Abstract
The aim of this study was to investigate the potential protective effect of Lycium barbarum polysaccharides (LBP) pretreatment against cadmium (Cd)-induced hepatotoxicity in rats. Wistar rats were divided into control group, LBP group (300 mg/kg orally, once a day, for 30 days), Cd group (CdCl2 4 mg/kg i.p. once), and LBP + Cd group (LBP 300 mg/kg orally, once a day, for 30 days + CdCl2 4 mg/kg i.p. 24 h after the last treatment). Cd liver injury was examined by morphological/histological changes, transaminases, total protein concentration, and oxidative stress evaluated by MDA, 3NT, GSH, SOD, and TEAC activities. Cd intoxication caused gross morphological changes with hyperemia of the parenchyma, increased volume, and disappearance of the anatomical limits of the lobes associated with an increase of ALT, GSH, and TEAC in plasma and a decrease of MDA, GSH, and TEAC in liver, SOD, and total proteins in plasma. LBP pretreatment caused a slight improvement in the histological architecture and in the 3NT amount together with a significant improvement of hematic parameters. On the basis of the obtained results, we can affirm that LBP pretreatment can ameliorate liver conditions, but further studies are needed to better evaluate the protective antioxidant effects of LBP against Cd-induced toxicity.
Similar content being viewed by others
References
Abdel Moneim AE, Dkhi MA, Al-Quraishy S (2011) The protective effect of flaxseed oil on lead acetate-induced renal toxicity in rats. J Hazard Mater 194:250–255
Ahsan H (2013) 3-Nitrotyrosine: a biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions. Hum Immunol 74:1392–1399
Alghasham A, Salem TA, Meki AM (2013) Effect of cadmium-polluted water on plasma levels of tumor necrosis factor-a, interleukin-6 and oxidative status biomarkers in rats: protective effect of curcumin. Food Chem Toxicol 59:160–164
Amara S, Abdelmelek H, Garrel C, Guiraud P, Douki T, Ravanat JL, Favier A, Sakly M, Ben Rhouma K (2008) Preventive effect of zinc against cadmium-induced oxidative stress in rat testis. J Reprod Dev 54(2):129–134
Arroyo VS, Flores KM, Ortiz LB, Gomez-Quiroz LE, Gutierrez-Ruiz MC (2012) Liver and cadmium toxicity. Drug Metab Toxicol 5:1–7
Bagchi D, Bagchi M, Hassoun EA, Stohs SJ (1996) Cadmium induced excretion of urinary lipid metabolites, DNA damage, glutathione depletion, and hepatic lipid peroxidation in Sprague-Dawley rats. Biol Trace Elem Res 52:143–154
Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87:1620–1624
Beckman JS, Ischiropoulos H, Zhu L, van der Woerd M, Smith C, Chen J, Harrison J, Martin JC, Tsai M (1992) Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch Biochem Biophys 298:438–445
Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG (2007) Mortality in randomized trials of antioxidants supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297:842–857
Casalino E, Calzaretti G, Sblano C, Landriscina C (2000) Cadmium-dependent enzyme activity alteration is not imputable to lipid peroxidation. Arch Biochem Biophys 383:288–295
Casalino E, Calzaretti G, Sblano C, Landriscina C (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179:37–50
Cheng D, Kong H (2011) The effect of Lycium barbarum polysaccharides on alcohol-induced oxidative stress in rats. Molecules 16:2542–2550
Cheng J, Zhou ZW, Sheng HP, He LJ, Fan XW, He ZX, Sun T, Zhang X, Zhao RJ, Gu L, Cao C, Zhou SF (2014) An evidence-based update on the pharmacological activities and possible molecular targets of Lycium barbarum polysaccharides. Drug Des Devel Ther 9:33–78
Daiber A, Münzel T (2012) Increased circulating levels of 3-nitrotyrosine autoantibodies: marker for or maker of cardiovascular disease. Circulation 126(20):2371–2373
Dietrich-Muszalska A, Olas B, Głowacki R, Bald E (2009) Oxidative/nitrative modifications of plasma proteins and thiols from patients with schizophrenia. Neuropsychobiology 59(1):1–7
Eghbaliferiz S, Iranshahi M (2016) Prooxidant activity of polyphenols, flavonoids, anthocyanins and carotenoids: updated review of mechanisms and catalyzing metals. Phytother Res 30:1379–1391
El-Boshy ME, Risha EF, Abdelhamid FM, Mubarak MS, Hadda TB (2015) Protective effects of selenium against cadmium induced hematological disturbances, immunosuppressive, oxidative stress and hepatorenal damage in rats. J Trace Elem Med Biol 9:104–110
El-Sokkary GH, Nafady AA, Shabash EH (2010) Melatonin administration ameliorates cadmium-induced oxidative stress and morphological changes in the liver of rat. Ecotoxicol Environ Safe 73:456–463
