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Grape seed proanthocyanidin extract ameliorates hepatic lipid accumulation and inflammation in grass carp (Ctenopharyngodon idella)

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Abstract

Hepatic lipid metabolism disorder due to excessive fat accumulation in fish is a significant problem in aquaculture. Studies have shown that grape seed procyanidin extract (GSPE) can regulate fish lipid metabolism and improve fish immunity. However, the mechanism is unclear. In this study, we used grass carp that stores excess fat in the liver as a model. In vitro, GSPE treatment of hepatocytes for 3 h significantly decreased TG content, accompanied with decreased expression of SREBP-1c, FAS, and ACC and increased expression of PPARα, ATGL, and LPL. GSPE treatment for 1 h significantly decreased expression of pro-inflammatory cytokines (TNFα, IL-6, IL-1β, and NF-κB) and increased the expression of anti-inflammatory cytokines (IL-10 and TGF-β1). In vivo, the administration of GSPE significantly reduced high-fat diet-induced increase of serum CHOL, TG, and HDL, but increased LDL content. GSPE treatment for 3 h increased expression of ATGL and LPL, and significantly decreased the expression of HFD-fed-induced SREBP-1c, ACC, FAS, PPARγ, PPARα, and H-FABP. GSPE treatment for 3 h also significantly decreased the expression of pro-inflammatory cytokines (TNFα, IL-6, and IL-1β) and increased the expression of the anti-inflammatory cytokine IL-10. The expression levels of the lipogenic miRNAs, miR-33, and miR-122, were suppressed both in vivo and in vitro by GSPE. In summary, GSPE had hypolipidemic and potential anti-inflammatory effects in the liver, potentially mediated by miR-33 and miR-122.

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Abbreviations

ACC:

Acetyl-CoA carboxylase

ALT:

Alanine aminotransferase

AST:

Aspartate aminotransferase

ATGL:

Adipose triglyceride lipase

CHOL:

Total cholesterol

CPT1:

Carnitine palmitoyltransferase 1

FABP:

Fatty acids-binding protein

FAS:

Fatty acid synthase

GSPE:

Grape seed procyanidin extract

HDL:

High-density lipoprotein

HFD:

High-fat diet

H-FABP:

Heart-type fatty acid-binding protein

IL-1β:

Interleukin-1β

IL-6:

Interleukin-6

IL-10:

Interleukin-10

LDL:

Low-density lipoprotein

LPL:

Lipoprotein lipase

MAPK:

Mitogen-activated protein kinase

miRNA:

MicroRNA

NF-κB:

Nuclear factor-κB

PPAR:

Peroxisome proliferator-activated receptor

SCD1:

Stearoyl-coenzyme A desaturase 1

SREBP-1:

Sterol regulatory element-binding proteins-1

TG:

Triglyceride

TGF-β1:

Transforming growth factor-β1

TNFα:

Tumor necrosis factor α

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Funding

This work was supported by the NSFC-United Fund Key Support Project of Henan (U1704109), the National Natural Science Foundation of China (31402311, 31672671, and 31872581), the Science and Technology Breakthrough Major Project in Henan Province (182102410031), and the Natural Science Foundation of Henan Province (162300410165).

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Authors and Affiliations

  1. College of Fisheries, Henan Normal University, 46 Jianshe Road, Xinxiang, 453007, People’s Republic of China

    Rong-Hua Lu, Chao-Bin Qin, Feng Yang, Wen-Ya Zhang, Yu-Ru Zhang, Guo-Kun Yang, Li-Ping Yang, Xiao-Lin Meng, Xiao Yan & Guo-Xing Nie

  2. Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Xinxiang, 453007, China

    Rong-Hua Lu, Feng Yang, Wen-Ya Zhang, Yu-Ru Zhang, Li-Ping Yang, Xiao-Lin Meng, Xiao Yan & Guo-Xing Nie

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  1. Rong-Hua Lu
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  2. Chao-Bin Qin
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Lu, RH., Qin, CB., Yang, F. et al. Grape seed proanthocyanidin extract ameliorates hepatic lipid accumulation and inflammation in grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 46, 1665–1677 (2020). https://doi.org/10.1007/s10695-020-00819-3

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