Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2

Summary: Skeletal muscle is a highly plastic organ that adapts to different metabolic states or functional demands. This study explored the impact of permanent glucose restriction (GR) on skeletal muscle composition and metabolism. Using Glut4m mice with defective glucose transporter 4, we conducted...

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Main Authors: Kaiyi Zhang, Ning Xie, Huaqiong Ye, Jiakun Miao, Boce Xia, Yu Yang, Huanqi Peng, Shuang Xu, Tianwen Wu, Cong Tao, Jinxue Ruan, Yanfang Wang, Shulin Yang
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004223026676
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author Kaiyi Zhang
Ning Xie
Huaqiong Ye
Jiakun Miao
Boce Xia
Yu Yang
Huanqi Peng
Shuang Xu
Tianwen Wu
Cong Tao
Jinxue Ruan
Yanfang Wang
Shulin Yang
author_facet Kaiyi Zhang
Ning Xie
Huaqiong Ye
Jiakun Miao
Boce Xia
Yu Yang
Huanqi Peng
Shuang Xu
Tianwen Wu
Cong Tao
Jinxue Ruan
Yanfang Wang
Shulin Yang
author_sort Kaiyi Zhang
collection DOAJ
description Summary: Skeletal muscle is a highly plastic organ that adapts to different metabolic states or functional demands. This study explored the impact of permanent glucose restriction (GR) on skeletal muscle composition and metabolism. Using Glut4m mice with defective glucose transporter 4, we conducted multi-omics analyses at different ages and after low-intensity treadmill training. The oxidative fibers were significantly increased in Glut4m muscles. Mechanistically, GR activated AMPK pathway, promoting mitochondrial function and beneficial myokine expression, and facilitated slow fiber formation via CaMK2 pathway. Phosphorylation-activated Perm1 may synergize AMPK and CaMK2 signaling. Besides, MAPK and CDK kinases were also implicated in skeletal muscle protein phosphorylation during GR response. This study provides a comprehensive signaling network demonstrating how GR influences muscle fiber types and metabolic patterns. These insights offer valuable data for understanding oxidative fiber formation mechanisms and identifying clinical targets for metabolic diseases.
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spelling doaj.art-41701b2e26f24b90b443040f37adc36b2023-12-10T06:16:59ZengElsevieriScience2589-00422024-01-01271108590Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2Kaiyi Zhang0Ning Xie1Huaqiong Ye2Jiakun Miao3Boce Xia4Yu Yang5Huanqi Peng6Shuang Xu7Tianwen Wu8Cong Tao9Jinxue Ruan10Yanfang Wang11Shulin Yang12State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China; Precision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, TERRA Teaching and Research Centre, Liège University, 5030 Gembloux, BelgiumState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education & Key Lab of Swine Genetics and Breeding of Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University, Wuhan 430070, China; Corresponding authorState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China; Corresponding authorState Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China; Corresponding authorSummary: Skeletal muscle is a highly plastic organ that adapts to different metabolic states or functional demands. This study explored the impact of permanent glucose restriction (GR) on skeletal muscle composition and metabolism. Using Glut4m mice with defective glucose transporter 4, we conducted multi-omics analyses at different ages and after low-intensity treadmill training. The oxidative fibers were significantly increased in Glut4m muscles. Mechanistically, GR activated AMPK pathway, promoting mitochondrial function and beneficial myokine expression, and facilitated slow fiber formation via CaMK2 pathway. Phosphorylation-activated Perm1 may synergize AMPK and CaMK2 signaling. Besides, MAPK and CDK kinases were also implicated in skeletal muscle protein phosphorylation during GR response. This study provides a comprehensive signaling network demonstrating how GR influences muscle fiber types and metabolic patterns. These insights offer valuable data for understanding oxidative fiber formation mechanisms and identifying clinical targets for metabolic diseases.http://www.sciencedirect.com/science/article/pii/S2589004223026676CompMetabolomicsOmicsGenomicsProteomics
spellingShingle Kaiyi Zhang
Ning Xie
Huaqiong Ye
Jiakun Miao
Boce Xia
Yu Yang
Huanqi Peng
Shuang Xu
Tianwen Wu
Cong Tao
Jinxue Ruan
Yanfang Wang
Shulin Yang
Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
iScience
Comp
Metabolomics
Omics
Genomics
Proteomics
title Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
title_full Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
title_fullStr Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
title_full_unstemmed Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
title_short Glucose restriction enhances oxidative fiber formation: A multi-omic signal network involving AMPK and CaMK2
title_sort glucose restriction enhances oxidative fiber formation a multi omic signal network involving ampk and camk2
topic Comp
Metabolomics
Omics
Genomics
Proteomics
url http://www.sciencedirect.com/science/article/pii/S2589004223026676
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