Silymarin alleviates hepatic oxidative stress and protects against metabolic disorders in high-fat diet-fed mice

References

• Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014;103:137–149.
   PubMed Web of Science ®Google Scholar
• Maddux BA, See W, Lawrence JC, Goldfine AL, Goldfine ID, Evans JL. Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolar concentrations of alpha-lipoic acid. Diabetes 2001;50:404–410.
   PubMed Web of Science ®Google Scholar
• Matsuoka T, Kajimoto Y, Watada H, Kaneto H, Kishimoto M, Umayahara Y, et al. Glycation-dependent, reactive oxygen species-mediated suppression of the insulin gene promoter activity in HIT cells. J Clin Invest 1997;99:144–150.
   PubMed Web of Science ®Google Scholar
• Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752–1761.
   PubMed Web of Science ®Google Scholar
• Milagro FI, Campion J, Martinez JA. Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity 2006;14:1118–1123.
   PubMed Web of Science ®Google Scholar
• Gumieniczek A. Oxidative stress in kidney and liver of alloxan-induced diabetic rabbits: effect of repaglinide. Acta Diabetol 2005;42:75–81.
   PubMed Web of Science ®Google Scholar
• Pereira S, Park E, Mori Y, Haber CA, Han P, Uchida T, et al. FFA-induced hepatic insulin resistance in vivo is mediated by PKC delta, NADPH oxidase, and oxidative stress. Am J Physiol-Endocrinol Metabol 2014;307:E34–E46.
   PubMed Web of Science ®Google Scholar
• Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006;116:3015–3025.
   PubMed Web of Science ®Google Scholar
• Boden G, She PX, Mozzoli M, Cheung P, Gumireddy K, Reddy P, et al. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappa B pathway in rat liver. Diabetes 2005;54:3458–3465.
   PubMed Web of Science ®Google Scholar
• Li NX, Karin M. Is NF-kappa B the sensor of oxidative stress? FASEB J 1999;13:1137–1143.
   PubMed Web of Science ®Google Scholar
• Kono H, Rusyn I, Yin M, Gabele E, Yamashina S, Dikalova A, et al. NADPH oxidase-derived free radicals are key oxidants in alcohol-induced liver disease. J Clin Invest 2000;106:867–872.
   PubMed Web of Science ®Google Scholar
• Schreck R, Albermann K, Baeuerle PA. Nuclear factor kappa B – an oxidative stress responsive transcription factor of eukaryotic cells (A review). Free Rad Res Commun 1992;17:221–237.
   PubMed Web of Science ®Google Scholar
• Tesoriere L, Attanzio A, Allegra M, Gentile C, Livrea MA. Indicaxanthin inhibits NADPH oxidase (NOX)-1 activation and NF-κB-dependent release of inflammatory mediators and prevents the increase of epithelial permeability in IL-1 beta-exposed Caco-2 cells. Br J Nutr 2014;111:415–423.
   PubMed Web of Science ®Google Scholar
• Pasarin M, Abraldes JG, Rodriguez-Vilarrupla A, La Mura V, Garcia-Pagan JC, Bosch J. Insulin resistance and liver microcirculation in a rat model of early NAFLD. J Hepatol 2011;55:1095–1102.
   PubMed Web of Science ®Google Scholar
• Davis-Searles PR, Nakanishi Y, Kim NC, Graf TN, Oberlies NH, Wani MC, et al. Milk thistle and prostate cancer: differential effects of pure flavonolignans from Silybum marianum on anti proliferative end points in human prostate carcinoma cells. Cancer Res 2005;65:4448–4457.
   Google Scholar
• Patel N, Joseph C, Corcoran GB, Ray SD. Silymarin modulates doxorubicin-induced oxidative stress, Bcl-xL and p53 expression while preventing apoptotic and necrotic cell death in the liver. Toxicol Appl Pharmacol 2010;245:143–152.
   PubMed Web of Science ®Google Scholar
• Huseini HF, Larijani B, Heshmat R, Fakhrzadeh H, Radjabipour B, Toliat T, Raza M. The efficacy of Silybum marianum (L.) Gaertn. (Silymarin) in the treatment of type II diabetes: a randomized, double-blind, placebo-controlled, clinical trial. Phytother Res 2006;20:1036–1039.
   PubMed Web of Science ®Google Scholar
• Velussi M, Cernigoi AM, DeMonte A, Dapas F, Caffau C, Zilli M. Long-term (12 months) treatment with an anti-oxidant drug (silymarin) is effective on hyperinsulinemia, exogenous insulin need and malondialdehyde levels in cirrhotic diabetic patients. J Hepatol 1997;26:871–879.
   PubMed Web of Science ®Google Scholar
• Velussi M, Cernigoi AM, Viezzoli L, Dapas F, Caffau C, Zilli M. Silymarin reduces hyperinsulinemia, malondialdehyde levels, and daily insulin need in cirrhotic diabetic patients. Curr Ther Res – Clin Exp 1993;53:533–545.
   Web of Science ®Google Scholar
• Maghrani M, Zeggwagh NA, Lemhadri A, El Amraoui M, Michel JB, Eddouks M. Study of the hypoglycaemic activity of Fraxinus excelsior and Silybum marianum in an animal model of type 1 diabetes mellitus. J Ethnopharmacol 2004;91:309–316.
   PubMed Web of Science ®Google Scholar
• Soto CP, Perez BL, Favari LP, Reyes JL. Prevention of alloxan-induced diabetes mellitus in the rat by silymarin. Comp Biochem Physiol C – Pharmacol Toxicol Endocrinol 1998;119:125–129.
