Cited by 425Phagocytosis and Immune RegulationCancer, Hypoxia, and MetabolismImmune cells in cancer

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HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells

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Zhang, Huimin, Lu, Haiquan, Xiang, Lisha, Bullen, John W., Zhang, Chuanzhao, Samanta, Debangshu, Gilkes, Daniele M., He, Jianjun, Semenza, Gregg L.·2015·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1520032112PMC PMC4653179

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Abstract

Increased expression of CD47 has been reported to enable cancer cells to evade phagocytosis by macrophages and to promote the cancer stem cell phenotype, but the molecular mechanisms regulating CD47 expression have not been determined. Here we report that hypoxia-inducible factor 1 (HIF-1) directly activates transcription of the CD47 gene in hypoxic breast cancer cells. Knockdown of HIF activity or CD47 expression increased the phagocytosis of breast cancer cells by bone marrow-derived macrophages. CD47 expression was increased in mammosphere cultures, which are enriched for cancer stem cells, and CD47 deficiency led to cancer stem cell depletion. Analysis of datasets derived from thousands of patients with breast cancer revealed that CD47 expression was correlated with HIF target gene expression and with patient mortality. Thus, CD47 expression contributes to the lethal breast cancer phenotype that is mediated by HIF-1.

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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
Retracted
RETRACTED: Hypoxia-inducible factors are required for chemotherapy resistance of breast cancer stem cells
Samanta, D., Gilkes, D. M., Chaturvedi, P., Xiang, L., & Semenza, G. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421438111 · Cited by 460
Self-citation
Retracted
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
Retracted
RETRACTED ARTICLE: HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs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
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
Retracted
RETRACTED: Hypoxia-inducible factors mediate coordinated RhoA-ROCK1 expression and signaling in breast cancer cells
Gilkes, D. M., Xiang, L., Lee, S. J., Chaturvedi, P., Hubbi, M. E., Wirtz, D., & Semenza, G. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321510111 · Cited by 184
Self-citation
Retracted
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989
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The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11412 · Cited by 12,129

