Cited by 797Ferroptosis and cancer prognosisCancer, Hypoxia, and MetabolismIron Metabolism and Disorders

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NFS1 undergoes positive selection in lung tumours and protects cells from ferroptosis

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Alvarez, Samantha W., Sviderskiy, Vladislav O., Terzi, Erdem M., Papagiannakopoulos, Thales, Moreira, Andre L., Adams, Sylvia, Sabatini, David M., Birsoy, Kıvanç, Possemato, Richard·2017·Nature

DOI 10.1038/nature24637PMC PMC5808442

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Abstract

Environmental nutrient levels impact cancer cell metabolism, resulting in context-dependent gene essentiality. Here, using loss-of-function screening based on RNA interference, we show that environmental oxygen levels are a major driver of differential essentiality between in vitro model systems and in vivo tumours. Above the 3-8% oxygen concentration typical of most tissues, we find that cancer cells depend on high levels of the iron-sulfur cluster biosynthetic enzyme NFS1. Mammary or subcutaneous tumours grow despite suppression of NFS1, whereas metastatic or primary lung tumours do not. Consistent with a role in surviving the high oxygen environment of incipient lung tumours, NFS1 lies in a region of genomic amplification present in lung adenocarcinoma and is most highly expressed in well-differentiated adenocarcinomas. NFS1 activity is particularly important for maintaining the iron-sulfur co-factors present in multiple cell-essential proteins upon exposure to oxygen compared to other forms of oxidative damage. Furthermore, insufficient iron-sulfur cluster maintenance robustly activates the iron-starvation response and, in combination with inhibition of glutathione biosynthesis, triggers ferroptosis, a non-apoptotic form of cell death. Suppression of NFS1 cooperates with inhibition of cysteine transport to trigger ferroptosis in vitro and slow tumour growth. Therefore, lung adenocarcinomas select for expression of a pathway that confers resistance to high oxygen tension and protects cells from undergoing ferroptosis in response to oxidative damage.

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Authors: Alvarez, S. W., Sviderskiy, V. O., Terzi, E. M., Papagiannakopoulos, T., Moreira, A. L., Adams, S., Sabatini, D. M., Birsoy, K., & Possemato, R.
Affiliations: NYU Langone’s Laura and Isaac Perlmutter Cancer Center (US)
Broad Institute (US)
Corresponding author: Sabatini, David M.
Birsoy, Kıvanç
Possemato, Richard
ORCID: Sviderskiy, Vladislav O.
Terzi, Erdem M.
Papagiannakopoulos, Thales
Moreira, Andre L.
Adams, Sylvia
Sabatini, David M.
Birsoy, Kıvanç
Possemato, Richard
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2017-11-22
Volume: 551
Issue: 7682
Pages: 639-643
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature24637
PMC: PMC5808442
OpenAlex: W2770709665
Cited by: 787
References: 34
Citations by year: 2026: 63 · 2025: 90 · 2024: 116 · 2023: 105 · 2022: 138 · 2021: 148 · 2020: 57 · 2019: 46 · 2018: 20 · 2017: 2
FWCI: 28.28
Type: journal article
Language: en
Update notices: correction (2022-09-14)
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
PMC
Funders: Leukemia and Lymphoma Society
Broad Institute
Agios Pharmaceuticals
Scheme for Promotion of Academic and Research Collaboration
National Institutes of Health (1s10od018338-01, 1s10od010584-01a1, 1s10od016304-01, CA129105, CA168940)
National Cancer Institute (K99CA168940, R01CA103866, K22CA193660, R01CA129105, R00CA168940, P30CA016087)
National Institute of General Medical Sciences (T32GM007308, T32GM115313)
National Institute of Allergy and Infectious Diseases (T32AI007389, R37AI047389)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Ferroptosis and cancer prognosis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords: NFS1, iron-sulfur cluster assembly, ferroptosis, lung adenocarcinoma, tumor hypoxia, high oxygen tension, oxidative damage, iron starvation response, glutathione synthesis, cysteine transport, gene amplification, tumour metastasis, cancer metabolism
MeSH terms: Animals, Carcinoma, Non-Small-Cell Lung, Cysteine, Glutathione, Humans, Iron-Sulfur Proteins, Lung Neoplasms, Neoplasm Metastasis, Oxygen, Carbon-Sulfur Lyases, Cell Death, Oxidative Stress, RNA Interference, Cell Line, Tumor, Mice

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NFS1 undergoes positive selection in lung tumours and protects cells from ferroptosis

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