CD24 Is an Effector of HIF-1–Driven Primary Tumor Growth and Metastasis
Open accessPublished version of a preprint
Abstract
Hypoxia drives malignant progression in part by promoting accumulation of the oncogenic transcription factor hypoxia inducible factor–1α (HIF-1α) in tumor cells. Tumor aggressiveness also relates to elevation of the cancer stem cell–associated membrane protein CD24, which has been causally implicated in tumor formation and metastasis in experimental models. Here, we link these two elements by showing that hypoxia induces CD24 expression through a functional hypoxia responsive element in the CD24 promoter. HIF-1α overexpression induced CD24 mRNA and protein under normoxic conditions, with this effect traced to a recruitment of endogenous HIF-1α to the CD24 promoter. Short hairpin RNA–mediated attenuation of HIF-1α or CD24 expression reduced cancer cell survival in vitro and in vivo at the levels of primary and metastatic tumor growth. CD24 overexpression in HIF-1α–depleted cancer cells rescued this decrease, whereas HIF-1α overexpression in CD24-depleted cells did not. Analysis of clinical tumor specimens revealed a correlation between HIF-1α and CD24 levels and an association of their coexpression to decreased patient survival. Our results establish a mechanistic linkage between 2 critically important molecules in cancer, identifying CD24 as a critical HIF-1α transcriptional target and biologic effector, strengthening the rationale to target CD24 for cancer therapy. Cancer Res; 72(21); 5600–12. ©2012 AACR.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Hypoxia arises in many solid tumors, particularly in regions far from the tumor blood vessels.
“Hypoxia, a term used to describe the lack of oxygen, 12 arises in many solid tumors, particularly in regions that are far from the tumor blood vessels.13”
From Catalase-Integrated Hyaluronic Acid as Nanocarriers for Enhanced Photodynamic Therapy in Solid Tumor (2019) · cites this paper as [13]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Targeting HIF-1 for cancer therapy
Semenza, G. L. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1187 · Cited by 6,717 · see citing works
Wang, G. L., Jiang, B. H., Rue, E. A., & Semenza, G. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5510 · Cited by 6,212 · see citing works
Radical Cystectomy in the Treatment of Invasive Bladder Cancer: Long-Term Results in 1,054 Patients
Stein, J. P., Lieskovsky, G., Cote, R., Groshen, S. G., Feng, A., Boyd, S. D., Skinner, E. C., Bochner, B. H., Thangathurai, D., Mikhail, M., et al. (2001) · Journal of Clinical Oncology · doi:10.1200/jco.2001.19.3.666 · Cited by 3,527 · see citing works
MatInspector and beyond: promoter analysis based on transcription factor binding sites
Cartharius, K., Frech, K., Grote, K., Klocke, B., Haltmeier, M., Klingenhoff, A., Frisch, M., Bayerlein, M., & Werner, T. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti473 · Cited by 1,962 · see citing works
Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A., Kim, T.-Y., Huang, L. E., Pavletich, N., Chau, V., & Kaelin, W. G. (2000) · Nature Cell Biology · doi:10.1038/35017054 · Cited by 1,577 · see citing works
Hypoxia-Inducible Factors, Stem Cells, and Cancer
Keith, B., & Simon, M. C. (2007) · Cell · doi:10.1016/j.cell.2007.04.019 · Cited by 1,179 · see citing works
Integrative molecular concept modeling of prostate cancer progression
Tomlins, S. A., Mehra, R., Rhodes, D. R., Cao, X., Wang, L., Dhanasekaran, S. M., Sundaram, S. K., Wei, J. T., Rubin, M. A., Pienta, K. J., et al. (2006) · Nature Genetics · doi:10.1038/ng1935 · Cited by 909 · see citing works
Self-citationLee, T. K., Castilho, A., Cheung, V. C. H., Tang, K. H., Ma, S., & Ng, I. O. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.06.005 · Cited by 586 · see citing works
Hypoxic gene expression and metastasis
Le, Q., Denko, N. C., & Giaccia, A. J. (2004) · Cancer and Metastasis Reviews · doi:10.1023/b:canc.0000031768.89246.d7 · Cited by 466 · see citing works
Hypoxia-driven selection of the metastatic phenotype
Sullivan, R., & Graham, C. H. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9062-2 · Cited by 411 · see citing works
The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease
Giaccia, A. J., Simon, M. C., & Johnson, R. (2004) · Genes & Development · doi:10.1101/gad.1243304 · Cited by 380 · see citing works
Baumann, P., Cremers, N., Kroese, F., Orend, G., Chiquet-Ehrismann, R., Uede, T., Yagita, H., & Sleeman, J. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0619 · Cited by 346 · see citing works
Metastasis: a therapeutic target for cancer
Steeg, P. S., & Theodorescu, D. (2008) · Nature Clinical Practice Oncology · doi:10.1038/ncponc1066 · Cited by 330 · see citing works
Self-citationTumour Biological Aspects of CD24, A Mucin-Like Adhesion Molecule
Kristiansen, G., Sammar, M., & Altevogt, P. (2004) · Journal of Molecular Histology · doi:10.1023/b:hijo.0000032357.16261.c5 · Cited by 316 · see citing works
Self-citationHypoxia, gene expression, and metastasis
Chan, D. A., & Giaccia, A. J. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9063-1 · Cited by 276 · see citing works
CD24 Is Expressed in Ovarian Cancer and Is a New Independent Prognostic Marker of Patient Survival
Kristiansen, G., Denkert, C., Schlüns, K., Dahl, E., Pilarsky, C. P., & Hauptmann, S. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64398-2 · Cited by 261 · see citing works
Self-citationCell type-specific DNA methylation patterns in the human breast
Bloushtain-Qimron, N., Yao, J., Snyder, E. L., Shipitsin, M., Campbell, L. L., Mani, S. A., Hu, M., Chen, H., Ustyansky, V., Antosiewicz, J., et al. (2008) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0805206105 · Cited by 243 · see citing works
Increased expression of hypoxia inducible factor-1alpha in rat and human prostate cancer.
