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Published in: Metabolic Brain Disease 3/2015

01-06-2015 | Research Article

Blueberry treatment decreased D-galactose-induced oxidative stress and brain damage in rats

Authors: Jale Çoban, Işın Doğan-Ekici, A. Fatih Aydın, Esra Betül-Kalaz, Semra Doğru-Abbasoğlu, Müjdat Uysal

Published in: Metabolic Brain Disease | Issue 3/2015

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Abstract

D-galactose (GAL) causes aging-related changes and oxidative stress in the organism. We investigated the effect of whole fresh blueberry (BB) (Vaccinium corymbosum L.) treatment on oxidative stress in age-related brain damage model. Rats received GAL (300 mg/kg; s.c.; 5 days per week) alone or together with 5 % (BB1) and 10 % (BB2) BB containing chow for two months. Malondialdehyde (MDA),protein carbonyl (PC) and glutathione (GSH) levels, and Cu Zn-superoxide dismutase (SOD), glutathione peroxidase (GSH-Px) and glutathione transferase (GST) activities as well as acetylcholinesterase (AChE) activities were determined. Expressions of B cell lymphoma-2 (Bcl-2), Bax and caspase-3 were also evaluated in the brain by immunohistochemistry. MDA and PC levels and AChE activity increased, but GSH levels, SOD and GSH-Px activities decreased together with histopathological structural damage in the brain of GAL-treated rats. BB treatments, especially BB2 reduced MDA and PC levels and AChE activity and elevated GSH levels and GSH-Px activity. BB1 and BB2 treatments diminished apoptosis and ameliorated histopathological findings in the brain of GAL-treated rats. These results indicate that BB partially prevented the shift towards an imbalanced prooxidative status and apoptosis together with histopathological amelioration by acting as an antioxidant (radical scavenger) itself in GAL-treated rats.
Literature
go back to reference Anand KV, Jaabir MSM, Thomas PA, Geraldine P (2012) Protective role of chrysin against oxidative stress in D-galactose-induced aging in an experimental rat model. Geriatr Gerontol Int 12:741–750CrossRefPubMed Anand KV, Jaabir MSM, Thomas PA, Geraldine P (2012) Protective role of chrysin against oxidative stress in D-galactose-induced aging in an experimental rat model. Geriatr Gerontol Int 12:741–750CrossRefPubMed
go back to reference Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8:111–120CrossRefPubMed Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8:111–120CrossRefPubMed
go back to reference Aydın AF, Küçükgergin C, Ozdemirler-Erata G, Koçak-Toker N, Uysal M (2010) The effect of carnosine treatment on prooxidant-antioxidant balance in liver, heart and brain tissues of male aged rats. Biogerontology 11:103–109CrossRefPubMed Aydın AF, Küçükgergin C, Ozdemirler-Erata G, Koçak-Toker N, Uysal M (2010) The effect of carnosine treatment on prooxidant-antioxidant balance in liver, heart and brain tissues of male aged rats. Biogerontology 11:103–109CrossRefPubMed
go back to reference Banji D, Banji OJF, Dasaroju S, Kumar K (2013) Curcumin and piperine abrogate lipid and protein oxidation induced by galactose in rat brain. Brain Res 1515:1–11CrossRefPubMed Banji D, Banji OJF, Dasaroju S, Kumar K (2013) Curcumin and piperine abrogate lipid and protein oxidation induced by galactose in rat brain. Brain Res 1515:1–11CrossRefPubMed
go back to reference Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888PubMed Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888PubMed
go back to reference Bingül I, Başaran-Küçükgergin C, Tekkeşin MS, Olgaç V, Doğru-Abbasoğlu S, Uysal M (2013) Effect of blueberry pretreatment on diethylnitrosamine- induced oxidative stres and liver injury in rats. Environ Toxicol Pharmacol 36:529–538CrossRefPubMed Bingül I, Başaran-Küçükgergin C, Tekkeşin MS, Olgaç V, Doğru-Abbasoğlu S, Uysal M (2013) Effect of blueberry pretreatment on diethylnitrosamine- induced oxidative stres and liver injury in rats. Environ Toxicol Pharmacol 36:529–538CrossRefPubMed
