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Effects of berberine on growth, liver histology, and expression of lipid-related genes in blunt snout bream (Megalobrama amblycephala) fed high-fat diets

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Abstract

Fatty liver of cultured fish often correlates closely with poor growth and low harvest yield. Some Chinese herbs can reduce hepatic fat storage. This study aimed to examine lipid-lowering effect of berberine (BBR) in blunt snout bream (Megalobrama amblycephala). Triplicate groups of fish were fed four experimental diets: low-fat diet (LFD, 5% fat), high-fat diet (HFD, 15% fat), and HFD supplemented with 50 or 100 mg BBR/kg diet (BBR50, BBR100). After 8-week feeding, growth performance, liver histology and fat deposition, and hepatic genes expression were examined. The results showed significant reduction of growth performance and feed intake in fish fed HFD compared to those fed the LFD and BBR50 diets. Supplementing 50 mg BBR/kg to the HFD significantly improved weight gain and feed intake. Higher hepatic fat content and histological abnormalities were found in the liver of fish receiving HFD, and BBR50 and BBR100 could attenuate these abnormalities of liver. Expression of CPT I, AOX, ApoB100, ApoE, and PGC-1α genes was significantly decreased in fish fed HFD, and 50 and 100 mg/kg BBR supplementation could revert the downregulation of these genes. Also, the expression of FATP, LPL, and LDLR genes was upregulated in HFD-fed fish, and their expression was significantly decreased by 50 and 100 mg/kg BBR supplementation. In conclusion, supplementing BBR to HFD could attenuate liver fat deposition and disorders. The fat-lowering effects of BBR appear to be mediated by activating genes related with fatty acid oxidation and decreasing genes for fatty acid uptake.

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Abbreviations

ACAD:

Acyl-CoA dehydrogenase

ALT:

Alanine aminotransferase

AMPK:

AMP-activated protein kinase

AOX:

Acyl-CoA oxidase

Apo B (E):

Apolipoprotein B (E)

BBR:

Berberine

CPT I:

Carnitine palmitoyltransferase I

FABP:

Fatty acid binding protein

FACS:

Fatty acyl-CoA synthetase

FATP:

Fatty acid transport protein

LDLR:

Low-density lipoprotein receptor

LPL:

Lipoprotein lipase

PGC-1α:

Peroxisome proliferator-activated receptor-gamma coactivator-1α

PPAR:

Peroxisome proliferator-activated receptor

SCD:

Stearoyl-CoA desaturase

References

  • Abidi P, Zhou Y, Jiang JD, Liu J (2005) Extracellular signal-regulated kinase-dependent stabilization of hepatic low-density lipoprotein receptor mRNA by herbal medicine berberine. Arterioscler Thromb Vasc Biol 25:2170–2176

    Article  PubMed  CAS  Google Scholar 

  • Beamish F, Medland T (1986) Protein sparing effects in large rainbow trout, Salmo gairdneri. Aquaculture 55:35–42

    Article  Google Scholar 

  • Bolla S, Nicolaisen O, Amin A (2011) Liver alterations induced by long term feeding on commercial diets in Atlantic halibut (Hippoglossus hippoglossus L.) females. Histological and biochemical aspects. Aquaculture 312:117–125

    Article  CAS  Google Scholar 

  • Brusq J-M, Ancellin N, Grondin P, Guillard R, Martin S, Saintillan Y, Issandou M (2006) Inhibition of lipid synthesis through activation of AMP kinase: an additional mechanism for the hypolipidemic effects of berberine. J Lipid Res 47:1281–1288

    Article  PubMed  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2011) Primer sequence disclosure: a clarification of the MIQE guidelines. Clin Chem 57:919–921

    Article  PubMed  CAS  Google Scholar 

  • Chen P, Chen J, Guo Z (2006) Preliminary research on the effect of Si-Ni-San on carp’s liver protection and recovery. Feed Ind 27:28–31

    Google Scholar 

  • Chiu HK, Qian K, Ogimoto K, Morton GJ, Wisse BE, Agrawal N, McDonald TO, Schwartz MW, Dichek HL (2010) Mice lacking hepatic lipase are lean and protected against diet-induced obesity and hepatic steatosis. Endocrinology 151:993–1001

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Domitrović R, Cvijanović O, Pernjak-Pugel E, Škoda M, Mikelić L, Crnčević-Orlić Ž (2013) Berberine exerts nephroprotective effect against cisplatin-induced kidney damage through inhibition of oxidative/nitrosative stress, inflammation, autophagy and apoptosis. Food Chem Toxicol 62:397–406

