No CrossRef data available.
Article contents
Dietary chenodeoxycholic acid attenuates high-fat diet-induced growth retardation, lipid accumulation and bile acid metabolism disorder in the liver of yellow catfish Pelteobagrus fulvidraco
Published online by Cambridge University Press: 31 October 2023
Abstract
This experiment was conducted to investigate whether dietary chenodeoxycholic acid (CDCA) could attenuate high-fat (HF) diet-induced growth retardation, lipid accumulation and bile acid (BA) metabolism disorder in the liver of yellow catfish Pelteobagrus fulvidraco. Yellow catfish (initial weight: 4·40 (sem 0·08) g) were fed four diets: the control (105·8 g/kg lipid), HF diet (HF group, 159·6 g/kg lipid), the control supplemented with 0·9 g/kg CDCA (CDCA group) and HF diet supplemented with 0·9 g/kg CDCA (HF + CDCA group). CDCA supplemented in the HF diet significantly improved growth performance and feed utilisation of yellow catfish (P < 0·05). CDCA alleviated HF-induced increment of hepatic lipid and cholesterol contents by down-regulating the expressions of lipogenesis-related genes and proteins and up-regulating the expressions of lipololysis-related genes and proteins. Compared with the control group, CDCA group significantly reduced cholesterol level (P < 0·05). CDCA significantly inhibited BA biosynthesis and changed BA profile by activating farnesoid X receptor (P < 0·05). The contents of CDCA, taurochenodeoxycholic acid and glycochenodeoxycholic acid were significantly increased with the supplementation of CDCA (P < 0·05). HF-induced elevation of cholic acid content was significantly attenuated by the supplementation of CDCA (P < 0·05). Supplementation of CDCA in the control and HF groups could improve the liver antioxidant capacity. This study proved that CDCA could improve growth retardation, lipid accumulation and BA metabolism disorder induced by HF diet, which provided new insight into understanding the physiological functions of BA in fish.
- Type
- Research Article
- Information
- Copyright
- © The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society
References
Boujard, T, Gélineau, A, Covès, D, et al. (2004) Regulation of feed intake, growth, nutrient and energy utilisation in European seabass (Dicentrarchus labrax) fed high fat diets. Aquaculture 231, 529–545.CrossRefGoogle Scholar
Luo, G, Xu, JH, Teng, YJ, et al. (2010) Effects of dietary lipid levels on the growth, digestive enzyme, feed utilization and fatty acid composition of Japanese sea bass (Lateolabrax japonicus L.) reared in freshwater. Aquacult Res 41, 210–219.CrossRefGoogle Scholar
Rueda-Jasso, R, Conceicao, LEC, Dias, J, et al. (2004) Effect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 231, 417–433.CrossRefGoogle Scholar
Lu, KL, Wang, LN, Zhang, DD, et al. (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, 65–76.CrossRefGoogle ScholarPubMed
Chen, W, Gao, S, Chang, K, et al. (2023) Dietary sodium butyrate supplementation improves fish growth, intestinal microbiota composition, and liver health in largemouth bass (Micropterus salmoides) fed high-fat diets. Aquaculture 564, 739040.CrossRefGoogle Scholar
Jin, M, Pan, T, Tocher, DR, et al. (2019) Dietary choline supplementation attenuated high-fat diet-induced inflammation through regulation of lipid metabolism and suppression of NFκB activation in juvenile black seabream (Acanthopagrus schlegelii). J Nutr Sci 8, e38.CrossRefGoogle ScholarPubMed
Li, J, Zhang, Z, Kong, A, et al. (2022) Dietary L-carnitine regulates liver lipid metabolism via simultaneously activating fatty acid β-oxidation and suppressing endoplasmic reticulum stress in large yellow croaker fed with high-fat diets. Br J Nutr 129, 29–40.CrossRefGoogle ScholarPubMed
Han, CY, Kim, TH, Koo, JH, et al. (2009) Farnesoid X receptor as a regulator of fuel consumption and mitochondrial function. Arch Pharm Res 39, 1062–1074.CrossRefGoogle Scholar
Russell, DW (2009) Fifty years of advances in bile acid synthesis and metabolism. J Lipid Res 50, 120–125.CrossRefGoogle ScholarPubMed