Eybl V, Kotyzova D, Koutensky J (2006) Comparative study of natural antioxidants - curcumin, resveratrol and melatonin - in cadmium-induced oxidative damage in mice. Toxicology 225:150–156
Fouad AA, Qureshi HA, Yacoubi MT, Al-Melhim WN (2009) Protective role of carnosine in mice with cadmium-induced acute hepatotoxicity. Food and Chem Toxicol 47:2863–2870
Gadau SD (2012) Nitrosative stress induces proliferation and viability changes in high glucose-exposed rat schwannoma cells. Neuro Endocrinol Lett 33(3):279–284
Gadau S (2013) Nitrosative-induced posttranslational α-tubulin changes on high-glucose-exposed schwannoma cell line. Neuro Endocrinol Lett 34(5):372–382
Gong P, Chen F, Wang L, Wang J, Jin S, Ma Y (2014) Protective effects of blueberries (Vaccinium corymbosum L.) extract against cadmium-induced hepatotoxicity in mice. Environ Toxicol Pharmacol 37:1015–1027
Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18(9):685–716
Hassoun EA, Stohs SJ (1996) Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology 112:219–226
Honda A, Komuro H, Hasegawa T, Seko Y, Shimada A, Nagase H, Hozumi I, Inuzuka T, Hara H, Fujiwara Y, Satoh M (2010) Resistance of metallothionein-III null mice to cadmium induced acute hepatotoxicity. J Toxicol Sci 35:209–215
Karaka S, Eraslan G (2013) The effects of flaxseed oil on cadmium-induced oxidative stress in rats. Biol Trace Elem Res 155:423–430
Kawata M, Suzuki KT (1983) Relation between metal and glutathione concentrations in mouse liver after cadmium, zinc, or copper loading. Toxicol Lett 15:131–137
Kayama F, Yoshida T, Elwell MR, Luster MI (1995) Role of tumor necrosis factor-alpha in cadmium induced hepatotoxicity. Toxicol Appl Pharmacol 131:224–234
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(2):431–437
Lawal AO, Lawal AF, Olongodudu A, Adeniran OY, Omonkhua A, Obi F (2011) Antioxidant effects of heated garlic juice on cadmium-induced liver damage in rats as compared to ascorbic acid. J Toxicol Sci 36(5):549–557
Lewinska A, Wnuk M, Slota E, Bartosz G (2007) Total anti-oxidant capacity of cell culture media. Clin Exp Pharmacol Physiol 34:781–786
Liu J, Kershaw WC, Liu YP, Klaassen CD (1992) Cadmium-induced hepatic endothelial cell injury in inbred strains of mice. Toxicology 75:51–62
Liu F, Jan KY (2000) DNA damage in arsenite and cadmium treated bovine aortic endothelial cells. Free Radic Biol Med 28(1):55–63
Lowry HO, Rosebrough JN, Farr AL, Randall JR (1951) Protein measurement with the folin phenol reagent. J Biol Chem 93:265–275
Mangialasche F, Polidori MC, Monastero R, Ercolani S, Camarda C, Cecchetti R, Mecocci P (2009) Biomarkers of oxidative and nitrosative damage in Alzheimer’s disease and mild cognitive impairment. Ageing Res Rev 8(4):285–305
Matovic V, Buha A, Bulat Z, Dukic-Cosic D (2011) Cadmium toxicity revised: focus on oxidative stress inductions and interactions with zinc and magnesium. Arch High Rad Toksiko 62:65–76
Matovic V, Buha A, Bulat Z, Dukic-Cosic D, Miljkovic M, Ivanisevic J, Kotur-Stevulievic J (2012) Route-dependent effects of cadmium/cadmium and magnesium acute treatment of parameters of oxidative stress in rat liver. Food Chem Toxicol 50:552–557
Mihm MJ, Jing L, Bauer JA (2000) Nitrotyrosine causes selective vascular endothelial dysfunction and DNA damage. J Cardiovasc Pharmacol 36:182–187
Moore T, Le A, Niemi AK, Kwan T, Cusmano-Ozog K, Enns GM, Cowan TM (2013) A new LC-MS/MS method for the clinical determination of reduced and oxidized glutathione from whole blood. J Chromatogr B Analyt Technol Biomed Life Sci 929:51–55
Morris G, Maes M (2014) Oxidative and nitrosative stress and immune-inflammatory pathways in patients with myalgic encephalomyelitis (ME)/chronic fatigue syndrome (CFS). Curr Neuropharmacol 12(2):168–185
Nakazawa H, Fukuyama N, Takizawa S, Tsuji C, Yoshitake M, Ishida H (2000) Nitrotyrosine formation and its role in various pathological conditions. Free Radic Res 33(6):771–784
Newairy AA, El-Sharaky AS, Badreldeen MM, Eweda SM, Sheweita SA (2007) The hepatoprotective effects of selenium against cadmium toxicity in rats. Toxicology 242:23–30
Nolan CV, Shaikh ZA (1986) The vascular endothelium as a target tissue in acute cadmium toxicity. Life Sci 39(16):1403–1409
Parakh S, Spencer DM, Halloran MA, Soo KY, Atkin JD (2013) Redox regulation in amyotrophic lateral sclerosis. Oxidative Med Cell Longev:408681. doi:10.1155/2013/408681
