Abstract
This study has assessed the protective efficacy of Silybum marianum seed oil (SMSO) in the context of CCl4-induced injury and oxidative stress in murine liver. Based on the GC-MS analysis, linoleic and stearic acids, tocopherol, ascorbic acid 2,6 dihexadecanoate and other constituents were identified in SMSO. Swiss mice received oral doses of SMSO daily for 21 days (10 g/kg b.w.) and subsequently injected i.p. with CCl4 (50% v/v in olive oil; 1 ml/kg) on the 22nd day. CCl4 administration induced an elevation of serum amino- and glutamyl transferases activities and an increased peroxidation, as well as a decrease of SOD, CAT, GPx, GR and GST activities in liver. SMSO successfully prevented oxidative stress and restored the biochemical parameters, hepatic architecture and expression of TNF-alpha. These findings suggest that SMSO was effective in counteracting the damaging effects of CCl4-induced injury in hepatocytes, probably due to its inherent antioxidant properties.
References
[1] Jones A.L., Anatomy of the normal liver., Hepatology: a text book of liver disease, 3rd ed., Zakin D and Boyer TD, Philadelphia: W.B. Saunders, 1996 Search in Google Scholar
[2] Sturgill M., Lambert G.H., Xenobiotic-induced hepatotoxicity: mechanisms of liver injury and methods of monitoring hepatic function, Clin. Chem., 1997, 43 (8), 1512-1526 10.1093/clinchem/43.8.1512Search in Google Scholar
[3] Oesterreicher C.H., Trauner M., Xenobiotic-induced liver injury and fibrosis, Expert Opin. Drug Metab. Toxicol., 2012, 8(5), 571-80 10.1517/17425255.2012.674511Search in Google Scholar PubMed
[4] Clawson G.A., Mechanism of carbon tetrachloride hepatotoxicity, Pathol. Immunopathol. Res., 1989, 8(2), 104-112 10.1159/000157141Search in Google Scholar PubMed
[5] Weber L.W., Boll M., Stampfl A., Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model, Critical Rev. Toxicol., 2003, 33 (2), 105-136 10.1080/713611034Search in Google Scholar PubMed
[6] Muriel P., Rivera-Espinoza Y., Beneficial drugs for liver diseases, J. Appl. Toxicol., 2008, 28(2), 93–103 10.1002/jat.1310Search in Google Scholar PubMed
[7] Vitaglione P., Morisco F., Caporaso N., Fogliano V., Dietary Antioxidant Compounds and Liver Health, Critical Rev. Food Sci. Nutrition, 2004, 44(7-8), 575–586 10.1080/10408690490911701Search in Google Scholar PubMed
[8] Lee C.P., Shih P.H., Hsu C.L., Yen G.C., Hepatoprotection of tea seed oil (Camellia oleifera Abel.) against CCl4-induced oxidative damage in rats, Food Chem Toxicol., 2008, 45(6), 888–895 10.1016/j.fct.2006.11.007Search in Google Scholar PubMed
[9] Prasanthi K., Muralidhara M., Rajini P.S., Fenvalerat-induced oxidative damage in rat tissues and its attenuation by dietary sesame oil, Food Chem Toxicol., 2005, 43(2), 299-306 10.1016/j.fct.2004.10.005Search in Google Scholar PubMed
[10] Hsu Y.W., Tsai C.F., Che W.K., Lu F.J., Protective effects of seabuckthorn (Hippophae rhamnoides L.) seed oil against carbon tetrachloride-induced hepatotoxicity in mice, Food Chem. Toxicol., 2009, 47(9), 2281–2288 10.1016/j.fct.2009.06.015Search in Google Scholar PubMed
[11] Maheswary M.U., Rao P.G.M., Antihepatotoxic effect of grape seed oil in rat, Indian J. Pharmacol., 2005, 37(3), 179-182 10.4103/0253-7613.16216Search in Google Scholar
[12] Haddad Y., Vallerand D., Brault A., Haddad P.S., Antioxidant and hepatoprotective effects of silibinin in a rat model of nonalcoholic steatohepatitis, Evidence-Based Complementary and Alternative Medicine, 2011, ID 647903, 10 pages 10.1093/ecam/nep164Search in Google Scholar PubMed PubMed Central
[13] Shaker M.E., Zalata K.R., Mehal W.Z., Shiha G.E., Ibrahim T.M., Comparison of imatinib, nilotinib and silymarin in the treatment of carbon tetrachloride-induced hepatic oxidative stress, injury and fibrosis, Toxicol. Appl. Pharmacol., 2011, 252(2), 165–175 10.1016/j.taap.2011.02.004Search in Google Scholar PubMed PubMed Central
