Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics

Background: Thalamic hemorrhage pain (THP), a subtype of central post-stroke pain (CPSP), commonly develops following ischemic or hemorrhagic injury to the thalamus. Current therapeutic options remain inadequate due to the absence of well-defined molecular targets. This study aime...

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Main Authors: Chen Yang, Ju Gao, Yaqun Li, Yinggang Xiao, Tianfeng Huang
Format: Article
Language:English
Published: IMR Press 2025-07-01
Series:Journal of Integrative Neuroscience
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Online Access:https://www.imrpress.com/journal/JIN/24/7/10.31083/JIN38130
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author Chen Yang
Ju Gao
Yaqun Li
Yinggang Xiao
Tianfeng Huang
author_facet Chen Yang
Ju Gao
Yaqun Li
Yinggang Xiao
Tianfeng Huang
author_sort Chen Yang
collection DOAJ
description Background: Thalamic hemorrhage pain (THP), a subtype of central post-stroke pain (CPSP), commonly develops following ischemic or hemorrhagic injury to the thalamus. Current therapeutic options remain inadequate due to the absence of well-defined molecular targets. This study aimed to elucidate critical genes implicated in THP pathogenesis through an integrated multi-omics approach. Methods: A mouse model of THP was established and mice were divided into THP and control groups. Comprehensive multi-omics profiling involving transcriptomics, proteomics, metabolomics, ribosome profiling (Ribo-seq), and single-cell RNA sequencing (scRNA-seq) was conducted. Differentially expressed genes (DEGs), differentially expressed proteins (DEPs), ribosome footprint-associated DEGs (RF-DEGs), and differentially expressed metabolites (DEMs) were identified via comparative expression analyses. Hub genes were extracted from the DEGs and subsequently intersected with scRNA-seq DEGs, DEPs, and RF-DEGs to define key gene candidates. These genes underwent gene set enrichment analysis (GSEA), disease association mapping, and drug prediction. Expression levels of key genes were used to delineate critical cell populations, followed by analyses of intercellular communication and pseudotemporal differentiation trajectories. Orthogonal partial least squares discriminant analysis was used to validate the model. Results: The THP mouse model was successfully validated. Multi-omics analyses yielded distinct profiles of DEGs, single-cell DEGs, DEPs, RF-DEGs, and DEMs, which were functionally annotated through enrichment strategies. Notably, 12 hub genes were prioritized, of which eight key genes (ferritin light chain 1 (Ftl1), tropomyosin 4 (Tpm4), C-C motif chemokine ligand 3 (Ccl3), C-C motif chemokine ligand 4 (Ccl4), C-C motif chemokine receptor 2 (Ccr2), interleukin 33 (Il33), C-X-C motif chemokine ligand 2 (Cxcl2), and Lymphocyte antigen 6 complex, locus C2 (Ly6c2) were identified. These genes were predominantly associated with oxidative phosphorylation and ribosomal pathways. Further analyses revealed strong associations with necrotic and inflammatory processes, and compounds such as alprostadil and anisomycin were identified as potential therapeutic agents. Single-cell analyses highlighted six pivotal cell types, including endothelial cells and macrophages. Intercellular communication networks and lineage progression patterns of these cells were systematically characterized, alongside spatial and temporal expression profiles of key genes. Conclusions: This study established a validated THP mouse model and employed a multi-omics integration strategy to identify eight key genes and associated molecular pathways. These findings provide novel mechanistic insights into THP pathogenesis and highlight promising targets for therapeutic intervention.
