Cited by 710Cancer, Hypoxia, and MetabolismMetabolism, Diabetes, and CancerPI3K/AKT/mTOR signaling in cancer

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Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides

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Birsoy, Kıvanç, Possemato, Richard, Lorbeer, Franziska K., Bayraktar, Erol C., Thiru, Prathapan, Yucel, Burcu, Wang, Tim, Chen, Walter W., Clish, Clary B., Sabatini, David M.·2014·Nature

DOI 10.1038/nature13110PMC PMC4012432

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Abstract

As the concentrations of highly consumed nutrients, particularly glucose, are generally lower in tumours than in normal tissues, cancer cells must adapt their metabolism to the tumour microenvironment. A better understanding of these adaptations might reveal cancer cell liabilities that can be exploited for therapeutic benefit. Here we developed a continuous-flow culture apparatus (Nutrostat) for maintaining proliferating cells in low-nutrient media for long periods of time, and used it to undertake competitive proliferation assays on a pooled collection of barcoded cancer cell lines cultured in low-glucose conditions. Sensitivity to low glucose varies amongst cell lines, and an RNA interference (RNAi) screen pinpointed mitochondrial oxidative phosphorylation (OXPHOS) as the major pathway required for optimal proliferation in low glucose. We found that cell lines most sensitive to low glucose are defective in the OXPHOS upregulation that is normally caused by glucose limitation as a result of either mitochondrial DNA (mtDNA) mutations in complex I genes or impaired glucose utilization. These defects predict sensitivity to biguanides, antidiabetic drugs that inhibit OXPHOS, when cancer cells are grown in low glucose or as tumour xenografts. Notably, the biguanide sensitivity of cancer cells with mtDNA mutations was reversed by ectopic expression of yeast NDI1, a ubiquinone oxidoreductase that allows bypass of complex I function. Thus, we conclude that mtDNA mutations and impaired glucose utilization are potential biomarkers for identifying tumours with increased sensitivity to OXPHOS inhibitors.

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Authors: Birsoy, K., Possemato, R., Lorbeer, F. K., Bayraktar, E. C., Thiru, P., Yucel, B., Wang, T., Chen, W. W., Clish, C. B., & Sabatini, D. M.
Affiliations: Broad Institute (US)
Whitehead Institute for Biomedical Research (US)
Corresponding author: Sabatini, David M.
ORCID: Birsoy, Kıvanç
Possemato, Richard
Lorbeer, Franziska K.
Bayraktar, Erol C.
Thiru, Prathapan
Chen, Walter W.
Clish, Clary B.
Sabatini, David M.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2014-03-16
Volume: 508
Issue: 7494
Pages: 108-112
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature13110
PMC: PMC4012432
OpenAlex: W2104696999
Cited by: 710
References: 27
Citations by year: 2026: 17 · 2025: 44 · 2024: 58 · 2023: 46 · 2022: 60 · 2021: 75 · 2020: 83 · 2019: 71 · 2018: 51 · 2017: 49 · 2016: 61 · 2015: 59 · 2014: 35
FWCI: 21.80
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
National Cancer Institute (CA129105, K99CA168940, CA103866, R01CA103866, R01CA129105, R00CA168940)
National Institute of General Medical Sciences (T32GM007287)
National Institute of Allergy and Infectious Diseases (AI-07389, T32AI007389)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK043351)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
Keywords: glucose limitation, biguanides, mitochondrial oxidative phosphorylation, cancer metabolism, mitochondrial DNA mutations, complex I, antidiabetic drugs, OXPHOS inhibitors, continuous flow culture, tumor microenvironment, NDI1, glucose utilization, cancer cell lines, drug sensitivity biomarkers
MeSH terms: Adenosine Triphosphate, Animals, Biguanides, Culture Media, DNA, Mitochondrial, Glucose, Humans, Hypoglycemic Agents, Male, Mitochondria, Mutation, Neoplasm Transplantation, Neoplasms, Oxidative Phosphorylation, Phenformin, Cell Culture Techniques, Xenograft Model Antitumor Assays, Saccharomyces cerevisiae Proteins, RNA Interference, Electron Transport Complex I, Cell Line, Tumor, Cell Proliferation, Mice, Molecular Typing

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Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides

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