go back to reference Çoban J, Betül-Kalaz E, Aydın AF, Doğan-Ekici I, Doğru-Abbasoğlu S, Uysal M (2014) Bluberry treatment attenuates D-galactose-induced oxidative stress and tissue damage in rat liver. Geriatr Gerontol Int 14:490–497CrossRefPubMed Çoban J, Betül-Kalaz E, Aydın AF, Doğan-Ekici I, Doğru-Abbasoğlu S, Uysal M (2014) Bluberry treatment attenuates D-galactose-induced oxidative stress and tissue damage in rat liver. Geriatr Gerontol Int 14:490–497CrossRefPubMed
go back to reference Çoban J, Evran B, Özkan F, Çevik A, Doğru-Abbasoğlu S, Uysal M (2013) The effect of blueberry feeding on lipids and oxidative stress in serum, liver and aorta of guinea pigs fed on high cholesterol diet. Biosci Biotechnol Biochem 77:389–391PubMed Çoban J, Evran B, Özkan F, Çevik A, Doğru-Abbasoğlu S, Uysal M (2013) The effect of blueberry feeding on lipids and oxidative stress in serum, liver and aorta of guinea pigs fed on high cholesterol diet. Biosci Biotechnol Biochem 77:389–391PubMed
go back to reference Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefPubMed Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefPubMed
go back to reference Giacalone M, DiSacco F, Traupe I, Topini R, Forfori F, Giunta F (2011) Antioxidant and neuroprotective properties of blueberry polyphenols: a critical review. Nutr Neurosci 14:119–125CrossRefPubMed Giacalone M, DiSacco F, Traupe I, Topini R, Forfori F, Giunta F (2011) Antioxidant and neuroprotective properties of blueberry polyphenols: a critical review. Nutr Neurosci 14:119–125CrossRefPubMed
go back to reference Goyarzu P, Malin DH, Lau FC, Taglialatela G, Moon WD, Jennings R, Moy E, Moy D, Lippold S, Shukitt-Hale B, Joseph JA (2004) Blueberry supplemented diet: effects on object recognition memory and nuclear factor-kappa B levels in aged rats. Nutr Neurosci 7:75–83CrossRefPubMed Goyarzu P, Malin DH, Lau FC, Taglialatela G, Moon WD, Jennings R, Moy E, Moy D, Lippold S, Shukitt-Hale B, Joseph JA (2004) Blueberry supplemented diet: effects on object recognition memory and nuclear factor-kappa B levels in aged rats. Nutr Neurosci 7:75–83CrossRefPubMed
go back to reference Habig WH, Jacoby WB (1981) Assays for differentation of glutathione s-transferases. Methods Enzymol 77:398–405CrossRefPubMed Habig WH, Jacoby WB (1981) Assays for differentation of glutathione s-transferases. Methods Enzymol 77:398–405CrossRefPubMed
go back to reference Hsia CH, Wang CH, Kuo YW, Ho YJ, Chen HL (2012) Fructo-oligosaccharide systemically diminished D-galactose-induced oxidative molecule damages in BALB/cJ mice. Br J Nutr 107:1787–1792CrossRefPubMed Hsia CH, Wang CH, Kuo YW, Ho YJ, Chen HL (2012) Fructo-oligosaccharide systemically diminished D-galactose-induced oxidative molecule damages in BALB/cJ mice. Br J Nutr 107:1787–1792CrossRefPubMed
go back to reference Hsieh HM, Wu WM, Hu ML (2009) Soy isoflavones attenuate oxidative stress and improve parameters related to aging and Alzheimer’s disease in C57BL/6 J mice treated with D-galactose. Food Chem Toxicol 47:625–632CrossRefPubMed Hsieh HM, Wu WM, Hu ML (2009) Soy isoflavones attenuate oxidative stress and improve parameters related to aging and Alzheimer’s disease in C57BL/6 J mice treated with D-galactose. Food Chem Toxicol 47:625–632CrossRefPubMed
go back to reference Joseph JA, Shukitt-Hale B, Casadesus G (2005) Reversing the deleterious effects of aging on neuronal communication and behavior: beneficial properties of fruit polyphenolic compounds. Am J Clin Nutr 81(1):313S–316SPubMed Joseph JA, Shukitt-Hale B, Casadesus G (2005) Reversing the deleterious effects of aging on neuronal communication and behavior: beneficial properties of fruit polyphenolic compounds. Am J Clin Nutr 81(1):313S–316SPubMed
