before the onset of metabolic diseases. Cell Mol Neurobiol 29:157–168PubMedCrossRefGoogle Scholar
  8. Bannister JV, Calabrese L (1987) Assays for SOD. Method. Biochem. Anal. 32:79–312Google Scholar
  9. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu V, Allard J, Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Couter DL, Shaw RJ, Navas P, Puigserver P, Ingram DK, Abo R, Sinclair D (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342PubMedCrossRefGoogle Scholar
  10. Behl C, Moosmann B (2002) Oxidative nerve cell death in Alzheimer’s disease and stroke: antioxidants as neuroprotective compounds. Biol. Chem. 383:521–536PubMedCrossRefGoogle Scholar
  11. Berg D, Youdim MB (2006) Role of iron in neurodegenerative disorders. Top. Magn. Reson. Imaging. 17:5–17PubMedCrossRefGoogle Scholar
  12. Bogdanov MB, Andreassen OA, Dedeoglu A, Ferrante RJ, Beal MF (2001) Increased oxidative damage to DNA in a transgenic mouse of Huntington’s disease. J Neurochem 79:1246–1249PubMedCrossRefGoogle Scholar
  13. Boqué N, Campión J, de La Iglesia R, de La Garza AL, Milagro FI, Roman BS, Bañuelos O, Martínez JA (2012) Screening of polyphenolic plant extracts for anti-obesity properties in Wistar rats. J Sci Food Agric. doi:10.1002/jsfa.5884 PubMedGoogle Scholar
  14. Burin MV, Falcão LD, Gonzaga LV, Fett R, Rosier JP, Bordignon-Luiz MT (2010) Colour, phenolic content and antioxidant activity of grape juice. Ciênc. tecnol. aliment. 30:1027–1032CrossRefGoogle Scholar
  15. Carbonaro M, Mattera M, Nicoli S, Bergamo P, Cappelloni M (2002) Modulation of antioxidant compounds in organic vs conventional fruit (Peach, Prumus persica L., and Pear, Pyrus communis L.). J Agric Food Chem 50:5458–5462PubMedCrossRefGoogle Scholar
  16. Castilla P, Echarri R, Dávalos A, Cerrato F, Ortega H, Teruel JL, Lucas MF, Gómez-Coronado D, Ortuño J, Lasunción MA (2006) Concentrated red grape juice exerts antioxidant, hypolipidemic, and antiinflammatory effects in both hemodialysis patients and healthy subjects. Am J Clin Nutr 84:252–262PubMedGoogle Scholar
  17. Dani C, Oliboni LS, Vanderlinde R, Bonatto D, Salvador M, Henriques JAP (2007) Phenolic content and antioxidant activities of white and purple juices manufactured with organically- or conventionally-produced grapes. Food Chem Toxicol 45:2574–2580PubMedCrossRefGoogle Scholar
  18. Dani C, Pasquali MAB, Oliveira MR, Umezu FM, Salvador M, Henriques JAP, Moreira JCF (2008) Protective effects of purple grape juice on carbon tetrachloride-induced oxidative stress in brains of adult Wistar rats. J Med Food 11:55–61PubMedCrossRefGoogle Scholar
  19. Dani C, Oliboni L, Umezu F, Salvador M, Moreira JC, Henriques JA (2009) Antioxidant and antigenotoxic activities of purple grape juice organic and conventional in adult rats. J Med Food 12:1111–1118PubMedCrossRefGoogle Scholar
  20. Dani C, Oliboni LS, Pra D, Bonatto D, Santos CEI, Yoneama ML, Dias JF, Salvador M, Henriques JAP (2012) Mineral content is related to antioxidant and antimutagenic properties of grape juice. GMR 41:3154–3163CrossRefGoogle Scholar
  21. Day AP, Kemp HJ, Bolton C, Hartog M, Stansbie D (1997) Effect of concentrated red grape juice consumption on serum antioxidant capacity and low-density lipoprotein oxidation. Ann Nutr Metab 41:353–357PubMedCrossRefGoogle Scholar
  22. Du Z, Yang Y, Hu Y, Sun Y, Zhang S, Peng W, Zhong Y, Huang X, Kong W (2012) A long-term high-fat diet increases oxidative stress, mitochondrial damage and apoptosis in the inner ear of d-galactose-induced aging rats. Hearing Res. 287:15–24CrossRefGoogle Scholar