Pasciu V, Baralla E, Varoni MV, Sedda T, Boatto G, Nieddu M, Burrai L, Demontis MP (2015) Preliminary analysis of oxidative stress parameters in Lister hooded rats after an acute oral treatment with 2,5-dimethoxyamphetamine. Glob Adv Res J Med and Medical Sci 4(7):337–346
Phan-Thi H, Durand P, Prost M, Prost E, Waché Y (2016) Effect of heat-processing on the antioxidant and prooxidant activities of b-carotene from natural and synthetic origins on red blood cells. Food Chem 190:1137–1144
Potterat O (2010) Goji (Lycium barbarum and L. chinense): phytochemistry, pharmacology and safety in the perspective of traditional uses and recent popularity. Planta Med 6(1):7–19
Pourfarzam M, Movahedian A, Sarrafzadegan N, Basati G, Samsamshariat SZ (2013) Association between plasma myeloperoxidase and free 3-nitrotyrosine levels in patients with coronary artery disease. Int J Clin Med 4:158–164
Rashid K, Sinha K, Sil PC (2013) An update on oxidative stress-mediated organ pathophysiology. Food Chem Toxicol 62:584–600
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237
Rikans LE, Yamano T (2000) Mechanisms of cadmium-mediated acute hepatotoxicity. J Biochem Mol Toxicol 14(2):110–117
Salganik RI (2001) The benefits and hazards of antioxidants: controlling apoptosis and other protective mechanisms in cancer patients and the human population. J Am Coll Nutr 20:464–472
Satarug S, Moore MR (2004) Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ Health Perspect 112(10):1099–1103
Sauer JM, Waalkes MP, Hooser SB, Kuester RK, McQueen CA, Sipes IG (1997) Suppression of Kupffer cell function prevents cadmium induced hepatocellular necrosis in the male Sprague-Dawley rat. Toxicology 121:155–164
Sayre LM, Perry G, Smithm MA (2008) Oxidative stress and neurotoxicity. Chem Res Toxicol 21(1):172–188
Shishehbor MH, Aviles RJ, Brennan ML, Fu X, Goormastic M, Pearce GL, Gokce N, Keaney JF Jr, Penn MS, Sprecher DL, Vita JA, Hazen SL (2003) Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 289:1675–1680
Souza JM, Peluffo G, Radi R (2008) Protein tyrosine nitration--functional alteration or just a biomarker. Free Radic Biol Med 45:357–366
Spanier AM, Traylor RD (1991) A rapid, direct chemical assay for the quantitative determination of thiobarbituric acid reactive substances in raw, cooked, and cooked/stored muscle foods. J Muscle Foods 2:165–176
Teng RJ, Wu TJ, Afolayan AJ, Konduri GG (2016) Nitrotyrosine impairs mitochondrial function in fetal lamb pulmonary artery endothelial cells. Am J Physiol Cell Physiol 310:80–88
Ukeda H, Maeda S, Ishii T, Sawamura M (1997) Spectrophotometric assay for superoxide dismutase based on tetrazolium salt 3′--1--(phenylamino)-carbonyl--3, 4-tetrazolium-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate reduction by xanthine-xanthine oxidase. Anal Biochem 251(2):206–209
Varoni MV, Palomba D, Gianorso S, Anania V (2003) Cadmium as an environmental factor of hypertension in animals: new perspectives on mechanisms. Vet Res Commun 27:807–810
Varoni MV, Palomba D, Macciotta NP, Antuofermo E, Deiana G, Baralla E, Anania V, Demontis MP (2010) Brain renin-angiotensin system modifies the blood pressure response to intracerebroventricular cadmium in rats. Drug and Chem Toxicol 33(3):302–309
Wu HT, He XJ, Hong YK, Ma T, Xu YP, Li HH (2010) Chemical characterization of Lycium barbarum polysaccharides and its inhibition against liver oxidative injury of high-fat mice. Int J Biol Macromol 46(5):540–543
Xiao J, Liong EC, King YP, Chang RC, Fung ML, Xu AM, So KF, Tipoe GL (2013) Lycium barbarum Polysaccharides protect rat liver from non-alcoholic steatohepatitis-induced injury. Nutr Diabetes 3:e81
Yamano T, Shimizu M, Noda T (1998) Age-related change in cadmium-induced hepatotoxicity in wistar rats: role of Kupffer cells and neutrophils. Toxicol Appl Pharmacol 151:9–15
Yordi EG, Pérez EM, Villares EU, Matos MJ (2012) Antioxidant and pro-oxidant effects of polyphenolic compounds and structure–activity relationship evidence. Intech Open Access Publisher Shanghai China:23–48
Acknowledgements
We gratefully acknowledge Specchiasol for providing LBP powder.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Additional information
Responsible editor: Philippe Garrigues
Valeria Pasciu and Sergio Domenico Gadau contributed equally to this work.
Rights and permissions
About this article
Cite this article
Varoni, M.V., Pasciu, V., Gadau, S.D. et al. Possible antioxidant effect of Lycium barbarum polysaccharides on hepatic cadmium-induced oxidative stress in rats. Environ Sci Pollut Res 24, 2946–2955 (2017). https://doi.org/10.1007/s11356-016-8050-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-8050-x