Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway

Abstract Obesity represents a low‐grade chronic inflammation status, which is associated with compromised adaptive thermogenesis. However, the mechanisms underlying the defective activation of thermogenesis in chronic inflammation remain unclear. Here, a chronic inflammatory model is first estabolis...

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Main Authors: Yucheng Zhu, Ruiqi Yang, Zhangchao Deng, Bohua Deng, Kun Zhao, Chen Dai, Gang Wei, YanJiang Wang, Jinshui Zheng, Zhuqing Ren, Wentao Lv, Yingping Xiao, Zhinan Mei, Tongxing Song
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202310236
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author Yucheng Zhu
Ruiqi Yang
Zhangchao Deng
Bohua Deng
Kun Zhao
Chen Dai
Gang Wei
YanJiang Wang
Jinshui Zheng
Zhuqing Ren
Wentao Lv
Yingping Xiao
Zhinan Mei
Tongxing Song
author_facet Yucheng Zhu
Ruiqi Yang
Zhangchao Deng
Bohua Deng
Kun Zhao
Chen Dai
Gang Wei
YanJiang Wang
Jinshui Zheng
Zhuqing Ren
Wentao Lv
Yingping Xiao
Zhinan Mei
Tongxing Song
author_sort Yucheng Zhu
collection DOAJ
description Abstract Obesity represents a low‐grade chronic inflammation status, which is associated with compromised adaptive thermogenesis. However, the mechanisms underlying the defective activation of thermogenesis in chronic inflammation remain unclear. Here, a chronic inflammatory model is first estabolished by injecting mice with low‐dose lipopolysaccharide (LPS) before cold exposure, and then it is verified that LPS treatment can decrease the core body temperature of mice and alter the microbial distribution in epididymal white adipose tissue (eWAT). An adipose tissue‐resident bacterium Sphingomonas paucimobilis is identified as a potential inhibitor on the activation of brown fat and browning of inguinal WAT, resulting in defective adaptive thermogenesis. Mechanically, LPS and S. paucimobilis inhibit the production and release of 15‐HETE by suppressing its main metabolic enzyme 12 lipoxygenase (12‐LOX) and 15‐ Hydroxyeicosatetraenoic acid (15‐HETE) rescues the impaired thermogenesis. Interestingly, 15‐HETE directly binds to AMP‐activated protein kinase α (AMPKα) and elevates the phosphorylation of AMPK, leading to the activation of uncoupling protein 1 (UCP1) and mitochondrial oxidative phosphorylation (OXPHOS) complexes. Further analysis with human obesity subjects reveals that individuals with high body mass index displayed lower 15‐HETE levels. Taken together, this work improves the understanding of how chronic inflammation impairs adaptive thermogenesis and provides novel targets for alleviating obesity.
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spelling doaj-art-0237eeaeb73a4fc7bf2c22f3b88845e82025-08-20T02:52:41ZengWileyAdvanced Science2198-38442024-12-011147n/an/a10.1002/advs.202310236Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK PathwayYucheng Zhu0Ruiqi Yang1Zhangchao Deng2Bohua Deng3Kun Zhao4Chen Dai5Gang Wei6YanJiang Wang7Jinshui Zheng8Zhuqing Ren9Wentao Lv10Yingping Xiao11Zhinan Mei12Tongxing Song13College of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaCollege of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaCollege of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaCollege of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaDepartment of Endocrinology the Seventh Medical Center of Chinese PLA General Hospital Beijing 100700 ChinaInstitute of Organ Transplantation Tongji Hospital Tongji Medical College Huazhong University of Science and Technology Wuhan 430030 ChinaBeijing Key Laboratory of Diabetes Research and Care Department of Endocrinology, Beijing Diabetes Institute Beijing Tongren Hospital Capital Medical University Beijing 100730 ChinaBeijing Chao‐yang Hospital Capital Medical University Beijing 100020 ChinaState Key Laboratory of Agricultural Microbiology Huazhong Agricultural University Wuhan 430070 ChinaCollege of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products Institute of Agro‐Product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou 310021 ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products Institute of Agro‐Product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou 310021 ChinaCollege of Plant Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaCollege of Animal Science and Technology Huazhong Agricultural University Wuhan 430070 ChinaAbstract Obesity represents a low‐grade chronic inflammation status, which is associated with compromised adaptive thermogenesis. However, the mechanisms underlying the defective activation of thermogenesis in chronic inflammation remain unclear. Here, a chronic inflammatory model is first estabolished by injecting mice with low‐dose lipopolysaccharide (LPS) before cold exposure, and then it is verified that LPS treatment can decrease the core body temperature of mice and alter the microbial distribution in epididymal white adipose tissue (eWAT). An adipose tissue‐resident bacterium Sphingomonas paucimobilis is identified as a potential inhibitor on the activation of brown fat and browning of inguinal WAT, resulting in defective adaptive thermogenesis. Mechanically, LPS and S. paucimobilis inhibit the production and release of 15‐HETE by suppressing its main metabolic enzyme 12 lipoxygenase (12‐LOX) and 15‐ Hydroxyeicosatetraenoic acid (15‐HETE) rescues the impaired thermogenesis. Interestingly, 15‐HETE directly binds to AMP‐activated protein kinase α (AMPKα) and elevates the phosphorylation of AMPK, leading to the activation of uncoupling protein 1 (UCP1) and mitochondrial oxidative phosphorylation (OXPHOS) complexes. Further analysis with human obesity subjects reveals that individuals with high body mass index displayed lower 15‐HETE levels. Taken together, this work improves the understanding of how chronic inflammation impairs adaptive thermogenesis and provides novel targets for alleviating obesity.https://doi.org/10.1002/advs.20231023615‐HETEadaptive thermogenesisadipose tissuesAMPKchronic inflammationmicrobes
spellingShingle Yucheng Zhu
Ruiqi Yang
Zhangchao Deng
Bohua Deng
Kun Zhao
Chen Dai
Gang Wei
YanJiang Wang
Jinshui Zheng
Zhuqing Ren
Wentao Lv
Yingping Xiao
Zhinan Mei
Tongxing Song
Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
Advanced Science
15‐HETE
adaptive thermogenesis
adipose tissues
AMPK
chronic inflammation
microbes
title Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
title_full Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
title_fullStr Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
title_full_unstemmed Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
title_short Adipose Tissue‐Resident Sphingomonas Paucimobilis Suppresses Adaptive Thermogenesis by Reducing 15‐HETE Production and Inhibiting AMPK Pathway
title_sort adipose tissue resident sphingomonas paucimobilis suppresses adaptive thermogenesis by reducing 15 hete production and inhibiting ampk pathway
topic 15‐HETE
adaptive thermogenesis
adipose tissues
AMPK
chronic inflammation
microbes
url https://doi.org/10.1002/advs.202310236
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