Transcription factor NRF2 regulates miR-1 and miR-206 to drive tumorigenesis
Open accessAbstract
The mechanisms by which deregulated nuclear factor erythroid-2-related factor 2 (NRF2) and kelch-like ECH-associated protein 1 (KEAP1) signaling promote cellular proliferation and tumorigenesis are poorly understood. Using an integrated genomics and ¹³C-based targeted tracer fate association (TTFA) study, we found that NRF2 regulates miR-1 and miR-206 to direct carbon flux toward the pentose phosphate pathway (PPP) and the tricarboxylic acid (TCA) cycle, reprogramming glucose metabolism. Sustained activation of NRF2 signaling in cancer cells attenuated miR-1 and miR-206 expression, leading to enhanced expression of PPP genes. Conversely, overexpression of miR-1 and miR-206 decreased the expression of metabolic genes and dramatically impaired NADPH production, ribose synthesis, and in vivo tumor growth in mice. Loss of NRF2 decreased the expression of the redox-sensitive histone deacetylase, HDAC4, resulting in increased expression of miR-1 and miR-206, and not only inhibiting PPP expression and activity but functioning as a regulatory feedback loop that repressed HDAC4 expression. In primary tumor samples, the expression of miR-1 and miR-206 was inversely correlated with PPP gene expression, and increased expression of NRF2-dependent genes was associated with poor prognosis. Our results demonstrate that microRNA-dependent (miRNA-dependent) regulation of the PPP via NRF2 and HDAC4 represents a novel link between miRNA regulation, glucose metabolism, and ROS homeostasis in cancer cells.
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NRF2-mediated metabolic reprogramming and regulation of redox homeostasis likely underpin the strong co-selection of KEAP1 with LKB1 and KRAS mutations in NSCLC.
“Thus, NRF2- mediated metabolic reprogramming and regulation of redox homeostasis likely underpin the strong co-selection of KEAP1 with LKB1 and KRAS mutations in NSCLC at least partially because oncogenic KRAS itself promotes oxidative stress and anabolic metabolism and because KL NSCLC cells depend on the pentose phosphate pathway for NAPDH generation and for detoxification of reactive oxygen”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [94]
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- Authors
- Singh, A., Happel, C., Manna, S. K., Acquaah-Mensah, G., Carrerero, J., Kumar, S., Nasipuri, P., Krausz, K. W., Wakabayashi, N., Dewi, R., Boros, L. G., Gonzalez, F. J., Gabrielson, E., Wong, K. K., Girnun, G., & Biswal, S.
- Affiliations
- Johns Hopkins University (US)
- National Institutes of Health (US)
- Massachusetts College of Pharmacy and Health Sciences (US)
- Universitat de València (ES)
- University of Pittsburgh (US)
- University of Maryland, Baltimore (US)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2013-06-10
- Volume
- 123
- Issue
- 7
- Pages
- 2921-2934
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3696551
- OpenAlex
- W2005002977
- Cited by
- 333
- References
- 59
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 21 · 2023: 17 · 2022: 33 · 2021: 32 · 2020: 31 · 2019: 31 · 2018: 24 · 2017: 28 · 2016: 33 · 2015: 24 · 2014: 28 · 2013: 8 · 2012: 1
- FWCI
- 13.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Flight Attendant Medical Research Institute
- National Institutes of Health
- U.S. Public Health Service (122794, 163896, 141576, 166480, 140594)
- National Cancer Institute (R01CA166480, R01CA122794, R01CA140594, R01CA169919, R01CA140492, P01CA154303, P50CA058184, P30CA006973)
- National Institute of Environmental Health Sciences (P30ES003819)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- Nrf2, Keap1, miR-1, miR-206, microRNA regulation, pentose phosphate pathway, TCA cycle, glucose metabolism reprogramming, NADPH production, ribose synthesis, HDAC4, histone deacetylase, reactive oxygen species homeostasis, tumor growth, cancer metabolism, prognostic factors
- MeSH terms
- Animals, Base Sequence, Binding Sites, Carcinoma, Non-Small-Cell Lung, Cell Survival, Cell Transformation, Neoplastic, Citric Acid Cycle, Glucose, Humans, Lung Neoplasms, Mice, Nude, Neoplasm Transplantation, Oxidation-Reduction, Gene Expression Regulation, Neoplastic, Oligonucleotide Array Sequence Analysis, 3' Untranslated Regions, RNA Interference, MicroRNAs, Cell Line, Tumor, Tumor Burden, Cell Proliferation, NF-E2-Related Factor 2, Mice, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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