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Adaptation of AMPK-mTOR-signal pathways and lipid metabolism in response to low- and high-level rapeseed meal diet in Chinese perch (Siniperca chuatsi)

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Abstract

It is well known that carnivorous fish cannot use plant-proteins efficiently. They affect lipid metabolism of fish and cause serious problems to fish health. The reasons for this deficiency of fish metabolism are not known well. Chinese perch, a carnivorous fish, can accept artificial diet after domestication and is also considered as a novel model of fish for nutrition studies. Therefore, the aim of this study was to explore the effect of fish meal replacement by low- or high-rapeseed meal on lipid and glucose metabolism of Chinese perch. Three experimental diets were formulated with 0, 10%, and 30% rapeseed meal, named as Control, RSL, and RSH groups, respectively. After 8-weeks of the feeding trial, the inhibition of growth and fat deposition were observed in Chinese perch fed with rapeseed meal diets compared to the control group. Fish fed with RSL diets showed decreased food intake, serum low density lipoprotein (LDL), phosphorylated Grb10 (P < 0.05), inhibited fatty acid (FA) transport (lipoprotein lipase (LPL)), and glycerol synthesis (phosphoenol pyruvate carboxykinase (PEPCK)) in the liver. In addition, fish fed with RSL diets were also inhibited FA synthesis (fatty acid synthase (FAS), sterol regulatory element binding protein 1 (SREBP1), and Acetyl-CoA carboxylase (ACC1)), lipid uptake (hepatic lipase (HL)), β-oxidation (carnitine palmitoyltransferase I (CPT1)), and glycerol synthesis (PEPCK) in the visceral adipose tissue. Fish fed with RSH diets showed phosphorylated AMPK, inhibited FA synthesis (SREBP1, ACC1, and FAS), while enhanced lipolysis (hormone-sensitive lipase (HSL)), and then reduced Acetyl-CoA pool. In turn, β-oxidation (peroxisome proliferator-activated receptor-a (PPARα) and CPT1) was inhibited, while glycolysis (glucose-6-phosphatase (G6PD) and pyruvate carboxylase (PC)) were enhanced, consequently the lipid accumulation was decreased in the liver. Fish were also inhibited lipid uptake (LPL), that caused inhibiting of FA synthesis (SREBP1), β-oxidation (CPT1), glycerol synthesis (PEPCK), and in turn improved lipolysis (HSL) in the visceral adipose tissue. Our study suggested that both RSL and RSH diets decreased lipid accumulation in Chinese perch; however, the mechanism of lipid metabolism was different. Fish accepted less diet in RSL group, which inhibited lipid metabolism in the liver and in the visceral adipose tissues, while fish in RSH group activated AMPK pathway, inhibited FA synthesis, and enhanced lipolysis, which reduced Acetyl-CoA pool in the liver. Subsequently, lipid uptake and metabolism were inhibited in the visceral adipose tissue of RSH fish.

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All data used to arrival at conclusions of this paper are present in this manuscript. The raw data are available from the authors on request.

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Acknowledgements

This work was financially supported by China Agriculture Research System (CARS-46); National Key R&D Program of China (2018YFD0900400), the National Natural Science Foundation of China (31772822).

Funding

China Agriculture Research System (CARS-46); National Key R&D Program of China (2018YFD0900400), the National Natural Science Foundation of China (31772822).

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Authors and Affiliations

  1. College of Fisheries, Chinese Perch Research Center, Huazhong Agricultural University, Wuhan, 430070, China

    Jiao Li, Xu-Fang Liang, Muhammad Shoaib Alam, Haocan Luo, Yanpeng Zhang, Binbin Peng, Qianqian Xiao, Zhilu Zhang, Liwei Liu & Shan He

  2. Innovation Base for Chinese Perch Breeding, Key Lab of Freshwater Animal Breeding, Ministry of Agriculture, Wuhan, 430070, China

    Jiao Li, Xu-Fang Liang, Muhammad Shoaib Alam, Haocan Luo, Yanpeng Zhang, Binbin Peng, Qianqian Xiao, Zhilu Zhang, Liwei Liu & Shan He

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Contributions

X-FL conceived and designed the experiments; JL, MSA, HL, YZ, BP, QX, ZZ, SH, and LL performed the experiments; HL, YZ and BP, MSA, completed in feeding trial; JL, MSA, QX, ZZ and SH write and revised the manuscript.

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Correspondence to Xu-Fang Liang.

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All experimental procedures followed the guidance for animal protocol and were approved by Huazhong Agricultural University (Wuhan, Hubei, China).

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Li, J., Liang, XF., Alam, M.S. et al. Adaptation of AMPK-mTOR-signal pathways and lipid metabolism in response to low- and high-level rapeseed meal diet in Chinese perch (Siniperca chuatsi). J Comp Physiol B 191, 881–894 (2021). https://doi.org/10.1007/s00360-021-01393-7

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