[14] Au A.Y., Hasenwinkel J.M., Frondoza C.G., Silybin inhibits interleukin-1b-induced production of pro-inflammatory mediators in canine hepatocyte cultures, J. Vet. Pharmacol. Therap., 2010, 34(2), 120–129 10.1111/j.1365-2885.2010.01200.xSearch in Google Scholar PubMed
[15] Tsai J.H., Liu J.Y., Wu T.T., Ho P.C., Huang C.Y., Shyu J.C., et al., Effects of silymarin on the resolution of liver fibrosis induced by carbon tetrachloride in rats, J. Viral Hepatitis, 2008, 15(7), 508–514 10.1111/j.1365-2893.2008.00971.xSearch in Google Scholar PubMed
[16] Kshirsagar A., Ingawale D., Ashok P., Vyawahare N., Silymarin: A Comprehensive Review, Pharmacognosy Rev., 2009, 3(5), 126-134 Search in Google Scholar
[17] Abrol S., Trehan A., Katare O.P., Comparative study of different silymarin formulations: formulation, characterisation and In Vitro/In Vivo evaluation, Curr. Drug Delivery, 2005, 2(1), 45-51 10.2174/1567201052772870Search in Google Scholar PubMed
[18] Passerini N., Perissutti B., Albertini B., Franceschinis E., Lenaz D., Hasa D., et al., A new approach to enhance oral bioavailability of Silybum marianum dry extract: Association of mechanochemical activation and spray congealing, Phytomedicine, 2012, 19(2), 160–168 10.1016/j.phymed.2011.06.027Search in Google Scholar PubMed
[19] Wang Y., Zhang Z., Liu Z., Liu G., Duan C., Jia L., et al., In vitro and in vivo evaluation of silybin nanosuspensions for oral and intravenous delivery, Nanotechnology, 2010, 21, 155104 10.1088/0957-4484/21/15/155104Search in Google Scholar PubMed
[20] Kasdallah-Grissa A., Nakbia A., Koubaaa N., El-Fazaâb S., Gharbib N., Kamounb Aet al., Dietary virgin olive oil protects against lipid peroxidation and improves antioxidant status in the liver of rats chronically exposed to ethanol, Nutrition Res., 2008, 28(7), 472–479 10.1016/j.nutres.2008.03.014Search in Google Scholar PubMed
[21] Hermenean A., Popescu C., Ardelean A., Stan M., Hadaruga N., Mihali C.V., et al., Hepatoprotective Effect of Berberis vulgaris L.extract/beta-cyclodextrin on carbon tetrachloride – induced acute toxicity in mice, Int. J. Mol. Sci., 2012, 13(7), 9014-934 10.3390/ijms13079014Search in Google Scholar PubMed PubMed Central
[22] Aebi H., Catalase, Methods of Enzymatic Analysis, Bergmeyer, H.U., Ed. Academic Press: New York, NY, USA., 1974, 673–677 10.1016/B978-0-12-091302-2.50032-3Search in Google Scholar
[23] Paoletti F., Mocali A., Determination of superoxide dismutase activity by purely chemical system based on NADP(H) oxidation, Meth. Enzymol., 1990, 186, 209–221 10.1016/0076-6879(90)86110-HSearch in Google Scholar
[24] Beutler E., Red Cell Metabolism, A Manual of Biochemical Methods, Beutler E. Ed., Grune and Stratton: Orlando, FL, USA. 1984, 68–73 Search in Google Scholar
[25] Goldberg D.M., Spooner R.J., Glutathione Reductase, Methods of Enzymatic Analysis, Bergmeyer H.U. Ed., Verlag Chemie: Weinheim, Germany, 1983, 258–265 Search in Google Scholar
[26] Habig W.H., Pabst M.J., Jakoby W.B., Glutathione S-transferases. The first enzymatic step in mercapturic acid formation, J. Biol. Chem., 1974, 249(22), 7130–7139 10.1016/S0021-9258(19)42083-8Search in Google Scholar
[27] Del Rio D., Pellegrini N., Colombi B., Bianchi M., Serafini M., Torta F., et al., Rapid fluorimetric method to detect total plasma malondialdehyde with mild derivatization conditions, Clin. Chem., 2003, 49(4), 690-692 10.1373/49.4.690Search in Google Scholar
[28] Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J., Protein measurement with the Folin phenol reagent, J. Biol. Chem.,1951, 193, 265–275 10.1016/S0021-9258(19)52451-6Search in Google Scholar
[29] Johnson D.E., Kroenung C., Mechanism of early carbon tetrachloride toxicity in cultured rat hepatocytes, Pharmacol. Toxicol., 1998, 83(6), 231-239 10.1111/j.1600-0773.1998.tb01475.xSearch in Google Scholar PubMed