go back to reference Kim H, Bartley GE, Rimando AM, Yokoyama W (2010) Hepatic gene expressions related to lower plasma cholesterol in hamsters fed high-fat diets supplemented with blueberry peels and peel extract. J Agric Food Chem 58:3984–3891CrossRefPubMed Kim H, Bartley GE, Rimando AM, Yokoyama W (2010) Hepatic gene expressions related to lower plasma cholesterol in hamsters fed high-fat diets supplemented with blueberry peels and peel extract. J Agric Food Chem 58:3984–3891CrossRefPubMed
go back to reference Krikorian R, Shidler MD, Nash TA, Kalt W, Vinqvist-Tymchuk S-HB, Joseph JA (2010) Blueberry supplementation improves memory in older adults. J Agric Food Chem 958:3996–4000CrossRef Krikorian R, Shidler MD, Nash TA, Kalt W, Vinqvist-Tymchuk S-HB, Joseph JA (2010) Blueberry supplementation improves memory in older adults. J Agric Food Chem 958:3996–4000CrossRef
go back to reference Lan Z, Liu J, Chen L, Fu Q, Luo J, Qu R, Kong L, Ma S (2012) Danggui-Shaoyao-San ameliorates cognition deficits and attenuates oxidative stress-related neuronal apoptosis in d-galactose-induced senescent mice. J Ethnopharmacol 141:386–395CrossRefPubMed Lan Z, Liu J, Chen L, Fu Q, Luo J, Qu R, Kong L, Ma S (2012) Danggui-Shaoyao-San ameliorates cognition deficits and attenuates oxidative stress-related neuronal apoptosis in d-galactose-induced senescent mice. J Ethnopharmacol 141:386–395CrossRefPubMed
go back to reference Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium–deficient rat liver. Biochem Biophys Res Commun 71:952–958CrossRefPubMed Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium–deficient rat liver. Biochem Biophys Res Commun 71:952–958CrossRefPubMed
go back to reference Liu LC, Wang CJ, Lee CC, Su SC, Chen HL, Hsu JD, Lee HJ (2010) Aqueous extract of Hibiscus sabdariffa L. decelerates acetaminophen-induced acute liver damage by reducing cell death and oxidative stress in mouse experimental models. J Sci Food Agric 90:329–337CrossRefPubMed Liu LC, Wang CJ, Lee CC, Su SC, Chen HL, Hsu JD, Lee HJ (2010) Aqueous extract of Hibiscus sabdariffa L. decelerates acetaminophen-induced acute liver damage by reducing cell death and oxidative stress in mouse experimental models. J Sci Food Agric 90:329–337CrossRefPubMed
go back to reference Malin DH, Lee DR, Goyarzu P, Chang YH, Ennis LJ, Beckett E, Shukitt-Hale B, Joseph JA (2011) Short-term blueberry-enriched diet prevents and reverses object recognition memory loss in aging rats. Nutrition 27:338–342CrossRefPubMed Malin DH, Lee DR, Goyarzu P, Chang YH, Ennis LJ, Beckett E, Shukitt-Hale B, Joseph JA (2011) Short-term blueberry-enriched diet prevents and reverses object recognition memory loss in aging rats. Nutrition 27:338–342CrossRefPubMed
go back to reference Mao Z, Zheng YL, Zhang YQ, Han BP, Zhu XW, Chang Q, Hu XB (2007) The anti-apoptosis effects of daidzein in the brain of D-galactose treated mice. Molecules 12:1455–1470CrossRefPubMed Mao Z, Zheng YL, Zhang YQ, Han BP, Zhu XW, Chang Q, Hu XB (2007) The anti-apoptosis effects of daidzein in the brain of D-galactose treated mice. Molecules 12:1455–1470CrossRefPubMed
go back to reference Milbury PE, Kalt W (2010) Xenobiotic metabolism and berry flavonoid transport across the blood–brain barrier. J Agric Food Chem 58:3950–3956CrossRefPubMed Milbury PE, Kalt W (2010) Xenobiotic metabolism and berry flavonoid transport across the blood–brain barrier. J Agric Food Chem 58:3950–3956CrossRefPubMed
go back to reference Mylorie AA, Collins H, Umbles C, Kyle J (1986) Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 82:512–520CrossRef Mylorie AA, Collins H, Umbles C, Kyle J (1986) Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 82:512–520CrossRef
