Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction

Abstract Deubiquitinating modification of proteins is involved in the pathogenesis of diseases. Here, we investigated the role and regulating mechanism of a deubiquitinating enzyme (DUB), ovarian tumor domain-containing protein 1 (OTUD1), in diabetic cardiomyopathy (DCM). We find a significantly inc...

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Main Authors: Xue Han, Ruyi Zheng, Jiajia Zhang, Yanan Liu, Ze Li, Guoxuan Liu, Jianing Zheng, Weiqi Li, Zijun Liang, Mengyang Wang, Jie Yu, Qiaojuan Shi, Huazhong Ying, Guang Liang
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61901-z
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author Xue Han
Ruyi Zheng
Jiajia Zhang
Yanan Liu
Ze Li
Guoxuan Liu
Jianing Zheng
Weiqi Li
Zijun Liang
Mengyang Wang
Jie Yu
Qiaojuan Shi
Huazhong Ying
Guang Liang
author_facet Xue Han
Ruyi Zheng
Jiajia Zhang
Yanan Liu
Ze Li
Guoxuan Liu
Jianing Zheng
Weiqi Li
Zijun Liang
Mengyang Wang
Jie Yu
Qiaojuan Shi
Huazhong Ying
Guang Liang
author_sort Xue Han
collection DOAJ
description Abstract Deubiquitinating modification of proteins is involved in the pathogenesis of diseases. Here, we investigated the role and regulating mechanism of a deubiquitinating enzyme (DUB), ovarian tumor domain-containing protein 1 (OTUD1), in diabetic cardiomyopathy (DCM). We find a significantly increased OTUD1 expression in diabetic mouse hearts, and single-cell RNA sequencing shows OTUD1 mainly distributing in cardiomyocytes. Cardiomyocyte-specific OTUD1 knockout prevents cardiac hypertrophy and dysfunction in both type 2 and type 1 diabetic male mice. OTUD1 deficiency restores cardiac AMPK activity and mitochondrial function in diabetic hearts and cardiomyocytes. Mechanistically, OTUD1 binds to AMPKα2 subunit, deubiquitinates AMPKα2 at K60/K379 sites, and then inhibits AMPKT172 phosphorylation through impeding the interaction of AMPKα2 and its upstream kinase CAMKK2. Finally, silencing AMPKα2 in cardiomyocytes abolishes the cardioprotective effects of OTUD1 deficiency in diabetic mice. In conclusion, this work identifies a direct regulatory DUB of AMPK and presents a OTUD1-AMPK axis in cardiomyocytes for driving DCM.
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issn 2041-1723
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spelling doaj-art-700cd9ab6bfc40c69d2fa948f36d62532025-08-20T03:43:16ZengNature PortfolioNature Communications2041-17232025-07-0116112010.1038/s41467-025-61901-zCardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunctionXue Han0Ruyi Zheng1Jiajia Zhang2Yanan Liu3Ze Li4Guoxuan Liu5Jianing Zheng6Weiqi Li7Zijun Liang8Mengyang Wang9Jie Yu10Qiaojuan Shi11Huazhong Ying12Guang Liang13Zhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeDepartment of Pharmacology, College of Pharmacy, Beihua UniversityZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeZhejiang Provincial Key Laboratory of Laboratory Animals and Safety Research, School of Pharmaceutical Sciences, Hangzhou Medical CollegeDepartment of Cardiology, the First Affiliated Hospital, Wenzhou Medical UniversityAbstract Deubiquitinating modification of proteins is involved in the pathogenesis of diseases. Here, we investigated the role and regulating mechanism of a deubiquitinating enzyme (DUB), ovarian tumor domain-containing protein 1 (OTUD1), in diabetic cardiomyopathy (DCM). We find a significantly increased OTUD1 expression in diabetic mouse hearts, and single-cell RNA sequencing shows OTUD1 mainly distributing in cardiomyocytes. Cardiomyocyte-specific OTUD1 knockout prevents cardiac hypertrophy and dysfunction in both type 2 and type 1 diabetic male mice. OTUD1 deficiency restores cardiac AMPK activity and mitochondrial function in diabetic hearts and cardiomyocytes. Mechanistically, OTUD1 binds to AMPKα2 subunit, deubiquitinates AMPKα2 at K60/K379 sites, and then inhibits AMPKT172 phosphorylation through impeding the interaction of AMPKα2 and its upstream kinase CAMKK2. Finally, silencing AMPKα2 in cardiomyocytes abolishes the cardioprotective effects of OTUD1 deficiency in diabetic mice. In conclusion, this work identifies a direct regulatory DUB of AMPK and presents a OTUD1-AMPK axis in cardiomyocytes for driving DCM.https://doi.org/10.1038/s41467-025-61901-z
spellingShingle Xue Han
Ruyi Zheng
Jiajia Zhang
Yanan Liu
Ze Li
Guoxuan Liu
Jianing Zheng
Weiqi Li
Zijun Liang
Mengyang Wang
Jie Yu
Qiaojuan Shi
Huazhong Ying
Guang Liang
Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
Nature Communications
title Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
title_full Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
title_fullStr Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
title_full_unstemmed Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
title_short Cardiomyocyte OTUD1 drives diabetic cardiomyopathy via directly deubiquitinating AMPKα2 and inducing mitochondrial dysfunction
title_sort cardiomyocyte otud1 drives diabetic cardiomyopathy via directly deubiquitinating ampkα2 and inducing mitochondrial dysfunction
url https://doi.org/10.1038/s41467-025-61901-z
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