Abstract
Glycyrrhiza total flavones (GTF) have been confirmed to possess anti-oxidation and lipid-lowering effects, but whether they have a protective effect on fatty liver injury in tilapia (Oreochromis niloticus) is unknown. Thus, the aim of this study was to investigate the protective effects of GTF on liver injury induced by a high-fat diet (HFD) and its underlying mechanism in fish. A total of 180 tilapia were randomly divided into four experimental groups: normal control group (basic diet, 6% crude fat), HFD group (fed with HFD, 21% crude fat), and two GTF treatment groups (addition of 0.1 and 1.0 g/kg of GTF to the high-fat diet). After 90 days of feeding, blood and liver tissues were collected to measure biochemical parameters, mRNA levels, and protein expression to evaluate the liver protection of GTF. Compared with the HFD group, addition of GTF to the diet significantly reduced the indexes of liver enzyme activity and fat metabolism in serum. In liver, addition of GTF to the diet upregulated mRNA levels of the oxidative stress-related genes glutathione transferase alpha (GSTα) and NAD(P)H dehydrogenase (NQO1), and downregulated mRNA level of kelch-like epichlorohydrin-associated protein 1 (Keap1). GTF treatments also significantly reduced mitogen-activated protein kinase 8 (MAPK8) and caspase 3 (CAS-3) protein expression. Meanwhile, GTF treatments downregulated mRNA levels of toll-like receptor1 (TLR1), toll-like receptor5 (TLR5), interleukin 1 receptor-associated kinase (IRAK1), tumor necrosis factor receptor-related factor 6 (TRAF6), complement 3 (C3), heat shock protein 70 (HSP70), and immunoglobulin M (IgM). These results showed that GTF had a well protective effect against fatty liver injury caused by an HFD in tilapia. The beneficial effects of these flavones may be related to changes of nuclear factor-related factor 2 and TLR signaling pathways.
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References
Allard J, Le Guillou D, Begriche K, Fromenty B (2019) Drug-induced liver injury in obesity and nonalcoholic fatty liver disease. Adv Pharmacol 85:75–107. https://doi.org/10.1016/bs.apha.2019.01.003
Cai L-S, Wang L, Song K, Lu K-L, Zhang C-X, Rahimnejad S (2020) Evaluation of protein requirement of spotted seabass (Lateolabrax maculatus) under two temperatures, and the liver transcriptome response to thermal stress. Aquaculture 516:734615. https://doi.org/10.1016/j.aquaculture.2019.734615
Chen HY, Yan L, Wang JH, Geng M, & Yang XB. (2009a). Protective effect of extraction of Glycyrrhiza Uralensis Fisch.on CC14 induced acute hepatic injury in mice. Chinese Journal of Information on Traditional Chinese Medicine, 16(7), 24–25. doi:https://doi.org/10.3969/j.issn.1005-5304.2009.07.010
Chen MF, Wu HB, Zeng H, Dai L, Zhu S, Xu D et al (2009b) Effect of Baogan Fugong decoction on gene expression of TLR2, TLR4 in liver tissue of rats with experimental hepatitis induced by lipopolysaccharides. Chin J Integr Tradit Western Med on Liver Dis 19(4):224–226. https://doi.org/10.3969/j.issn.1005-0264.2009.04.012
Chen Y, Sun R (2011) Toll-like receptors in acute liver injury and regeneration. Int Immunopharmacol 11(10):1433–1441. https://doi.org/10.1016/j.intimp.2011.04.023
Chiang WD, Huang CY, Paul CR, Lee ZY, Lin WT (2016) Lipolysis stimulating peptides of potato protein hydrolysate effectively suppresses high-fat-diet-induced hepatocyte apoptosis and fibrosis in aging rats. Food Nutr Res 60:31417. https://doi.org/10.3402/fnr.v60.31417
