Cited by 475Cancer, Hypoxia, and MetabolismMetabolism, Diabetes, and CancerAngiogenesis and VEGF in Cancer

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Regulation of cancer cell metabolism by hypoxia-inducible factor 1

Semenza, Gregg L.·2009·Seminars in Cancer Biology

DOI 10.1016/j.semcancer.2008.11.009

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Abstract

The induction of hypoxia-inducible factor 1 (HIF-1) activity, either as a result of intratumoral hypoxia or loss-of-function mutations in the VHL gene, leads to a dramatic reprogramming of cancer cell metabolism involving increased glucose transport into the cell, increased conversion of glucose to pyruvate, and a concomitant decrease in mitochondrial metabolism and mitochondrial mass. Blocking these adaptive metabolic responses to hypoxia leads to cell death due to toxic levels of reactive oxygen species. Targeting HIF-1 or metabolic enzymes encoded by HIF-1 target genes may represent a novel therapeutic approach to cancer.

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Woo, Y. M., Shin, Y., Lee, E. J., Lee, S., Jeong, S. H., Kong, H. K., Park, E. Y., Kim, H. K., Han, J., Chang, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132285 · Cited by 129
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Woolf, E. C., Curley, K. L., Liu, Q., Turner, G. H., Charlton, J. A., Preul, M. C., & Scheck, A. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130357 · Cited by 122
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Wahl, D. R., Byersdorfer, C. A., Ferrara, J. L. M., Opipari, A. W., & Glick, G. D. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01148.x · Cited by 125
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Menard, J. A., Christianson, H. C., Kucharzewska, P., Bourseau-Guilmain, E., Svensson, K. J., Lindqvist, E., Chandran, V. I., Kjellén, L., Welinder, C., Bengzon, J., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-2831 · Cited by 110
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Liu, X., Chen, Z., Xu, C., Leng, X., Cao, H., Ouyang, G., & Xiao, W. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv379 · Cited by 112
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Authors: Semenza, G. L.
Affiliations: Johns Hopkins University (US)
Corresponding author: Semenza, Gregg L.
ORCID: Semenza, Gregg L.
Venue: Seminars in Cancer Biology
Publisher: Elsevier BV
Published: 2009-02
Volume: 19
Issue: 1
Pages: 12-16
ISSN: 1044-579X (ISSN-L)
DOI: 10.1016/j.semcancer.2008.11.009
OpenAlex: W2102416115
Cited by: 469
References: 67
Citations by year: 2026: 14 · 2025: 11 · 2024: 15 · 2023: 19 · 2022: 14 · 2021: 28 · 2020: 21 · 2019: 21 · 2018: 22 · 2017: 29 · 2016: 36 · 2015: 32 · 2014: 33 · 2013: 35 · 2012: 35
FWCI: 2.46
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Seminars in Cancer Biology (publishedVersion)
PubMed (publishedVersion)
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 › Angiogenesis and VEGF in Cancer
Keywords: HIF-1, cancer metabolism, tumor hypoxia, VHL gene, glucose transport, glycolysis, mitochondrial metabolism, reactive oxygen species, HIF-1 target genes, metabolic reprogramming, cancer therapy
MeSH terms: Animals, Glycolysis, Humans, Neoplasms, Cell Hypoxia, Gene Expression Regulation, Neoplastic, Reactive Oxygen Species, Hypoxia-Inducible Factor 1, Von Hippel-Lindau Tumor Suppressor Protein, Metabolic Networks and Pathways

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Regulation of cancer cell metabolism by hypoxia-inducible factor 1

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