Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner

Inflammation is associated with a wide range of medical conditions, most leading causes of death, and high healthcare costs. It can thus benefit from new insights. Here we extended previous studies and found that oxidation of human native mtRNA to ‘mitoxRNA’ strongly potentiated IFNβ and TNFα immuno...

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Main Authors: Hung-Yun Lin, Ramon B. Ramos, Dana R. Crawford
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Redox Report
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Online Access:https://www.tandfonline.com/doi/10.1080/13510002.2025.2491845
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author Hung-Yun Lin
Ramon B. Ramos
Dana R. Crawford
author_facet Hung-Yun Lin
Ramon B. Ramos
Dana R. Crawford
author_sort Hung-Yun Lin
collection DOAJ
description Inflammation is associated with a wide range of medical conditions, most leading causes of death, and high healthcare costs. It can thus benefit from new insights. Here we extended previous studies and found that oxidation of human native mtRNA to ‘mitoxRNA’ strongly potentiated IFNβ and TNFα immunostimulation in human cells, and that this newly identified type 1 interferon potentiation was transcriptional. This potentiation was significantly greater than with mtDNA oxidation, and t-butylhydroperoxide (tBHP) oxidation of RNA was more proinflammatory than hydrogen peroxide (HP). mtRNA triggered a modest increase in apoptosis that was not potentiated by oxidation, and mtDNA triggered a much greater increase. For native mtRNA, we found that chloroquine-inhibitable endosomes and MDA5 are key signaling pathways for IFNβ and TNFα production. For mitoxRNAs, RNAseq revealed a major increase in both tBHP- and HP-mitoxRNA modulated genes compared with native mtRNA. This increase was very prominent for interferon-related genes, identifying them as important mediators of this powerful oxidation effect. Moderately different gene modulations and KEGG pathways were observed for tBHP- versus HP-mitoxRNAs. These studies reveal the profound effect that mitochondrial RNA oxidation has on immunostimulation, providing new insights into DAMP inflammation and identifying potential therapeutic targets to minimize DAMP mtRNA/mitoxRNA-mediated inflammation.
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spelling doaj-art-09c7a82161284dfcad1312fc4c93bb9b2025-08-20T02:26:46ZengTaylor & Francis GroupRedox Report1351-00021743-29282025-12-0130110.1080/13510002.2025.2491845Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated mannerHung-Yun Lin0Ramon B. Ramos1Dana R. Crawford2Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei, TaiwanDepartment of Molecular and Cellular Physiology, Albany Medical College, Albany, NY, USADepartment of Immunology and Microbial Disease, Albany Medical College, Albany, NY, USAInflammation is associated with a wide range of medical conditions, most leading causes of death, and high healthcare costs. It can thus benefit from new insights. Here we extended previous studies and found that oxidation of human native mtRNA to ‘mitoxRNA’ strongly potentiated IFNβ and TNFα immunostimulation in human cells, and that this newly identified type 1 interferon potentiation was transcriptional. This potentiation was significantly greater than with mtDNA oxidation, and t-butylhydroperoxide (tBHP) oxidation of RNA was more proinflammatory than hydrogen peroxide (HP). mtRNA triggered a modest increase in apoptosis that was not potentiated by oxidation, and mtDNA triggered a much greater increase. For native mtRNA, we found that chloroquine-inhibitable endosomes and MDA5 are key signaling pathways for IFNβ and TNFα production. For mitoxRNAs, RNAseq revealed a major increase in both tBHP- and HP-mitoxRNA modulated genes compared with native mtRNA. This increase was very prominent for interferon-related genes, identifying them as important mediators of this powerful oxidation effect. Moderately different gene modulations and KEGG pathways were observed for tBHP- versus HP-mitoxRNAs. These studies reveal the profound effect that mitochondrial RNA oxidation has on immunostimulation, providing new insights into DAMP inflammation and identifying potential therapeutic targets to minimize DAMP mtRNA/mitoxRNA-mediated inflammation.https://www.tandfonline.com/doi/10.1080/13510002.2025.2491845Mitochondriaoxidative stressT-butylhydroperoxidehydrogen peroxidetype 1 interferonsproinflammatory cytokines
spellingShingle Hung-Yun Lin
Ramon B. Ramos
Dana R. Crawford
Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
Redox Report
Mitochondria
oxidative stress
T-butylhydroperoxide
hydrogen peroxide
type 1 interferons
proinflammatory cytokines
title Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
title_full Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
title_fullStr Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
title_full_unstemmed Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
title_short Oxidation of human mitochondrial RNA strongly potentiates immunostimulation in an interferon-associated manner
title_sort oxidation of human mitochondrial rna strongly potentiates immunostimulation in an interferon associated manner
topic Mitochondria
oxidative stress
T-butylhydroperoxide
hydrogen peroxide
type 1 interferons
proinflammatory cytokines
url https://www.tandfonline.com/doi/10.1080/13510002.2025.2491845
work_keys_str_mv AT hungyunlin oxidationofhumanmitochondrialrnastronglypotentiatesimmunostimulationinaninterferonassociatedmanner
AT ramonbramos oxidationofhumanmitochondrialrnastronglypotentiatesimmunostimulationinaninterferonassociatedmanner
AT danarcrawford oxidationofhumanmitochondrialrnastronglypotentiatesimmunostimulationinaninterferonassociatedmanner