Di Naso FC, Porto RR, Fillmann HS, Maggioni L, Padoin AV, Ramos RJ et al (2015) Obesity depresses the anti-inflammatory HSP70 pathway, contributing to NAFLD progression. Obesity (silver Spring) 23(1):120–129. https://doi.org/10.1002/oby.20919
Diehl AM, Day C (2017) Cause, pathogenesis, and treatment of nonalcoholic steatohepatitis. N Engl J Med 377(21):2063–2072. https://doi.org/10.1056/NEJMra1503519
YZ Dong L Li M Espe KL Lu 2020 Hydroxytyrosol Attenuates Hepatic Fat Accumulation via Activating Mitochondrial Biogenesis and Autophagy through the AMPK Pathway 68 35 9377 9386 10.1021/acs.jafc.0c03310
Du ZY (2014) Causes of fatty liver in farmed fish: a review and new perspectives. Journal of Fisheries of China 38(09):1628–1638
Feng YJ, Hu BQ, & Zhou JH. (2016). Effects of Glycyrrhiza flavonoids on blood glucose, blood lipid and antioxidant capacity in diabetic rats 56(3), 23–25. doi:https://doi.org/10.3969/j.issn.1002-266X.2016.03.008
Ghezelbash B, Shahrokhi N, Khaksari M, Ghaderi-Pakdel F, & Asadikaram G. (2020). Hepatoprotective effects of Shilajit on high fat-diet induced non-alcoholic fatty liver disease (NAFLD) in rats. Horm Mol Biol Clin Investig, 41(1). doi:https://doi.org/10.1515/hmbci-2019-0040
Gong L, Tang H, Luo Z, Sun X, Tan X, Xie L et al (2020) Tamoxifen induces fatty liver disease in breast cancer through the MAPK8/FoxO pathway. Clin Trans Med 10(1):137–150. https://doi.org/10.1002/ctm2.5
SH Gou M He BB Li NY Zhu JM Ni 2020 Hepatoprotective effect of total flavonoids from Glycyrrhiza uralensis Fisch in liver injury mice Nat Prod Res 1–5 10.1080/14786419.2020.1824223
Guan LC, Gao HT, Xu LS (2015) The role and mechanism of adiponectin and JNK1 in non-alcoholic fatty liver rats. J Practical Med 12:1915–1917. https://doi.org/10.3969/j.issn.1006-5725.2015.12.005
Hendrikx T, Watzenböck ML, Walenbergh SM, Amir S, Gruber S, Kozma MO et al (2016) Low levels of IgM antibodies recognizing oxidation-specific epitopes are associated with human non-alcoholic fatty liver disease. BMC Med 14(1):107. https://doi.org/10.1186/s12916-016-0652-0
Huo X, Yang S, Sun X, Meng X, & Zhao Y. (2018). Protective effect of glycyrrhizic acid on alcoholic liver injury in rats by modulating lipid metabolism. Molecules, 23(7). doi:https://doi.org/10.3390/molecules23071623
Itani SI, Ruderman NB, Schmieder F, Boden G (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51(7):2005–2011. https://doi.org/10.2337/diabetes.51.7.2005
Jia R, Cao LP, Du JL, He Q, Gu ZY, Jeney G et al (2020a) Effects of high-fat diet on antioxidative status, apoptosis and inflammation in liver of tilapia (Oreochromis niloticus) via Nrf2, TLRs and JNK pathways. Fish Shellfish Immunol 104:391–401. https://doi.org/10.1016/j.fsi.2020.06.025
Jia R, Cao LP, Du JL, He Q, Yin GJ (2020b) Effects of high-fat diet on steatosis, endoplasmic reticulum stress and autophagy in liver of tilapia (Oreochromis niloticus). Front Mar Sci 7:363.https://doi.org/10.3389/fmars.2020.00363
Jia R, Du J, Cao L, Li Y, Johnson O, Gu Z et al (2019a) Antioxidative, inflammatory and immune responses in hydrogen peroxide-induced liver injury of tilapia (GIFT, Oreochromis niloticus). Fish Shellfish Immunol 84:894–905. https://doi.org/10.1016/j.fsi.2018.10.084
Jia R, Li Y, Cao L, Du J, Zheng T, Qian H et al (2019b) Antioxidative, anti-inflammatory and hepatoprotective effects of resveratrol on oxidative stress-induced liver damage in tilapia (Oreochromis niloticus). Comp Biochem Physiol C Toxicol Pharmacol 215:56–66. https://doi.org/10.1016/j.cbpc.2018.10.002
Jing J. (2015). Study on protective mechanism of flavonoids from Glycyrrhiza uralensis on non-alcoholic fatty liver disease in rats. (Master), Ningxia Medical University.