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spelling doaj-art-642fa2e73c8841708df13c176aa669032025-08-20T03:44:28ZengIMR PressJournal of Integrative Neuroscience0219-63522025-07-012473813010.31083/JIN38130S0219-6352(25)00971-4Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omicsChen Yang0Ju Gao1Yaqun Li2Yinggang Xiao3Tianfeng Huang4Department of Anesthesiology, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University, 225001 Yangzhou, Jiangsu, ChinaDepartment of Anesthesiology, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University, 225001 Yangzhou, Jiangsu, ChinaDepartment of Pain Management, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University, 225001 Yangzhou, Jiangsu, ChinaDepartment of Anesthesiology, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University, 225001 Yangzhou, Jiangsu, ChinaDepartment of Anesthesiology, Northern Jiangsu People’s Hospital Affiliated to Yangzhou University, 225001 Yangzhou, Jiangsu, ChinaBackground: Thalamic hemorrhage pain (THP), a subtype of central post-stroke pain (CPSP), commonly develops following ischemic or hemorrhagic injury to the thalamus. Current therapeutic options remain inadequate due to the absence of well-defined molecular targets. This study aimed to elucidate critical genes implicated in THP pathogenesis through an integrated multi-omics approach. Methods: A mouse model of THP was established and mice were divided into THP and control groups. Comprehensive multi-omics profiling involving transcriptomics, proteomics, metabolomics, ribosome profiling (Ribo-seq), and single-cell RNA sequencing (scRNA-seq) was conducted. Differentially expressed genes (DEGs), differentially expressed proteins (DEPs), ribosome footprint-associated DEGs (RF-DEGs), and differentially expressed metabolites (DEMs) were identified via comparative expression analyses. Hub genes were extracted from the DEGs and subsequently intersected with scRNA-seq DEGs, DEPs, and RF-DEGs to define key gene candidates. These genes underwent gene set enrichment analysis (GSEA), disease association mapping, and drug prediction. Expression levels of key genes were used to delineate critical cell populations, followed by analyses of intercellular communication and pseudotemporal differentiation trajectories. Orthogonal partial least squares discriminant analysis was used to validate the model. Results: The THP mouse model was successfully validated. Multi-omics analyses yielded distinct profiles of DEGs, single-cell DEGs, DEPs, RF-DEGs, and DEMs, which were functionally annotated through enrichment strategies. Notably, 12 hub genes were prioritized, of which eight key genes (ferritin light chain 1 (Ftl1), tropomyosin 4 (Tpm4), C-C motif chemokine ligand 3 (Ccl3), C-C motif chemokine ligand 4 (Ccl4), C-C motif chemokine receptor 2 (Ccr2), interleukin 33 (Il33), C-X-C motif chemokine ligand 2 (Cxcl2), and Lymphocyte antigen 6 complex, locus C2 (Ly6c2) were identified. These genes were predominantly associated with oxidative phosphorylation and ribosomal pathways. Further analyses revealed strong associations with necrotic and inflammatory processes, and compounds such as alprostadil and anisomycin were identified as potential therapeutic agents. Single-cell analyses highlighted six pivotal cell types, including endothelial cells and macrophages. Intercellular communication networks and lineage progression patterns of these cells were systematically characterized, alongside spatial and temporal expression profiles of key genes. Conclusions: This study established a validated THP mouse model and employed a multi-omics integration strategy to identify eight key genes and associated molecular pathways. These findings provide novel mechanistic insights into THP pathogenesis and highlight promising targets for therapeutic intervention.https://www.imrpress.com/journal/JIN/24/7/10.31083/JIN38130thalamic hemorrhagepaingenomicsproteomicsmetabolomicsrna sequencinggenes
spellingShingle Chen Yang
Ju Gao
Yaqun Li
Yinggang Xiao
Tianfeng Huang
Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
Journal of Integrative Neuroscience
thalamic hemorrhage
pain
genomics
proteomics
metabolomics
rna sequencing
genes
title Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
title_full Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
title_fullStr Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
title_full_unstemmed Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
title_short Identification and Mechanistic Studies of Key Genes in Thalamic Hemorrhage Pain by Multi-omics
title_sort identification and mechanistic studies of key genes in thalamic hemorrhage pain by multi omics
topic thalamic hemorrhage
pain
genomics
proteomics
metabolomics
rna sequencing
genes
url https://www.imrpress.com/journal/JIN/24/7/10.31083/JIN38130
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AT yaqunli identificationandmechanisticstudiesofkeygenesinthalamichemorrhagepainbymultiomics
AT yinggangxiao identificationandmechanisticstudiesofkeygenesinthalamichemorrhagepainbymultiomics
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