Regional glutamine deficiency in tumours promotes dedifferentiation through inhibition of histone demethylation
Open accessAbstract
Poorly organized tumour vasculature often results in areas of limited nutrient supply and hypoxia. Despite our understanding of solid tumour responses to hypoxia, how nutrient deprivation regionally affects tumour growth and therapeutic response is poorly understood. Here, we show that the core region of solid tumours displayed glutamine deficiency compared with other amino acids. Low glutamine in tumour core regions led to dramatic histone hypermethylation due to decreased α-ketoglutarate levels, a key cofactor for the Jumonji-domain-containing histone demethylases. Using patient-derived (V600E)BRAF melanoma cells, we found that low-glutamine-induced histone hypermethylation resulted in cancer cell dedifferentiation and resistance to BRAF inhibitor treatment, which was largely mediated by methylation on H3K27, as knockdown of the H3K27-specific demethylase KDM6B and the methyltransferase EZH2 respectively reproduced and attenuated the low-glutamine effects in vitro and in vivo. Thus, intratumoral regional variation in the nutritional microenvironment contributes to tumour heterogeneity and therapeutic response.
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Severe glutamine deprivation in the core region of solid tumors leads to dramatic histone hypermethylation due to decreased α-KG levels and decreased activity of Jumonji domain-containing histone demethylases, resulting in cancer cell dedifferentiation and resistance to BRAF inhibitors.
“This severe glutamine deprivation leads to dramatic histone hypermethylation due to decreased α-KG levels subsequent to decreased activity of Jumonji domain-containing histone demethylases and results in cancer cell dedifferentiation and resistance to BRAF inhibitors103.”
From Glutamine reliance in cell metabolism (2020) · cites this paper as [103]
Solid tumors show glutamine-depleted cores, which promote histone hypermethylation, resulting in reduced expression of differentiation-related genes and cancer cell dedifferentiation.
“Furthermore, solid tumors, being metabolically heterogeneous, show glutamine‐depleted cores, which promote histone hypermethylation, resulting in the reduced expression of differentiation‐related genes and cancer cell dedifferentiation [238, 239].”
From Tumor microenvironment signaling and therapeutics in cancer progression (2023) · cites this paper as [238]
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- Authors
- Pan, M., Reid, M. A., Lowman, X. H., Kulkarni, R. P., Tran, T. Q., Liu, X., Yang, Y., Hernandez-Davies, J. E., Rosales, K. K., Li, H., Hugo, W., Song, C., Xu, X., Schones, D. E., Ann, D. K., Gradinaru, V., Lo, R. S., Locasale, J. W., & Kong, M.
- Affiliations
- City Of Hope National Medical Center (US)
- California Institute of Technology (US)
- Duke University (US)
- University of California, Los Angeles (US)
- University of California San Diego (US)
- Corresponding author
- Kong, Mei
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2016-09-12
- Volume
- 18
- Issue
- 10
- Pages
- 1090-1101
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC5536113
- OpenAlex
- W2520906756
- Cited by
- 368
- References
- 63
- Citations by year
- 2026: 24 · 2025: 26 · 2024: 41 · 2023: 53 · 2022: 42 · 2021: 48 · 2020: 47 · 2019: 36 · 2018: 28 · 2017: 19 · 2016: 3
- FWCI
- 11.93
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (KL2TR000122, KL2TR001882)
- National Cancer Institute (R00CA168997, R01CA183989, P30CA033572)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- glutamine deficiency, tumor hypoxia, tumor vasculature, histone demethylation, alpha-ketoglutarate, H3K27 methylation, KDM6B, EZH2, BRAF V600E melanoma, BRAF inhibitor resistance, tumor heterogeneity, tumor microenvironment
- MeSH terms
- Animals, Glutamine, Histones, Humans, Ketoglutaric Acids, Methylation, Methyltransferases, Neoplasms, DNA Methylation, Histone Demethylases
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