Wang, L, Sagada, G, Wang, CY, et al. (2023) Exogenous bile acids regulate energy metabolism and improve the health condition of farmed fish. Aquaculture 562, 738852.CrossRefGoogle Scholar
Ridlon, JM, Kang, DJ & Hylemon, PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47, 241–259.CrossRefGoogle ScholarPubMed
Hofmann, AF, Hagey, LR & Krasowski, MD (2010) Bile salts of vertebrates: structural variation and possible evolutionary significance. J Lipid Res 51, 226–246.CrossRefGoogle ScholarPubMed
Bilbao-Malavé, V, González-Zamora, J, de la Puente, M, et al. (2021) Mitochondrial dysfunction and endoplasmic reticulum stress in age related macular degeneration, role in pathophysiology, and possible new therapeutic strategies. Antioxidants 10, 1170.CrossRefGoogle ScholarPubMed
Du, J, Xiang, X, Xu, D, et al. (2021) FXR, a key regulator of lipid metabolism, is inhibited by ER stress-mediated activation of JNK and p38 MAPK in large yellow croakers (Larimichthys crocea) fed high fat diets. Nutrients 1312, 4343.CrossRefGoogle Scholar
Watanabe, M, Houten, SM, Wang, L, et al. (2013) Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 113, 1408–1418.CrossRefGoogle Scholar
Chiang, JY (2013) Bile acid metabolism and signaling. Compr Physiol 3, 1191–1212.CrossRefGoogle ScholarPubMed
Cariou, B (2008) The farnesoid X receptor (FXR) as a new target in non-alcoholic steatohepatitis. Diabetes Metab 34, 685–691.CrossRefGoogle ScholarPubMed
Li, J, Wang, T, Liu, P, et al. (2021) Hesperetin ameliorates hepatic oxidative stress and inflammation via the PI3K/AKT-Nrf2-ARE pathway in oleic acid-induced HepG2 cells and a rat model of high-fat diet-induced NAFLD. Food Funct 12, 3898–3918.CrossRefGoogle Scholar
Wang, YD, Chen, WD, Li, C, et al. (2015) Farnesoid X receptor antagonizes JNK signaling pathway in liver carcinogenesis by activating SOD3. Mol Endocrinol 29, 322–331.CrossRefGoogle ScholarPubMed
Dong, L, Han, X, Tao, X, et al. (2018) Protection by the total flavonoids from Rosa laevigata Michx fruit against lipopolysaccharide-induced liver injury in mice via modulation of FXR signaling. Foods 7, 88.CrossRefGoogle ScholarPubMed
Liao, ZB, Sun, B, Zhang, QG, et al. (2020) Dietary bile acids regulate the hepatic lipid homeostasis in tiger puffer fed normal or high-lipid diets. Aquaculture 519, 734935.CrossRefGoogle Scholar
Ding, T, Xu, N, Liu, YT, et al. (2020) Effect of dietary bile acid (BA) on the growth performance, body composition, antioxidant responses and expression of lipid metabolism-related genes of juvenile large yellow croaker (Larimichthys crocea) fed high-lipid diets. Aquaculture 518, 734768.CrossRefGoogle Scholar
Zhang, Y, Feng, H, Liang, XF, et al. (2022) Dietary bile acids reduce liver lipid deposition via activating farnesoid X receptor, and improve gut health by regulating gut microbiota in Chinese perch (Siniperca chuatsi). Fish Shellfish Immunol 121, 265–275.CrossRefGoogle ScholarPubMed
Yao, T, Gu, X, Liang, X, et al. (2021) Tolerance assessment of dietary bile acids in common carp (Cyprinus carpio L.) fed a high plant protein diet. Aquaculture 543, 737012.CrossRefGoogle Scholar
Xu, J, Xie, S, Chi, S, et al. (2022) Protective effects of taurocholic acid on excessive hepatic lipid accumulation via regulation of bile acid metabolism in grouper. Food Funct 13, 3050–3062.CrossRefGoogle ScholarPubMed
Zhou, JS, Chen, HJ, Ji, H, et al. (2018) Effect of dietary bile acids on growth, body composition, lipid metabolism and microbiota in grass carp (Ctenopharyngodon idella). Aquacult Nutr 24, 802–813
CrossRefGoogle Scholar
Du, J, Xu, H, Li, S, et al. (2017) Effects of dietary chenodeoxycholic acid on growth performance, body composition and related gene expression in large yellow croaker (Larimichthys crocea) fed diets with high replacement of fish oil with soybean oil. Aquaculture 479, 584–590.CrossRefGoogle Scholar
Yin, P, Xie, SW, Zhuang, ZX, et al. (2021) Dietary supplementation of bile acid attenuate adverse effects of high-fat diet on growth performance, antioxidant ability, lipid accumulation and intestinal health in juvenile largemouth bass (Micropterus salmoides). Aquaculture 531, 735864.CrossRefGoogle Scholar
