Superoxide Dismutase 1 Protects Hepatocytes from Type I Interferon-Driven Oxidative Damage

Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1−/− mice...

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Published inImmunity (Cambridge, Mass.) Vol. 43; no. 5; pp. 974 - 986
Main Authors Bhattacharya, Anannya, Hegazy, Ahmed N., Deigendesch, Nikolaus, Kosack, Lindsay, Cupovic, Jovana, Kandasamy, Richard K., Hildebrandt, Andrea, Merkler, Doron, Kühl, Anja A., Vilagos, Bojan, Schliehe, Christopher, Panse, Isabel, Khamina, Kseniya, Baazim, Hatoon, Arnold, Isabelle, Flatz, Lukas, Xu, Haifeng C., Lang, Philipp A., Aderem, Alan, Takaoka, Akinori, Superti-Furga, Giulio, Colinge, Jacques, Ludewig, Burkhard, Löhning, Max, Bergthaler, Andreas
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 17.11.2015
Elsevier Limited
Elsevier
The Authors. Published by Elsevier Inc
Subjects
Animals
Antioxidants
Antioxidants - metabolism
Biomedical research
Cloning
Colleges & universities
Enzymes
Experiments
Gene expression
Hepatitis, Viral, Animal - immunology
Hepatocytes - immunology
Human health and pathology
Immunity, Innate - immunology
Infections
Inflammation - immunology
Interferon Type I - immunology
Killer Cells, Natural - immunology
Life Sciences
Liver - immunology
Liver cancer
Mice
Mice, Inbred C57BL
Mortality
Oxidation-Reduction
Oxidative stress
Oxidative Stress - immunology
Pathogenesis
Pathology
Rodents
Scholarships & fellowships
Signal Transduction - immunology
Superoxide Dismutase - immunology
Superoxide Dismutase-1
T-Lymphocytes - immunology
Transcription, Genetic - immunology
Viral infections
Online AccessGet full text