Jing J, Zhao JY, Hua B, Xue MQ, Zhu YF, Liu G et al (2015a) Inhibitory effect of flavonoids from Glycyrrhiza uralensis on expressions of TGF-β1 and Caspase-3 in thioacetamide-induced hepatic fibrosis in rats. Zhongguo Zhong Yao Za Zhi 40(15):3034–3040
Jing J, Zhao JY, Hua B, Xue WQ, Zhu YF, Liu G et al (2015b) Inhibitory effect of flavonoids from Glycyrrhiza uralensis on expressions of TGF-β1 and Caspase-3 in thioacetamide-induced hepatic fibrosis in rats. Chin J Chin Materia Medica 40(15):3034–3040. https://doi.org/10.4268/cjcmm20151523
Jojima T, Wakamatsu S, Kase M, Iijima T, Maejima Y, Shimomura K, et al. (2019). The SGLT2 inhibitor canagliflozin prevents carcinogenesis in a mouse model of diabetes and non-alcoholic steatohepatitis-related hepatocarcinogenesis: association with SGLT2 expression in hepatocellular carcinoma. Int J Mol Sci, 20(20). doi:https://doi.org/10.3390/ijms20205237
Kang JS, Cheng LF, Yang J, Tao YC, Hu J (2012) Effect of total flavonoids of Glycyrrhiza uralensis on skin aging. Shandong Med J 52(42):34–35
Kawai T, Akira S (2007) TLR signaling. Semin Immunol 19(1):24–32. https://doi.org/10.1016/j.smim.2006.12.004
Ken CF, Chen CN, Ting CH, Pan CY, Chen JY (2017) Transcriptome analysis of hybrid tilapia (Oreochromis spp.) with Streptococcus agalactiae infection identifies Toll-like receptor pathway-mediated induction of NADPH oxidase complex and piscidins as primary immune-related responses. Fish Shellfish Immunol 70:106–120. https://doi.org/10.1016/j.fsi.2017.08.041
Kesar V, Odin JA (2014) Toll-like receptors and liver disease. Liver Int 34(2):184–196. https://doi.org/10.1111/liv.12315
Kiziltas S (2016) Toll-like receptors in pathophysiology of liver diseases. World J Hepatol 8(32):1354–1369. https://doi.org/10.4254/wjh.v8.i32.1354
Li J, Tan H, Zhou X, Zhang C, Jin H, Tian Y et al (2018) The protection of midazolam against immune mediated liver injury induced by lipopolysaccharide and galactosamine in mice. Front Pharmacol 9:1528. https://doi.org/10.3389/fphar.2018.01528
Li S, Zhou J, Xu S, Li J, Liu J, Lu Y, et al. (2019). Induction of Nrf2 pathway by Dendrobium nobile Lindl. alkaloids protects against carbon tetrachloride induced acute liver injury. Biomed Pharmacother, 117, 109073. doi:https://doi.org/10.1016/j.biopha.2019.109073
Liao Z, Zhang J, Liu B, Yan T, & Xu F. (2019). Polysaccharide from okra (Abelmoschus esculentus (L.) Moench) improves antioxidant capacity via PI3K/AKT pathways and Nrf2 translocation in a type 2 diabetes model. 24(10). doi:https://doi.org/10.3390/molecules24101906
Lin HC, Di WJ, Huang ZL, He LB (2019) Research progress of FAS gene. Jilin Ani Hus Veteri Med 40(12):10–11
Liu B, Fang Y, Yi R, Zhao X (2019) Preventive effect of blueberry extract on liver injury induced by carbon tetrachloride in mice. Foods 8(2):48. https://doi.org/10.3390/foods8020048
Liu CX, Wang W, Ma DL (2018) Effect of different extraction methods and antioxidant activity of total flavonoids from licorice. Fine Specialty Chem 26(12):27–30. https://doi.org/10.19482/j.cn11-3237.2018.12.08
