Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration

Birds' glycolipid metabolism has garnered considerable attention due to their fasting blood glucose levels being nearly twice those of mammals. While skeletal muscle is the primary insulin-sensitive tissue in mammals, the effects of insulin on chicken skeletal muscle remain unclear. In this stu...

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Main Authors: Xiangli Zhang, Pengfei Du, Ziyang Wang, Yao Zhu, Xuemeng Si, Wen Chen, Yanqun Huang
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579124011970
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author Xiangli Zhang
Pengfei Du
Ziyang Wang
Yao Zhu
Xuemeng Si
Wen Chen
Yanqun Huang
author_facet Xiangli Zhang
Pengfei Du
Ziyang Wang
Yao Zhu
Xuemeng Si
Wen Chen
Yanqun Huang
author_sort Xiangli Zhang
collection DOAJ
description Birds' glycolipid metabolism has garnered considerable attention due to their fasting blood glucose levels being nearly twice those of mammals. While skeletal muscle is the primary insulin-sensitive tissue in mammals, the effects of insulin on chicken skeletal muscle remain unclear. In this study, the insulin-responsive metabolites were identified in broiler's pectoralis muscle (after 16 h of fasting) using widely targeted metabolomics. Glycolipid concentrations were measured using kits, and the expression of key genes involved in glucose metabolism was assessed via quantitative real-time PCR (qRT-PCR). The insulin tolerance test, performed by injecting 5 IU/kg body weight of insulin, demonstrated a rapid drop in blood glucose levels from 0 to 15 min, with a consistent reduction observed at 120 min (P < 0.01). Insulin did not alter glucose and glycogen content in chicken pectoralis; however, low-density lipoprotein (LDL, P < 0.05) levels were upregulated in the early phase (15 min). With an extended insulin duration (120 min), pectoralis glucose content increased (P < 0.05), accompanied by a reduction in TG levels (P < 0.05). Metabolomic analysis revealed that insulin promotes the downregulation of 63 out of 71 metabolites at 15 min and the upregulation of 101 out of 134 metabolites at 120 min, mainly associated with lysine degradation and thyroid hormone signaling pathways, respectively. 7 metabolites were dynamically modulated in the same manner over time (2 up-up and 5 down-down). Early insulin inhibited glycolysis, evidenced by the reduction in phosphoenolpyruvate levels and hexokinase 2 (HK2) expression; however, insulin promoted glucose uptake through the activation of glucose transporter 4 (GLUT4) and enhanced glycolysis, accompanied by elevated fatty acid metabolism at the later phase.In conclusion, insulin dynamically regulates the metabolomics of the pectoralis muscle over time. Initially, chicken muscle tissues downregulate metabolic activities to accommodate the new signaling state, followed by significant upregulation to meet heightened metabolic demands. Extended insulin monitoring promotes glucose uptake and glycolysis, alongside enhanced fatty acid metabolism. This research provides insights into the potential mechanisms of insulin action in chicken muscles.
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series Poultry Science
spelling doaj-art-6511cbfa2a2e49a3b775308e85caad272025-01-22T05:40:44ZengElsevierPoultry Science0032-57912025-01-011041104619Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended durationXiangli Zhang0Pengfei Du1Ziyang Wang2Yao Zhu3Xuemeng Si4Wen Chen5Yanqun Huang6College of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCorresponding authors.; College of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaBirds' glycolipid metabolism has garnered considerable attention due to their fasting blood glucose levels being nearly twice those of mammals. While skeletal muscle is the primary insulin-sensitive tissue in mammals, the effects of insulin on chicken skeletal muscle remain unclear. In this study, the insulin-responsive metabolites were identified in broiler's pectoralis muscle (after 16 h of fasting) using widely targeted metabolomics. Glycolipid concentrations were measured using kits, and the expression of key genes involved in glucose metabolism was assessed via quantitative real-time PCR (qRT-PCR). The insulin tolerance test, performed by injecting 5 IU/kg body weight of insulin, demonstrated a rapid drop in blood glucose levels from 0 to 15 min, with a consistent reduction observed at 120 min (P < 0.01). Insulin did not alter glucose and glycogen content in chicken pectoralis; however, low-density lipoprotein (LDL, P < 0.05) levels were upregulated in the early phase (15 min). With an extended insulin duration (120 min), pectoralis glucose content increased (P < 0.05), accompanied by a reduction in TG levels (P < 0.05). Metabolomic analysis revealed that insulin promotes the downregulation of 63 out of 71 metabolites at 15 min and the upregulation of 101 out of 134 metabolites at 120 min, mainly associated with lysine degradation and thyroid hormone signaling pathways, respectively. 7 metabolites were dynamically modulated in the same manner over time (2 up-up and 5 down-down). Early insulin inhibited glycolysis, evidenced by the reduction in phosphoenolpyruvate levels and hexokinase 2 (HK2) expression; however, insulin promoted glucose uptake through the activation of glucose transporter 4 (GLUT4) and enhanced glycolysis, accompanied by elevated fatty acid metabolism at the later phase.In conclusion, insulin dynamically regulates the metabolomics of the pectoralis muscle over time. Initially, chicken muscle tissues downregulate metabolic activities to accommodate the new signaling state, followed by significant upregulation to meet heightened metabolic demands. Extended insulin monitoring promotes glucose uptake and glycolysis, alongside enhanced fatty acid metabolism. This research provides insights into the potential mechanisms of insulin action in chicken muscles.http://www.sciencedirect.com/science/article/pii/S0032579124011970InsulinChicken pectoralisMetabolomicsGlycolipid metabolism
spellingShingle Xiangli Zhang
Pengfei Du
Ziyang Wang
Yao Zhu
Xuemeng Si
Wen Chen
Yanqun Huang
Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
Poultry Science
Insulin
Chicken pectoralis
Metabolomics
Glycolipid metabolism
title Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
title_full Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
title_fullStr Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
title_full_unstemmed Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
title_short Distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose-lipid metabolism with extended duration
title_sort distinct dynamic regulation of pectoralis muscle metabolomics by insulin and the promotion of glucose lipid metabolism with extended duration
topic Insulin
Chicken pectoralis
Metabolomics
Glycolipid metabolism
url http://www.sciencedirect.com/science/article/pii/S0032579124011970
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