go back to reference Neto CC (2007) Cranberry and blueberry: evidence for protective effects against cancer and vascular diseases. Mol Nutr Food Res 51:652–664CrossRefPubMed Neto CC (2007) Cranberry and blueberry: evidence for protective effects against cancer and vascular diseases. Mol Nutr Food Res 51:652–664CrossRefPubMed
go back to reference Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefPubMed Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefPubMed
go back to reference Papandreou MA, Dimakopoulou A, Linardaki ZI, Cordopatis P, Klimis-Zacas D, Margarity M, Lamari FN (2009) Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav Brain Res 198:352–358CrossRefPubMed Papandreou MA, Dimakopoulou A, Linardaki ZI, Cordopatis P, Klimis-Zacas D, Margarity M, Lamari FN (2009) Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav Brain Res 198:352–358CrossRefPubMed
go back to reference Parıldar-Karpuzoğlu H, Mehmetçik G, Özdemirler-Erata G, Doğru-Abbasoğlu S, Koçak-Toker N, Uysal M (2008) The effect of taurine treatment on prooxidant-antioxidant balance in livers and brains of old rats. Pharmacol Rep 60:673–678PubMed Parıldar-Karpuzoğlu H, Mehmetçik G, Özdemirler-Erata G, Doğru-Abbasoğlu S, Koçak-Toker N, Uysal M (2008) The effect of taurine treatment on prooxidant-antioxidant balance in livers and brains of old rats. Pharmacol Rep 60:673–678PubMed
go back to reference Peng C, Zuo Y, Kwan KM, Liang Y, Ma KY, Chan HYE, Huang Y, Yu H, Chen ZY (2012) Blueberry extract prolongs lifespan of Drosophila melanogaster. Exp Gerontol 47:170–178CrossRefPubMed Peng C, Zuo Y, Kwan KM, Liang Y, Ma KY, Chan HYE, Huang Y, Yu H, Chen ZY (2012) Blueberry extract prolongs lifespan of Drosophila melanogaster. Exp Gerontol 47:170–178CrossRefPubMed
go back to reference Prakash A, Kumar A (2013) Pioglitazone alleviates the mitochondrial apoptotic pathway and mito-oxidative damage in the d-galactose-induced mouse model. Clin Exp Pharmacol Physiol 40:644–651CrossRefPubMed Prakash A, Kumar A (2013) Pioglitazone alleviates the mitochondrial apoptotic pathway and mito-oxidative damage in the d-galactose-induced mouse model. Clin Exp Pharmacol Physiol 40:644–651CrossRefPubMed
go back to reference Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363CrossRefPubMed Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363CrossRefPubMed
go back to reference Ruan Q, Hu X, Ao H, Ma H, Gao Z, Liu F, Kong D, Bao Z, Yu Z (2014) The neurovascular protective effects of huperzine A on D-galactose-induced inflammatory damage in the rat hippocampus. Gerontology (In press) Ruan Q, Hu X, Ao H, Ma H, Gao Z, Liu F, Kong D, Bao Z, Yu Z (2014) The neurovascular protective effects of huperzine A on D-galactose-induced inflammatory damage in the rat hippocampus. Gerontology (In press)
go back to reference Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefPubMed Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefPubMed
go back to reference Tsai SJ, Yin MC (2012) Anti-oxidative, anti-glycativeand anti-apoptotic effects of oleanolic acid in brain of mice treated by D-galactose. Eur J Pharmacol 689:81–88CrossRefPubMed Tsai SJ, Yin MC (2012) Anti-oxidative, anti-glycativeand anti-apoptotic effects of oleanolic acid in brain of mice treated by D-galactose. Eur J Pharmacol 689:81–88CrossRefPubMed
go back to reference Wang Y, Chang CF, Chou J, Chen HL, Deng X, Harvey BK, Cadet JL, Bickford PC (2005) Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage. Exp Neurol 193:75–84CrossRefPubMed Wang Y, Chang CF, Chou J, Chen HL, Deng X, Harvey BK, Cadet JL, Bickford PC (2005) Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage. Exp Neurol 193:75–84CrossRefPubMed
