ROS-Generating Mitochondrial DNA Mutations Can Regulate Tumor Cell Metastasis
Open accessAbstract
Mutations in mitochondrial DNA (mtDNA) occur at high frequency in human tumors, but whether these mutations alter tumor cell behavior has been unclear. We used cytoplasmic hybrid (cybrid) technology to replace the endogenous mtDNA in a mouse tumor cell line that was poorly metastatic with mtDNA from a cell line that was highly metastatic, and vice versa. Using assays of metastasis in mice, we found that the recipient tumor cells acquired the metastatic potential of the transferred mtDNA. The mtDNA conferring high metastatic potential contained G13997A and 13885insC mutations in the gene encoding NADH (reduced form of nicotinamide adenine dinucleotide) dehydrogenase subunit 6 ( ND6 ). These mutations produced a deficiency in respiratory complex I activity and were associated with overproduction of reactive oxygen species (ROS). Pretreatment of the highly metastatic tumor cells with ROS scavengers suppressed their metastatic potential in mice. These results indicate that mtDNA mutations can contribute to tumor progression by enhancing the metastatic potential of tumor cells.
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mtDNA mutations cause alterations in the mitochondrial electron transport chain which promotes aerobic glycolysis, a hallmark property necessary for tumor growth and metastasis in lung cancer.
“mtDNA mutations cause alterations in the mitochondrial electron transport chain which promotes aerobic glycolysis, a hallmark property necessary for tumor growth and metastasis in lung cancer.”
From Reactive Oxygen Species, Toxicity, Oxidative Stress, and Antioxidants: Chronic Diseases and Aging (2023) · cites this paper as Ishikawa et al. 2008
ROS-mediated signaling promotes metastasis in addition to its involvement in tumor initiation and maintenance.
“ROS-mediated signaling is not only involved in tumor initiation and maintenance; it also promotes metastasis.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [76]
Transfer of mutant mitochondria to a poorly metastatic tumor cell line was sufficient to increase the metastatic potential of the recipient cell line.
“Transfer of mutant mitochondria to a poorly metastatic tumor cell line was sufficient to increase the metastatic potential of the recipient cell line.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [76]
The G13997A mutation in the gene encoding the ND6 subunit of mitochondrial complex I is associated with high HIF activity and increased metastatic potential.
“This mutation is also associated with high HIF activity and increased metastatic potential 76, 77.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [76]
The increased metastatic potential resulting from transfer of mutant mitochondria was inhibited by treatment with antioxidants.
“Notably, this metastasis was inhibited by treatment with antioxidants 76.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [76]
Cells harboring the G13997A mutation in the gene encoding the ND6 subunit of mitochondrial complex I are characterized by respiratory deficiency and high ROS production.
“Cells harboring the G13997A mutation in the gene encoding the ND6 subunit of mitochondrial complex I are characterized by respiratory deficiency and high ROS production.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [76]
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- Authors
- Ishikawa, K., Takenaga, K., Akimoto, M., Koshikawa, N., Yamaguchi, A., Imanishi, H., Nakada, K., Honma, Y., & Hayashi, J.-I.
- Affiliations
- University of Tsukuba (JP)
- Corresponding author
- Ishikawa, Kaori
- Takenaga, Keizo
- Hayashi, Jun-Ichi
- ORCID
- Venue
- Science
- Published
- 2008-05-02
- Volume
- 320
- Issue
- 5876
- Pages
- 661-664
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2070143299
- Cited by
- 1,444
- References
- 27
- Citations by year
- 2026: 38 · 2025: 56 · 2024: 54 · 2023: 85 · 2022: 81 · 2021: 108 · 2020: 99 · 2019: 88 · 2018: 76 · 2017: 96 · 2016: 89 · 2015: 84 · 2014: 67 · 2013: 85 · 2012: 75
- FWCI
- 35.97
- Type
- journal article
- Language
- en
- Open access
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (acceptedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Terrestrial Environment Research Center (University of Tsukuba) (submittedVersion, cc-by-nc-nd)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer and biochemical research
- Keywords
- mitochondrial DNA mutations, metastasis, reactive oxygen species, ND6, cybrid cells, ROS scavengers, tumor progression, mitochondrial DNA transfer
- MeSH terms
- Acetylcysteine, Animals, Antineoplastic Agents, DNA, Mitochondrial, DNA, Neoplasm, HeLa Cells, Humans, Hybrid Cells, Mutation, NADH Dehydrogenase, Neoplasm Metastasis, Free Radical Scavengers, Reactive Oxygen Species, Electron Transport Complex I, Cell Line, Tumor, Mice
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