Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)

Our previous study on plant oil substitution for fish oil found that corn oil induced inflammatory responses in grouper, while olive oil was effective in anti-inflammatory and immune enhancing. As a vital active ingredient in olive oil, squalene has been widely studied for its antioxidant and anti-i...

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Main Authors: Xiaobo Yan, Simiao Pan, Xiangxiang Suo, Weibin Huang, Tao Li, Shuang Zhang, Yuanzhi Yang, Beiping Tan, Xiaohui Dong
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Aquaculture Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352513424006124
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author Xiaobo Yan
Simiao Pan
Xiangxiang Suo
Weibin Huang
Tao Li
Shuang Zhang
Yuanzhi Yang
Beiping Tan
Xiaohui Dong
author_facet Xiaobo Yan
Simiao Pan
Xiangxiang Suo
Weibin Huang
Tao Li
Shuang Zhang
Yuanzhi Yang
Beiping Tan
Xiaohui Dong
author_sort Xiaobo Yan
collection DOAJ
description Our previous study on plant oil substitution for fish oil found that corn oil induced inflammatory responses in grouper, while olive oil was effective in anti-inflammatory and immune enhancing. As a vital active ingredient in olive oil, squalene has been widely studied for its antioxidant and anti-inflammatory properties. Therefore, the present study was designed to use corn oil as the main lipid source to create a model of inflammation or low immunity and investigate the regulatory effect of squalene on the immunity of grouper, and to perform hepatic transcriptomic and metabolomic assays of grouper using omics technology, with the aim of providing basic data for the study of the mechanism of squalene. The results showed: squalene ingestion did not affect the growth performance of grouper (P > 0.05) but significantly improved immunity and the resistance of grouper to Vibrio harveyi (P < 0.05). Transcriptomic and metabolomic analyses showed that squalene activated the Wnt/β-Catenin signaling pathway and PI3K-Akt signaling pathway. Western blot results showed that squalene ingestion significantly upregulated Wnt/β-Catenin protein expression and downregulated the Axin protein expression (P < 0.05). Above results demonstrated that squalene enhanced immunity and disease resistance in grouper may be related to the activation of PI3K-Akt/ Wnt/β-Catenin signaling pathway, while the activation of β-Catenin could reduce the inflammatory response by inhibiting NF-κB-mediated inflammatory factors. The findings will contribute to the application of squalene as an immune enhancer for aquaculture and medical industry.
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spelling doaj-art-a981e859dcea44f2a3542f750395675b2025-02-06T05:12:02ZengElsevierAquaculture Reports2352-51342025-03-0140102524Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)Xiaobo Yan0Simiao Pan1Xiangxiang Suo2Weibin Huang3Tao Li4Shuang Zhang5Yuanzhi Yang6Beiping Tan7Xiaohui Dong8Laboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, China; Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong 524000, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaLaboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, China; Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong 524000, China; Correspondence to: Laboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China.Laboratory of Aquatic Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China; GuangDong Engineering Technology Research Center of Aquatic Animals Precision Nutrition and High Efficiency Feed, Zhanjiang, Guangdong 524088, China; Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong 524000, China; Correspondence to: Laboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China.Our previous study on plant oil substitution for fish oil found that corn oil induced inflammatory responses in grouper, while olive oil was effective in anti-inflammatory and immune enhancing. As a vital active ingredient in olive oil, squalene has been widely studied for its antioxidant and anti-inflammatory properties. Therefore, the present study was designed to use corn oil as the main lipid source to create a model of inflammation or low immunity and investigate the regulatory effect of squalene on the immunity of grouper, and to perform hepatic transcriptomic and metabolomic assays of grouper using omics technology, with the aim of providing basic data for the study of the mechanism of squalene. The results showed: squalene ingestion did not affect the growth performance of grouper (P > 0.05) but significantly improved immunity and the resistance of grouper to Vibrio harveyi (P < 0.05). Transcriptomic and metabolomic analyses showed that squalene activated the Wnt/β-Catenin signaling pathway and PI3K-Akt signaling pathway. Western blot results showed that squalene ingestion significantly upregulated Wnt/β-Catenin protein expression and downregulated the Axin protein expression (P < 0.05). Above results demonstrated that squalene enhanced immunity and disease resistance in grouper may be related to the activation of PI3K-Akt/ Wnt/β-Catenin signaling pathway, while the activation of β-Catenin could reduce the inflammatory response by inhibiting NF-κB-mediated inflammatory factors. The findings will contribute to the application of squalene as an immune enhancer for aquaculture and medical industry.http://www.sciencedirect.com/science/article/pii/S2352513424006124SqualeneInflammatoryTranscriptomicMetabolomicWnt/β-Catenin♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu
spellingShingle Xiaobo Yan
Simiao Pan
Xiangxiang Suo
Weibin Huang
Tao Li
Shuang Zhang
Yuanzhi Yang
Beiping Tan
Xiaohui Dong
Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
Aquaculture Reports
Squalene
Inflammatory
Transcriptomic
Metabolomic
Wnt/β-Catenin
♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu
title Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
title_full Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
title_fullStr Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
title_full_unstemmed Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
title_short Integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper (♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu)
title_sort integrative transcriptomic and metabolomic reveals squalene alleviating the inflammatory response and enhancing immunity of hybrid grouper ♀ epinephelus fuscoguttatus ♂ e lanceolatu
topic Squalene
Inflammatory
Transcriptomic
Metabolomic
Wnt/β-Catenin
♀ Epinephelus fuscoguttatus × ♂ E. lanceolatu
url http://www.sciencedirect.com/science/article/pii/S2352513424006124
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