   PubMed Web of Science ®Google Scholar
• Guigas B, Naboulsi R, Villanueva GR, Taleux N, Lopez-Novoa JM, Leverve XM, El-Mir M-Y. The flavonoid Silibinin decreases glucose-6-phosphate hydrolysis in perifused rat Hepatocytes by an inhibitory effect on glucose-6-phosphatase. Cell Physiol Biochem 2007;20:925–934.
   PubMed Web of Science ®Google Scholar
• Colturato CP, Constantin RP, Maeda AS Jr, Constantin RP, Yamamoto NS, Bracht A, et al. Metabolic effects of silibinin in the rat liver. Chem Biol Interact 2012;195:119–132.
   PubMed Web of Science ®Google Scholar
• Granger DL, Taintor RR, Boockvar KS, Hibbs JB Jr. Measurement of nitrate and nitrite in biological samples using nitrate reductase and Griess reaction. Methods Enzymol 1996;268:142–151.
   PubMed Web of Science ®Google Scholar
• Flohe L, Gunzler WA. Assays of glutathione peroxidase. Methods Enzymol 1984;105:114–121.
   PubMed Web of Science ®Google Scholar
• Griffith OW. Determination of glutathione and glutathione disufide using glutathione reductase and 2 vinylpyridine. Anal Biochem 1980;106:207–212.
   PubMed Web of Science ®Google Scholar
• Niehaus WG, Samuelss B. Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 1968;6:126.
   PubMedGoogle Scholar
• Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen NT, Zingraff J, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 1996;49:1304–1313.
   PubMed Web of Science ®Google Scholar
• Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245–313.
   PubMed Web of Science ®Google Scholar
• Gao D, Griffiths HR, Bailey CJ. Oleate protects against palmitate-induced insulin resistance in L6 myotubes. Br J Nutr 2009;102:1557–1563.
   PubMed Web of Science ®Google Scholar
• Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006;440:944–948.
   PubMed Web of Science ®Google Scholar
• Bashan AB-DaN. Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid Redox Signal 2005;7:1553–1567.
   PubMed Web of Science ®Google Scholar
• Chtourou Y, Garoui EM, Boudawara T, Zeghal N. Protective role of silymarin against manganese-induced nephrotoxicity and oxidative stress in rat. Environ Toxicol 2014;29:1147–1154.
   PubMed Web of Science ®Google Scholar
• Das SK, Vasudevan DM. Protective effects of silymarin, a milk thistle (Silybium marianum) derivative on ethanol-induced oxidative stress in liver. Indian J Biochem Biophys 2006;43:306–311.
   PubMed Web of Science ®Google Scholar
• Koujan SE, Gargari BP, Mobasseri M, Valizadeh H, Asghari-Jafarabadi M. Effects of Silybum marianum (L.) Gaertn. (silymarin) extract supplementation on antioxidant status and hs-CRP in patients with type 2 diabetes mellitus: a randomized, triple-blind, placebo-controlled clinical trial. Phytomedicine 2015;22:290–296.
   PubMed Web of Science ®Google Scholar
• Rohrdanz E, Ohler S, Tran-Thi QH, Kahl R. The phytoestrogen daidzein affects the antioxidant enzyme system of rat hepatoma H4IIE cells. J Nutr 2002;132:370–375.
   PubMed Web of Science ®Google Scholar
• Bataller R, Schwabe RF, Choi YH, Yang L, Paik YH, Lindquist J, et al. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 2003;112:1383–1394.
   PubMed Web of Science ®Google Scholar
• De Minicis S, Brenner DA. NOX in liver fibrosis. Arch Biochem Biophys 2007;462:266–272.
   PubMed Web of Science ®Google Scholar
• Yan S-L, Yang H-T, Lee Y-J, Lin C-C, Chang M-H, Yin M-C. Asiatic acid ameliorates hepatic lipid accumulation and insulin resistance in mice consuming a high-fat diet. J Agri Food Chem 2014;62:4625–4631.
   PubMed Web of Science ®Google Scholar
• Brar SS, Kennedy TP, Sturrock AB, Huecksteadt TP, Quinn MT, Murphy TM, et al. NADPH oxidase promotes NF-kappa B activation and proliferation in human airway smooth muscle. Am J Physiol – Lung Cell Mol Physiol 2002;282:L782–L795.
   PubMed Web of Science ®Google Scholar
• Polyak SJ, Morishima C, Lohmann V, Pal S, Lee DYW, Liu YZ, et al. Identification of hepatoprotective flavonolignans from silymarin. Proc Natl Acad Sci USA 2010;107:5995–5999.
   PubMed Web of Science ®Google Scholar
• Anrather J, Racchumi G, Iadecola C. NF-kappa B regulates phagocytic NADPH oxidase by inducing the expression of gp91(phox). J Biol Chem 2006;281:5657–5667.
   PubMed Web of Science ®Google Scholar
• Kim K-A, Gu W, Lee I-A, Joh E-H, Kim D-H. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. Plos One 2012;7:e47713.
   PubMed Web of Science ®Google Scholar
• Kim JS, Yeo S, Shin DG, Bae YS, Lee JJ, Chin BR, et al. Glycogen synthase kinase 3 beta and beta-catenin pathway is involved in toll-like receptor 4-mediated NADPH oxidase 1 expression in macrophages. FEBS J 2010;277:2830–2837.
   PubMed Web of Science ®Google Scholar
• Liang CF, Liu JTC, Wang Y, Xu AM, Vanhoutte PM. Toll-like receptor 4 mutation protects obese mice against endothelial dysfunction by decreasing NADPH oxidase isoforms 1 and 4. Arterioscler Thromb Vascular Biol 2013;33:777–784.
   PubMed Web of Science ®Google Scholar