The DOI matches its Crossref record; 252 of the 256 references it cites were found in a registry or an index.
Hypoxia-inducible factors promote breast cancer stem cell specification and maintenance in response to hypoxia or cytotoxic chemotherapy
Abstract
Clinical studies have revealed that breast cancers contain regions of intratumoral hypoxia (reduced oxygen availability), which activates hypoxia-inducible factors (HIFs). The relationship between intratumoral hypoxia, distant metastasis and cancer mortality has been well established. A major mechanism by which intratumoral hypoxia contributes to disease progression is through induction of the breast cancer stem cell (BCSC) phenotype. BCSCs are a small subpopulation of cells with the capability for self-renewal. BCSCs have been implicated in resistance to chemotherapy, disease recurrence, and metastasis. In this review, we will discuss our current understanding of the molecular mechanisms underlying HIF-dependent induction of the BCSC phenotype in response to hypoxia or chemotherapy.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Hypoxia-inducible factors (HIFs) play critical roles in cancer progression by activating the transcription of a large battery of genes encoding proteins that play key roles in angiogenesis, glucose metabolism, invasion/metastasis, stem cell specification, protumoral inflammatory responses, and tumor immune evasion (18, 23–27).”
From HIF inhibitor 32-134D eradicates murine hepatocellular carcinoma in combination with anti-PD1 therapy (2022) · cites this paper as [27]
Citations
Cites
3 retracted
Items 201–252 of 252
The role of MAP kinases and MAP kinase phosphatase-1 in resistance to breast cancer treatment
Haagenson, K. K., & Wu, G. S. (2010) · Cancer and Metastasis Reviews · doi:10.1007/s10555-010-9208-5 · Cited by 103
Quinlan, K. G. R., Nardini, M., Verger, A., Francescato, P., Yaswen, P., Corda, D., Bolognesi, M., & Crossley, M. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00680-06 · Cited by 102
Cowger, J. J. M., Zhao, Q., Isovic, M., & Torchia, J. (2006) · Oncogene · doi:10.1038/sj.onc.1210126 · Cited by 101
The hypoxic microenvironment upgrades stem-like properties of ovarian cancer cells
Liang, D., Ma, Y., Liu, J., Trope, C. G., Holm, R., Nesland, J. M., & Suo, Z. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-201 · Cited by 99
Zheng, G., Dahl, J. A., Niu, Y., Fu, Y., Klungland, A., Yang, Y., & He, C. (2013) · RNA Biology · doi:10.4161/rna.24711 · Cited by 98
Lu, H., Tran, T. M. L., Park, Y., Chen, I., Lan, J., Xie, Y., & Semenza, G. L. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0270 · Cited by 96
Self-citationDynamic regulation of stem cell specification and maintenance by hypoxia-inducible factors
Semenza, G. L. (2015) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2015.09.004 · Cited by 94
Self-citation2i Maintains a Naive Ground State in ESCs through Two Distinct Epigenetic Mechanisms
Sim, Y.-J., Kim, M.-S., Nayfeh, A., Yun, Y., Kim, S. J., Park, K.-T., Kim, C., & Kim, K.-S. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.04.001 · Cited by 92
Chanmee, T., Ontong, P., Mochizuki, N., Kongtawelert, P., Konno, K., & Itano, N. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.564120 · Cited by 90
Tang, B., Qi, G., Tang, F., Yuan, S., Wang, Z., Liang, X., Li, B., Yu, S., Liu, J., Huang, Q., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-3029 · Cited by 89
Littlepage, L. E., Adler, A. S., Kouros‐Mehr, H., Huang, G., Chou, J., Krig, S. R., Griffith, O. L., Korkola, J. E., Qu, K., Lawson, D. A., et al. (2012) · Cancer Discovery · doi:10.1158/2159-8290.cd-12-0093 · Cited by 88
HIF-1-Dependent Induction of Jumonji Domain-Containing Protein (JMJD) 3 under Hypoxic Conditions
Lee, H.-Y., Choi, K. Y., Oh, H., Park, Y.-K., & Park, H. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.2250 · Cited by 86
Cheloni, G., Tanturli, M., Tusa, I., DeSouza, N. H., Shan, Y., Gozzini, A., Mazurier, F., Rovida, E., Li, S., & Sbarba, P. D. (2017) · Blood · doi:10.1182/blood-2016-10-745588 · Cited by 84
REST is a hypoxia-responsive transcriptional repressor
Cavadas, M. A. S., Mesnieres, M., Crifò, B., Manresa, M. C., Selfridge, A. C., Keogh, C. E., Fábián, Z., Scholz, C. C., Nolan, K. A., Rocha, L. M. A., et al. (2016) · Scientific Reports · doi:10.1038/srep31355 · Cited by 81
Dysregulation of CD47 and the ligands thrombospondin 1 and 2 in multiple myeloma
