The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling

Background: Recent studies have revealed importance of human umbilical cord blood (HUCB)-derived exosomes (HUCB-Exo) in central nervous system diseases, but the role of HUCB-Exo in hypoxic-ischemic encephalopathy (HIE) remains unclear. This study aims to explore the mechanisms of HUCB-Exo in HIE. Me...

Full description

Saved in:
Bibliographic Details
Main Authors: Menghua Zhao, Yizhong Wu, Li Huang, Juanmei Wang, Aimin Zhang
Format: Article
Language:English
Published: Elsevier 2025-12-01
Series:Regenerative Therapy
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S235232042500149X
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849424406071214080
author Menghua Zhao
Yizhong Wu
Li Huang
Juanmei Wang
Aimin Zhang
author_facet Menghua Zhao
Yizhong Wu
Li Huang
Juanmei Wang
Aimin Zhang
author_sort Menghua Zhao
collection DOAJ
description Background: Recent studies have revealed importance of human umbilical cord blood (HUCB)-derived exosomes (HUCB-Exo) in central nervous system diseases, but the role of HUCB-Exo in hypoxic-ischemic encephalopathy (HIE) remains unclear. This study aims to explore the mechanisms of HUCB-Exo in HIE. Methods: HIE models were constructed in 7-day-old neonatal rats using classical Rice-Vannucci modeling, and SH-SY5Y cells were induced by oxygen-glucose deprivation/reperfusion (OGD/R) injury, followed by intervention with HUCB and HUBC-Exo, either non-transfected or transfected with si-NC/si-MFG-E8. Results: HUBC-Exo decreased cerebral infarct size and cerebral water content in HIE neonatal rats and improved short-term and long-term neurological function. HUBC-Exo down-regulated Beclin1, ATG7, and LC3 II/I expression, while promoting p62 expression in HIE neonatal rats. After HUBC-Exo treatment, NCOA4 and ACSL4 expression in HIE neonatal rats decreased, while FTH1, SLC7A11, and GPX4 expression were increased. In addition, HUBC-Exo decreased Fe2+, MDA, and ROS levels in HIE neonatal rats. Similarly, these in vivo results were observed in vitro. HUBC-Exo inhibited autophagy and ferroptosis in OGD/R-induced SH-SY5Y cells, and MFG-E8 silencing interrupted HUBC-Exo action. Further results showed that HUBC-Exo-derived MFG-E8 promoted p-GSK3β/GSK3β and Active-β-catenin/β-catenin levels in OGD/R-induced SH-SY5Y cells. Importantly, the GSK3β agonist LiCl revoked the promotion of HUBC-Exosi-MFG-E8 on autophagy and ferroptosis in OGD/R-induced SH-SY5Y cells. HUBC-Exo MFG-E8 inhibited autophagy and ferroptosis, thereby alleviating brain damage in HIE neonatal rats. Conclusion: Our results suggested that HUBC-Exo-transmitted MFG-E8 inhibited autophagy and ferroptosis through GSK3β/β-catenin signaling, thereby alleviating brain injury in HIE neonatal rats, which provided a new idea for treating HIE.
format Article
id doaj-art-6da000cb205145b2bba5677757cc34d2
institution Kabale University
issn 2352-3204
language English
publishDate 2025-12-01
publisher Elsevier
record_format Article
series Regenerative Therapy
spelling doaj-art-6da000cb205145b2bba5677757cc34d22025-08-20T03:30:13ZengElsevierRegenerative Therapy2352-32042025-12-013032133210.1016/j.reth.2025.06.016The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signalingMenghua Zhao0Yizhong Wu1Li Huang2Juanmei Wang3Aimin Zhang4Department of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, Changsha, 410005, China; Corresponding author. Department of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, 61 Jie-Fang West Road, Fu-Rong District, Changsha, 410005, China.Department of Gastroenterology, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, Changsha, 410005, ChinaDepartment of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, Changsha, 410005, ChinaDepartment of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, Changsha, 410005, ChinaDepartment of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, Changsha, 410005, China; Corresponding author. Department of Pediatrics, Hunan Provincial People's Hospital, The First Affiliated Hospital