Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study

Aim of the studyTo establish a cross-tissue bioinformatics model for identifying conserved key genes and immune infiltration mechanisms in ischemia-reperfusion injury (IRI) with experimental validation in limb IRI, including pharmacological targeting of the WNT5A/PLC pathway.Materials and methodsTra...

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Main Authors: Qiyun Shi, Taotao Tian, Yanfeng Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1491928/full
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author Qiyun Shi
Taotao Tian
Yanfeng Li
author_facet Qiyun Shi
Taotao Tian
Yanfeng Li
author_sort Qiyun Shi
collection DOAJ
description Aim of the studyTo establish a cross-tissue bioinformatics model for identifying conserved key genes and immune infiltration mechanisms in ischemia-reperfusion injury (IRI) with experimental validation in limb IRI, including pharmacological targeting of the WNT5A/PLC pathway.Materials and methodsTranscriptomic data from CTGF-stimulated cardiac myocytes (GSE36073) were analyzed as a surrogate for limb IRI due to shared pathological mechanisms. Random forest, LASSO regression, algorithms identified feature genes, validated in a rat limb IRI model using RT-qPCR, and histology. Pharmacological inhibition (WNT5A inhibitor Box5, PLC inhibitor U-73122) was performed to assess pathway involvement. Immune cell infiltration patterns were analyzed via CIBERSORT.ResultsFrom 169 differentially expressed genes (116 upregulated, 53 downregulated), machine learning identified four key genes (WNT5A, PLCG, ITPR1, CAMK2A), significantly upregulated in experimental limb IRI (P<0.01). Pharmacological inhibition confirmed their functional roles: Box5 and U-73122 treatment reduced expression of WNT5A and PLC versus IRI controls (P<0.05), showing IRI-induced muscle fiber disruption, edema, and inflammation. Immune analysis revealed myeloid polarization shifts (increased M1, decreased M2 macrophages; P<0.05). WNT5A correlated negatively with memory immune cells, while PLCG, ITPR1, and CAMK2A correlated with lymphocyte subpopulations.ConclusionWe identified a conserved molecular signature across cardiac and skeletal muscle IRI, with WNT5A/PLC pathway components as mechanistically validated therapeutic targets. Our cross-tissue bioinformatic approach, reinforced by pharmacological and histological evidence, provides a novel framework for IRI analysis when direct patient data are unavailable. Combined targeting of macrophage polarization and cellular activation the WNT5A/PLC axis may offer synergistic therapeutic potential.
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spelling doaj-art-d5a2eb33707446feb481b5cd1ef2fccc2025-08-20T02:28:19ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-05-011610.3389/fimmu.2025.14919281491928Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental studyQiyun Shi0Taotao Tian1Yanfeng Li2Medical Center of Cervical and Lumbar Pain (Tui Na Therapy), Luoyang Orthopedic-Traumatological Hospital Of Henan Province (Henan Provincial Orthopedic Hospital), Luoyang, ChinaMedical Center of Cervical and Lumbar Pain (Tui Na Therapy), Luoyang Orthopedic-Traumatological Hospital Of Henan Province (Henan Provincial Orthopedic Hospital), Luoyang, ChinaMedical Center of Microsurgery, Luoyang Orthopedic-Traumatological Hospital Of Henan Province (Henan Provincial Orthopedic Hospital), Zhengzhou, ChinaAim of the studyTo establish a cross-tissue bioinformatics model for identifying conserved key genes and immune infiltration mechanisms in ischemia-reperfusion injury (IRI) with experimental validation in limb IRI, including pharmacological targeting of the WNT5A/PLC pathway.Materials and methodsTranscriptomic data from CTGF-stimulated cardiac myocytes (GSE36073) were analyzed as a surrogate for limb IRI due to shared pathological mechanisms. Random forest, LASSO regression, algorithms identified feature genes, validated in a rat limb IRI model using RT-qPCR, and histology. Pharmacological inhibition (WNT5A inhibitor Box5, PLC inhibitor U-73122) was performed to assess pathway involvement. Immune cell infiltration patterns were analyzed via CIBERSORT.ResultsFrom 169 differentially expressed genes (116 upregulated, 53 downregulated), machine learning identified four key genes (WNT5A, PLCG, ITPR1, CAMK2A), significantly upregulated in experimental limb IRI (P<0.01). Pharmacological inhibition confirmed their functional roles: Box5 and U-73122 treatment reduced expression of WNT5A and PLC versus IRI controls (P<0.05), showing IRI-induced muscle fiber disruption, edema, and inflammation. Immune analysis revealed myeloid polarization shifts (increased M1, decreased M2 macrophages; P<0.05). WNT5A correlated negatively with memory immune cells, while PLCG, ITPR1, and CAMK2A correlated with lymphocyte subpopulations.ConclusionWe identified a conserved molecular signature across cardiac and skeletal muscle IRI, with WNT5A/PLC pathway components as mechanistically validated therapeutic targets. Our cross-tissue bioinformatic approach, reinforced by pharmacological and histological evidence, provides a novel framework for IRI analysis when direct patient data are unavailable. Combined targeting of macrophage polarization and cellular activation the WNT5A/PLC axis may offer synergistic therapeutic potential.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1491928/fulllimb ischemia-reperfusion injurymulti-tissue network analysisimmune microenvironmentbioinformatics modelingtherapeutic hub genes
spellingShingle Qiyun Shi
Taotao Tian
Yanfeng Li
Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
Frontiers in Immunology
limb ischemia-reperfusion injury
multi-tissue network analysis
immune microenvironment
bioinformatics modeling
therapeutic hub genes
title Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
title_full Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
title_fullStr Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
title_full_unstemmed Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
title_short Identification of key genes and immune infiltration mechanisms in limb ischemia-reperfusion injury: a bioinformatics and experimental study
title_sort identification of key genes and immune infiltration mechanisms in limb ischemia reperfusion injury a bioinformatics and experimental study
topic limb ischemia-reperfusion injury
multi-tissue network analysis
immune microenvironment
bioinformatics modeling
therapeutic hub genes
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1491928/full
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AT taotaotian identificationofkeygenesandimmuneinfiltrationmechanismsinlimbischemiareperfusioninjuryabioinformaticsandexperimentalstudy
AT yanfengli identificationofkeygenesandimmuneinfiltrationmechanismsinlimbischemiareperfusioninjuryabioinformaticsandexperimentalstudy