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Abstract Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1−/− mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1−/− and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. [Display omitted] [Display omitted] •Viral infection leads to redox dysregulation including the downregulation of SOD1•Sod1−/− mice exhibit aggravated viral hepatitis, which is rescued by antioxidants•IFN-I signaling via STAT1 drives SOD1 downregulation and early liver damage•Ablation of IFN-I signaling ameliorates viral hepatitis in Sod1−/− and WT mice Bergthaler and colleagues show that superoxide dismutase 1 protects the liver from type I interferon-driven oxidative damage in viral hepatitis. Liver damage was mediated by hepatocyte-intrinsic IFNAR1-STAT1 signaling.
AbstractList Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1).Sod1-/-mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation ofSod1and caused oxidative liver damage inSod1-/-and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. Video Abstract
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1(-/-) mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1(-/-) and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. VIDEO ABSTRACT.
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1−/− mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1−/− and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. [Display omitted] [Display omitted] •Viral infection leads to redox dysregulation including the downregulation of SOD1•Sod1−/− mice exhibit aggravated viral hepatitis, which is rescued by antioxidants•IFN-I signaling via STAT1 drives SOD1 downregulation and early liver damage•Ablation of IFN-I signaling ameliorates viral hepatitis in Sod1−/− and WT mice Bergthaler and colleagues show that superoxide dismutase 1 protects the liver from type I interferon-driven oxidative damage in viral hepatitis. Liver damage was mediated by hepatocyte-intrinsic IFNAR1-STAT1 signaling.
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1(-/-) mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1(-/-) and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. VIDEO ABSTRACT.
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1-/- mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1-/- and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage. Video Abstract
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified virus-induced early transcriptional changes in the redox pathways in the liver, including downregulation of superoxide dismutase 1 (Sod1). Sod1(-/-) mice exhibited increased inflammation and aggravated liver damage upon viral infection, which was independent of T and NK cells and could be ameliorated by antioxidant treatment. Type I interferon (IFN-I) led to a downregulation of Sod1 and caused oxidative liver damage in Sod1(-/-) and wild-type mice. Genetic and pharmacological ablation of the IFN-I signaling pathway protected against virus-induced liver damage. These results delineate IFN-I mediated oxidative stress as a key mediator of virus-induced liver damage and describe a mechanism of innate-immunity-driven pathology, linking IFN-I signaling with antioxidant host defense and infection-associated tissue damage.
• Viral infection leads to redox dysregulation including the downregulation of SOD1 • Sod1 −/− mice exhibit aggravated viral hepatitis, which is rescued by antioxidants • IFN-I signaling via STAT1 drives SOD1 downregulation and early liver damage • Ablation of IFN-I signaling ameliorates viral hepatitis in Sod1 −/− and WT mice Bergthaler and colleagues show that superoxide dismutase 1 protects the liver from type I interferon-driven oxidative damage in viral hepatitis. Liver damage was mediated by hepatocyte-intrinsic IFNAR1-STAT1 signaling.
Author Hildebrandt, Andrea
Arnold, Isabelle
Panse, Isabel
Kandasamy, Richard K.
Schliehe, Christopher
Vilagos, Bojan
Colinge, Jacques
Xu, Haifeng C.
Takaoka, Akinori
Löhning, Max
Ludewig, Burkhard
Deigendesch, Nikolaus
Bergthaler, Andreas
Kosack, Lindsay
Baazim, Hatoon
Superti-Furga, Giulio
Cupovic, Jovana
Bhattacharya, Anannya
Merkler, Doron
Flatz, Lukas
Lang, Philipp A.
Kühl, Anja A.
Khamina, Kseniya
Aderem, Alan
Hegazy, Ahmed N.
AuthorAffiliation 3 German Rheumatism Research Center (DRFZ), a Leibniz Institute, 10117 Berlin, Germany
8 Department of Neuropathology, University Medicine Göttingen, Robert-Koch Strasse 40, 37099 Goettingen, Germany
9 Department of Medicine I for Gastroenterology, Infectious Disease and Rheumatology, Campus Benjamin Franklin, Charité-Universitätsmedizin Berlin, Hindenburgdamm 30, 12200 Berlin, Germany
14 Center for Physiology and Pharmacology, Medical University of Vienna, Lazarettgasse 14, 1090 Vienna, Austria
10 Department of Gastroenterology, Heinrich-Heine-University, Moorenstrasse 5, 40225 Düsseldorf, Germany
11 Department of Molecular Medicine II, Heinrich Heine University, Universitätsstrasse 1, 40225 Düsseldorf, Germany
1 CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Lazarettgasse 14 AKH BT25.3, 1090 Vienna, Austria
12 Seattle Biomedical Research Institute, 307 Westlake Avenue North, Suite 500, Seattle, WA 98109-5219, USA
13 Division of Signaling in Cancer and Immuno
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– name: 10 Department of Gastroenterology, Heinrich-Heine-University, Moorenstrasse 5, 40225 Düsseldorf, Germany
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– name: 7 Department of Pathology and Immunology, University of Geneva, Centre Médical Universitaire, 1 rue Michel Servet, 1211 Geneva, Switzerland
– name: 14 Center for Physiology and Pharmacology, Medical University of Vienna, Lazarettgasse 14, 1090 Vienna, Austria
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Copyright 2015 The Authors
Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
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2015 The Authors 2015
Copyright_xml – notice: 2015 The Authors
– notice: Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
– notice: Copyright Elsevier Limited Nov 17, 2015
– notice: Distributed under a Creative Commons Attribution 4.0 International License
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Snippet Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we...
Tissue damage caused by viral hepatitis is a major cause of morbidity and mortality worldwide. Using a mouse model of viral hepatitis, we identified...
• Viral infection leads to redox dysregulation including the downregulation of SOD1 • Sod1 −/− mice exhibit aggravated viral hepatitis, which is rescued by...
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SubjectTerms Animals
Antioxidants
Antioxidants - metabolism
Biomedical research
Cloning
Colleges & universities
Enzymes
Experiments
Gene expression
Hepatitis, Viral, Animal - immunology
Hepatocytes - immunology
Human health and pathology
Immunity, Innate - immunology
Infections
Inflammation - immunology
Interferon Type I - immunology
Killer Cells, Natural - immunology
Life Sciences
Liver - immunology
Liver cancer
Mice
Mice, Inbred C57BL
Mortality
Oxidation-Reduction
Oxidative stress
Oxidative Stress - immunology
Pathogenesis
Pathology
Rodents
Scholarships & fellowships
Signal Transduction - immunology
Superoxide Dismutase - immunology
Superoxide Dismutase-1
T-Lymphocytes - immunology
Transcription, Genetic - immunology
Viral infections
Title Superoxide Dismutase 1 Protects Hepatocytes from Type I Interferon-Driven Oxidative Damage
URI https://dx.doi.org/10.1016/j.immuni.2015.10.013
https://www.ncbi.nlm.nih.gov/pubmed/26588782
https://www.proquest.com/docview/1735318697
https://www.proquest.com/docview/1735331230
https://www.proquest.com/docview/1751215129
https://hal.umontpellier.fr/hal-02336008
https://pubmed.ncbi.nlm.nih.gov/PMC4658338
Volume 43
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