Gong, G, Dan, C, Xiao, S, et al. (2018) Chromosomal-level assembly of yellow catfish genome using third-generation DNA sequencing and Hi-C analysis. GigaScience 7, 120.Google ScholarPubMed
Han, Q, Tian, Z, Xia, W, et al. (2005) Optimal dietary lipid requirement of yellow catfish Pelteobagrus fulvidraco
. Fish Sci 24, 8–11.Google Scholar
Zheng, K, Zhu, X, Han, D, et al. (2010) Effects of dietary lipid levels on growth, survival and lipid metabolism during early ontogeny of Pelteobagrus vachelli larvae. Aquaculture 299, 121–127.CrossRefGoogle Scholar
Zhu, H, Qiang, J, He, J, et al. (2021) Physiological parameters and gut microbiome associated with different dietary lipid levels in hybrid yellow catfish (Tachysurus fulvidraco♀× Pseudobagrus vachellii♂). Comp Biochem Physiol Part D Genomics Proteomics 37, 100777.CrossRefGoogle ScholarPubMed
Ling, SC, Wu, K, Zhang, DG, et al. (2019) Endoplasmic reticulum stress-mediated autophagy and apoptosis alleviate dietary fat-induced triglyceride accumulation in the intestine and in isolated intestinal epithelial cells of yellow catfish. J Nutr 149, 1732–1741.CrossRefGoogle ScholarPubMed
Fei, S, Xia, Y, Chen, Z, et al. (2022) A high-fat diet alters lipid accumulation and oxidative stress and reduces the disease resistance of overwintering hybrid yellow catfish (Pelteobagrus fulvidraco♀×P. vachelli♂). Aquacult Rep 23, 101043.Google Scholar
Song, YF, Hogstrand, C, Ling, SC, et al. (2020) Creb-Pgc1α pathway modulates the interaction between lipid droplets and mitochondria and influences high fat diet-induced changes of lipid metabolism in the liver and isolated hepatocytes of yellow catfish. J Nutr Biochem 80, 108364.CrossRefGoogle ScholarPubMed
Yang, SB, Zhao, T, Wu, LX, et al. (2020) Effects of dietary carbohydrate sources on lipid metabolism and SUMOylation modification in the liver tissues of yellow catfish. Br J Nutr 124, 1241–1250.CrossRefGoogle ScholarPubMed
AOAC (2006) Association of Official Analytical Chemists, Official Methods of Analysis 16th. Arlington, VA: AOAC. 0066–961X.Google Scholar
Jin, M, Pan, T, Cheng, X, et al. (2019) Effects of supplemental dietary L-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet. Aquaculture 504, 199–209.CrossRefGoogle Scholar
Peng, X, Feng, L, Jiang, W, et al. (2019) Supplementation exogenous bile acid improved growth and intestinal immune function associated with NF-κB and TOR signalling pathways in on-growing grass carp (Ctenopharyngodon idella): enhancement the effect of protein-sparing by dietary lipid. Fish Shellfish Immunol 92, 552–569.CrossRefGoogle ScholarPubMed
Jiang, M, Wen, H, Gou, GW, et al. (2018) Preliminary study to evaluate the effects of dietary bile acids on growth performance and lipid metabolism of juvenile genetically improved farmed tilapia (Oreochromis niloticus) fed plant ingredient-based diets. Aquacult Nutr 24, 1175–1183.CrossRefGoogle Scholar
Li, Y, Liang, SS, Shao, YR, et al. (2021) Impacts of dietary konjac glucomannan supplementation on growth, antioxidant capacity, hepatic lipid metabolism and inflammatory response in golden pompano (Trachinotus ovatus) fed a high fat diet. Aquaculture 545, 737113.CrossRefGoogle Scholar
Desouky, HE, Jiang, GZ, Zhang, DD, et al. (2020) Influences of glycyrrhetinic acid (GA) dietary supplementation on growth, feed utilization, and expression of lipid metabolism genes in channel catfish (Ictalurus punctatus) fed a high-fat diet. Fish Physiol Biochem 46, 653–663.CrossRefGoogle ScholarPubMed
Teodoro, JS, Zouhar, P, Flachs, P, et al. (2014) Enhancement of brown fat thermogenesis using chenodeoxycholic acid in mice. Int J Obes 38, 1027–1034.CrossRefGoogle ScholarPubMed
Li, JN & Dawson, PA (2019) Animal models to study bile acid metabolism. Biochim Biophys Acta Mol Basis Dis 1865, 895–911.CrossRefGoogle ScholarPubMed
Chun, HJ, Shim, YJ & Kwon, YH (2022) Cholic acid supplementation accelerates the progression of nonalcoholic fatty liver disease to the procarcinogenic state in mice fed a high-fat and high-cholesterol diet. J Nutr Biochem 100, 108869.CrossRefGoogle Scholar
