Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11

Background: Diabetic cardiomyopathy (DCM) is a prevalent and severe complication of diabetes, for which effective management strategies remain limited. Ubiquitin-specific protease 38 (USP38) has been associated with various cardiovascular diseases. In this study, we investigate the role of USP38 in...

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Main Authors: Zheng Xiao, Yucheng Pan, Hong Meng, Zongze Qu, Liang Guo, Bin Kong, Wei Shuai, He Huang
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231725002174
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author Zheng Xiao
Yucheng Pan
Hong Meng
Zongze Qu
Liang Guo
Bin Kong
Wei Shuai
He Huang
author_facet Zheng Xiao
Yucheng Pan
Hong Meng
Zongze Qu
Liang Guo
Bin Kong
Wei Shuai
He Huang
author_sort Zheng Xiao
collection DOAJ
description Background: Diabetic cardiomyopathy (DCM) is a prevalent and severe complication of diabetes, for which effective management strategies remain limited. Ubiquitin-specific protease 38 (USP38) has been associated with various cardiovascular diseases. In this study, we investigate the role of USP38 in the pathogenesis of DCM. Methods: Cardiomyocyte-specific transgenic and knockout USP38 mice were generated, and diabetic mouse model was established using streptozotocin injections. Neonatal rat cardiomyocytes exposed to high glucose conditions were utilized for in vitro experiments. Cardiac remodeling was assessed through echocardiography, electrophysiological analysis, histological assessment, and molecular analysis. Results: USP38 expression was significantly upregulated in DCM. Cardiomyocyte-specific USP38 overexpression aggravated cardiac dysfunction, cardiac inflammation and myocardial fibrosis, mitochondrial dysfunction, and increased vulnerability to ventricular arrhythmia in diabetic mice. Conversely, cardiomyocyte-specific USP38 deletion improved cardiac structural and electrical remodeling and attenuated mitochondrial impairment. Similar results were observed in vitro. Mechanistically, RNA-sequencing analysis, immunoprecipitation and mass spectrometry analysis and lipidomic analysis demonstrated that USP38 directly interacts with Acy-CoA dehydrogenase (ACAD11), deubiquitinating and inactivating it. This leads to abnormal fatty acid oxidation and subsequent activation of the receptor for advanced glycation end products (RAGE) pathway in diabetic heart. Pharmacological inhibition of RAGE using FPS-ZM1 hampered cardiac remodeling and dysfunction in cardiomyocyte-specific USP38 overexpressing diabetic mice. Conclusion: The study demonstrates that USP38 exacerbates diabetes-induced cardiac remodeling and DCM via post-translational modification of ACAD11, highlighting a novel therapeutic target for DCM.
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spelling doaj-art-07a5e1296d474737ab8ee25948b47ac72025-08-20T02:02:24ZengElsevierRedox Biology2213-23172025-07-018410370410.1016/j.redox.2025.103704Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11Zheng Xiao0Yucheng Pan1Hong Meng2Zongze Qu3Liang Guo4Bin Kong5Wei Shuai6He Huang7Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, China; Corresponding author. Department of Cardiology, Renmin Hospital of Wuhan University, 238 Jiefang Road, Wuhan 430060, Hubei, China.Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Cardiovascular Research Institute of Wuhan University, Wuhan, China; Corresponding author. Department of Cardiology, Renmin Hospital of Wuhan University, 238 jiefang Road, Wuhan 430060, Hubei, China.Background: Diabetic cardiomyopathy (DCM) is a prevalent and severe complication of diabetes, for which effective management strategies remain limited. Ubiquitin-specific protease 38 (USP38) has been associated with various cardiovascular diseases. In this study, we investigate the role of USP38 in the pathogenesis of DCM. Methods: Cardiomyocyte-specific transgenic and knockout USP38 mice were generated, and diabetic mouse model was established using streptozotocin injections. Neonatal rat cardiomyocytes exposed to high glucose conditions were utilized for in vitro experiments. Cardiac remodeling was assessed through echocardiography, electrophysiological analysis, histological assessment, and molecular analysis. Results: USP38 expression was significantly upregulated in DCM. Cardiomyocyte-specific USP38 overexpression aggravated cardiac dysfunction, cardiac inflammation and myocardial fibrosis, mitochondrial dysfunction, and increased vulnerability to ventricular arrhythmia in diabetic mice. Conversely, cardiomyocyte-specific USP38 deletion improved cardiac structural and electrical remodeling and attenuated mitochondrial impairment. Similar results were observed in vitro. Mechanistically, RNA-sequencing analysis, immunoprecipitation and mass spectrometry analysis and lipidomic analysis demonstrated that USP38 directly interacts with Acy-CoA dehydrogenase (ACAD11), deubiquitinating and inactivating it. This leads to abnormal fatty acid oxidation and subsequent activation of the receptor for advanced glycation end products (RAGE) pathway in diabetic heart. Pharmacological inhibition of RAGE using FPS-ZM1 hampered cardiac remodeling and dysfunction in cardiomyocyte-specific USP38 overexpressing diabetic mice. Conclusion: The study demonstrates that USP38 exacerbates diabetes-induced cardiac remodeling and DCM via post-translational modification of ACAD11, highlighting a novel therapeutic target for DCM.http://www.sciencedirect.com/science/article/pii/S2213231725002174Diabetic cardiomyopathyUbiquitin-specific protease 38Mitochondrial dysfunctionAcyl-CoA dehydrogenase 11Receptors of advanced glycemic end products
spellingShingle Zheng Xiao
Yucheng Pan
Hong Meng
Zongze Qu
Liang Guo
Bin Kong
Wei Shuai
He Huang
Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
Redox Biology
Diabetic cardiomyopathy
Ubiquitin-specific protease 38
Mitochondrial dysfunction
Acyl-CoA dehydrogenase 11
Receptors of advanced glycemic end products
title Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
title_full Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
title_fullStr Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
title_full_unstemmed Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
title_short Ubiquitin-specific protease 38 exacerbates diabetic cardiomyopathy via post-translational modification of ACAD11
title_sort ubiquitin specific protease 38 exacerbates diabetic cardiomyopathy via post translational modification of acad11
topic Diabetic cardiomyopathy
Ubiquitin-specific protease 38
Mitochondrial dysfunction
Acyl-CoA dehydrogenase 11
Receptors of advanced glycemic end products
url http://www.sciencedirect.com/science/article/pii/S2213231725002174
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