Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT

Abstract Characterized by UCP1 expression and abundant mitochondria, brown adipose tissue (BAT) plays a crucial role in energy balance by converting chemical energy into heat through the cost of ATP production. In this study, it was demonstrated that Trib3 is a critical determinant of BAT-mediated e...

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Main Authors: Hyejin Yeo, Ji-Hye Lim, Ji Eom, MinJeong Kim, Hyeji Kwon, Sang-Wook Kang, Youngsup Song
Format: Article
Language:English
Published: Nature Publishing Group 2024-12-01
Series:Experimental and Molecular Medicine
Online Access:https://doi.org/10.1038/s12276-024-01361-5
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author Hyejin Yeo
Ji-Hye Lim
Ji Eom
MinJeong Kim
Hyeji Kwon
Sang-Wook Kang
Youngsup Song
author_facet Hyejin Yeo
Ji-Hye Lim
Ji Eom
MinJeong Kim
Hyeji Kwon
Sang-Wook Kang
Youngsup Song
author_sort Hyejin Yeo
collection DOAJ
description Abstract Characterized by UCP1 expression and abundant mitochondria, brown adipose tissue (BAT) plays a crucial role in energy balance by converting chemical energy into heat through the cost of ATP production. In this study, it was demonstrated that Trib3 is a critical determinant of BAT-mediated energy expenditure and whole-body energy homeostasis. Under 60% high-fat diet conditions, Trib3 expression in BAT was elevated. Mice deficient in Trib3 are resistant to diet-induced obesity and exhibit improved glucose homeostasis due to enhanced BAT activity. Furthermore, brown adipocyte progenitor cells (APCs) lacking Trib3 exhibited increased proliferation and promoted brown adipocyte differentiation and mitochondrial biogenesis, contributing to the increase in the maximal thermogenic capacity of BAT in Trib3-deficient mice. Mechanistically, it was discovered that Trib3 expression is upregulated by free fatty acids at the transcriptional level and synergistically upregulated by DAG-PKC at the posttranslational level. This occurs through the modulation of COP1-mediated Trib3 protein turnover. Interestingly, the level of Trib3 expression in BAT increased with age. Trib3 knockout mice were protected from aging-related weight gain and impaired glucose homeostasis. These results suggest that Trib3 acts as an obesity- and aging-associated factor that negatively regulates BAT activity and that the loss of Trib3 may provide a beneficial approach to prevent obesity and aging-associated metabolic syndrome by increasing the thermogenic capacity of BAT.
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spelling doaj-art-8fd9b3220a2d4274b89065ac434b5e8f2024-12-29T12:11:12ZengNature Publishing GroupExperimental and Molecular Medicine2092-64132024-12-0156122690270210.1038/s12276-024-01361-5Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BATHyejin Yeo0Ji-Hye Lim1Ji Eom2MinJeong Kim3Hyeji Kwon4Sang-Wook Kang5Youngsup Song6Department of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Biochemistry and Molecular Biology, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineDepartment of Brain Science, Brain Korea 21 Project, Asan Medical Center, University of Ulsan College of MedicineAbstract Characterized by UCP1 expression and abundant mitochondria, brown adipose tissue (BAT) plays a crucial role in energy balance by converting chemical energy into heat through the cost of ATP production. In this study, it was demonstrated that Trib3 is a critical determinant of BAT-mediated energy expenditure and whole-body energy homeostasis. Under 60% high-fat diet conditions, Trib3 expression in BAT was elevated. Mice deficient in Trib3 are resistant to diet-induced obesity and exhibit improved glucose homeostasis due to enhanced BAT activity. Furthermore, brown adipocyte progenitor cells (APCs) lacking Trib3 exhibited increased proliferation and promoted brown adipocyte differentiation and mitochondrial biogenesis, contributing to the increase in the maximal thermogenic capacity of BAT in Trib3-deficient mice. Mechanistically, it was discovered that Trib3 expression is upregulated by free fatty acids at the transcriptional level and synergistically upregulated by DAG-PKC at the posttranslational level. This occurs through the modulation of COP1-mediated Trib3 protein turnover. Interestingly, the level of Trib3 expression in BAT increased with age. Trib3 knockout mice were protected from aging-related weight gain and impaired glucose homeostasis. These results suggest that Trib3 acts as an obesity- and aging-associated factor that negatively regulates BAT activity and that the loss of Trib3 may provide a beneficial approach to prevent obesity and aging-associated metabolic syndrome by increasing the thermogenic capacity of BAT.https://doi.org/10.1038/s12276-024-01361-5
spellingShingle Hyejin Yeo
Ji-Hye Lim
Ji Eom
MinJeong Kim
Hyeji Kwon
Sang-Wook Kang
Youngsup Song
Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
Experimental and Molecular Medicine
title Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
title_full Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
title_fullStr Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
title_full_unstemmed Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
title_short Diet-induced obesity and aging-induced upregulation of Trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of BAT
title_sort diet induced obesity and aging induced upregulation of trib3 interfere with energy homeostasis by downregulating the thermogenic capacity of bat
url https://doi.org/10.1038/s12276-024-01361-5
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