Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma

Abstract Glioblastoma (GBM) is the most aggressive primary brain malignancy in adults, with high recurrence rates and resistance to standard therapies. This study explores mitochondrial transplantation as a novel method to enhance the radiobiological effect (RBE) of ionizing radiation (IR) by increa...

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Main Authors: Kent L. Marshall, Murugesan Velayutham, Valery V. Khramtsov, Alan Mizener, Christopher P. Cifarelli
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-91331-2
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author Kent L. Marshall
Murugesan Velayutham
Valery V. Khramtsov
Alan Mizener
Christopher P. Cifarelli
author_facet Kent L. Marshall
Murugesan Velayutham
Valery V. Khramtsov
Alan Mizener
Christopher P. Cifarelli
author_sort Kent L. Marshall
collection DOAJ
description Abstract Glioblastoma (GBM) is the most aggressive primary brain malignancy in adults, with high recurrence rates and resistance to standard therapies. This study explores mitochondrial transplantation as a novel method to enhance the radiobiological effect (RBE) of ionizing radiation (IR) by increasing mitochondrial density in GBM cells, potentially boosting reactive oxygen species (ROS) production and promoting radiation-induced cell death. Using cell-penetrating peptides (CPPs), mitochondria were transplanted into GBM cell lines U3035 and U3046. Transplanted mitochondria were successfully incorporated into recipient cells, increasing mitochondrial density significantly. Mitochondrial chimeric cells demonstrated enhanced ROS generation post-irradiation, as evidenced by increased electron paramagnetic resonance (EPR) signal intensity and fluorescent ROS assays. The transplanted mitochondria retained functionality and viability for up to 14 days, with mitochondrial DNA (mtDNA) sequencing confirming high transfection and retention rates. Notably, mitochondrial transplantation was feasible in radiation-resistant GBM cells, suggesting potential clinical applicability. These findings support mitochondrial transplantation as a promising strategy to overcome therapeutic resistance in GBM by amplifying ROS-mediated cytotoxicity, warranting further investigation into its efficacy and mechanisms in vivo.
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spelling doaj-art-c5e35218fabc439f9fd74fb2e2588eb02025-08-20T01:57:27ZengNature PortfolioScientific Reports2045-23222025-03-0115111410.1038/s41598-025-91331-2Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastomaKent L. Marshall0Murugesan Velayutham1Valery V. Khramtsov2Alan Mizener3Christopher P. Cifarelli4Department of Neurosurgery, Rockefeller Neuroscience Institute, West Virginia UniversityDepartment of Biochemistry and Molecular Medicine, West Virginia UniversityDepartment of Biochemistry and Molecular Medicine, West Virginia UniversityWest Virginia University Cancer InstituteDepartment of Neurosurgery, Rockefeller Neuroscience Institute, West Virginia UniversityAbstract Glioblastoma (GBM) is the most aggressive primary brain malignancy in adults, with high recurrence rates and resistance to standard therapies. This study explores mitochondrial transplantation as a novel method to enhance the radiobiological effect (RBE) of ionizing radiation (IR) by increasing mitochondrial density in GBM cells, potentially boosting reactive oxygen species (ROS) production and promoting radiation-induced cell death. Using cell-penetrating peptides (CPPs), mitochondria were transplanted into GBM cell lines U3035 and U3046. Transplanted mitochondria were successfully incorporated into recipient cells, increasing mitochondrial density significantly. Mitochondrial chimeric cells demonstrated enhanced ROS generation post-irradiation, as evidenced by increased electron paramagnetic resonance (EPR) signal intensity and fluorescent ROS assays. The transplanted mitochondria retained functionality and viability for up to 14 days, with mitochondrial DNA (mtDNA) sequencing confirming high transfection and retention rates. Notably, mitochondrial transplantation was feasible in radiation-resistant GBM cells, suggesting potential clinical applicability. These findings support mitochondrial transplantation as a promising strategy to overcome therapeutic resistance in GBM by amplifying ROS-mediated cytotoxicity, warranting further investigation into its efficacy and mechanisms in vivo.https://doi.org/10.1038/s41598-025-91331-2GlioblastomaMitochondriaROSEPRRadiationCell-penetrating peptide
spellingShingle Kent L. Marshall
Murugesan Velayutham
Valery V. Khramtsov
Alan Mizener
Christopher P. Cifarelli
Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
Scientific Reports
Glioblastoma
Mitochondria
ROS
EPR
Radiation
Cell-penetrating peptide
title Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
title_full Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
title_fullStr Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
title_full_unstemmed Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
title_short Enhancing radiation-induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
title_sort enhancing radiation induced reactive oxygen species generation through mitochondrial transplantation in human glioblastoma
topic Glioblastoma
Mitochondria
ROS
EPR
Radiation
Cell-penetrating peptide
url https://doi.org/10.1038/s41598-025-91331-2
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AT valeryvkhramtsov enhancingradiationinducedreactiveoxygenspeciesgenerationthroughmitochondrialtransplantationinhumanglioblastoma
AT alanmizener enhancingradiationinducedreactiveoxygenspeciesgenerationthroughmitochondrialtransplantationinhumanglioblastoma
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