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Additional file 8 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
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Additional file 3 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
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Additional file 7 of Mitophagy promotes sorafenib resistance through hypoxia-inducible ATAD3A dependent Axis
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Additional file 2 of Mitophagy promotes sorafenib resistance through hypoxia-inducible ATAD3A dependent Axis
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Additional file 3 of Decoding of the surfaceome and endocytome in primary glioblastoma cells identifies potential target antigens in the hypoxic tumor niche
de Oliveira, K. G., Bång-Rudenstam, A., Beyer, S., Boukredine, A., Hugo Talbot, A., Governa, V., Johansson, M. C., Månsson, A.-S., Forsberg‐Nilsson, K., Bengzon, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26685948
Additional file 1 of Decoding of the surfaceome and endocytome in primary glioblastoma cells identifies potential target antigens in the hypoxic tumor niche
de Oliveira, K. G., Bång-Rudenstam, A., Beyer, S., Boukredine, A., Hugo Talbot, A., Governa, V., Johansson, M. C., Månsson, A.-S., Forsberg‐Nilsson, K., Bengzon, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25302999
Additional file 3 of Prognostic stratification based on HIF-1α signaling for evaluating hypoxia status and immune landscape in hepatocellular carcinoma
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Additional file 6 of Mitophagy promotes sorafenib resistance through hypoxia-inducible ATAD3A dependent Axis
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Additional file 9 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
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Additional file 2 of Decoding of the surfaceome and endocytome in primary glioblastoma cells identifies potential target antigens in the hypoxic tumor niche
de Oliveira, K. G., Bång-Rudenstam, A., Beyer, S., Boukredine, A., Hugo Talbot, A., Governa, V., Johansson, M. C., Månsson, A.-S., Forsberg‐Nilsson, K., Bengzon, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25303153
Additional file 1 of Docosahexaenoic acid (DHA) impairs hypoxia-induced cellular and exosomal overexpression of immune-checkpoints and immunomodulatory molecules in different subtypes of breast cancer cells
Maralbashi, S., Aslan, C., Kahroba, H., Asadi, M., Soltani‐Zangbar, M. S., Haghnavaz, N., Jadidi, F., Salari, F., & Kazemi, T. (2024) · Figshare · doi:10.6084/m9.figshare.25341272
Additional file 5 of Mitophagy promotes sorafenib resistance through hypoxia-inducible ATAD3A dependent Axis
Wu, H., Wang, T., Liu, Y., Li, X., Xu, S., Wu, C., Zou, H., Cao, M., Jin, G., Lang, J., et al. (2020) · Figshare · doi:10.6084/m9.figshare.13339326
Additional file 2 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
Chen, X.-J., Guo, C.-H., Wang, Z.-C., Yang, Y., Pan, Y., Liang, J.-Y., Sun, M., Fan, L.-S., Liang, L., & Wang, W. (2024) · Figshare · doi:10.6084/m9.figshare.26662993
Additional file 10 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
Chen, X.-J., Guo, C.-H., Wang, Z.-C., Yang, Y., Pan, Y., Liang, J.-Y., Sun, M., Fan, L.-S., Liang, L., & Wang, W. (2024) · Figshare · doi:10.6084/m9.figshare.26663017
Additional file 4 of Mitophagy promotes sorafenib resistance through hypoxia-inducible ATAD3A dependent Axis
Wu, H., Wang, T., Liu, Y., Li, X., Xu, S., Wu, C., Zou, H., Cao, M., Jin, G., Lang, J., et al. (2020) · Figshare · doi:10.6084/m9.figshare.13339323
Additional file 4 of Hypoxia-induced ZEB1 promotes cervical cancer immune evasion by strengthening the CD47-SIRPα axis
Chen, X.-J., Guo, C.-H., Wang, Z.-C., Yang, Y., Pan, Y., Liang, J.-Y., Sun, M., Fan, L.-S., Liang, L., & Wang, W. (2024) · Figshare · doi:10.6084/m9.figshare.26662999

Authors: Zhang, H., Lu, H., Xiang, L., Bullen, J. W., Zhang, C., Samanta, D., Gilkes, D. M., He, J., & Semenza, G. L.
Affiliations: Johns Hopkins University (US)
First Affiliated Hospital of Xi'an Jiaotong University (CN)
ORCID: Zhang, Huimin
Lu, Haiquan
Xiang, Lisha
Zhang, Chuanzhao
Gilkes, Daniele M.
He, Jianjun
Semenza, Gregg L.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2015-10-28
Volume: 112
Issue: 45
Pages: E6215-23
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1520032112
PMC: PMC4653179
OpenAlex: W1853160207
Cited by: 420
References: 62
Citations by year: 2026: 22 · 2025: 33 · 2024: 62 · 2023: 46 · 2022: 57 · 2021: 48 · 2020: 52 · 2019: 29 · 2018: 31 · 2017: 17 · 2016: 21 · 2015: 1
FWCI: 11.48
Type: journal article
Language: en
Update notices: correction (2024-09-25)
Open access: bronze
doi.org
Licence: www.pnas.org/site/misc/userlicense.xhtml (vor, 183 d)
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: American Cancer Society (122437-RP-12-090-01-COUN)
U.S. Department of Defense (W81XWH-12-1-0464)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords: HIF-1, CD47, breast cancer, phagocytosis evasion, macrophages, cancer stem cells, hypoxia, transcriptional regulation, mammospheres, patient mortality, prognostic factors
MeSH terms: Analysis of Variance, Breast Neoplasms, Female, Humans, Luciferases, Phagocytosis, Neoplastic Stem Cells, Immunoblotting, Gene Expression Regulation, Neoplastic, DNA Primers, Tumor Escape, RNA, Small Interfering, Cell Line, Tumor, Chromatin Immunoprecipitation, Hypoxia-Inducible Factor 1, CD47 Antigen, Real-Time Polymerase Chain Reaction

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HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells

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