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Research paper

Quantitative proteomics analysis based on tandem mass tag labeling coupled with labeling coupled with liquid chromatography-tandem mass spectrometry discovers the effect of silibinin on non-alcoholic fatty liver disease in mice

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Pages 6750-6766 | Received 05 Jan 2022, Accepted 18 Feb 2022, Published online: 04 Mar 2022

References

  • Leamy AK, Egnatchik RA, Young JD. Molecular mechanisms and the role of saturated fatty acids in the progression of non-alcoholic fatty liver disease. Prog Lipid Res. 2013;52:165–174.
  • Yu Y, Cai J, She Z, et al. Insights into the Epidemiology, Pathogenesis, and Therapeutics of Nonalcoholic Fatty Liver Diseases. Adv Sci (Weinheim, Baden-Wurttemberg, Germany). 2019;6(4):1801585.
  • Gentile CL, Pagliassotti MJ. The role of fatty acids in the development and progression of nonalcoholic fatty liver disease. J Nutr Biochem. 2008;19(9):567–576.
  • Utzschneider KM, Kahn SE. Review: the role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006;91(12):4753–4761.
  • Day CP, James OFW. Steatohepatitis: a tale of two “hits”? Gastroenterology. 1998;114(4):842–845.
  • Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004;114(2):147–152.
  • Arab JP, Arrese M, Trauner M. Recent Insights into the Pathogenesis of nonalcoholic fatty liver disease. Annual Review of Pathology: Mechanisms of Disease. 2018;13(1):321–350.
  • Tittel G, Wagner H. Hochleistungsflüssigchromatographische trennung von silymarinen und deren bestimmung im rohextrakt von silybum marianum gaertn. Journal of Chromatography A. 1977;135(2):499–501.
  • Raghu R, Karthikeyan S. Zidovudine and isoniazid induced liver toxicity and oxidative stress: evaluation of mitigating properties of silibinin. Environ Toxicol Pharmacol. 2016;46:217–226.
  • Stiuso P, Scognamiglio I, Murolo M, et al. Serum oxidative stress markers and lipidomic profile to detect NASH patients responsive to an antioxidant treatment: a pilot study. Oxid Med Cell Longev. 2014;2014:169216.
  • Loguercio C, Andreone P, Brisc C, et al. Silybin combined with phosphatidylcholine and vitamin E in patients with nonalcoholic fatty liver disease: a randomized controlled trial. Free Radic Biol Med. 2012;52:1658–1665.
  • Federico A, Trappoliere M, Tuccillo C, et al. A new silybin-vitamin E-phospholipid complex improves insulin resistance and liver damage in patients with non-alcoholic fatty liver disease: preliminary observations. Gut. 2006;55:901–902.
  • Huseini HF, Larijani B, Heshmat R, et al. 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.
  • Alsaggar M, Bdour S, Ababneh Q, et al. Silibinin attenuates adipose tissue inflammation and reverses obesity and its complications in diet-induced obesity model in mice. BMC Pharmacol Toxicol. 2020;21:8.
  • Cui CX, Deng JN, Yan L, et al. Silibinin Capsules improves high fat diet-induced nonalcoholic fatty liver disease in hamsters through modifying hepatic de novo lipogenesis and fatty acid oxidation. J Ethnopharmacol. 2017;208:24–35.
  • Grattagliano I, et al. A silybin-phospholipids complex counteracts rat fatty liver degeneration and mitochondrial oxidative changes. World J Gastroenterol. 2013;19(20):3007–3017.
  • Haddad Y, Vallerand D, Brault A, et al. Antioxidant and hepatoprotective effects of silibinin in a rat model of nonalcoholic steatohepatitis. Evid Based Complement Alternat Med. 2011;2011: nep164.
  • Yao J, Zhi M, Gao X, et al. Effect and the probable mechanisms of silibinin in regulating insulin resistance in the liver of rats with non-alcoholic fatty liver. Braz J Med Biol Res = Rev Bras Pesqui Med Biol. 2013;46(3):270–277.
  • Loguercio C. Silybin and the liver: from basic research to clinical practice. World J Gastroenterol. 2011;17(18):2288–2301.
  • Salamone F, Galvano F, Cappello F, et al. Silibinin modulates lipid homeostasis and inhibits nuclear factor kappa B activation in experimental nonalcoholic steatohepatitis. Transl Res. 2012;159(6):477–486.
  • Yao J, Zhi M, Minhu C. Effect of silybin on high-fat-induced fatty liver in rats. Braz J Med Biol Res = Rev Bras Pesqui Med Biol. 2011;44(7):652–659.
  • Chen X, Ma H, Gao Y, et al. Long non-coding RNA AC012668 suppresses non-alcoholic fatty liver disease by competing for microRNA miR-380-5p with lipoprotein-related protein LRP2. Bioengineered. 2021;12(1):6738–6747.
