NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition

Abstract In the early stage of intracerebral hemorrhage (ICH), rebleeding occurs when blood from the initial hematoma permeates the surrounding brain parenchyma through the disrupted blood–brain barrier (BBB), exacerbating brain injury. Neuroinflammation is a critical driver of the pathological proc...

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Main Authors: Di Hu, Cheng Huang, Ling Tang, Jiawen Lei, Jiaqi Wang, Wenzheng Hu, Minshan Chen, Siyuan Song, Lin Lu, Pingyi Xu
Format: Article
Language:English
Published: Springer 2025-06-01
Series:Cellular and Molecular Life Sciences
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Online Access:https://doi.org/10.1007/s00018-025-05755-0
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author Di Hu
Cheng Huang
Ling Tang
Jiawen Lei
Jiaqi Wang
Wenzheng Hu
Minshan Chen
Siyuan Song
Lin Lu
Pingyi Xu
author_facet Di Hu
Cheng Huang
Ling Tang
Jiawen Lei
Jiaqi Wang
Wenzheng Hu
Minshan Chen
Siyuan Song
Lin Lu
Pingyi Xu
author_sort Di Hu
collection DOAJ
description Abstract In the early stage of intracerebral hemorrhage (ICH), rebleeding occurs when blood from the initial hematoma permeates the surrounding brain parenchyma through the disrupted blood–brain barrier (BBB), exacerbating brain injury. Neuroinflammation is a critical driver of the pathological processes underlying this phenomenon. Research on microglia near early hematomas revealed that promoting the transition of microglia to the M2 phenotype could mitigate perihematomal inflammatory damage. Recent studies have shown that the nuclear receptor-related 1 protein (NR4A2) can regulate microglial function and inhibit inflammation. However, the functions of NR4A2 in the development of ICH are still unclear. In this study, we explored the potential protective effect and mechanism of NR4A2 in ICH models. Our results demonstrated that the expression of NR4A2 was significantly decreased in both ICH rats and cell models. Increasing NR4A2 activity could effectively decrease the hematoma volume, improve the neurological prognosis and alleviate perihematomal BBB damage. In vivo and in vitro experiments revealed that NR4A2 inhibited perihematomal inflammatory damage by driving microglial polarization toward the anti-inflammatory M2 phenotype. Mechanistically, NR4A2 targeted TLR4 and inhibited the TRAF6/NF-κB pathway, thereby promoting M2 microglial polarization, reducing inflammatory cell extravasation and maintaining the integrity of the BBB. Conversely, the protective effects of NR4A2 were negated when CRX-527 (a TLR4 agonist) was introduced. These findings suggest that NR4A2 represents a promising therapeutic target for ICH. Graphical abstract
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spelling doaj-art-1e6ed025e64e4b3fb86ab1767e8aace02025-08-20T03:24:22ZengSpringerCellular and Molecular Life Sciences1420-90712025-06-0182112310.1007/s00018-025-05755-0NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibitionDi Hu0Cheng Huang1Ling Tang2Jiawen Lei3Jiaqi Wang4Wenzheng Hu5Minshan Chen6Siyuan Song7Lin Lu8Pingyi Xu9Department of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The Second Affiliated Hospital (Xinqiao Hospital), Army Medical University (Third Military Medical University)Department of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Guangzhou Medical UniversityAbstract In the early stage of intracerebral hemorrhage (ICH), rebleeding occurs when blood from the initial hematoma permeates the surrounding brain parenchyma through the disrupted blood–brain barrier (BBB), exacerbating brain injury. Neuroinflammation is a critical driver of the pathological processes underlying this phenomenon. Research on microglia near early hematomas revealed that promoting the transition of microglia to the M2 phenotype could mitigate perihematomal inflammatory damage. Recent studies have shown that the nuclear receptor-related 1 protein (NR4A2) can regulate microglial function and inhibit inflammation. However, the functions of NR4A2 in the development of ICH are still unclear. In this study, we explored the potential protective effect and mechanism of NR4A2 in ICH models. Our results demonstrated that the expression of NR4A2 was significantly decreased in both ICH rats and cell models. Increasing NR4A2 activity could effectively decrease the hematoma volume, improve the neurological prognosis and alleviate perihematomal BBB damage. In vivo and in vitro experiments revealed that NR4A2 inhibited perihematomal inflammatory damage by driving microglial polarization toward the anti-inflammatory M2 phenotype. Mechanistically, NR4A2 targeted TLR4 and inhibited the TRAF6/NF-κB pathway, thereby promoting M2 microglial polarization, reducing inflammatory cell extravasation and maintaining the integrity of the BBB. Conversely, the protective effects of NR4A2 were negated when CRX-527 (a TLR4 agonist) was introduced. These findings suggest that NR4A2 represents a promising therapeutic target for ICH. Graphical abstracthttps://doi.org/10.1007/s00018-025-05755-0NR4A2NeuroinflammationMicroglial polarizationBlood–brain barrierTLR4TRAF6/NF-κB
spellingShingle Di Hu
Cheng Huang
Ling Tang
Jiawen Lei
Jiaqi Wang
Wenzheng Hu
Minshan Chen
Siyuan Song
Lin Lu
Pingyi Xu
NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
Cellular and Molecular Life Sciences
NR4A2
Neuroinflammation
Microglial polarization
Blood–brain barrier
TLR4
TRAF6/NF-κB
title NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
title_full NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
title_fullStr NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
title_full_unstemmed NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
title_short NR4A2 attenuates early brain injury after intracerebral hemorrhage by promoting M2 microglial polarization via TLR4/TRAF6/NF-κB pathway inhibition
title_sort nr4a2 attenuates early brain injury after intracerebral hemorrhage by promoting m2 microglial polarization via tlr4 traf6 nf κb pathway inhibition
topic NR4A2
Neuroinflammation
Microglial polarization
Blood–brain barrier
TLR4
TRAF6/NF-κB
url https://doi.org/10.1007/s00018-025-05755-0
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