Danielsen, J. M. R., Knudsen, L. M., Dahl, I. M. S., Lodahl, M., & Rasmussen, T. (2007) · British Journal of Haematology · doi:10.1111/j.1365-2141.2007.06729.x · Cited by 81
Post‐transcriptional regulation of the DUSP6/MKP‐3 phosphatase by MEK/ERK signaling and hypoxia
Bermúdez, O. M., Jouandin, P., Rottier, J., Bourcier, C., Pagès, G., & Gimond, C. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22339 · Cited by 79
Cancer stem cells and hypoxia-inducible factors (Review)
Tong, W., Tong, G., & Liu, Y. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4417 · Cited by 78
Effect of Disrupting Seven-in-Absentia Homolog 2 Function on Lung Cancer Cell Growth
Ahmed, A. U., Schmidt, R. L., Park, C. H., Reed, N. R., Hesse, S. E., Thomas, C. F., Molina, J. R., Deschamps, C. C., Yang, P., Aubry, M. C., et al. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn365 · Cited by 76
Cao, Y., Lin, S., Wang, Y., Chin, Y. E., Kang, L., & Mi, J. (2017) · Theranostics · doi:10.7150/thno.18992 · Cited by 76
CXCR4 receptor positive spheroid forming cells are responsible for tumor invasion in vitro
Krohn, A., Song, Y., Muehlberg, F. L., Droll, L. H., Beckmann, C., & Alt, E. (2009) · Cancer Letters · doi:10.1016/j.canlet.2009.02.005 · Cited by 75
HIF-1α and TAZ serve as reciprocal co-activators in human breast cancer cells
Xiang, L., Gilkes, D. M., Hu, H., Luo, W., Bullen, J. W., Liang, H., & Semenza, G. L. (2015) · Oncotarget · doi:10.18632/oncotarget.4190 · Cited by 73
Self-citationThe ZNF217 oncogene is a candidate organizer of repressive histone modifiers
Banck, M. S., Li, S., Nishio, H., Wang, C., Beutler, A. S., & Walsh, M. J. (2009) · Epigenetics · doi:10.4161/epi.4.2.7953 · Cited by 72
Krig, S. R., Miller, J. K., Frietze, S. E., Beckett, L. A., Neve, R. M., Farnham, P., Yaswen, P., & Sweeney, C. A. (2010) · Oncogene · doi:10.1038/onc.2010.289 · Cited by 71
Hypoxia-Induced Downregulation of DUSP-2 Phosphatase Drives Colon Cancer Stemness
Hou, P., Li, Y.-H., Lin, S., Lin, S.-C., Lee, J., Lin, B.-W., Liou, J., Chang, J., Kuo, C., Liu, Y.-M., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2990 · Cited by 71
HSP90 Inhibitor 17-AAG Selectively Eradicates Lymphoma Stem Cells
Newman, B. W., Liu, Y., Lee, H.-F., Sun, D., & Wang, Y. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3600 · Cited by 68
Desidero, T. D., Xu, P., Man, S., Bocci, G., & Kerbel, R. S. (2015) · Oncotarget · doi:10.18632/oncotarget.6377 · Cited by 66
Implications of Hypoxia in Breast Cancer Metastasis to Bone
Gilkes, D. M. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17101669 · Cited by 65
Bousquet, G., Bouchtaoui, M. E., Tan, S., Lebœuf, C., de BAZELAIRE, C., Ratajczak, P., Giacchetti, S., de Roquancourt, A., Bertheau, P., Verneuil, L., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.16925 · Cited by 64
Fan, H., & Guan, J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.200717 · Cited by 63
Metabolic Regulation of Redox Status in Stem Cells
Perales‐Clemente, E., Folmes, C. D. L., & Terzic, A. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6000 · Cited by 59
Interleukin‐6 contributes to chemoresistance in MDA‐MB‐231 cells via targeting HIF‐1α
Wang, K., Zhu, X., Zhang, K., Yin, Y., Chen, Y., & Zhang, T. (2018) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22039 · Cited by 59
Thillainadesan, G., Isovic, M., Loney, E. R., Andrews, J. D., Tini, M., & Torchia, J. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00246-08 · Cited by 57
The regulation of transcriptional repression in hypoxia
Cavadas, M. A. S., Cheong, A., & Taylor, C. T. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.02.024 · Cited by 55
Mao, X., Yan, M., Xue, X., Zhang, X., Ren, H.-G., Guo, G., Wang, P., Zhang, W., & Huo, J. (2011) · Laboratory Investigation · doi:10.1038/labinvest.2011.56 · Cited by 55
Zhou, X., & Lei, Q. (2016) · Protein & Cell · doi:10.1007/s13238-016-0288-z · Cited by 54
Histone methylase MLL1 coordinates with HIF and regulate lncRNA HOTAIR expression under hypoxia
Bhan, A., Deb, P., Shihabeddin, N., Ansari, K. I., Brotto, M., & Mandal, S. S. (2017) · Gene · doi:10.1016/j.gene.2017.07.069 · Cited by 54
Regulation of the breast cancer stem cell phenotype by hypoxia-inducible factors
Semenza, G. L. (2015) · Clinical Science · doi:10.1042/cs20150451 · Cited by 52
Self-citationKershaw, M. H., & Smyth, M. J. (2013) · Science · doi:10.1126/science.1241716 · Cited by 39