  23. Dulloo AG, Duret C, Rohrer D, Girardier L, Mensi N, Fathi M, Chantre P, Vandermander J (1999) Efficacy of a green tea extract rich in catechin polyphenols and caffeine in increasing 24-h energy expenditure and fat oxidation in humans. Am J Clin Nutr 70:1040–1045PubMedGoogle Scholar
  24. Durak I, Avci A, Kaçmaz M, Büyükkoçak S, Cimen MY, Elgün S, Oztürk HS (1999) Comparison of antioxidant potentials of red wine, white wine, grape juice and alcohol. Curr Med Res Opin 15:316–320PubMedCrossRefGoogle Scholar
  25. Emiliano AF, de Carvalho LC, da Silva C, Cordeiro V, da Costa CA, de Oliveira PB, Queiroz EF, Moreira DD, Boaventura GT, de Moura RS, Resende AC (2011) Metabolic disorders and oxidative stress programming in offspring of rats fed a high-fat diet during lactation: effects of a Vinifera grape skin (ACH 09) extract. J. Cardiovasc. Pharm. 58:319–328CrossRefGoogle Scholar
  26. Estadella D, Oyama L, Dâmaso A, Ribeiro E, Nascimento C (2004) Effect of palatable hyperlipidic diet on lipid metabolism of sedentary and exercised rats. Nutrition. 20:218–224PubMedCrossRefGoogle Scholar
  27. Fachinetto R, Burger ME, Wagner C, Wondracek DC, Brito VB, Nogueira CW, Ferreira J, Rocha JBT (2005) High fat diet increases the incidence of orofacial dyskinesia and oxidative stress in specific brain regions of rats. Pharmacol. Biochem. Behav. 81:585–592PubMedCrossRefGoogle Scholar
  28. Fernández-Fernández L, Comes G, Bolea I, Valente T, Ruiz J, Murtra P, Ramirez B, Anglés N, Reguant J, Morelló JR, Boada M, Hidalgo J, Escorihuela RM, Unzeta M (2012) LMN diet, rich in polyphenols and polyunsaturated fatty acids, improves mouse cognitive decline associated with aging and Alzheimer’s disease. Behav Brain Res 228:261–271PubMedCrossRefGoogle Scholar
  29. Fontana L, Klein S (2007) Aging, adiposity, and calorie restriction. JAMA 297:986–994PubMedCrossRefGoogle Scholar
  30. Frankel EN, Bosanek CA, Meyer AS, Silliman K, Kirk LL (1998) Commercial grape Juices inhibit the in vitro oxidation of human low density lipoproteins. J. Agric Food Chem. 46:834–838CrossRefGoogle Scholar
  31. Fuleki T, Ricardo-da-Silva JM (2003) Effects of cultivar and processing method on the contents of catechins and procyanidins in grape juice. J. Agric. Food. Chem. 51:640–646PubMedCrossRefGoogle Scholar
  32. Funchal C, Carvalho CAS, Gemelli T, Centeno AS, Guerra RB, Salvador M, Dani C, Coitinho A, Gomez R (2010) Effect of acute administration of 3-butyl-1-phenyl-2-(phenyltelluro)oct-en-1-one on oxidative stress in cerebral cortex, hippocampus, and cerebellum of rats. Cell Mol Neurobiol 30:1135–1142PubMedCrossRefGoogle Scholar
  33. Ghalami J, Zardooz H, Rostamkhani F, Farrokhi B, Hedayati M (2011) High-fat diet did not change metabolic response to acute stress in rats. EXCLI J 10:205–217Google Scholar
  34. Gollücke A, Catharino R, Souza J, Eberlin A, Tavares D (2008) Evolution of major phenolic components and radical scavenging activity of grape juices through concentration process and storage. Food Chem 112:868–873CrossRefGoogle Scholar
  35. Grundy S, Chair J, Stephen R, Donato KA, Eckel RH, Franclin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome. Circulation 112:285–290CrossRefGoogle Scholar
  36. Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18:685–716PubMedCrossRefGoogle Scholar
  37. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634–1658PubMedCrossRefGoogle Scholar
  38. Halliwell B, Gutteridge JMC (2007) Measurement of reactive species. In: Free radicals in biology and medicine, 4th edn. Oxford University Press, New York pp 268–340Google Scholar