  • Anderson NL, Esquer-Blasco R, Richardson F, et al. The effects of peroxisome proliferators on protein abundances in mouse liver. Toxicol Appl Pharmacol. 1996;137(1):75–89.
  • Arce A, Aicher L, Wahl D, et al. Changes in the liver protein pattern of female Wistar rats treated with the hypoglycemic agent SDZ PGU 693. Life Sci. 1998;63(25):2243–2250.
  • Poon TCW, Yip -T-T, Chan ATC, et al. Comprehensive proteomic profiling identifies serum proteomic signatures for detection of hepatocellular carcinoma and its subtypes. Clin Chem. 2003;49(5):752–760.
  • Cheng Y, Hou T, Ping J, et al. Quantitative succinylome analysis in the liver of non-alcoholic fatty liver disease rat model. Proteome Sci. 2016;14(1):3.
  • Guo H, Guo H, and Zhang L, et al. Dynamic TMT-based quantitative proteomics analysis of critical initiation process of totipotency during cotton somatic embryogenesis transdifferentiation. Int J Mol Sci. 2019;20(7): 1691.
  • Erdjument-Bromage H, Huang FK, Neubert TA. Sample Preparation for Relative Quantitation of Proteins Using Tandem Mass Tags (TMT) and Mass Spectrometry (MS). Methods Mol Biol. 2018;1741:135–149.
  • Zou B, Ge -Z-Z, Zhang Y, et al. Persimmon tannin accounts for hypolipidemic effects of persimmon through activating of AMPK and suppressing NF-κB activation and inflammatory responses in high-fat diet rats. Food Funct 2014;5(7):1536–1546.
  • Nair A, Morsy MA, Jacob S. Dose translation between laboratory animals and human in preclinical and clinical phases of drug development. Drug Development Research. 2018;79(8):373–382.
  • Wang F, Chen S, Ren L, et al. The effect of silibinin on protein expression profile in white adipose tissue of obese mice. Front Pharmacol. 2020;11:55.
  • Greenberg AS, Coleman RA, Kraemer FB, et al. The role of lipid droplets in metabolic disease in rodents and humans. J Clin Invest. 2011;121(6):2102–2110.
  • Brasaemle DL. Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res. 2007;48(12):2547–2559.
  • Brasaemle DL, Wolins NE. Packaging of fat: an evolving model of lipid droplet assembly and expansion. J Biol Chem. 2012;287(4):2273–2279.
  • Gross DA, Zhan C, Silver DL. Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proc Natl Acad Sci U S A. 2011;108(49):19581–19586.
  • Carr RM, Peralta G, Yin X, et al. Absence of perilipin 2 prevents hepatic steatosis, glucose intolerance and ceramide accumulation in alcohol-fed mice. PLoS One. 2014;9(5):e97118.
  • Varela GM, Antwi DA, Dhir R, et al. Inhibition of ADRP prevents diet-induced insulin resistance. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2008;295(3):G621–8.
  • Dalen KT, Ulven SM, Arntsen BM, et al. PPARα activators and fasting induce the expression of adipose differentiation-related protein in liver. J Lipid Res. 2006;47(5):931–943.
  • Imai Y, Boyle S, Varela GM, et al. Effects of perilipin 2 antisense oligonucleotide treatment on hepatic lipid metabolism and gene expression. Physiol Genomics. 2012;44(22):1125–1131.
  • Chang BH-J, Li L, Paul A, et al. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol Cell Biol. 2006;26(3):1063–1076.
  • Imai Y, Varela GM, Jackson MB, et al. Reduction of hepatosteatosis and lipid levels by an adipose differentiation-related protein antisense oligonucleotide. Gastroenterology. 2007;132(5):1947–1954.
  • Ishii K-A, Takamura T. [Non-alcoholic fatty liver disease (NAFLD) /non-alcoholic steatohepatitis (NASH) and nutrition]. Clin Calcium. 2016;26(3):363–367. CliCa1603363367.
  • Ress C. Mechanisms of intrahepatic triglyceride accumulation. World J Gastroenterol. 2016;22(4):1664–1673.
  • Kohjima M, Enjoji M, Higuchi N, et al. Re-evaluation of fatty acid metabolism-related gene expression in nonalcoholic fatty liver disease. Int J Mol Med. 2007;20(3):351–358.
  • Chen Z, Gropler MC, Norris J, et al. Alterations in Hepatic metabolism in fld mice reveal a role for lipin 1 in regulating VLDL-triacylglyceride secretion. Arterioscler Thromb Vasc Biol. 2008;28(10):1738–1744.
  • Finck BN, Gropler MC, Chen Z, et al. Lipin 1 is an inducible amplifier of the hepatic PGC-1α/PPARα regulatory pathway. Cell Metab. 2006;4(3):199–210.
