Hypoxia induces a lipogenic cancer cell phenotype via HIF1α-dependent and -independent pathways
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// Alessandro Valli 1,2,7 , Miguel Rodriguez 3,4 , Loukas Moutsianas 5 , Roman Fischer 2 , Vita Fedele 2 , Hong-Lei Huang 2 , Ruud Van Stiphout 1 , Dylan Jones 1 , Michael Mccarthy 2 , Maria Vinaxia 3,4 , Kaori Igarashi 6 , Maya Sato 6 , Tomoyoshi Soga 6 , Francesca Buffa 1 , James Mccullagh 7 , Oscar Yanes 3,4 , Adrian Harris 1,* and Benedikt Kessler 2,* 1 Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK 2 Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK 3 Centre for Omic Sciences, Rovira i Virgili University, Reus, Spain 4 Biomedical Research Centre in Diabetes and Associated Metabolic Disorders, Madrid, Spain 5 The Wellcome Trust Centre for Human Genetics, Nuffield Department of Medicine, Oxford, UK 6 Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, Japan 7 Mass Spectrometry Research Facility CRL, Department of Chemistry, University of Oxford, Oxford, UK * equal senior authors Correspondence: Alessandro Valli, email: // Keywords : cancer metabolism, fatty acids, HIF1α, HIF2α, hypoxia, Kennedy pathway, lipidomics, PAF Received : June 01, 2014 Accepted : December 10, 2014 Published : December 11, 2014 Abstract The biochemistry of cancer cells diverges significantly from normal cells as a result of a comprehensive reprogramming of metabolic pathways. A major factor influencing cancer metabolism is hypoxia, which is mediated by HIF1α and HIF2α. HIF1α represents one of the principal regulators of metabolism and energetic balance in cancer cells through its regulation of glycolysis, glycogen synthesis, Krebs cycle and the pentose phosphate shunt. However, less is known about the role of HIF1α in modulating lipid metabolism. Lipids serve cancer cells to provide molecules acting as oncogenic signals, energetic reserve, precursors for new membrane synthesis and to balance redox biological reactions. To study the role of HIF1α in these processes, we used HCT116 colorectal cancer cells expressing endogenous HIF1α and cells in which the hif1α gene was deleted to characterize HIF1α-dependent and independent effects on hypoxia regulated lipid metabolites. Untargeted metabolomics integrated with proteomics revealed that hypoxia induced many changes in lipids metabolites. Enzymatic steps in fatty acid synthesis and the Kennedy pathway were modified in a HIF1α-dependent fashion. Palmitate, stearate, PLD3 and PAFC16 were regulated in a HIF-independent manner. Our results demonstrate the impact of hypoxia on lipid metabolites, of which a distinct subset is regulated by HIF1α.
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The HIF-1α-independent metabolic signature involved HIF-2α upregulation in association with impaired fatty acid β-oxidation, increased cellular lipid storage, and increased cell proliferation; palmitate and stearate accumulated in a HIF-1α-independent manner.
“This HIF-1α-independent metabolic signature involved HIF-2α upregulation in association with impaired fatty acid (FA) β-oxidation, increased cellular lipid storage, and increased cell proliferation, while palmitate and stearate were observed to accumulate in a HIF-1α-independent manner [96].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [96]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredAccumulation of fatty acids provides metabolic precursors for β-oxidation in proliferating cells recovering after re-oxygenation, and fatty acids can act as a free radical buffer via lipid peroxidation.
“Accumulation of fatty acids provides metabolic precursors for β-oxidation in proliferating cells recovering after re-oxygenation, and fatty acids can also act as a free radical buffer via lipid peroxidation [96].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [96]
The Results section, “Hypoxic profile of fatty acids” (page not supplied), reports fatty-acid accumulation under hypoxia. The Discussion mentions fatty-acid β-oxidation as a source of acetyl-CoA, but does not say the accumulated fatty acids fuel proliferating cells after re-oxygenation. The passages found also do not support free-radical buffering via lipid peroxidation. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe C-16 homolog of PAF accumulated in hypoxia in a HIF-1α-/HIF-2α-independent manner due to reduced PAFC16 catabolism from lowered levels of PLD3.
