USP53 Drives Ethanol-Induced Myocardial Injury by Promoting K63 Deubiquitination-Dependent RIPK1 Activation at K377

Alcoholic cardiomyopathy (ACM) is a type of dilated cardiomyopathy unrelated to ischemia, which develops as a consequence of chronic alcohol consumption. While ethanol-induced irreversible cardiomyocyte death is implicated in ACM development and progression, the precise molecular mechanisms involved...

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Main Authors: Jichen Pan, Xiaolin Liu, Xiao Li, Shanshan Wang, Yuliang Zhao, Chong Yuan, Dongdong Liu, Liyan Wang, Meng Zhang, Fengming Liu, Mei Zhang, Shen Dai
Format: Article
Language:English
Published: American Association for the Advancement of Science (AAAS) 2025-01-01
Series:Research
Online Access:https://spj.science.org/doi/10.34133/research.0823
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Summary:Alcoholic cardiomyopathy (ACM) is a type of dilated cardiomyopathy unrelated to ischemia, which develops as a consequence of chronic alcohol consumption. While ethanol-induced irreversible cardiomyocyte death is implicated in ACM development and progression, the precise molecular mechanisms involved are still obscure. In the current study, we demonstrate that ethanol exposure promotes receptor-interacting serine/threonine-protein kinase 1 (RIPK1) autophosphorylation and enhances pRIPK1-associated apoptosis and necroptosis in ACM models both in vivo and in vitro. Through co-immunoprecipitation (Co-IP) combined with liquid chromatography–tandem mass spectrometry (LC-MS/MS) analysis, we identified ubiquitin-specific protease 53 (USP53) as a pivotal deubiquitinase involved in modulating RIPK1 activation following ethanol stimulation in cardiomyocytes. Mechanistically, we found that ethanol induced up-regulation of USP53 via transcriptional induction by early growth response 1 (EGR1). Subsequently, USP53 interacted with the intermediate domain of RIPK1 and removed K63-linked ubiquitination at lysine-377 (K377), facilitating RIPK1 phosphorylation and triggering downstream apoptotic and necroptotic pathways in cardiac cells. Further, alcohol-fed cardiomyocyte-specific USP53 knockout (USP53CKO) mice exhibited improved survival rates and less cardiomyocyte death in hearts compared with the control group. Our study identifies USP53 as a novel regulator of RIPK1-dependent cell death and advances our understanding of the mechanistic pathways of ACM. These results highlight the USP53–RIPK1 signaling axis as a potential therapeutic target for mitigating ACM progression.
ISSN:2639-5274