Cecil, D. L., Slota, M., O'Meara, M. M., Curtis, B. C., Gad, E. A., Dang, Y., Herendeen, D. R., Rastetter, L., & Disis, M. L. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1678 · Cited by 34
Nallanthighal, S., Elmaliki, K., & Reliene, R. (2017) · Nutrition and Cancer · doi:10.1080/01635581.2017.1359318 · Cited by 32
Hypoxamirs and Mitochondrial Metabolism
Cottrill, K. A., Chan, S. Y., & Loscalzo, J. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5641 · Cited by 27
Wong, N. K. Y., Fuller, M. E., Sung, S., Wong, F., & Karsan, A. (2012) · Cancer Medicine · doi:10.1002/cam4.18 · Cited by 27
Berghaus, L. J., Giguère, S., & Sturgill, T. L. (2014) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2014.03.010 · Cited by 27
Tomaz, R. A., Harman, J. J., Karimlou, D., Weavers, L., Fritsch, L., Bou-Kheir, T., Bell, E., del Valle, I., Niakan, K. K., Fisher, C. L., et al. (2017) · Development · doi:10.1242/dev.142489 · Cited by 23
Increased SIAH expression predicts ductal carcinoma in situ (DCIS) progression to invasive carcinoma
Behling, K. C., Tang, A., Freydin, B., Chervoneva, I., Kadakia, S., Schwartz, G. F., Rui, H., & Witkiewicz, A. K. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-1254-8 · Cited by 23
Cho, K. H., Yu, S., Cho, D. Y., Park, C. G., & Lee, H. Y. (2015) · BMC Cancer · doi:10.1186/s12885-015-1864-y · Cited by 23
Tanaka, T., Ikegami, Y., Nakazawa, H., Kuriyama, N., Oki, M., Hanai, J.-I., Sukhatme, V. P., & Kaneki, M. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25411 · Cited by 23
Guo, L., Zheng, P., Fan, H., Wang, H., Xu, W., & Zhou, W. (2017) · Bioscience Reports · doi:10.1042/bsr20171137 · Cited by 22
DeCastro, A., Cherukuri, P., Balboni, A., & DiRenzo, J. (2014) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-14-0194 · Cited by 20
Histone demethylase JMJD2C: epigenetic regulators in tumors
Zhang, C., Wang, Z., Ji, Q., & Li, Q. (2017) · Oncotarget · doi:10.18632/oncotarget.19176 · Cited by 13
Hypoxia mediated expression of stem cell markers in VHL-associated hemangioblastomas
Ponnaluri, V. K. C., Vavilala, D. T., Prakash, S., & Mukherji, M. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.07.028 · Cited by 10
Lu, H., Clauser, K. R., Tam, W. L., Fröse, J., Ye, X., Eaton, E. N., Reinhardt, F., Donnenberg, V. S., Bhargava, R., Carr, S. A., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3281 · Cited by 9
Flagged first, then by citations
4 of the 256 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Hypoxia-inducible factors: cancer progression and clinical translation
Wicks, E. E., & Semenza, G. L. (2022) · Journal of Clinical Investigation · doi:10.1172/jci159839 · Cited by 626
Self-citationHIFs, angiogenesis, and metabolism: Elusive enemies in breast cancer
de Heer, E. C., Jalving, M., & Harris, A. L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137552 · Cited by 372
Bai, R., Li, Y., Jian, L., Yue-hui, Y., Zhao, L., & Wei, M. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01645-2 · Cited by 296
The role of hypoxia‐inducible factor 1 in tumor immune evasion
Li, Y., Wu, W., Wang, X., Fang, L., Adam, V., Nepovimová, E., Wu, Q., & Kuča, K. (2020) · Medicinal Research Reviews · doi:10.1002/med.21771 · Cited by 276
Targeting Breast Cancer Stem Cells
Zhang, L., Chen, W., Liu, S., & Chen, C. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.76187 · Cited by 196
Metadata
- Authors
- Xiang, L., & Semenza, G. L.
- Affiliations
- Sichuan University (CN)
- Johns Hopkins University (US)
- Corresponding author
- Gregg L. Semenza
- Venue
- Advances in Cancer Research
- Publisher
- Elsevier
- Published
- 2019
- Volume
- 141
- Pages
- 175-212
- ISSN
- 0065-230X (ISSN-L)
- OpenAlex
- W2904539422
- Cited by
- 71
- References
- 256
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 10 · 2023: 8 · 2022: 12 · 2021: 14 · 2020: 12 · 2019: 5
- FWCI
- 9.82
- Type
- book chapter
- Language
- en
- Open access
- closed
- Locations
- Advances in cancer research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- hypoxia-inducible factor, breast cancer stem cells, intratumoral hypoxia, chemoresistance, self-renewal, metastasis, recurrence, HIF signaling
- MeSH terms
- Animals, Breast Neoplasms, Female, Humans, Neoplastic Stem Cells, Cell Hypoxia, Cell Line, Tumor, Hypoxia-Inducible Factor 1, alpha Subunit
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review