Regulation of Reactive Oxygen Species and the Antioxidant Protein DJ-1 in Mastocytosis
Neoplastic accumulation of mast cells in systemic mastocytosis (SM) associates with activating mutations in the receptor tyrosine kinase KIT. Constitutive activation of tyrosine kinase oncogenes has been linked to imbalances in oxidant/antioxidant mechanisms in other myeloproliferative disorders. Ho...
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Published in | PloS one Vol. 11; no. 9; p. e0162831 |
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Main Authors | , , , , , , , , , , |
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Language | English |
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09.09.2016
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Abstract | Neoplastic accumulation of mast cells in systemic mastocytosis (SM) associates with activating mutations in the receptor tyrosine kinase KIT. Constitutive activation of tyrosine kinase oncogenes has been linked to imbalances in oxidant/antioxidant mechanisms in other myeloproliferative disorders. However, the impact of KIT mutations on the redox status in SM and the potential therapeutic implications are not well understood. Here, we examined the regulation of reactive oxygen species (ROS) and of the antioxidant protein DJ-1 (PARK-7), which increases with cancer progression and acts to lessen oxidative damage to malignant cells, in relationship with SM severity. ROS levels were increased in both indolent (ISM) and aggressive variants of the disease (ASM). However, while DJ-1 levels were reduced in ISM with lower mast cell burden, they rose in ISM with higher mast cell burden and were significantly elevated in patients with ASM. Studies on mast cell lines revealed that activating KIT mutations induced constant ROS production and consequent DJ-1 oxidation and degradation that could explain the reduced levels of DJ-1 in the ISM population, while IL-6, a cytokine that increases with disease severity, caused a counteracting transcriptional induction of DJ-1 which would protect malignant mast cells from oxidative damage. A mouse model of mastocytosis recapitulated the biphasic changes in DJ-1 and the escalating IL-6, ROS and DJ-1 levels as mast cells accumulate, findings which were reversed with anti-IL-6 receptor blocking antibody. Our findings provide evidence of increased ROS and a biphasic regulation of the antioxidant DJ-1 in variants of SM and implicate IL-6 in DJ-1 induction and expansion of mast cells with KIT mutations. We propose consideration of IL-6 blockade as a potential adjunctive therapy in the treatment of patients with advanced mastocytosis, as it would reduce DJ-1 levels making mutation-positive mast cells vulnerable to oxidative damage. |
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AbstractList | Neoplastic accumulation of mast cells in systemic mastocytosis (SM) associates with activating mutations in the receptor tyrosine kinase KIT. Constitutive activation of tyrosine kinase oncogenes has been linked to imbalances in oxidant/antioxidant mechanisms in other myeloproliferative disorders. However, the impact of KIT mutations on the redox status in SM and the potential therapeutic implications are not well understood. Here, we examined the regulation of reactive oxygen species (ROS) and of the antioxidant protein DJ-1 (PARK-7), which increases with cancer progression and acts to lessen oxidative damage to malignant cells, in relationship with SM severity. ROS levels were increased in both indolent (ISM) and aggressive variants of the disease (ASM). However, while DJ-1 levels were reduced in ISM with lower mast cell burden, they rose in ISM with higher mast cell burden and were significantly elevated in patients with ASM. Studies on mast cell lines revealed that activating KIT mutations induced constant ROS production and consequent DJ-1 oxidation and degradation that could explain the reduced levels of DJ-1 in the ISM population, while IL-6, a cytokine that increases with disease severity, caused a counteracting transcriptional induction of DJ-1 which would protect malignant mast cells from oxidative damage. A mouse model of mastocytosis recapitulated the biphasic changes in DJ-1 and the escalating IL-6, ROS and DJ-1 levels as mast cells accumulate, findings which were reversed with anti-IL-6 receptor blocking antibody. Our findings provide evidence of increased ROS and a biphasic regulation of the antioxidant DJ-1 in variants of SM and implicate IL-6 in DJ-1 induction and expansion of mast cells with KIT mutations. We propose consideration of IL-6 blockade as a potential adjunctive therapy in the treatment of patients with advanced mastocytosis, as it would reduce DJ-1 levels making mutation-positive mast cells vulnerable to oxidative damage. Neoplastic accumulation of mast cells in systemic mastocytosis (SM) associates with activating mutations in the receptor tyrosine kinase KIT. Constitutive activation of tyrosine kinase oncogenes has been linked to imbalances in oxidant/antioxidant mechanisms in other myeloproliferative disorders. However, the impact of KIT mutations on the redox status in SM and the potential therapeutic implications are not well understood. Here, we examined the regulation of reactive oxygen species (ROS) and of the antioxidant protein DJ-1 (PARK-7), which increases with cancer progression and acts to lessen oxidative damage to malignant cells, in relationship with SM severity. ROS levels were increased in both indolent (ISM) and aggressive variants of the disease (ASM). However, while DJ-1 levels were reduced in ISM with lower mast cell burden, they rose in ISM with higher mast cell burden and were significantly elevated in patients with ASM. Studies on mast cell lines revealed that activating