[30] Slater T.F., Lipid peroxidation, Biochem. Soc. Transactions, 1983, 10, 70-71 10.1042/bst0100070Search in Google Scholar PubMed
[31] Rubalya V.S., Neelameagam P., Gayathri K., Estimating antioxidant stability in sunflower and rice bran oil on heating using in vitro analysis, Biomedicine, 2009, 29, 31-36 Search in Google Scholar
[32] El-Mallah M.H., El-Shami S.M., Hassanein M.M., Detailed studies on some lipids of Silybum marinarum (L.) seed oil, Grasas y Aceites., 2003, 54(4), 397-402 10.3989/gya.2003.v54.i4.227Search in Google Scholar
[33] Khan I., Khattak H.U., Ullah I., Bangash .FK., Study of the physicochemical properties of Silybum marianum seed oil, J. Chem. Soc. Pak., 2007, 29(6), 545-548 Search in Google Scholar
[34] Wang T., Hicks K.B., Moreau R., Antioxidant activity of phytosterols, oryzanol, and other phytosterol conjugates, J. Am. Oil Chem. Soc., 2002, 79, 1201-1206 10.1007/s11746-002-0628-xSearch in Google Scholar
[35] Weber N., Murkherjee K.D., Plant sterols and steryl esters in functional foods and nutraceuticals, Shahidi F. (Ed.), Nutraceutical and specialty lipids and their co-products, CRC Press, Taylor & Francis Group, 2006, 483-508 10.1201/9781420015911.ch27Search in Google Scholar
[36] Kabuto H., Yamamishi T.T., Janjua N., Takayama F., Mankura M., Effects of squalene/squalane on dopamine levels, antioxidant enzyme activity and fatty acid composition in the striatum of Parkinson’s disease mouse model, J. Oleo. Sci., 2013, 62(1), 21-28 10.5650/jos.62.21Search in Google Scholar PubMed
[37] Becker E., Messner B., Berndt J., Two mechanisms of CCl4-induced fatty liver: lipid peroxidation or covalent binding studied in cultured rat hepatocytes, Free Radic. Res. Commun.,1987, 3 (-5), 299-308 10.3109/10715768709069797Search in Google Scholar
[38] Manna P., Bhattacharyya S., Das J., Ghosh J., Sil P., Phytomedicinal role of Pithecellobium dulce against CCl4-mediated hepatic oxidative impairments and necrotic cell death, Evidence-Based Complementary and Alternative Medicine, 2011, 832805, 17 pages 10.1093/ecam/neq065Search in Google Scholar
[39] Yavuz T., Delibas N., Yildirim B., Altuntas I., Candir O., Cora A., et al., Vascular wall damage in rats induced by methidathion and ameliorating effect of vitamins E and C, Arch. Toxicol., 2004, 78(11), 655–9 10.1007/s00204-004-0593-9Search in Google Scholar
[40] Shiryaeva A., Arkandyeva A., Emelyanova L., Sakuta G., Morozov V., Superoxide anion production by the respiratory chain of hepatocytes of rats with experimental toxic hepatitis, J. Bioener. Biomemebranes, 2009, 41(4), 379-385 10.1007/s10863-009-9234-6Search in Google Scholar
[41] Yim M.B., Chock P.B., Stadtman E.R., Enzyme function of copper, zinc superoxide dismutase as a free radical generator, J. Biol. Chem., 1993, 268, 4099-4105 10.1016/S0021-9258(18)53585-7Search in Google Scholar
[42] Ames B.M., Shigenaga M.K., Hagen T., Oxidants, antioxidants and the degenerative diseases of aging, Proc. Nat. Acad. Sci., 1993, 90(17), 7915-7922 10.1073/pnas.90.17.7915Search in Google Scholar
[43] Siemeniuk E., Kolodziejczyk L., Skrzydlewska E., Oxidative modifications of rat liver cell components during Fasciola hepatica infection, Toxicol. Mechanism Meth., 2008, 18(6), 519-524 10.1080/15376510701624001Search in Google Scholar
[44] Chen S., Zou L., Li L., Wu T., The protective effect of glycyrrheticnic acid on carbon tetrachloride-induced chronic liver fibrosis in mice via up-regulation of Nrf-2, PLOS One, 2013, 8(1), e53662 10.1371/journal.pone.0053662Search in Google Scholar
[45] Starke D.W., Chen Y., Bapna C.P., Lesnefsky E.J., Mieyal J.J., Sensitivity of protein sulfhydryl repair enzymes to oxidative stress, Free Rad. Biol. Med., 1997, 23(3), 373-384 10.1016/S0891-5849(97)00009-9Search in Google Scholar