Liu T, Xu QL, Zhao Y (2015a) Expression of Toll-like receptor 4 in rat model of nonalcoholic fatty liver disease induced by hyperlipidemia. J Clin Hepatol 31(12):2073–2076. https://doi.org/10.3969/j.issn.1001-5256.2015.12.021
Liu Y, Cao L, Du J, Jia R, Wang J, Xu P et al (2015b) Protective effects of Lycium barbarum polysaccharides against carbon tetrachloride-induced hepatotoxicity in precision-cut liver slices in vitro and in vivo in common carp (Cyprinus carpio L.). Comp Biochem Physiol C Toxicol Pharmacol 169:65–72. https://doi.org/10.1016/j.cbpc.2014.12.005
Liu ZC. (2011). Research on effects of fore-feeding on FAS expression and law of fat deposition in goose fatty liver. (Doctor), Jilin Agricultural University.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lu HC, Zhang T (2010) Effect of tea polyphenol on SOD and MDA levels in alcohol-induced liver injury. Progress in Veterinary Medicine 31(11):34–36. https://doi.org/10.3969/j.issn.1007-5038.2010.11.008
Lu KL, Wang LN, Zhang DD, Liu WB, Xu WN (2017) Berberine attenuates oxidative stress and hepatocytes apoptosis via protecting mitochondria in blunt snout bream Megalobrama amblycephala fed high-fat diets. Fish Physiol Biochem 43(1):65–76. https://doi.org/10.1007/s10695-016-0268-5
Lv H, Yang H, Wang Z, Feng H, Deng X, Cheng G et al (2019) Nrf2 signaling and autophagy are complementary in protecting lipopolysaccharide/d-galactosamine-induced acute liver injury by licochalcone A. Cell Death Dis 10(4):313. https://doi.org/10.1038/s41419-019-1543-z
Mao XP, Zhu SM, Cen XL (2020) Analysis of liver function, blood lipid and blood glucose levels in patients with different degrees of non-alcoholic fatty liver disease. J Math Med 33(11):1617–1619. https://doi.org/10.3969/j.issn.1004-4337.2020.11.016
Miura K, Ohnishi H (2014) Role of gut microbiota and Toll-like receptors in nonalcoholic fatty liver disease. World J Gastroenterol 20(23):7381–7391. https://doi.org/10.3748/wjg.v20.i23.7381
Okada K, Warabi E, Sugimoto H, Horie M, Gotoh N, Tokushige K et al (2013) Deletion of Nrf2 leads to rapid progression of steatohepatitis in mice fed atherogenic plus high-fat diet. J Gastroenterol 48(5):620–632. https://doi.org/10.1007/s00535-012-0659-z
Orrù C, Giordano S (2020) Nrf2 in neoplastic and non-neoplastic liver diseases. Cancers (basel) 12(10):2932. https://doi.org/10.3390/cancers12102932
Pérez S, Rius-Pérez S, Tormos AM, Finamor I, Nebreda ÁR, Taléns-Visconti R et al (2018) Age-dependent regulation of antioxidant genes by p38α MAPK in the liver. Redox Biol 16:276–284. https://doi.org/10.1016/j.redox.2018.02.017
Purohit V, Gao B, Song BJ (2009) Molecular mechanisms of alcoholic fatty liver. Alcohol Clin Exp Res 33(2):191–205. https://doi.org/10.1111/j.1530-0277.2008.00827.x
Rebl A, Goldammer T, Seyfert HM (2010) Toll-like receptor signaling in bony fish. Vet Immunol Immunopathol 134(3–4):139–150. https://doi.org/10.1016/j.vetimm.2009.09.021