  39. Han YS, Zheng WH, Bastianetto S, Chabot JG, Quirion R (2004) Neuroprotective effects of resveratrol against β-amyloid-induced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C. Br J. Pharmacol. 141:997–1005PubMedCrossRefGoogle Scholar
  40. Hatcher JF, Adibhatla RM (2008) Altered lipid metabolism in brain injury and disorders. Subcell Biochem 49:241–268PubMedCrossRefGoogle Scholar
  41. Hevel JM, Marletta MA (1994) Nitric oxide synthase assays. Methods Enzymol. 233:250–258PubMedCrossRefGoogle Scholar
  42. Hollis JH, Houchins JA, Blumberg JB, Mattes RD (2009) Effects of concord grape juice on appetite, diet, body weight, lipid profile, and antioxidant status of adults. J Am Col Nut 28:574–582Google Scholar
  43. Hsu TF, Kusumoto A, Abe K, Hosoda K, Kiso Y, Wang MF, Yamamoto S (2006) Polyphenol-enriched oolong tea increases fecal lipid excretion. Eur J Clin Nutr 60:1330–1336PubMedCrossRefGoogle Scholar
  44. Ischiropoulos H, Zhu L, Chen J, Tsai M, Martin JC, Smith CD, Beckman JS (1992) Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 298:431–437PubMedCrossRefGoogle Scholar
  45. Kalmijn S (2000) Fatty acid intake and the risk of dementia and cognitive decline: a review of clinical and epidemiological studies. J. Nutr. Health Aging. 4:202–207PubMedGoogle Scholar
  46. Kann O, Kovacs R (2007) Mitochondria and neuronal activity. Am. J. of Physiol. Cell Physiol. 292:641–657CrossRefGoogle Scholar
  47. Kataoka K, Takashima S, Shibata E, Hoshino E (2004) Body fat reduction by the long-term intake of catechins and the effects of physical activity. Prog Med. 24:3358–3370Google Scholar
  48. Kondrashov A, Sevcik R, Benakova H, Kostirova M, Stípek S (2009) The key role of grape variety or antioxidant capacity of red wine. J Clin. Nutr. Metab 4:41–46Google Scholar
  49. Lamuela-Raventos RM, Waterhouse AL (1994) Direct HPLC separation of wine phenolics. Am J Enol Vitic 45:1–5Google Scholar
  50. Lau F, Shukitt H, Joseph J (2005) The beneficial effects of fruit polyphenols on brain aging. Neurobiol Aging 26:128–132PubMedCrossRefGoogle Scholar
  51. Lehtinen MK, Bonni A (2006) Modeling oxidative stress in the central nervous system. Curr Mol Med 6:871–881PubMedCrossRefGoogle Scholar
  52. Li S, Pu XP (2011) Neuroprotective effect of kaempferol against a 1-methyl-4-phenyl-1-1,2,3,6-tetrahydropyridine-induced mouse model of Parkinson’s disease. Biol Pharm Bull 34:1291–1296PubMedCrossRefGoogle Scholar
  53. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–267PubMedGoogle Scholar
  54. Mandel SA, Amit T, Weinreb O, Reznichenko L, Youdim MBH (2008) Simultaneous manipulation of multiple brain target by green tea catechins: a potential neuroprotective strategy for Alzheimer’s and Parkinsons diseases. CNS Neurosci Ther 14:352–365PubMedCrossRefGoogle Scholar
  55. McMurtrey KD, Minn J, Pobanz K, Schultz TP (1994) Analysis of wines for resveratrol using direct injection high-pressure liquid chromatography with electrochemical detection. J. Agric Food Chem. 42:2077–2080CrossRefGoogle Scholar
  56. Medeiros MC, Mello A, Gemelli T, Teixeira C, de Almeida M, de Andrade RB, Wannmacher CMD, Guerra RB, Gomez R, Funchal C (2012) Effect of chronic administration of the vinyl chalcogenide 3-methyl-1-phenyl-2-(phenylseleno)oct-2-en-1-one on oxidative stress in different brain areas of rats. Neurochem Res 37:928–934PubMedCrossRefGoogle Scholar
  57. Mielke J, Nicolitch K, Avellaneda V, Earlam K, Ahuja T, Mealing G, Messier C (2006) Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice. Behav Brain Res 175:374–382PubMedCrossRefGoogle Scholar