of Hunan Normal University, 61 Jie-Fang West Road, Fu-Rong District, Changsha, 410005, China.Background: Recent studies have revealed importance of human umbilical cord blood (HUCB)-derived exosomes (HUCB-Exo) in central nervous system diseases, but the role of HUCB-Exo in hypoxic-ischemic encephalopathy (HIE) remains unclear. This study aims to explore the mechanisms of HUCB-Exo in HIE. Methods: HIE models were constructed in 7-day-old neonatal rats using classical Rice-Vannucci modeling, and SH-SY5Y cells were induced by oxygen-glucose deprivation/reperfusion (OGD/R) injury, followed by intervention with HUCB and HUBC-Exo, either non-transfected or transfected with si-NC/si-MFG-E8. Results: HUBC-Exo decreased cerebral infarct size and cerebral water content in HIE neonatal rats and improved short-term and long-term neurological function. HUBC-Exo down-regulated Beclin1, ATG7, and LC3 II/I expression, while promoting p62 expression in HIE neonatal rats. After HUBC-Exo treatment, NCOA4 and ACSL4 expression in HIE neonatal rats decreased, while FTH1, SLC7A11, and GPX4 expression were increased. In addition, HUBC-Exo decreased Fe2+, MDA, and ROS levels in HIE neonatal rats. Similarly, these in vivo results were observed in vitro. HUBC-Exo inhibited autophagy and ferroptosis in OGD/R-induced SH-SY5Y cells, and MFG-E8 silencing interrupted HUBC-Exo action. Further results showed that HUBC-Exo-derived MFG-E8 promoted p-GSK3β/GSK3β and Active-β-catenin/β-catenin levels in OGD/R-induced SH-SY5Y cells. Importantly, the GSK3β agonist LiCl revoked the promotion of HUBC-Exosi-MFG-E8 on autophagy and ferroptosis in OGD/R-induced SH-SY5Y cells. HUBC-Exo MFG-E8 inhibited autophagy and ferroptosis, thereby alleviating brain damage in HIE neonatal rats. Conclusion: Our results suggested that HUBC-Exo-transmitted MFG-E8 inhibited autophagy and ferroptosis through GSK3β/β-catenin signaling, thereby alleviating brain injury in HIE neonatal rats, which provided a new idea for treating HIE.http://www.sciencedirect.com/science/article/pii/S235232042500149XHypoxic-ischemic encephalopathyHUCB-ExoMFG-E8GSK3β/β-catenin pathwayAutophagyFerroptosis
spellingShingle Menghua Zhao
Yizhong Wu
Li Huang
Juanmei Wang
Aimin Zhang
The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
Regenerative Therapy
Hypoxic-ischemic encephalopathy
HUCB-Exo
MFG-E8
GSK3β/β-catenin pathway
Autophagy
Ferroptosis
title The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
title_full The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
title_fullStr The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
title_full_unstemmed The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
title_short The umbilical cord blood exosome MFG-E8 alleviates hypoxic-ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through GSK3β/β-catenin signaling
title_sort umbilical cord blood exosome mfg e8 alleviates hypoxic ischemic encephalopathy brain injury in neonatal rats by restoring autophagy flux and inhibiting ferroptosis through gsk3β β catenin signaling
topic Hypoxic-ischemic encephalopathy
HUCB-Exo
MFG-E8
GSK3β/β-catenin pathway
Autophagy
Ferroptosis
url http://www.sciencedirect.com/science/article/pii/S235232042500149X
work_keys_str_mv AT menghuazhao theumbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT yizhongwu theumbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT lihuang theumbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT juanmeiwang theumbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT aiminzhang theumbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT menghuazhao umbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT yizhongwu umbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT lihuang umbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT juanmeiwang umbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling
AT aiminzhang umbilicalcordbloodexosomemfge8alleviateshypoxicischemicencephalopathybraininjuryinneonatalratsbyrestoringautophagyfluxandinhibitingferroptosisthroughgsk3bbcateninsignaling