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The circadian rhythm regulates branched-chain amino acids metabolism in fast muscle of Chinese perch (Siniperca chuatsi) during short-term fasting by Clock-KLF15-Bcat2 pathway

Published online by Cambridge University Press:  14 November 2022

Xin Zhu ,
Jingjie Liu ,
Minglang Cai ,
Lingsheng Bao ,
Yaxiong Pan ,
Ping Wu ,
Wuying Chu Open the ORCID record for Wuying Chu [Opens in a new window]  and
Jianshe Zhang
Xin Zhu
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
Jingjie Liu
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
Minglang Cai
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, People’s Republic of China
Lingsheng Bao
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
Yaxiong Pan
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
Ping Wu
Affiliation:
State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal University, Changsha 410081, People’s Republic of China
Wuying Chu*
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
Jianshe Zhang*
Affiliation:
Hunan Provincial Key Laboratory of Nutrition and Quality Control of Aquatic Animals, College of Biological and Chemical Engineering, Changsha University, Changsha 410022, People’s Republic of China
*
*Corresponding authors: Wuying Chu, email chuwuying18@163.com; Jianshe Zhang, email jzhang@ccsu.edu.cn
*Corresponding authors: Wuying Chu, email chuwuying18@163.com; Jianshe Zhang, email jzhang@ccsu.edu.cn
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Abstract

As an internal time-keeping mechanism, circadian rhythm plays crucial role in maintaining homoeostasis when in response to nutrition change; meanwhile, branched-chain amino acids (BCAA) in skeletal muscle play an important role in preserving energy homoeostasis during fasting. Previous results from our laboratory suggested that fasting can influence peripheral circadian rhythm and BCAA metabolism in fish, but the relationship between circadian rhythm and BCAA metabolism, and whether circadian rhythm regulates BCAA metabolism to maintain physiological homoeostasis during fasting remains unclear. This study shows that the expression of fifteen core clock genes as well as KLF15 and Bcat2 is highly responsive to short-term fasting in fast muscle of Siniperca chuatsi, and the correlation coefficient between Clock and KLF15 expression is enhanced after fasting treatment. Furthermore, we demonstrate that the transcriptional expression of KLF15 is regulated by Clock, and the transcriptional expression of Bcat2 is regulated by KLF15 by using dual-luciferase reporter gene assay and Vivo-morpholinos-mediated gene knockdown technique. Therefore, fasting imposes a dynamic coordination of transcription between the circadian rhythm and BCAA metabolic pathways. The findings highlight the interaction between circadian rhythm and BCAA metabolism and suggest that fasting induces a switch in KLF15 expression through affecting the rhythmic expression of Clock, and then KLF15 promotes the transcription of Bcat2 to enhance the metabolism of BCAA, thus maintaining energy homoeostasis and providing energy for skeletal muscle as well as other tissues.

Keywords

Circadian rhythmBranched-chain amino acidsCatabolismEnergy homoeostasisShort-term fasting
Type
Research Article
Information
British Journal of Nutrition , Volume 130 , Issue 4 , 28 August 2023 , pp. 604 - 615
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Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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