Shen X, Guo H, Xu J, Wang J (2019) Inhibition of lncRNA HULC improves hepatic fibrosis and hepatocyte apoptosis by inhibiting the MAPK signaling pathway in rats with nonalcoholic fatty liver disease. J Cell Physiol 234(10):18169–18179. https://doi.org/10.1002/jcp.28450
Shin SM, Yang JH, Ki SH (2013) Role of the Nrf2-ARE pathway in liver diseases. Oxid Med Cell Longev 2013:763257. https://doi.org/10.1155/2013/763257
Shu M, Huang DD, Hung ZA, Hu XR, Zhang S (2016) Inhibition of MAPK and NF-κB signaling pathways alleviate carbon tetrachloride (CCl4)-induced liver fibrosis in Toll-like receptor 5 (TLR5) deficiency mice. Biochem Biophys Res Commun 471(1):233–239. https://doi.org/10.1016/j.bbrc.2016.01.119
Sun J, Fu J, Li L, Chen C, Wang H, Hou Y et al (2018) Nrf2 in alcoholic liver disease. Toxicol Appl Pharmacol 357:62–69. https://doi.org/10.1016/j.taap.2018.08.019
Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17(1):1–14. https://doi.org/10.1093/intimm/dxh186
Takeda K, & Akira S. (2015). Toll-like receptors. Curr Protoc Immunol, 109, 14.12.11–14.12.10. doi:https://doi.org/10.1002/0471142735.im1412s109
Tan Y, Zhang JN, Chen JH, Wang LJ, Liu HX (2009) Role of JNK signal transduction pathway in nonalcoholic fatty liver disease. Zhonghua Gan Zang Bing Za Zhi 17(11):821–825
Tang W, Jiang YF, Ponnusamy M, Diallo M (2014) Role of Nrf2 in chronic liver disease. World J Gastroenterol 20(36):13079–13087. https://doi.org/10.3748/wjg.v20.i36.13079
Tang XH, Chen SH, Lv GY, Su J, Huang MC (2010) Effects of Dendrobium Candidum on SOD, MDA and GSH-Px in mice model of acute alcoholic hepatic injury Zhejiang. J Tradit Chin Med 45(5):369–370. https://doi.org/10.3969/j.issn.0411-8421.2010.05.051
Tian WX (1994) Regulation of body fat level and fatty acid synthase activity in animals. Chem Life 1:5
Tian X, Xiong Q, Chen L, Wen JR, Ru Q (2019) Intervention of catalpol on high-fat diet induced nonalcoholic fatty liver disease in mice. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 41(6):746–755. https://doi.org/10.3881/j.issn.1000-503X.11110
Vauzour D, Rodriguez-Ramiro I, Rushbrook S, Ipharraguerre IR, Bevan D, Davies S et al (2018) n-3 fatty acids combined with flavan-3-ols prevent steatosis and liver injury in a murine model of NAFLD. Biochim Biophys Acta Mol Basis Dis 1864(1):69–78. https://doi.org/10.1016/j.bbadis.2017.10.002
Wang B, Xia XS, Li JT, Duan XH (2020) The role of cytochrome P4502E1 in glycyrrhizin treated nonalcoholic fatty liver disease. Journal of Kunming Medical University 41(4):11–17
Wang C, Cui Y, Li C, Zhang Y, Xu S, Li X et al (2013) Nrf2 deletion causes “benign” simple steatosis to develop into nonalcoholic steatohepatitis in mice fed a high-fat diet. Lipids Health Dis 12:165. https://doi.org/10.1186/1476-511x-12-165
Wang GS. (1991). Protective effect of total flavonoids of Glycyrrhiza uralensis on liver injury induced by carbon tetrachloride in mice. Inner Mongolia Medical University.