Xiong, F, Wu, S, Qin, L, et al. (2019) Transcriptome analysis of grass carp provides insights into disease-related genes and novel regulation pattern of bile acid feedback in response to lithocholic acid. Aquaculture 500, 613–621.CrossRefGoogle Scholar
Yu, J, Lo, JL, Huang, L, et al. (2002) Lithocholic acid decreases expression of bile salt export pump through farnesoid X receptor antagonist activity. J Biol Chem 277, 31441–31447.CrossRefGoogle ScholarPubMed
Li, T, Jahan, A & Chiang, JY (2006) Bile acids and cytokines inhibit the human cholesterol 7 α
-hydroxylase gene via the JNK/c-jun pathway in human liver cells. Hepatology 43, 1202–1210.CrossRefGoogle ScholarPubMed
Yang, L, Liu, M, Zhao, M, et al. (2023) Dietary bile acid supplementation could regulate the glucose, lipid metabolism, and microbiota of common carp (Cyprinus carpio L.) fed with a high-lipid diet. Aquacult Nutr 2023, 9953927.Google ScholarPubMed
Liu, N, Zhao, J, Wang, J, et al. (2016) Farnesoid X receptor ligand CDCA suppresses human prostate cancer cells growth by inhibiting lipid metabolism via targeting sterol response element binding protein 1. Am J Transl Res 8, 5118–5124.Google ScholarPubMed
Xu, H, Zhang, Q, Kim, SK, et al. (2020) Dietary taurine stimulates the hepatic biosynthesis of both bile acids and cholesterol in the marine teleost, tiger puffer (Takifugu rubripes). Br J Nutr 123, 1345–1356.CrossRefGoogle ScholarPubMed
Noh, K, Kim, YM, Kim, YW, et al. (2011) Farnesoid X receptor activation by chenodeoxycholic acid induces detoxifying enzymes through AMP-activated protein kinase and extracellular signal-regulated kinase 1/2-mediated phosphorylation of CCAAT/enhancer binding protein β
. Drug Metab Dispos 39, 1451–1459.CrossRefGoogle ScholarPubMed
Zhang, DG, Zhao, T, Hogstrand, C, et al. (2021) Oxidized fish oils increased lipid deposition via oxidative stress-mediated mitochondrial dysfunction and the CREB1-Bcl2-Beclin1 pathway in the liver tissues and hepatocytes of yellow catfish. Food Chem 360, 129814.CrossRefGoogle ScholarPubMed
Togawa, N, Takahashi, R, Hirai, S, et al. (2013) Gene expression analysis of the liver and skeletal muscle of psyllium-treated mice. Br J Nutr 109, 383–393.CrossRefGoogle ScholarPubMed
Betancor, MB, Ortega, A, de la Gándara, F, et al. (2019) Performance, feed utilization, and hepatic metabolic response of weaned juvenile Atlantic bluefin tuna (Thunnus thynnus L.): effects of dietary lipid level and source. Fish Physiol Biochem 45, 697–718.CrossRefGoogle ScholarPubMed
Kawabe, Y, Shimokawa, T, Matsumoto, A, et al. (1995) The molecular mechanism of the induction of the low density lipoprotein receptor by chenodeoxycholic acid in cultured human cells. Biochem Biophys Res Commun 208, 405–411.CrossRefGoogle ScholarPubMed
Nilsson, LM, Abrahamsson, A, Sahlin, S, et al. (2007) Bile acids and lipoprotein metabolism: effects of cholestyramine and chenodeoxycholic acid on human hepatic mRNA expression. Biochem Biophys Res Commun 357, 707–711.CrossRefGoogle ScholarPubMed
Pawlak, M, Lefebvre, P & Staels, B (2015) Molecular mechanism of PPARα action and its impact on lipid metabolism, inflammation and fibrosis in non-alcoholic fatty liver disease. J Hepatol 623, 720–733.CrossRefGoogle Scholar
López-Oliva, ME, Garcimartin, A & Muñoz-Martínez, E (2017) Dietary α-lactalbumin induced fatty liver by enhancing nuclear liver X receptor αβ/sterol regulatory element-binding protein-1c/PPARγ expression and minimising PPARα/carnitine palmitoyltransferase-1 expression and AMP-activated protein kinase α phosphorylation associated with atherogenic dyslipidaemia, insulin resistance and oxidative stress in Balb/c mice. Br J Nutr 118, 914–929.CrossRefGoogle ScholarPubMed
Pineda Torra, I, Claudel, T, Duval, C, et al. (2003) Bile acids induce the expression of the human peroxisome proliferator-activated receptor α gene via activation of the farnesoid X receptor. Mol Endocrinol 17, 259–272.CrossRefGoogle ScholarPubMed
Zheng et al. supplementary material
Tables S1-S3
File
43 KB