Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells

ABSTRACT: Glucose Transporter 4 (GLUT4) is a crucial protein facilitating glucose uptake and metabolism across cell membranes in mammals. However, information on GLUT4 in birds has historically been limited. In this study, we investigated the dynamic expression profile of chicken GLUT4 using real-ti...

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Main Authors: Lin Zhang, Pengna Luo, Huihong Li, Yuxian Pan, Huaiyong Zhang, Xuemeng Si, Wen Chen, Yanqun Huang
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579124009829
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author Lin Zhang
Pengna Luo
Huihong Li
Yuxian Pan
Huaiyong Zhang
Xuemeng Si
Wen Chen
Yanqun Huang
author_facet Lin Zhang
Pengna Luo
Huihong Li
Yuxian Pan
Huaiyong Zhang
Xuemeng Si
Wen Chen
Yanqun Huang
author_sort Lin Zhang
collection DOAJ
description ABSTRACT: Glucose Transporter 4 (GLUT4) is a crucial protein facilitating glucose uptake and metabolism across cell membranes in mammals. However, information on GLUT4 in birds has historically been limited. In this study, we investigated the dynamic expression profile of chicken GLUT4 using real-time quantitative PCR (RT-qPCR) and examined its potential effects and mechanisms via GLUT4 overexpression and RNA sequencing (RNA-seq) in chicken primary skeletal muscle satellite cells (CP-SMSCs). Our results demonstrated that chicken GLUT4 is differentially expressed across tissues, with predominant expression in skeletal muscles, and across developmental stages of CP-SMSCs, with notable upregulation during the phases of cell proliferation and early differentiation. Notably, 0.1 μM insulin for 60 min significantly elevated the expression of GLUT4 in CP-SMSCs (P < 0.05). GLUT4 overexpression in CP-SMSCs promoted cell proliferation, as evidenced by Cell Counting Kit-8 (CCK-8) (P < 0.05) and 5-Ethynyl-2′-Deoxyuridine (EDU) assays (P < 0.05), and enhanced glucose consumption following 0.1 μM insulin treatment (P < 0.05). However, it inhibited glucose consumption 12 h after the addition of 5 g/L glucose (P < 0.05). After overexpressing GLUT4, we identified 302 differentially expressed genes (DEGs) in CP-SMSCs, with 134 upregulated and 168 downregulated. These DEGs are primarily enriched in pathways such as oxidative phosphorylation, ribosome, cardiac muscle contraction, ATP metabolic processes, and mitochondrial protein complexes. Specifically, in the enriched oxidative phosphorylation pathway, the upregulated DEGs (12) encode mitochondrial proteins, while the downregulated DEGs (6) are nuclear genome-derived. The ribosomal pathway is predominantly inhibited, accompanying with the downregulation of the translocase of outer mitochondrial membrane 7 (TOMM7)/translocase of inner mitochondrial membrane 8 (TIMM8A) complex responsible for mitochondrial protein transport, and a reduction in 28S (LOC121106978) and 18S (LOC112533601) ribosomal rRNAs. In conclusion, chicken GLUT4 is dynamically modulated during development and acts as an insulin responder that significantly regulates cellular glucose uptake and cell proliferation. This regulation occurs mainly through enhancing the mitochondrial oxidative phosphorylation and inhibiting ribosomal pathway.
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publishDate 2024-12-01
publisher Elsevier
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series Poultry Science
spelling doaj-art-0d6629e6d8f34313992066d6f1342e0f2024-12-14T06:29:09ZengElsevierPoultry Science0032-57912024-12-0110312104403Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cellsLin Zhang0Pengna Luo1Huihong Li2Yuxian Pan3Huaiyong Zhang4Xuemeng Si5Wen Chen6Yanqun Huang7College 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, ChinaCollege of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaCorresponding author:; College of Animal Science and Technology, Henan Agricultural University, Zhengzhou, Henan 450046, ChinaABSTRACT: Glucose Transporter 4 (GLUT4) is a crucial protein facilitating glucose uptake and metabolism across cell membranes in mammals. However, information on GLUT4 in birds has historically been limited. In this study, we investigated the dynamic expression profile of chicken GLUT4 using real-time quantitative PCR (RT-qPCR) and examined its potential effects and mechanisms via GLUT4 overexpression and RNA sequencing (RNA-seq) in chicken primary skeletal muscle satellite cells (CP-SMSCs). Our results demonstrated that chicken GLUT4 is differentially expressed across tissues, with predominant expression in skeletal muscles, and across developmental stages of CP-SMSCs, with notable upregulation during the phases of cell proliferation and early differentiation. Notably, 0.1 μM insulin for 60 min significantly elevated the expression of GLUT4 in CP-SMSCs (P < 0.05). GLUT4 overexpression in CP-SMSCs promoted cell proliferation, as evidenced by Cell Counting Kit-8 (CCK-8) (P < 0.05) and 5-Ethynyl-2′-Deoxyuridine (EDU) assays (P < 0.05), and enhanced glucose consumption following 0.1 μM insulin treatment (P < 0.05). However, it inhibited glucose consumption 12 h after the addition of 5 g/L glucose (P < 0.05). After overexpressing GLUT4, we identified 302 differentially expressed genes (DEGs) in CP-SMSCs, with 134 upregulated and 168 downregulated. These DEGs are primarily enriched in pathways such as oxidative phosphorylation, ribosome, cardiac muscle contraction, ATP metabolic processes, and mitochondrial protein complexes. Specifically, in the enriched oxidative phosphorylation pathway, the upregulated DEGs (12) encode mitochondrial proteins, while the downregulated DEGs (6) are nuclear genome-derived. The ribosomal pathway is predominantly inhibited, accompanying with the downregulation of the translocase of outer mitochondrial membrane 7 (TOMM7)/translocase of inner mitochondrial membrane 8 (TIMM8A) complex responsible for mitochondrial protein transport, and a reduction in 28S (LOC121106978) and 18S (LOC112533601) ribosomal rRNAs. In conclusion, chicken GLUT4 is dynamically modulated during development and acts as an insulin responder that significantly regulates cellular glucose uptake and cell proliferation. This regulation occurs mainly through enhancing the mitochondrial oxidative phosphorylation and inhibiting ribosomal pathway.http://www.sciencedirect.com/science/article/pii/S0032579124009829chickenglucose transporter 4skeletal muscle satellite cellinsulinmitochondrial oxidative phosphorylation
spellingShingle Lin Zhang
Pengna Luo
Huihong Li
Yuxian Pan
Huaiyong Zhang
Xuemeng Si
Wen Chen
Yanqun Huang
Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
Poultry Science
chicken
glucose transporter 4
skeletal muscle satellite cell
insulin
mitochondrial oxidative phosphorylation
title Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
title_full Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
title_fullStr Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
title_full_unstemmed Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
title_short Chicken GLUT4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
title_sort chicken glut4 function via enhancing mitochondrial oxidative phosphorylation and inhibiting ribosome pathway in skeletal muscle satellite cells
topic chicken
glucose transporter 4
skeletal muscle satellite cell
insulin
mitochondrial oxidative phosphorylation
url http://www.sciencedirect.com/science/article/pii/S0032579124009829
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