Wang JW, Chen XY, Hu PY, Tan MM, Tang XG, Huang MC et al (2016) Effects of Linderae radix extracts on a rat model of alcoholic liver injury. Exp Ther Med 11(6):2185–2192. https://doi.org/10.3892/etm.2016.3244
Wang L, Zhang W, Ge CH, Yin RH, Xiao Y, Zhan YQ et al (2017) Toll-like receptor 5 signaling restrains T-cell/natural killer T-cell activation and protects against concanavalin A-induced hepatic injury. Hepatology 65(6):2059–2073. https://doi.org/10.1002/hep.29140
Wang Q, Wang YF, Zhang YX, Shi C, Guo QH, Han X et al (2019) Effects of Jiedu Hugan prescription on TLR3/TNF-α/JNK2 signaling pathway of drug-induced hepatotoxicity rats. Chin J Infor Tradit Chin Med 26(8):60–65. https://doi.org/10.3969/j.issn.1005-5304.2019.08.013
Wu LP, Zhang SX, Du SY, & Zhou RH. (2011). Progress of the status of fatty liver animal model. Modern Prev Med, 38(24), 5111–5113,5118.
Wu Q, Zhang D, Tao N, Zhu Q-N, Jin T, Shi J-S et al (2014) Induction of Nrf2 and metallothionein as a common mechanism of hepatoprotective medicinal herbs. Am J Chin Med 42(1):207–221
Wu YT, Sun Y, & Liu GD. (2013). Interention effect of total flavonoids of gycyrrhiza on hyperlipidenia model mice. Heilongjiang Medicine Journal(5), 774–776,777. doi:https://doi.org/10.3969/j.issn.1006-2882.2013.05.015
Xi BW, & Pan LK. (2021). Fish diseases and control measures in hot season. Scientific Fish Farming(8), 48–49. doi:DOI:https://doi.org/10.3969/j.issn.1004-843X.2021.08.027.
Xie TH, Li JX, Mao TY, Guo Y, Chen C, Han YF et al (2017) An ErChen and YinChen decoction ameliorates high-fat-induced nonalcoholic steatohepatitis in rats by regulating JNK1 signaling pathway. Evid Based Complement Alternat Med 2017:4603701. https://doi.org/10.1155/2017/4603701
Xiong X, Ren Y, Cui Y, Li R, Wang C, Zhang Y (2017) Obeticholic acid protects mice against lipopolysaccharide-induced liver injury and inflammation. Biomed Pharmacother 96:1292–1298. https://doi.org/10.1016/j.biopha.2017.11.083
Xu D, Xu M, Jeong S, Qian Y, Wu H, Xia Q et al (2018) The role of Nrf2 in liver disease: novel molecular mechanisms and therapeutic approaches. Front Pharmacol 9:1428. https://doi.org/10.3389/fphar.2018.01428
Yan J, Shen S, He Y, Li Z (2019) TLR5 silencing reduced hyperammonaemia-induced liver injury by inhibiting oxidative stress and inflammation responses via inactivating NF-κB and MAPK signals. Chem Biol Interact 299:102–110. https://doi.org/10.1016/j.cbi.2018.11.026
Yang Y, Yang L, Han Y, Wu Z, Chen P, Zhang H et al (2017) Protective effects of hepatocyte-specific glycyrrhetic derivatives against carbon tetrachloride-induced liver damage in mice. Bioorg Chem 72:42–50. https://doi.org/10.1016/j.bioorg.2017.03.009
Yang YQ, Yan XT, Wang K, Tian RM, Lu ZY, Wu LL et al (2018) Triptriolide alleviates lipopolysaccharide-induced liver injury by Nrf2 and NF-κB signaling pathways. Front Pharmacol 9:999. https://doi.org/10.3389/fphar.2018.00999
Yu Q, Huo J, Zhang Y, Liu K, Cai Y, Xiang T et al (2020) Tamoxifen-induced hepatotoxicity via lipid accumulation and inflammation in zebrafish. Chemosphere 239:124705. https://doi.org/10.1016/j.chemosphere.2019.124705
