Cited by 278Cancer, Hypoxia, and MetabolismMechanisms of cancer metastasisAngiogenesis and VEGF in Cancer

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Role of Hypoxia-Inducible Factors in Breast Cancer Metastasis

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Gilkes, Daniele M, Semenza, Gregg L·2013·Future Oncology

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Abstract

Human breast tumors contain regions of hypoxia in which cells that are located far from a functional blood vessel have significantly reduced oxygen concentrations when compared with normal mammary tissue. Breast cancer cells adapt to hypoxic conditions by increasing levels of hypoxia-inducible factors (HIFs), which induce the expression of multiple genes involved in angiogenesis, glucose utilization, resistance to oxidative stress, cell proliferation, resistance to apoptosis, invasion and metastasis. Breast cancer patients with increased HIF expression levels in primary tumor biopsies are at increased risk of metastasis. This is an important finding since 90% of breast cancer deaths are the result of metastasis, primarily to the bone, lungs, liver, brain and regional lymph nodes. Although the prognostic significance of reduced oxygen levels in primary breast tumors of cancer patients is well recognized, the mechanisms underlying hypoxia-induced, HIF-dependent breast cancer metastasis are just beginning to be uncovered. Recent studies have implicated HIF target genes in every step of the metastatic process. Drugs, such as digoxin, show the potential therapeutic effects of blocking HIF activity by decreasing primary tumor growth, vascularization, invasion and metastasis in animal models of breast cancer.

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7 retracted

Lysyl oxidase is essential for hypoxia-induced metastasis
Erler, J. T., Bennewith, K. L., Nicolau, M., Dornhöfer, N., Kong, C., Le, Q.-T., Chi, J.-T. A., Jeffrey, S. S., & Giaccia, A. J. (2006) · Nature · doi:10.1038/nature04695 · Cited by 1,309
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Hypoxia-inducible Factor 1 (HIF-1) Promotes Extracellular Matrix Remodeling under Hypoxic Conditions by Inducing P4HA1, P4HA2, and PLOD2 Expression in Fibroblasts
Gilkes, D. M., Bajpai, S. K., Chaturvedi, P., Wirtz, D., & Semenza, G. L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.442939 · Cited by 473
Self-citation
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RETRACTED: Acriflavine inhibits HIF-1 dimerization, tumor growth, and vascularization
Lee, K., Zhang, H., Qian, D. Z., Rey, S., Liu, J. O., & Semenza, G. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909353106 · Cited by 451
Self-citation
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RETRACTED ARTICLE: HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs
Zhang, H., Wong, C. C. L., Wei, H., Gilkes, D. M., Korangath, P., Chaturvedi, P., Schito, L., Chen, J., Krishnamachary, B., Winnard, P. T., et al. (2012) · Oncogene · doi:10.1038/onc.2011.365 · Cited by 326
Self-citation
Retracted
RETRACTED: Collagen Prolyl Hydroxylases Are Essential for Breast Cancer Metastasis
Gilkes, D. M., Chaturvedi, P., Bajpai, S., Wong, C. C., Wei, H., Pitcairn, S., Hubbi, M. E., Wirtz, D., & Semenza, G. L. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3963 · Cited by 296
Self-citation
Retracted
RETRACTED: Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells
Lee, K., Qian, D. Z., Rey, S., Wei, H., Liu, J. O., & Semenza, G. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812801106 · Cited by 289
Self-citation
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Procollagen lysyl hydroxylase 2 is essential for hypoxia-induced breast cancer metastasis
Gilkes, D. M., Bajpai, S., Wong, C. C., Chaturvedi, P., Hubbi, M. E., Wirtz, D., & Semenza, G. L. (2013) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-12-0629 · Cited by 252
Self-citation
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Molecular portraits of human breast tumours
Perou, C., Sørlie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Rees, C. A., Pollack, J., Ross, D., Johnsen, H., Akslen, L., et al. (2000) · Nature · doi:10.1038/35021093 · Cited by 16,551
Comprehensive molecular portraits of human breast tumours
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11412 · Cited by 12,129
Targeting HIF-1 for cancer therapy
Semenza, G. L. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1187 · Cited by 6,717 · cited 2×
“Clinically, this is supported by the finding that patients with primary tumors that have high HIF-1a levels have a greater likelihood of developing metastatic relapse and a shorter survival time [122].”
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Additional file 5 of Differential effects of HIF2α antagonist and HIF2α silencing in renal cancer and sensitivity to repurposed drugs
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Additional file 2 of MicroRNA-18a regulates the metastatic properties of oral squamous cell carcinoma cells via HIF-1α expression
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Additional file 1 of Differential effects of HIF2α antagonist and HIF2α silencing in renal cancer and sensitivity to repurposed drugs
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Additional file 1 of MicroRNA-18a regulates the metastatic properties of oral squamous cell carcinoma cells via HIF-1α expression
Kim, S., PARK, S. K., Oh, J.-H., Lee, S. S., Lee, Y., & Choi, J. (2022) · Figshare · doi:10.6084/m9.figshare.20967819
Additional file 2 of Assessment of hypoxia and oxidative-related changes in a lung-derived brain metastasis model by [64Cu][Cu(ATSM)] PET and proteomic studies
Fantin, J., Toutain, J., Pérès, E. A., Bernay, B., Mehani, S. M., Hélaine, C., Bourgeois, M., Brunaud, C., Chazalviel, L., Pontin, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.24634575
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Labrousse, G. (2016) · theses.fr (ABES) · doi:10.70675/88a3d193z31f1z4a68z944bz3d7f7316b069
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Fantin, J. (2023) · theses.fr (ABES) · doi:10.70675/17c3d7d3zde37z4e93z9446zc690e62f8a7a
Hypoxia-correlated functional photoacoustic tomography enhances breast tumor detection
Tong, X., Liu, C. Z., Ku, G., Santos, S. D., Invernizzi, M., Yee, L. D., Lai, L. L., & Wang, L. V. (2026) · Photoacoustics · doi:10.1016/j.pacs.2026.100897
BindingDB Entry 50013546: Total synthesis and biological evaluation of 7-hydroxyneolamellarin A as hypoxia-inducible factor-1α inhibitor for cancer therapy.
BindingDB (2022) · UC San Diego · doi:10.7270/q2p55s73
BindingDB Entry 50007923: Discovery of Novel Aryl Carboxamide Derivatives as Hypoxia-Inducible Factor 1α Signaling Inhibitors with Potent Activities of Anticancer Metastasis.
BindingDB (2021) · UC San Diego · doi:10.7270/q2cn7778