  • Ryu D, Oh K-J, Jo H-Y, et al. TORC2 regulates hepatic insulin signaling via a mammalian phosphatidic acid phosphatase, LIPIN1. Cell Metab. 2009;9(3):240–251.
  • Koo S-H, Satoh H, Herzig S, et al. PGC-1 promotes insulin resistance in liver through PPAR-α-dependent induction of TRB-3. Nat Med. 2004;10(5):530–534.
  • Kajimoto K, Suemitsu E, Sato Y, et al. Liver-Specific Silencing of Lipin1 Reduces Fat Mass as Well as Hepatic Triglyceride Biosynthesis in Mice. Biol Pharm Bull. 2016;39(10):1653–1661.
  • Leung T-M, Nieto N. CYP2E1 and oxidant stress in alcoholic and non-alcoholic fatty liver disease. J Hepatol. 2013;58(2):395–398.
  • Mantena SK, Vaughn DP, Andringa KK, et al. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo. Biochem J. 2009;417(1):183–193.
  • Drager LF, Li J, Reinke C, et al. Intermittent hypoxia exacerbates metabolic effects of diet-induced obesity. Obesity (Silver Spring,MD). 2011;19(11):2167–2174.
  • Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell. 2010;40(2):294–309.
  • Mylonis I, Sembongi H, Befani C, et al. Hypoxia causes triglyceride accumulation by HIF-1-mediated stimulation of lipin 1 expression. J Cell Sci. 2012;125(Pt 14):3485–3493.
  • Nishimoto T, Amano Y, Tozawa R, et al. Lipid-lowering properties of TAK-475, a squalene synthase inhibitor, in vivo and in vitro. Br J Pharmacol. 2003;139(5):911–918.
  • Liu J, Jiang S, Zhao Y, et al. Geranylgeranyl diphosphate synthase (GGPPS) regulates non-alcoholic fatty liver disease (NAFLD)-fibrosis progression by determining hepatic glucose/fatty acid preference under high-fat diet conditions. The Journal of Pathology. 2018;246(3):277–288.
  • Shimomura I, Bashmakov Y, Horton JD. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J Biol Chem. 1999;274(42):30028–30032.
  • Iorio A, Piacentini S, Polimanti R, et al. Functional variability of glutathione S-transferases in Basque populations. Am J Hum Biol. 2014;26(3):361–366.
  • Board PG, Menon D. Glutathione transferases, regulators of cellular metabolism and physiology. Biochim Biophys Acta. 2013;1830(5):3267–3288.
  • Liu F-P, Ma X, Li -M-M, et al. Hepatoprotective effects of Solanum nigrum against ethanol-induced injury in primary hepatocytes and mice with analysis of glutathione S-transferase A1. J Chin Med Assoc. 2016;79(2):65–71.
  • Ma X, Liu F, Li M, et al. Expression of glutathione S-transferase A1, a phase II drug-metabolizing enzyme in acute hepatic injury on mice. Exp Ther Med. 2017;14(4):3798–3804.
  • Singhal SS, Singh SP, Singhal P, et al. Antioxidant role of glutathione S-transferases: 4-Hydroxynonenal, a key molecule in stress-mediated signaling. Toxicol Appl Pharmacol. 2015;289(3):361–370.
  • Thompson KJ, Austin RG, Nazari SS. Altered fatty acid-binding protein 4 (FABP4) expression and function in human and animal models of hepatocellular carcinoma. Liver International: Official Journal of the International Association for the Study of the Liver. 2018;38(6):1074–1083.
  • Guy CA, Hoogendoorn B, Smith SK, et al. Promoter polymorphisms in glutathione-S-transferase genes affect transcription. Pharmacogenetics. 2004;14(1):45–51.
  • Sharma S, Adrogue JV, Golfman L, et al. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. The FASEB Journal. 2004;18(14):1692–1700.
  • Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology. 2003;144(12):5159–5165.
  • Nishida K, Otsu K. Inflammation and metabolic cardiomyopathy. Cardiovasc Res. 2017;113(4):389–398.
  • Maack C, Murphy E. Metabolic cardiomyopathies: fighting the next epidemic. Cardiovasc Res. 2017;113(4):367–369.
  • Goldberg IJ, Reue K, Abumrad NA, et al. Deciphering the role of lipid droplets in cardiovascular disease: a report from the 2017 national heart, lung, and blood institute workshop. Circulation. 2018;138(3):305–315.
  • Peterson LR, Herrero P, Schechtman KB, et al. Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation. 2004;109(18):2191–2196.
  • Taleb A, Ahmad KA, Ihsan AU, et al. Antioxidant effects and mechanism of silymarin in oxidative stress induced cardiovascular diseases. Biomed Pharmacothe. 2018;102:689–698.