  58. Molteni R, Barnard R, Ying Z, Roberts C, Gomez F (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112:03–814CrossRefGoogle Scholar
  59. Moses GSD, Jensen MD, Lue L, Walker DG, Sun AY, Simonyi A, Sun GY (2006) Secretory PLA2-IIA: a new inflammatory factor for Alzheimer’s disease. J Neuroinflamm 3:28CrossRefGoogle Scholar
  60. Office International de la Vigne et du Vin (2003). HPLC-determination of nine major anthocyanins in red and rose wine. Resolution OENO 22/2003Google Scholar
  61. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358PubMedCrossRefGoogle Scholar
  62. Osman HE, Maalej N, Shanmuganayagam D, Folts JD (1998) Grape juice but not orange or grapefruit juice inhibits platelet activity in dogs and monkeys (Macaca fasciularis). J Nutr 128:2307–2312PubMedGoogle Scholar
  63. Ozyurt H, Olmez I (2012) Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 60:208–212PubMedCrossRefGoogle Scholar
  64. Park KY, Park E, Kim JS, Kang MH (2003) Daily grape juice consumption reduces oxidative DNA damage and plasma free radical levels in healthy Koreans. Mutat Res 529:77–86PubMedCrossRefGoogle Scholar
  65. Park HJ, Jung UJ, Lee MK, Cho SJ, Jung HK, Hong JH, Park YB, Kim SR, Shim S, Jung J, Choi MS (2012) Modulation of lipid metabolism by polyphenol-rich grape skin extract improves liver steatosis and adiposity in high fat fed mice. Mol Nutr Food Res. doi:10.1002/mnfr.201200447 Google Scholar
  66. Peters U, Poole C, Arab L (2001) Does tea affect cardiovascular disease? A meta-analysis. Am J Epidemiol 154:495–503PubMedCrossRefGoogle Scholar
  67. Puglielli L (2007) Aging of the brain, neurotrophin signaling, and Alzheimer’s disease: is IGF1-R the common culprit? Neurobiol Aging 29:795–811PubMedCrossRefGoogle Scholar
  68. Raval AP, Dave KR, Pinzón MAP (2006) Resveratrol mimics ischemic preconditioning in the brain. J Cereb Blood Flow Metab 26:1141–1147PubMedGoogle Scholar
  69. Reznick AZ, Packer L (1994) Carbonyl assay for determination of oxidatively modified proteins. Methods Enzymol. 233:357–363PubMedCrossRefGoogle Scholar
  70. Ribeiro MCP, Barbosa NBV, de Almeida TM, Parcianello LM, Perottoni J, de Ávila DS, Rocha JBT (2009) High-fat diet and hydrochlorothiazide increase oxidative stress in brain of rats. Cell Biochem Funct 27:473–478PubMedCrossRefGoogle Scholar
  71. Robb EL, Winkelmolen L, Visanji N, Brotchie J, Stuart JA (2008) Dietary resveratrol administration increases MnSOD expression and activity in mouse brain. Biochem Biophys Res Commun 372:254–259PubMedCrossRefGoogle Scholar
  72. Rodrigues AD, Scheffel TB, Scola G, Santos MT, Fank B, de Freitas SC, Dani C, Vanderlinde R, Henriques JA, Coitinho AS, Salvador M (2012) Neuroprotective and anticonvulsant effects of organic and conventional purple grape juices on seizures in Wistar rats induced by pentylenetetrazole. Neurochem Int 60:799–805PubMedCrossRefGoogle Scholar
  73. Rodriguez EM, Casajeros MJ, Canals S, de Bernardo S, Mena MA (2012) Thiolic antioxidants protect from nitric oxide induced toxicity in fetal midbrain cultures. Neuropharmacology 43:877–888CrossRefGoogle Scholar
  74. Rumpler W, Seale J, Clevidence B, Judd J, Wiley E, Yamamoto S, Komatsu T, Sawaki T, Ishikura Y, Hosoda K (2001) Oolong tea increases metabolic rate and fat oxidation in men. J Nutr 131:2848–2852PubMedGoogle Scholar
  75. Scola G, Conte D, Spada PWD, Dani C, Vanderlinde R, Funchal C, Salvador M (2010) Flavan-3-ol compounds from wine wastes with in vitro and in vivo antioxidant activity. Nutrients. 2:1048–1059PubMedCrossRefGoogle Scholar
