M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling

Abstract Neuronal ferroptosis plays a vital role in the progression of neonatal hypoxic-ischemic brain damage (HIBD). M2-type microglia-derived exosomes (M2-exos) have been shown to protect neurons from ischemia–reperfusion (I/R) brain injury, but their impact on I/R-induced neuronal ferroptosis and...

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Main Authors: Jian Li, Qing Chen, Hao Gu
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-03091-8
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author Jian Li
Qing Chen
Hao Gu
author_facet Jian Li
Qing Chen
Hao Gu
author_sort Jian Li
collection DOAJ
description Abstract Neuronal ferroptosis plays a vital role in the progression of neonatal hypoxic-ischemic brain damage (HIBD). M2-type microglia-derived exosomes (M2-exos) have been shown to protect neurons from ischemia–reperfusion (I/R) brain injury, but their impact on I/R-induced neuronal ferroptosis and the underlying mechanisms remain poorly understood. In this study, we used an in vitro oxygen-glucose deprivation/reoxygenation (OGD/R) model in HT-22 neuronal cells to investigate how M2-exos modulate ferroptosis. We found that M2-exos were internalized by HT-22 cells and significantly attenuated OGD/R-induced ferroptosis. Mechanistically, M2-exos enhanced mitophagy, which was mediated by the upregulation of FUN14 domain-containing protein 1 (FUNDC1), thereby inhibiting ferroptosis. Further analysis revealed that M2-exos activated FUNDC1-dependent mitophagy through the AMP-activated protein kinase (AMPK)/UNC-51-like kinase 1 (ULK1) signaling pathway. Taken together, these findings suggest that M2-exos ameliorate I/R-induced neuronal ferroptosis by enhancing FUNDC1-mediated mitophagy through the activation of AMPK/ULK1 signaling pathway.
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spelling doaj-art-d600dd09cf994ecbbfbb20ff26f10ec32025-08-20T01:53:11ZengNature PortfolioScientific Reports2045-23222025-05-0115111110.1038/s41598-025-03091-8M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signalingJian Li0Qing Chen1Hao Gu2Department of Anesthesiology, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical UniversityDepartment of Anesthesiology, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical UniversityDepartment of Pediatrics, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical UniversityAbstract Neuronal ferroptosis plays a vital role in the progression of neonatal hypoxic-ischemic brain damage (HIBD). M2-type microglia-derived exosomes (M2-exos) have been shown to protect neurons from ischemia–reperfusion (I/R) brain injury, but their impact on I/R-induced neuronal ferroptosis and the underlying mechanisms remain poorly understood. In this study, we used an in vitro oxygen-glucose deprivation/reoxygenation (OGD/R) model in HT-22 neuronal cells to investigate how M2-exos modulate ferroptosis. We found that M2-exos were internalized by HT-22 cells and significantly attenuated OGD/R-induced ferroptosis. Mechanistically, M2-exos enhanced mitophagy, which was mediated by the upregulation of FUN14 domain-containing protein 1 (FUNDC1), thereby inhibiting ferroptosis. Further analysis revealed that M2-exos activated FUNDC1-dependent mitophagy through the AMP-activated protein kinase (AMPK)/UNC-51-like kinase 1 (ULK1) signaling pathway. Taken together, these findings suggest that M2-exos ameliorate I/R-induced neuronal ferroptosis by enhancing FUNDC1-mediated mitophagy through the activation of AMPK/ULK1 signaling pathway.https://doi.org/10.1038/s41598-025-03091-8MicrogliaExosomeFerroptosisMitophagyIschemia/reperfusion
spellingShingle Jian Li
Qing Chen
Hao Gu
M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
Scientific Reports
Microglia
Exosome
Ferroptosis
Mitophagy
Ischemia/reperfusion
title M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
title_full M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
title_fullStr M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
title_full_unstemmed M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
title_short M2 microglia-derived exosomes reduce neuronal ferroptosis via FUNDC1-mediated mitophagy by activating AMPK/ULK1 signaling
title_sort m2 microglia derived exosomes reduce neuronal ferroptosis via fundc1 mediated mitophagy by activating ampk ulk1 signaling
topic Microglia
Exosome
Ferroptosis
Mitophagy
Ischemia/reperfusion
url https://doi.org/10.1038/s41598-025-03091-8
work_keys_str_mv AT jianli m2microgliaderivedexosomesreduceneuronalferroptosisviafundc1mediatedmitophagybyactivatingampkulk1signaling
AT qingchen m2microgliaderivedexosomesreduceneuronalferroptosisviafundc1mediatedmitophagybyactivatingampkulk1signaling
AT haogu m2microgliaderivedexosomesreduceneuronalferroptosisviafundc1mediatedmitophagybyactivatingampkulk1signaling