CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration

IntroductionHeart failure (HF) is the most common complication following myocardial infarction (MI) and frequently occurs during the postinfarction recovery phase. Despite the well-established association between HF and MI, the underlying molecular mechanisms driving their transition remain poorly u...

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Main Authors: Jingya Xu, Zhonghua Dong, Zhaodong Li, Xuan Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Genetics
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Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2025.1592985/full
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author Jingya Xu
Jingya Xu
Zhonghua Dong
Zhaodong Li
Xuan Wang
Xuan Wang
author_facet Jingya Xu
Jingya Xu
Zhonghua Dong
Zhaodong Li
Xuan Wang
Xuan Wang
author_sort Jingya Xu
collection DOAJ
description IntroductionHeart failure (HF) is the most common complication following myocardial infarction (MI) and frequently occurs during the postinfarction recovery phase. Despite the well-established association between HF and MI, the underlying molecular mechanisms driving their transition remain poorly understood.MethodsThe aim of this study was to identify key regulatory genes involved in this transition via advanced computational tools. We conducted a comprehensive analysis of differentially expressed genes (DEGs) via Limma software, leveraging five independent datasets retrieved from the Gene Expression Omnibus (GEO) database: GSE59867, GSE62646, GSE168281, GSE267644, and GSE269269. Our multistep analytical pipeline included weighted gene coexpression network analysis (WGCNA) to map interacting genes, machine learning algorithms for robust classification, functional annotation via Kyoto Encyclopedia of Genes and Genomes (KEGG) to explore biological pathways, CIBERSORT correlation analysis linking hub genes with immune cell states, transcriptional regulation profiling of key hubs, and single-cell sequencing to assess the functional relevance of these hubs.ResultsOur findings revealed that 413 DEGs were significantly different between MI and HF. WGCNA identified 98 genes associated with both conditions. Machine learning filtering further prioritized 10 hub genes: GPER1, E2F5, DZIP3, CYLD, ADAMTS2, ZNF366, ST14, SNORD28, LHFPL2, and HIVEP2. These hubs were significantly associated with immune-related processes, suggesting their potential role in the pathogenesis of HF after MI. Single-cell transcriptomic analysis demonstrated that CYLD exhibited the strongest correlation with the transition from MI to HF; using random forest modelling, we validated its predictive value in this context.DiscussionIn conclusion, our study identified CYLD as a critical regulator of the transition from MI to HF. Our findings underscore the potential of hub genes as targets for novel therapeutic interventions aimed at mitigating MI-to-HF progression and improving patient outcomes.
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spelling doaj-art-520ae27ea5854c3e861f31f740bceb4f2025-08-20T03:47:19ZengFrontiers Media S.A.Frontiers in Genetics1664-80212025-06-011610.3389/fgene.2025.15929851592985CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integrationJingya Xu0Jingya Xu1Zhonghua Dong2Zhaodong Li3Xuan Wang4Xuan Wang5Department of Clinical Pharmacy, The First Affiliated Hospital of Shandong First Medical University and Shandong Provincial Qianfoshan Hospital, Shandong Engineering and Technology Research Center for Pediatric Drug Development, Shandong Medicine and Health Key Laboratory of Clinical Pharmacy, Jinan, ChinaCollege of Pharmacy, Shandong University of Traditional Chinese Medicine, Jinan, ChinaDepartment of Clinical Pharmacy, The First Affiliated Hospital of Shandong First Medical University and Shandong Provincial Qianfoshan Hospital, Shandong Engineering and Technology Research Center for Pediatric Drug Development, Shandong Medicine and Health Key Laboratory of Clinical Pharmacy, Jinan, ChinaGuangdong Key Laboratory of Regional Immunity and Diseases, Department of Pathogen Biology, Shenzhen University School of Medicine, Shenzhen, ChinaDepartment of Clinical Pharmacy, The First Affiliated Hospital of Shandong First Medical University and Shandong Provincial Qianfoshan Hospital, Shandong Engineering and Technology Research Center for Pediatric Drug Development, Shandong Medicine and Health Key Laboratory of Clinical Pharmacy, Jinan, ChinaCollege of Pharmacy, Shandong University of Traditional Chinese Medicine, Jinan, ChinaIntroductionHeart failure (HF) is the most common complication following myocardial infarction (MI) and frequently occurs during the postinfarction recovery phase. Despite the well-established association between HF and MI, the underlying molecular mechanisms driving their transition remain poorly understood.MethodsThe aim of this study was to identify key regulatory genes involved in this transition via advanced computational tools. We conducted a comprehensive analysis of differentially expressed genes (DEGs) via Limma software, leveraging five independent datasets retrieved from the Gene Expression Omnibus (GEO) database: GSE59867, GSE62646, GSE168281, GSE267644, and GSE269269. Our multistep analytical pipeline included weighted gene coexpression network analysis (WGCNA) to map interacting genes, machine learning algorithms for robust classification, functional annotation via Kyoto Encyclopedia of Genes and Genomes (KEGG) to explore biological pathways, CIBERSORT correlation analysis linking hub genes with immune cell states, transcriptional regulation profiling of key hubs, and single-cell sequencing to assess the functional relevance of these hubs.ResultsOur findings revealed that 413 DEGs were significantly different between MI and HF. WGCNA identified 98 genes associated with both conditions. Machine learning filtering further prioritized 10 hub genes: GPER1, E2F5, DZIP3, CYLD, ADAMTS2, ZNF366, ST14, SNORD28, LHFPL2, and HIVEP2. These hubs were significantly associated with immune-related processes, suggesting their potential role in the pathogenesis of HF after MI. Single-cell transcriptomic analysis demonstrated that CYLD exhibited the strongest correlation with the transition from MI to HF; using random forest modelling, we validated its predictive value in this context.DiscussionIn conclusion, our study identified CYLD as a critical regulator of the transition from MI to HF. Our findings underscore the potential of hub genes as targets for novel therapeutic interventions aimed at mitigating MI-to-HF progression and improving patient outcomes.https://www.frontiersin.org/articles/10.3389/fgene.2025.1592985/fullheart failuremyocardial infarctionWGCNAmachine learningsingle-cell sequencing analysishub genes
spellingShingle Jingya Xu
Jingya Xu
Zhonghua Dong
Zhaodong Li
Xuan Wang
Xuan Wang
CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
Frontiers in Genetics
heart failure
myocardial infarction
WGCNA
machine learning
single-cell sequencing analysis
hub genes
title CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
title_full CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
title_fullStr CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
title_full_unstemmed CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
title_short CYLD as a key regulator of myocardial infarction-to-heart failure transition revealed by multi-omics integration
title_sort cyld as a key regulator of myocardial infarction to heart failure transition revealed by multi omics integration
topic heart failure
myocardial infarction
WGCNA
machine learning
single-cell sequencing analysis
hub genes
url https://www.frontiersin.org/articles/10.3389/fgene.2025.1592985/full
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