  76. Sies H (1991) Oxidative stress: from basic research to clinical application. Am J Med 91:31–38CrossRefGoogle Scholar
  77. Silver HJ, Dietrich MS, Niswender KD (2011) Effects of grapefruit, grapefruit juice and water preloads on energy balance, weight loss, body composition, and cardiometabolic risk in free-living obese adults. Nutr Metab 8:8. doi:10.1186/1743-7075-8-8 CrossRefGoogle Scholar
  78. Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteau reagent. In: Packer L (ed) Methods in enzymology, oxidant and antioxidants, 541 Part A edn. Academic Press, San Diego, pp 159–178Google Scholar
  79. Sinha K, Chaudhary G, Gupta YK (2002) Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion modelo of stroke in rats. Life Sci 71:655–665PubMedCrossRefGoogle Scholar
  80. Solfrizzi V, Panza F, Capurso A (2003) The role of diet in cognitive decline. J Neural Transm Gen Sect 110:95–110Google Scholar
  81. Soulis G, Kitraki E, Gerozissis K (2005) Early neuroendocrine alterations in female rats following a diet moderately enriched in fat. Cell Mol Neurobiol 25:869–880PubMedCrossRefGoogle Scholar
  82. Stamler JS, Toone EJ (2002) The decomposition of thionitrites. Curr Opin Chem Biol 6:779–785PubMedCrossRefGoogle Scholar
  83. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84PubMedCrossRefGoogle Scholar
  84. Venables MC, Hulston CJ, Cox HR, Jeukendrup AE (2008) Green tea extract ingestion, fat oxidation, and glucose tolerance in healthy humans. Am J Clin Nutr 87:778–784PubMedGoogle Scholar
  85. Venturini CD, Merlo S, Souto AA, Fernandes MC, Gomez R, Rhoden CR (2011) Resveratrol and red wine function as antioxidants in the central nervous system without cellular proliferative effects during experimental diabetes. Oxid Med Cell Longev. 6:434–441Google Scholar
  86. Vingtdeux V, Werringloer UD, Zhao H, Davies P, Marambaud P (2008) Therapeutic potential of resveratrol in Alzheimer’s disease. BMC Neurosci 9:6CrossRefGoogle Scholar
  87. Xia N, Daiber A, Habermeier A, Closs EI, Thum T, Spanier G, Lu Q, Oelze M, Torzewski M, Lackner KJ, Munzel T, Forstermann U, Li H (2010) Resveratrol reverses endothelial nitric-oxide synthase uncoupling in apolipoprotein E knockout mice. J Pharmacol Exp Ther 335:149–154PubMedCrossRefGoogle Scholar
  88. Yamakura F, Matsumoto T, Ikedal K, Taka H, Fujimura T, Murayama K, Watanabe E, Tamaki M, Imai T, Takamori K (2005) Nitrated and oxidized products of a single tryptophan residue in human Cu, Zn-superoxide dismutase treated with either peroxynitritecarbon dioxide or myeloperoxidase-hydrogen peroxide-nitrite. J Biochem 138:57–69PubMedCrossRefGoogle Scholar
  89. Zern TL, Fernandez ML (2005) Cardioprotective effect of dietary of polyphenols. J Nutr 135:1911–1917PubMedGoogle Scholar
  90. Zhong L, Furne JK, Levitt MD (2006) An extract of black, green, and mulberry teas causes malabsorption of carbohydrate but not of triacylglycerol in healthy volunteers. Am J Clin Nutr 84:551–555PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Marcia Gilceane Cardozo
    • 1
  • Niara Medeiros
    • 1
  • Denise dos Santos Lacerda
    • 1
  • Daniela Campos de Almeida
    • 1
  • João Antônio Pegas Henriques
    • 2
    • 3
  • Caroline Dani
    • 1
  • Cláudia Funchal
    • 1
  1. 1.Centro Universitário Metodista do IPAPorto AlegreBrazil
  2. 2.Departamento de Biofísica, Centro de BiotecnologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.Instituto de BiotecnologiaUniversidade de Caxias do SulCaxias do SulBrazil

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