    Article  PubMed  CAS  Google Scholar 

  • Du ZY (2014) Causes of fatty liver in cultured fish: a review and perspectives. J Fish China 38:1628–1638

    Google Scholar 

  • Du L, Kang Y, Park MK et al (2003) Effects of 13-alkyl-substituted berberine alkaloids on the expression of COX-II. TNF-alpha. iNOS and iL-12 production in LPS-stimulated macrophages. Life Sci 73:1401–1412

    Article  CAS  Google Scholar 

  • Du ZY, Clouet P, Huang LM, Degrace P, Zheng WH, He JG, Tian LX, Liu YJ (2008) Utilization of different dietary lipid sources at high level in herbivorous grass carp (Ctenopharyngodon idella): mechanism related to hepatic fatty acid oxidation. Aquac Nutr 14:77–92

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Fuentes EN, Safian D, Einarsdottir IE, Valdés JA, Elorza AA, Molina A, Björnsson BT (2013) Nutritional status modulates plasma leptin, AMPK and TOR activation, and mitochondrial biogenesis: implications for cell metabolism and growth in skeletal muscle of the fine flounder. Gen Comp Endocrinol 186:172–180

    Article  PubMed  CAS  Google Scholar 

  • Hansen JØ, Berge GM, Hillestad M, Krogdahl Å, Galloway TF, Holm H, Holm J, Ruyter B (2008) Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels. Aquaculture 284:159–166

    Article  CAS  Google Scholar 

  • Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

    Article  CAS  Google Scholar 

  • Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Biochim Biophys Acta (BBA) 1486:1–17

    Article  CAS  Google Scholar 

  • Kim WS, Lee YS, Cha SH, Jeong HW, Choe SS, Lee MR, Oh GT, Park HS, Lee KU, Lane MD, Kim JB (2009) Berberine improves lipid dysregulation in obesity by controlling central and peripheral AMPK activity. Am J Physiol Endocrinol Metab 296:E812–E819

    Article  PubMed  CAS  Google Scholar 

  • Kong W, Wei J, Abidi P, Lin M, Inaba S, Li C, Wang Y, Wang Z, Si S, Pan H, Wang S, Wu J, Wang Y, Li Z, Liu J, Jiang JD (2004) Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 10:1344–1351

    Article  PubMed  CAS  Google Scholar 

  • Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, Hohnen-Behrens C, Gosby A, Kraegen EW, James DE, Kim JB (2006) Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55:2256–2264

    Article  PubMed  CAS  Google Scholar 

  • Li XF, Jiang YY, Liu WB, Ge XP (2012) Protein-sparing effect of dietary lipid in practical diets for blunt snout bream (Megalobrama amblycephala) fingerlings: effects on digestive and metabolic responses. Fish Physiol Biochem 38:529–541

    Article  PubMed  CAS  Google Scholar 

  • Lin D, Mao YQ, Cai FS (1990) Nutritional lipid liver disease of grass carp Ctenopharyngodon idullus Chinese. J Oceanol Limnol 8:363–373

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lu KL, Xu WN, Li XF, Liu WB, Wang LN, Zhang CN (2013) Hepatic triacylglycerol secretion, lipid transport and tissue lipid uptake in blunt snout bream (Megalobrama amblycephala) fed high-fat diet. Aquaculture 408-409:160–168

    Article  CAS  Google Scholar 

  • Lu KL, Xu WN, Liu WB, Wang LN, Zhang CN, Li XF (2014a) Association of mitochondrial dysfunction with oxidative stress and immune suppression in Blunt Snout Bream Megalobrama amblycephala fed a high-fat diet. J Aquat Anim Health 26:100–112

    Article  PubMed  CAS  Google Scholar 

  • Lu KL, Xu WN, Wang LN, Zhang DD, Zhang CN, Liu WB (2014b) Hepatic β-oxidation and regulation of carnitine palmitoyltransferase (CPT) I in blunt snout bream Megalobrama amblycephala fed a high fat diet. PLoS One 9:e93135

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 43:65–73

    Article  PubMed  CAS  Google Scholar 

  • Lupatsch, Kissil, Sklan, Pfeffer (2015) Effects of varying dietary protein and energy supply on growth, body composition and protein utilization in gilthead seabream (Sparus aurata L.). Aquac Nutr 7:71–80

