Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury

Hepatic ischemia-reperfusion injury (IRI) poses a significant clinical challenge in liver surgery and transplantation, primarily mediated through oxidative stress, mitochondrial dysfunction, and inflammatory activation. Herein, we developed SOD2-Res@CVs, an engineered vesicular platform combining SO...

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Main Authors: Pu Shen, Kaijun Huang, Xuanlin Zhang, Guiyuan Yin, Meiting Qin, Hua Ma, Zhijin Fan, Yuhui Liao
Format: Article
Language:English
Published: Elsevier 2025-10-01
Series:Materials Today Bio
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Online Access:http://www.sciencedirect.com/science/article/pii/S2590006425007859
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author Pu Shen
Kaijun Huang
Xuanlin Zhang
Guiyuan Yin
Meiting Qin
Hua Ma
Zhijin Fan
Yuhui Liao
author_facet Pu Shen
Kaijun Huang
Xuanlin Zhang
Guiyuan Yin
Meiting Qin
Hua Ma
Zhijin Fan
Yuhui Liao
author_sort Pu Shen
collection DOAJ
description Hepatic ischemia-reperfusion injury (IRI) poses a significant clinical challenge in liver surgery and transplantation, primarily mediated through oxidative stress, mitochondrial dysfunction, and inflammatory activation. Herein, we developed SOD2-Res@CVs, an engineered vesicular platform combining SOD2-overexpressing mesenchymal stem cell-derived vesicles with liver-targeted and ROS-responsive resveratrol (Res)-loaded liposomes for multi-mechanistic intervention. In vivo imaging demonstrated that SOD2-Res@CVs selectively accumulated in IRI-damaged hepatic tissues. Within oxidative stress microenvironments, the system exhibited responsive liberation of SOD2 and resveratrol, which cooperatively mitigated oxidative damage through redox homeostasis modulation - evidenced by reduced lipid peroxidation (MDA suppression) and enhanced antioxidant defense (GSH/SOD2 upregulation). This therapeutic cascade facilitated mitochondrial structural and functional restoration via multiple pathways: Resveratrol specifically activated PINK1-mediated mitophagy, as confirmed by increased LC3 and beclin-1 expression, thereby promoting selective clearance of depolarized mitochondria. Comparative analyses revealed SOD2-Res@CVs' superior therapeutic efficacy over individual components in histological recovery and organ function preservation. Transcriptomic profiling further validated the system's multi-target regulatory capacity, highlighting its concurrent suppression of oxidative stress pathways, mitigation of inflammatory signaling, and improvement of mitochondrial bioenergetics during IRI progression. This study establishes SOD2-Res@CVs as a multifunctional nanotherapeutic strategy that harmonizes spatial targeting with pathological microenvironment responsiveness and a promising approach for liver protection in transplantation.
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spelling doaj-art-f34434f67f5f4bcbab3b2dfd37ff1a5c2025-08-23T04:48:57ZengElsevierMaterials Today Bio2590-00642025-10-013410221510.1016/j.mtbio.2025.102215Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injuryPu Shen0Kaijun Huang1Xuanlin Zhang2Guiyuan Yin3Meiting Qin4Hua Ma5Zhijin Fan6Yuhui Liao7Department of Anesthesiology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, ChinaDepartment of General Surgery, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, 510080, China; Corresponding authors.Huaihe Hospital of Henan University, Kaifeng, 475000, ChinaInstitute for Engineering Medicine, Kunming Medical University, Kunming, 650500, ChinaOrgan Transplant Center, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, ChinaInstitute for Engineering Medicine, Kunming Medical University, Kunming, 650500, China; Corresponding author.Institute for Engineering Medicine, Kunming Medical University, Kunming, 650500, China; Corresponding authors.Institute for Engineering Medicine, Kunming Medical University, Kunming, 650500, China; Corresponding author.Hepatic ischemia-reperfusion injury (IRI) poses a significant clinical challenge in liver surgery and transplantation, primarily mediated through oxidative stress, mitochondrial dysfunction, and inflammatory activation. Herein, we developed SOD2-Res@CVs, an engineered vesicular platform combining SOD2-overexpressing mesenchymal stem cell-derived vesicles with liver-targeted and ROS-responsive resveratrol (Res)-loaded liposomes for multi-mechanistic intervention. In vivo imaging demonstrated that SOD2-Res@CVs selectively accumulated in IRI-damaged hepatic tissues. Within oxidative stress microenvironments, the system exhibited responsive liberation of SOD2 and resveratrol, which cooperatively mitigated oxidative damage through redox homeostasis modulation - evidenced by reduced lipid peroxidation (MDA suppression) and enhanced antioxidant defense (GSH/SOD2 upregulation). This therapeutic cascade facilitated mitochondrial structural and functional restoration via multiple pathways: Resveratrol specifically activated PINK1-mediated mitophagy, as confirmed by increased LC3 and beclin-1 expression, thereby promoting selective clearance of depolarized mitochondria. Comparative analyses revealed SOD2-Res@CVs' superior therapeutic efficacy over individual components in histological recovery and organ function preservation. Transcriptomic profiling further validated the system's multi-target regulatory capacity, highlighting its concurrent suppression of oxidative stress pathways, mitigation of inflammatory signaling, and improvement of mitochondrial bioenergetics during IRI progression. This study establishes SOD2-Res@CVs as a multifunctional nanotherapeutic strategy that harmonizes spatial targeting with pathological microenvironment responsiveness and a promising approach for liver protection in transplantation.http://www.sciencedirect.com/science/article/pii/S2590006425007859Hepatic ischemia-reperfusion injuryCellular vesiclesMesenchymal stem cellMitochondrial homeostasisResveratrol
spellingShingle Pu Shen
Kaijun Huang
Xuanlin Zhang
Guiyuan Yin
Meiting Qin
Hua Ma
Zhijin Fan
Yuhui Liao
Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
Materials Today Bio
Hepatic ischemia-reperfusion injury
Cellular vesicles
Mesenchymal stem cell
Mitochondrial homeostasis
Resveratrol
title Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
title_full Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
title_fullStr Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
title_full_unstemmed Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
title_short Genetically engineered MSC-derived hybrid cellular vesicles for ROS-scavenging and mitochondrial homeostasis in hepatic ischemia-reperfusion injury
title_sort genetically engineered msc derived hybrid cellular vesicles for ros scavenging and mitochondrial homeostasis in hepatic ischemia reperfusion injury
topic Hepatic ischemia-reperfusion injury
Cellular vesicles
Mesenchymal stem cell
Mitochondrial homeostasis
Resveratrol
url http://www.sciencedirect.com/science/article/pii/S2590006425007859
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