Zaki SM, Fattah SA, Hassan DS (2019) The differential effects of high-fat and high-fructose diets on the liver of male albino rat and the proposed underlying mechanisms. Folia Morphol (warsz) 78(1):124–136. https://doi.org/10.5603/FM.a2018.0063
Zhang CY, Cao LP, Du JL, Jia R, Gu ZY, Yin GJ et al (2018a) Nrf2 mediate protective effects of curcumin against carbon tetrachloride (CCl4)-induced liver injury in Carassius auratus. Jiangsu Journal of Agricultural Sciences 34(1):114–121. https://doi.org/10.3969/j.issn.1000-4440.2018.01.017
Zhang E, Yin S, Zhao S, Zhao C, Yan M, Fan L et al (2020) Protective effects of glycycoumarin on liver diseases. Phytother Res 34(6):1191–1197. https://doi.org/10.1002/ptr.6598
Zhang FX, Song JX, Liu XD, Shan H (2019) Antioxidation and immune activity of licorice flavonoids. Chin J Veteri Sci 39(6):1180–1183. https://doi.org/10.16303/j.cnki.1005-4545.2019.06.24
Zhang J, Fan N, Peng Y (2018b) Heat shock protein 70 promotes lipogenesis in HepG2 cells. Lipids Health Dis 17(1):73. https://doi.org/10.1186/s12944-018-0722-8
Zhao SY, Wang NP, Zhong ZG, Nong ZX (2005) Experimental study on apoptosis of hepatoma cells induced by total flavonoids of Glycyrrhiza uralensis Fisch. J Guangxi Med Univ 22(2):235–237. https://doi.org/10.3969/j.issn.1005-930X.2005.02.028
Zhao YF, & Song QH. (2012). Talk about fish hepatobiliary syndrome. Scientific Fish Farming(8), 13–18.
Zheng T, Jia R, Cao L, Du J, Gu Z, He Q et al (2021) Effects of chronic glyphosate exposure on antioxidative status, metabolism and immune response in tilapia (GIFT, Oreochromis niloticus). Comp Biochem Physiol C Toxicol Pharmacol 239:108878. https://doi.org/10.1016/j.cbpc.2020.108878
Zhou W, Rahimnejad S, Lu K (2019) Effects of berberine on growth, liver histology, and expression of lipid-related genes in blunt snout bream (Megalobrama amblycephala) fed high-fat diets. Fish Physiol Biochem 45(1):83–91. https://doi.org/10.1007/s10695-018-0536-7
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This work was supported by the Central Public-interest Scientific Institution Basal Research Fund of China (2019JBFM10) and Jiangsu Provincial Natural Science Foundation of China (NO. BK20201143).
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Jin-Liang Du: experiment design and paper writing. Li-Ping Cao: data analysis. Rui Jia: validation. Zheng-Yan Gu and Qin He: investigation. Pao Xu and. Galina Jeney: paper review and editing. Guo-Jun Yin and Yu-zhong Ma: conceptualization, project administration.
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Du, J., Jia, R., Cao, L. et al. Regulatory effects of Glycyrrhiza total flavones on fatty liver injury induced by a high-fat diet in tilapia (Oreochromis niloticus) via the Nrf2 and TLR signaling pathways. Aquacult Int 30, 1527–1548 (2022). https://doi.org/10.1007/s10499-021-00787-2
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DOI: https://doi.org/10.1007/s10499-021-00787-2