KIT mutations induced constant ROS production and consequent DJ-1 oxidation and degradation that could explain the reduced levels of DJ-1 in the ISM population, while IL-6, a cytokine that increases with disease severity, caused a counteracting transcriptional induction of DJ-1 which would protect malignant mast cells from oxidative damage. A mouse model of mastocytosis recapitulated the biphasic changes in DJ-1 and the escalating IL-6, ROS and DJ-1 levels as mast cells accumulate, findings which were reversed with anti-IL-6 receptor blocking antibody. Our findings provide evidence of increased ROS and a biphasic regulation of the antioxidant DJ-1 in variants of SM and implicate IL-6 in DJ-1 induction and expansion of mast cells with KIT mutations. We propose consideration of IL-6 blockade as a potential adjunctive therapy in the treatment of patients with advanced mastocytosis, as it would reduce DJ-1 levels making mutation-positive mast cells vulnerable to oxidative damage. |
Audience | Academic |
Author | Kim, Do-Kyun Olivera, Ana Beaven, Michael A Schwartz, Lawrence B Bandara, Geethani Bai, Yun Komarow, Hirsh Prussin, Calman Kulinski, Joseph M Metcalfe, Dean D Desai, Avanti |
AuthorAffiliation | 1 Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America 3 Department of Internal Medicine, Virginia Commonwealth University, Richmond, Virginia, United States of America 2 Laboratory of Molecular Immunology, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Maryland, United States of America Toho Daigaku, JAPAN |
AuthorAffiliation_xml | – name: 3 Department of Internal Medicine, Virginia Commonwealth University, Richmond, Virginia, United States of America – name: 2 Laboratory of Molecular Immunology, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Maryland, United States of America – name: 1 Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – name: Toho Daigaku, JAPAN |
Author_xml | – sequence: 1 givenname: Do-Kyun surname: Kim fullname: Kim, Do-Kyun organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 2 givenname: Michael A surname: Beaven fullname: Beaven, Michael A organization: Laboratory of Molecular Immunology, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 3 givenname: Joseph M surname: Kulinski fullname: Kulinski, Joseph M organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 4 givenname: Avanti surname: Desai fullname: Desai, Avanti organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 5 givenname: Geethani surname: Bandara fullname: Bandara, Geethani organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 6 givenname: Yun surname: Bai fullname: Bai, Yun organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 7 givenname: Calman surname: Prussin fullname: Prussin, Calman organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 8 givenname: Lawrence B surname: Schwartz fullname: Schwartz, Lawrence B organization: Department of Internal Medicine, Virginia Commonwealth University, Richmond, Virginia, United States of America – sequence: 9 givenname: Hirsh surname: Komarow fullname: Komarow, Hirsh organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 10 givenname: Dean D surname: Metcalfe fullname: Metcalfe, Dean D organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 11 givenname: Ana surname: Olivera fullname: Olivera, Ana organization: Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceptualization: AO DKK MAB DDM. Data curation: DKK. Formal analysis: DKK. Funding acquisition: DKK DDM. Investigation: DKK MAB JMK AD AO. Methodology: DKK GB YB. Project administration: DKK AO MAB DDM. Resources: YB CP LBS HK DDM. Supervision: AO MAB DDM. Validation: DKK. Visualization: DKK MAB AO DDM. Writing – original draft: AO MAB. Writing – review & editing: AO DDM MAB LBS. |
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Snippet | Neoplastic accumulation of mast cells in systemic mastocytosis (SM) associates with activating mutations in the receptor tyrosine kinase KIT. Constitutive... |
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SubjectTerms | Adoptive Transfer Adult Allergies Animals Antioxidants Antioxidants (Nutrients) Antioxidants - metabolism Biology Biology and Life Sciences Blocking antibodies Cancer Cell Line Damage Development and progression Extracellular Space - metabolism Gene expression Genetic aspects Health aspects Homeostasis Humans Immunology Infectious diseases Interleukin 6 Interleukin 6 receptors Kinases Laboratories Mast cells Mast Cells - metabolism Mastocytoma - pathology Mastocytosis Mastocytosis - blood Mastocytosis - metabolism Medical prognosis Medicine and Health Sciences Mice Middle Aged Mutation Mutation - genetics Myeloproliferative diseases Oxidation Oxidative stress Oxidizing agents Oxygen PARK7 protein Parkinson's disease Patients Physical Sciences Protein Deglycase DJ-1 - blood Protein Deglycase DJ-1 - genetics Protein Deglycase DJ-1 - metabolism Protein-tyrosine kinase receptors Proteins Proteolysis Proto-Oncogene Proteins c-kit - genetics Proto-Oncogene Proteins c-kit - metabolism Reactive oxygen species Reactive Oxygen Species - blood Reactive Oxygen Species - metabolism Receptors, Interleukin-6 - metabolism Research and Analysis Methods Transcription Transcription, Genetic Tyrosine |
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Title | Regulation of Reactive Oxygen Species and the Antioxidant Protein DJ-1 in Mastocytosis |
URI | https://www.ncbi.nlm.nih.gov/pubmed/27611333 https://www.proquest.com/docview/1818054935 https://search.proquest.com/docview/1819122867 https://search.proquest.com/docview/1827882588 https://pubmed.ncbi.nlm.nih.gov/PMC5017616 https://doaj.org/article/3e0167753f844c6f8eb86c65501568f3 http://dx.doi.org/10.1371/journal.pone.0162831 |
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