go back to reference Wilson MA, Shukitt-Hale B, Kalt W, Ingram DK, Joseph JA, Wolkow CA (2006) Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell 5:59–68CrossRefPubMedCentralPubMed Wilson MA, Shukitt-Hale B, Kalt W, Ingram DK, Joseph JA, Wolkow CA (2006) Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell 5:59–68CrossRefPubMedCentralPubMed
go back to reference Wu W, Wang X, Xiang Q, Meng X, Peng Y, Du N, Liu Z, Sun Q, Wang C, Liu X (2014) Astaxanthin alleviates brain aging in rats by attenuating oxidative stress and increasing BDNF levels. Food Funct 5:158–166CrossRefPubMed Wu W, Wang X, Xiang Q, Meng X, Peng Y, Du N, Liu Z, Sun Q, Wang C, Liu X (2014) Astaxanthin alleviates brain aging in rats by attenuating oxidative stress and increasing BDNF levels. Food Funct 5:158–166CrossRefPubMed
go back to reference Xian YF, Lin ZX, Zhao M, Mao QQ, Ip SP, Che CT (2011) Uncaria rhynchophylla ameliorates cognitive deficits induced by D-galactose in mice. Planta Med 77:1977–1983CrossRefPubMed Xian YF, Lin ZX, Zhao M, Mao QQ, Ip SP, Che CT (2011) Uncaria rhynchophylla ameliorates cognitive deficits induced by D-galactose in mice. Planta Med 77:1977–1983CrossRefPubMed
go back to reference Yang YC, Lin HY, Su KY, Chen CH, Yu YL, Lin CC, Yu SL, Yan HY, Su KJ, Chen YL (2012) Rutin, a flavonoid that is a main component of saussurea involucrata, attenuates the senescence effect in D-galactose aging mouse model. Evid Based Complement Alternat Med 2012:980276PubMedCentralPubMed Yang YC, Lin HY, Su KY, Chen CH, Yu YL, Lin CC, Yu SL, Yan HY, Su KJ, Chen YL (2012) Rutin, a flavonoid that is a main component of saussurea involucrata, attenuates the senescence effect in D-galactose aging mouse model. Evid Based Complement Alternat Med 2012:980276PubMedCentralPubMed
go back to reference Zafra-Stone S, Yasmin T, Bagchi M, Chatterjee A, Vinson JA, Bagchi D (2007) Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol Nutr Food Res 51:675–683CrossRefPubMed Zafra-Stone S, Yasmin T, Bagchi M, Chatterjee A, Vinson JA, Bagchi D (2007) Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol Nutr Food Res 51:675–683CrossRefPubMed
go back to reference Zhang WW, Sun QX, Liu YH, Gao W, Li YH, Lu K, Wang Z (2011) Chronic administration of Liu Wei Dihuang protects rat’s brain against D-galactose-induced impairment of cholinergic system. Acta Physiol Sin 63:245–255 Zhang WW, Sun QX, Liu YH, Gao W, Li YH, Lu K, Wang Z (2011) Chronic administration of Liu Wei Dihuang protects rat’s brain against D-galactose-induced impairment of cholinergic system. Acta Physiol Sin 63:245–255
go back to reference Zhang X, Jin C, Li Y, Guan S, Han F, Zhang S (2013) Catalpol improves cholinergic function and reduces inflammatory cytokines in the senescent mice induced by D-galactose. Food Chem Toxicol 58:50–55CrossRefPubMed Zhang X, Jin C, Li Y, Guan S, Han F, Zhang S (2013) Catalpol improves cholinergic function and reduces inflammatory cytokines in the senescent mice induced by D-galactose. Food Chem Toxicol 58:50–55CrossRefPubMed
go back to reference Zhong SZ, Ge QH, Qu R, Li Q, Ma SP (2009) Paeonol attenuates neurotoxicity and ameliorates cognitive impairment induced by d-galactose in ICR mice. J Neurol Sci 277:58–64CrossRefPubMed Zhong SZ, Ge QH, Qu R, Li Q, Ma SP (2009) Paeonol attenuates neurotoxicity and ameliorates cognitive impairment induced by d-galactose in ICR mice. J Neurol Sci 277:58–64CrossRefPubMed
Metadata
Title
Blueberry treatment decreased D-galactose-induced oxidative stress and brain damage in rats
Authors
Jale Çoban
Işın Doğan-Ekici
A. Fatih Aydın
Esra Betül-Kalaz
Semra Doğru-Abbasoğlu
Müjdat Uysal
Publication date
01-06-2015
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 3/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-014-9643-z

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