Authors: Gilkes, D. M., & Semenza, G. L.
Affiliations: Johns Hopkins University (US)
ORCID: Gilkes, Daniele M
Semenza, Gregg L
Venue: Future Oncology
Publisher: Informa UK Limited
Published: 2013-10-24
Volume: 9
Issue: 11
Pages: 1623-1636
ISSN: 1479-6694 (ISSN-L)
1744-8301
DOI: 10.2217/fon.13.92
PMC: PMC4659402
OpenAlex: W2126797928
Cited by: 274
References: 126
Citations by year: 2026: 2 · 2025: 17 · 2024: 20 · 2023: 22 · 2022: 24 · 2021: 40 · 2020: 26 · 2019: 29 · 2018: 25 · 2017: 22 · 2016: 15 · 2015: 17 · 2014: 12 · 2013: 1
FWCI: 1.24
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Future Oncology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (U54-CA143868)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: hypoxia-inducible factor, breast cancer metastasis, tumor hypoxia, angiogenesis, glucose metabolism, oxidative stress resistance, apoptosis resistance, cell invasion, HIF target genes, prognostic factors, digoxin, HIF inhibitors, tumor vascularization
MeSH terms: Endothelial PAS Domain-Containing Protein 1, Animals, Antineoplastic Agents, Breast Neoplasms, Cell Movement, Cell Survival, Female, Humans, Lymphatic Metastasis, Neoplasm Invasiveness, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, Epithelial-Mesenchymal Transition, Tumor Microenvironment

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Role of Hypoxia-Inducible Factors in Breast Cancer Metastasis

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