    Article  Google Scholar 

  • Mo WY, Lun CH, Choi WM, Man YB, Wong MH (2016) Enhancing growth and non-specific immunity of grass carp and Nile tilapia by incorporating Chinese herbs (Astragalus membranaceus and Lycium barbarum) into food waste based pellets. Environ Pollut 219:475–482

    Article  PubMed  CAS  Google Scholar 

  • Morais S, Knoll-Gellida A, André M, Barthe C, Babin PJ (2007) Conserved expression of alternative splicing variants of peroxisomal acyl-CoA oxidase 1 in vertebrates and developmental and nutritional regulation in fish. Physiol Genomics 28:239–252

    Article  PubMed  CAS  Google Scholar 

  • Musso G, Gambino R, Cassader M (2009) Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Prog Lipid Res 48:1–26

    Article  PubMed  CAS  Google Scholar 

  • Peres H, Gonçalves P, Oliva-Teles A (1999) Glucose tolerance in gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax). Aquaculture 179:415–423

    Article  CAS  Google Scholar 

  • Richard N, Kaushik SL, Panserat S, Corraze G (2006) Replacing dietary fish oil by vegetable oils has little effect on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96:299–309

    Article  PubMed  CAS  Google Scholar 

  • Shan WJ, Huang L, Zhou Q, Meng FC, Li XS (2011) Synthesis, biological evaluation of 9-N-substituted berberine derivatives as multi-functional agents of antioxidant, inhibitors of acetylcholinesterase, butyrylcholinesterase and amyloid-β aggregation. Eur J Med Chem 46:5885–5893

    Article  PubMed  CAS  Google Scholar 

  • Siow YL, Sarna L, Karmin O (2011) Redox regulation in health and disease—therapeutic potential of berberine. Food Res Int 44:2409–2417

    Article  CAS  Google Scholar 

  • Wang H, Lu S, Du J, Yao Y, Berschneider HM, Black DD (2001) Regulation of apolipoprotein secretion by long-chain polyunsaturated fatty acids in newborn swine enterocytes. Am J Physiol Gastrointest Liver Physiol 280:G1137–G1142

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Li Y, Hou C, Gao Y, Wang Y (2015) Physiological and molecular changes in large yellow croaker (Pseudosciaena crocea R.) with high-fat diet-induced fatty liver disease. Aquac Res 46:272–282

    Article  CAS  Google Scholar 

  • Watanabe T (1982) Lipid nutrition in fish. Comp Biochem Physiol B Comp Biochem 73:3–15

    Article  Google Scholar 

  • Yoon M (2009) The role of PPARa in lipid metabolism and obesity: focusing on the effects of estrogen on PPARa actions. Pharmacol Res 60:151–159

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Li C, Yang J, Zhang T, Zhou Q (2016) Berberine is a potent agonist of peroxisome proliferator activated receptor alpha. Front Biosci 21:1052

    Article  CAS  Google Scholar 

  • Zhang P, Ma D, Wang Y, Zhang M, Qiang X, Liao M, Liu X, Wu H, Zhang Y (2014) Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice. Food Chem Toxicol 74:225–232

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Lu K, Jiang G, Liu W, Dong Z, Tian H, Li X (2015) A global transcriptional analysis of Megalobrama amblycephala revealing the molecular determinants of diet-induced hepatic steatosis. Gene 570:255–263

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Li C, Wang L, Ji H, Zhu T (2015) Hepatoprotective effects of a Chinese herbal formulation, Yingchen decoction, on olaquindox-induced hepatopancreas injury in Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 41:153–163

    Article  PubMed  CAS  Google Scholar 

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Funding

This work was funded by National Nature Science Foundation of China (31602171), Nature Science Foundation of Fujian Province (2017J05056) and Foundation of Fujian Provincial Education Department (JAT160258).

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Authors and Affiliations

  1. Fisheries College, Jimei University, Xiamen, 361021, China

    Wenhao Zhou, Samad Rahimnejad & Kangle Lu

  2. College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China

    Lina Wang & Wenbin Liu

Authors
  1. Wenhao Zhou
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  2. Samad Rahimnejad
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  3. Kangle Lu
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  4. Lina Wang
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  5. Wenbin Liu
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Corresponding author

Correspondence to Kangle Lu.

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Zhou, W., Rahimnejad, S., Lu, K. et al. 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, 83–91 (2019). https://doi.org/10.1007/s10695-018-0536-7

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