“The C-16 homolog of PAF was found to accumulate in hypoxia in a HIF-1α-/HIF-2α-independent manner due to reduced PAFC16 catabolism from lowered levels of PLD3 [96].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [96]
The Results section reports PAFC16 accumulation under hypoxia in HIF1α- and HIF2α-deficient colorectal cancer cells. The Discussion reports reduced PLD3 protein levels, but does not establish that reduced PLD3 caused the accumulation; it instead suggests reduced PAFC16 catabolism may result from decreased activity of an oxygen-dependent monooxygenase. Page numbers are not provided in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredHypoxia induces changes in several lipid metabolites by both HIF-dependent and HIF-independent mechanisms.
“hypoxia was also found to induce changes in several lipid metabolites by both HIF-dependent and HIF-independent mechanisms [96].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [96]
Enzymatic steps in fatty acid synthesis and the Kennedy pathway were altered in a HIF-1α-dependent manner, whereas palmitate, stearate, PLD3, and PAFC16 were regulated in a HIF-1α-independent manner.
“Enzymatic steps in fatty acid synthesis and the Kennedy pathway were altered in a HIF-1α-dependent manner, whereas palmitate, stearate, phospholipase D3 (PLD3), and platelet-activating factor homologous C16 (PAFC16) were regulated in a HIF-1α-independent manner [96].”
From HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells (2021) · cites this paper as [96]
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- Authors
- Valli, A., Rodriguez, M., Moutsianas, L., Fischer, R., Fedele, V., Huang, H.-L., Van Stiphout, R., Jones, D., Mccarthy, M., Vinaxia, M., Igarashi, K., Sato, M., Soga, T., Buffa, F., Mccullagh, J., Yanes, O., Harris, A., & Kessler, B.
- Affiliations
- University of Oxford (GB)
- Centre for Omic Sciences (ES)
- Centre for Human Genetics (GB)
- Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK
- Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK
- Institute for Advanced Biosciences, Keio University (JP)
- Centre for Omic Sciences, Rovira i Virgili University, Reus, Spain
- Corresponding author
- Harris, Adrian
- Kessler, Benedikt
- ORCID
- Venue
- Oncotarget
- Publisher
- Impact Journals, LLC
- Published
- 2014-12-11
- Volume
- 6
- Issue
- 4
- Pages
- 1920-1941
- ISSN
- 1949-2553 (ISSN-L)
- PMC
- PMC4385826
- OpenAlex
- W1884217239
- Cited by
- 79
- References
- 79
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 4 · 2023: 4 · 2022: 8 · 2021: 10 · 2020: 10 · 2019: 8 · 2018: 10 · 2017: 6 · 2016: 6 · 2015: 3
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- cc-by
- Locations
- Oncotarget (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio istituzionale della Ricerca - Bocconi (submittedVersion)
- Funders
- Cancer Research UK (11359, 16466, 18974)
- National Institute for Health and Care Research (NF-SI-0611-10163)
- University of Oxford
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- HIF-1α, HIF-2α, lipogenesis, lipid metabolism, Kennedy pathway, fatty acid synthesis, lipidomics, PAF, colorectal cancer, HCT116 cells, cancer metabolism, tumor microenvironment
- MeSH terms
- Endothelial PAS Domain-Containing Protein 1, Acetyl-CoA C-Acyltransferase, Acetyl-CoA Carboxylase, Aged, Fatty Acids, Female, Humans, Lipids, Male, Middle Aged, Platelet Activating Factor, Blotting, Western, Colorectal Neoplasms, Signal Transduction, Cell Hypoxia, Genomics, RNA Interference, Proteomics, HCT116 Cells, Cell Line, Tumor, Lipid Metabolism, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit, Metabolomics
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