[46] Tamai K., Satih K., Tsuchida S., Hatayama I., Maki T., Sato K., Specific inactivation of glutathione S transferase in class Pi by SH-modifiers, Biochem. Biophys. Res. Commun., 1990, 167, 331-338 10.1016/0006-291X(90)91769-OSearch in Google Scholar
[47] Arab K., Rossary A., Soulere L., Steghens J.P., Conjugated linoleic acid unlike other unsaturated fatty acids, strongly induces glutathione synthesis without any lipoperoxidation, Brit. J. Nut., 2008, 96(5), 811-819 10.1017/BJN20061910Search in Google Scholar
[48] Prabu S.M., Shagirtha K., Renugadevi J., Amelioration of cadmium-induced oxidative stress, impairment in lipids and plasma lipoproteins by the combined treatment with quercetin and α-tocopherol in rats, J. Food Sci., 2010, 75(7), 132-140 10.1111/j.1750-3841.2010.01757.xSearch in Google Scholar
[49] Chen L.H., Interaction of vitamin E and ascorbic acid, In vivo, 1989, 3(3), 199-209 Search in Google Scholar
[50] Bandopadhyay D., Das D., Banerjee R.K., Reactive oxygen species: Oxidative damage and pathogenesis, Curr. Sci., 1999, 77(5), 658-666 Search in Google Scholar
[51] Sudheesh N.P., Ajith T.A., Janardhanan K.K., Hepatoprotective effects of DL-a-lipoic acid and a-Tocopherol through amelioration of the mitochondrial oxidative stress in acetaminophen challenged rats, Toxicol. Mechanism Meth., 2013, 23(5), 368–376 10.3109/15376516.2013.769289Search in Google Scholar
[52] Belury M.A., Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action, Ann. Rev. Nutr., 2002, 22, 505-531 10.1146/annurev.nutr.22.021302.121842Search in Google Scholar
[53] Klein E., Weber N., In vitro test for the effectiveness of antioxidants as inhibitors of thiyl radical-induced reaction fatty acids, J. Agric. Food Chem., 2001, 49(3), 1224-1227 10.1021/jf000725mSearch in Google Scholar
[54] Conforti F., Sosa S., Marrelli M., Menichini F., Statti G.A., Uzunov D., et al., In vivo anti-inflammatory and in vivo antioxidant activities of Mediterranean dietary plants, J. Ethnopharmacol., 2008, 116, 144-151 10.1016/j.jep.2007.11.015Search in Google Scholar
[55] Mirmiran P., Bahadoran Z., Azizi F., Functional foods-based diet as a novel dietary approach for management of type 2 diabetes and its complication: A review, World J. Diabetes, 2014, 5(3), 267-281 10.4239/wjd.v5.i3.267Search in Google Scholar
[56] Ozturk F., Gul M., Ates B., Ozturk I.C., Cetin A., Vardi N., et al., Protective effect of apricot (Prunus armeniaca L.) on hepatic steatosis and damage induced by carbon tetrachloride in Wistar rats, British J. Nutr., 2009, 102(12), 1767–1775 10.1017/S0007114509991322Search in Google Scholar
[57] Domitrovic R., Jakovac H, Blagojevic G., Hepatoprotective activity of berberine is mediated by inhibition of TNF-alpha, COX-2, and iNOS expression in CCl4-intoxicated mice, Toxicology, 2011, 280, 33–43 10.1016/j.tox.2010.11.005Search in Google Scholar
[58] Chamulitrat W., Blazka M.E., Jordan S.J., Luster M.I., Mason R.P., Tumor necrosis factor-α and nitric oxide production in endotoxin-primed rats administered carbon tetrachloride, Life Sci., 1995, 57(24), 2273–2280 10.1016/0024-3205(95)02220-DSearch in Google Scholar
[59] Garcia-Bailo B., Roke K., Mutch D.M., El-Sohemy A., Badawi A., Association between circulating ascorbic acid, α-tocopherol, 25-hydroxyvitamin D and plasma cytokine concentrations in young adults: a cross-sectional study, Nutr. Met., 2012, 9, 102-110 10.1186/1743-7075-9-102Search in Google Scholar PubMed PubMed Central
[60] Micallef M.A., Garg M.L., Anti-inflammatory and cardioprotective effects of n-3 polyunsaturated fatty acids and plant sterols in hyperlipidemic individuals, Atherosclerosis, 2009, 204(2), 476-482 10.1016/j.atherosclerosis.2008.09.020Search in Google Scholar PubMed
©2015 Anca Hermenean et al.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.
