Oncogenic MCT-1 activation promotes YY1-EGFR-MnSOD signaling and tumor progression
Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that balances antioxidative and oxidative stress in cancer cells is unclear. Here, we determined that oncogenic multiple copies in T-cell malignancy...
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Published in | Oncogenesis (New York, NY) Vol. 6; no. 4; p. e313 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Nature Publishing Group UK
10.04.2017
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Abstract | Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that balances antioxidative and oxidative stress in cancer cells is unclear. Here, we determined that oncogenic multiple copies in T-cell malignancy 1 (MCT-1) activity promotes the generation of intracellular ROS and mitochondrial superoxide. Overexpression of MCT-1 suppresses p53 accumulation but elevates the manganese-dependent superoxide dismutase (MnSOD) level via the YY1-EGFR signaling cascade, which protects cells against oxidative damage. Conversely, restricting ROS generation and/or targeting YY1 in lung cancer cells effectively inhibits the EGFR-MnSOD signaling pathway and cell invasiveness induced by MCT-1. Significantly, MCT-1 overexpression in lung cancer cells promotes tumor progression, necrosis and angiogenesis, and increases the number of tumor-promoting M2 macrophages and cancer-associated fibroblasts in the microenvironment. Clinical evidence further confirms that high expression of MCT-1 is associated with an increase in YY1, EGFR and MnSOD expression, accompanied by tumor recurrence, poor overall survival and EGFR mutation status in patients with lung cancers. Together, these data indicate that the MCT-1 oncogenic pathway is implicated in oxidative metabolism and lung carcinogenesis. |
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AbstractList | Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that balances antioxidative and oxidative stress in cancer cells is unclear. Here, we determined that oncogenic multiple copies in T-cell malignancy 1 (MCT-1) activity promotes the generation of intracellular ROS and mitochondrial superoxide. Overexpression of MCT-1 suppresses p53 accumulation but elevates the manganese-dependent superoxide dismutase (MnSOD) level via the YY1-EGFR signaling cascade, which protects cells against oxidative damage. Conversely, restricting ROS generation and/or targeting YY1 in lung cancer cells effectively inhibits the EGFR-MnSOD signaling pathway and cell invasiveness induced by MCT-1. Significantly, MCT-1 overexpression in lung cancer cells promotes tumor progression, necrosis and angiogenesis, and increases the number of tumor-promoting M2 macrophages and cancer-associated fibroblasts in the microenvironment. Clinical evidence further confirms that high expression of MCT-1 is associated with an increase in YY1, EGFR and MnSOD expression, accompanied by tumor recurrence, poor overall survival and EGFR mutation status in patients with lung cancers. Together, these data indicate that the MCT-1 oncogenic pathway is implicated in oxidative metabolism and lung carcinogenesis. Abstract Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that balances antioxidative and oxidative stress in cancer cells is unclear. Here, we determined that oncogenic multiple copies in T-cell malignancy 1 (MCT-1) activity promotes the generation of intracellular ROS and mitochondrial superoxide. Overexpression of MCT-1 suppresses p53 accumulation but elevates the manganese-dependent superoxide dismutase (MnSOD) level via the YY1-EGFR signaling cascade, which protects cells against oxidative damage. Conversely, restricting ROS generation and/or targeting YY1 in lung cancer cells effectively inhibits the EGFR-MnSOD signaling pathway and cell invasiveness induced by MCT-1. Significantly, MCT-1 overexpression in lung cancer cells promotes tumor progression, necrosis and angiogenesis, and increases the number of tumor-promoting M2 macrophages and cancer-associated fibroblasts in the microenvironment. Clinical evidence further confirms that high expression of MCT-1 is associated with an increase in YY1, EGFR and MnSOD expression, accompanied by tumor recurrence, poor overall survival and EGFR mutation status in patients with lung cancers. Together, these data indicate that the MCT-1 oncogenic pathway is implicated in oxidative metabolism and lung carcinogenesis. Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that balances antioxidative and oxidative stress in cancer cells is unclear. Here, we determined that oncogenic multiple copies in T-cell malignancy 1 (MCT-1) activity promotes the generation of intracellular ROS and mitochondrial superoxide. Overexpression of MCT-1 suppresses p53 accumulation but elevates the manganese-dependent superoxide dismutase (MnSOD) level via the YY1-EGFR signaling cascade, which protects cells against oxidative damage. Conversely, restricting ROS generation and/or targeting YY1 in lung cancer cells effectively inhibits the EGFR-MnSOD signaling pathway and cell invasiveness induced by MCT-1. Signicantly, MCT-1 overexpression in lung cancer cells promotes tumor progression, necrosis and angiogenesis, and increases the number of tumor-promoting M2 macrophages and cancer-associated broblasts in the microenvironment. Clinical evidence further conrms that high expression of MCT-1 is associated with an increase in YY1, EGFR and MnSOD expression, accompanied by tumor recurrence, poor overall survival and EGFR mutation status in patients with lung cancers. Together, these data indicate that the MCT-1 oncogenic pathway is implicated in oxidative metabolism and lung carcinogenesis. |
Author | Chen, Y-A Chen, L-M Shen, P-C Tseng, H-Y Wang, Y-C Hsu, H-L Jen, J Lin, T-D |
Author_xml | – sequence: 1 givenname: H-Y surname: Tseng fullname: Tseng, H-Y organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes – sequence: 2 givenname: Y-A surname: Chen fullname: Chen, Y-A organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes – sequence: 3 givenname: J surname: Jen fullname: Jen, J organization: Department of Pharmacology, National Cheng Kung University – sequence: 4 givenname: P-C surname: Shen fullname: Shen, P-C organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes – sequence: 5 givenname: L-M surname: Chen fullname: Chen, L-M organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes – sequence: 6 givenname: T-D surname: Lin fullname: Lin, T-D organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes – sequence: 7 givenname: Y-C surname: Wang fullname: Wang, Y-C organization: Department of Pharmacology, National Cheng Kung University – sequence: 8 givenname: H-L surname: Hsu fullname: Hsu, H-L email: hsinling88@nhri.org.tw organization: Institute of Molecular and Genomic Medicine, National Health Research Institutes |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28394354$$D View this record in MEDLINE/PubMed |
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Snippet | Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular mechanism that... Abstract Tumor cells often produce high levels of reactive oxygen species (ROS) and display an increased ROS scavenging system. However, the molecular... |
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SubjectTerms | 13/1 13/105 13/109 13/31 631/67/1612/1350 631/67/2327 631/67/327 64/60 82/51 82/80 Apoptosis Cell Biology Gene expression Human Genetics Internal Medicine Medicine Medicine & Public Health Oncology Original original-article Oxidative stress Proteins Signal transduction Tumorigenesis |
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Title | Oncogenic MCT-1 activation promotes YY1-EGFR-MnSOD signaling and tumor progression |
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