Zhong, H., Agani, F. H., Baccala, A. A., Laughner, E., Rioseco‐Camacho, N., Wb, I., Simons, J. W., & Semenza, G. L. (1998) · PubMed · Cited by 232 · see citing works
Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells.
Xu, L., & Fidler, I. J. (2000) · PubMed · Cited by 223 · see citing works
Theodoropoulos, V. (2004) · European Urology · doi:10.1016/j.eururo.2004.04.008 · Cited by 223 · see citing works
CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells
Schabath, H., Runz, S., Joumaa, S., & Altevogt, P. (2006) · Journal of Cell Science · doi:10.1242/jcs.02741 · Cited by 190 · see citing works
Sagiv, E., Starr, A., Rozovski, U., Khosravi, R., Altevogt, P., Wang, T. C., & Arber, N. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6463 · Cited by 163 · see citing works
Smith, S. C., Oxford, G., Wu, Z., Nitz, M. D., Conaway, M. R., Frierson, H. F., Hampton, G. M., & Theodorescu, D. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3855 · Cited by 147 · see citing works
Self-citationSuzuki, T., Kiyokawa, N., Taguchi, T., Sekino, T., Katagiri, Y. U., & Fujimoto, J. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.9.5567 · Cited by 146 · see citing works
RalA and RalB: Antagonistic Relatives in Cancer Cell Migration
Oxford, G., Owens, C. R., Titus, B. J., Foreman, T. L., Herlevsen, M. C., Smith, S. C., & Theodorescu, D. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-1957 · Cited by 139 · see citing works
Self-citationMolecular Concepts Analysis Links Tumors, Pathways, Mechanisms, and Drugs
Rhodes, D. R., Sundaram, S. K., Tomlins, S. A., Mahavisno, V., Kasper, N. M., Varambally, R., Barrette, T. R., Ghosh, D., Varambally, S., & Chinnaiyan, A. M. (2007) · Neoplasia · doi:10.1593/neo.07292 · Cited by 139 · see citing works
Self-citationThe CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells.
Friederichs, J., Zeller, Y., Hafezi‐Moghadam, A., Gröne, H., Ley, K. F., & Altevogt, P. (2000) · PubMed · Cited by 133 · see citing works
Hypoxia-induced elevation in interleukin-8 expression by human ovarian carcinoma cells.
Xu, L., Xie, K., Mukaida, N., Matsushima, K., & Fidler, I. J. (1999) · PubMed · Cited by 128 · see citing works
Scheurer, S. B., Raybak, J. N., Roesli, C., Neri, D., & Elia, G. (2004) · PROTEOMICS · doi:10.1002/pmic.200300689 · Cited by 120 · see citing works
Tumor Hypoxia and Gene Expression: Implications for Malignant Progression and Therapy
Sutherland, R. M. (1998) · Acta Oncologica · doi:10.1080/028418698430278 · Cited by 119 · see citing works
Overdevest, J. B., Thomas, S., Kristiansen, G., Hansel, D. E., Smith, S. C., & Theodorescu, D. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0519 · Cited by 119 · see citing works
Self-citationRepressor roles for TCF-4 and Sfrp1 in Wnt signaling in breast cancer
Shulewitz, M. J., Soloviev, I., Wu, T., Koeppen, H., Polakis, P. G., & Sakanaka, C. (2006) · Oncogene · doi:10.1038/sj.onc.1209470 · Cited by 111 · see citing works
Chaudary, N., & Hill, R. P. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2971 · Cited by 105 · see citing works
Profiling the Evolution of Human Metastatic Bladder Cancer
Nicholson, B. E., Frierson, H. F., Conaway, M. R., Seraj, J., Harding, M. A., Hampton, G. M., & Theodorescu, D. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0826 · Cited by 86 · see citing works
Self-citationExpression of Ral GTPases, Their Effectors, and Activators in Human Bladder Cancer
Smith, S. C., Oxford, G., Baras, A. S., Owens, C. R., Havaleshko, D. M., Brautigan, D. L., Safo, M. K., & Theodorescu, D. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2419 · Cited by 82 · see citing works
Self-citationSrc phosphorylation of RhoGDI2 regulates its metastasis suppressor function
Wu, Y., Moissoglu, K., Wang, H., Wang, X., Frierson, H. F., Schwartz, M. A., & Theodorescu, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810094106 · Cited by 80 · see citing works
Self-citationMolecular markers of prostate cancer
Bradford, T. J., Tomlins, S. A., Wang, X., & Chinnaiyan, A. M. (2006) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2006.07.004 · Cited by 79 · see citing works
Self-citationNectadrin, the heat-stable antigen, is a cell adhesion molecule.
Kadmon, G., Eckert, M., Sammar, M., Schachner, M., & Altevogt, P. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.118.5.1245 · Cited by 75 · see citing works
CD24‐dependent MAPK pathway activation is required for colorectal cancer cell proliferation
Wang, W., Wang, X., Peng, L., Deng, Q., Liang, Y., Qing, H., & Jiang, B. (2009) · Cancer Science · doi:10.1111/j.1349-7006.2009.01370.x · Cited by 73 · see citing works
Kristiansen, G., Machado, E., Bretz, N. P., Rupp, C., Winzer, K., König, A.-K., Moldenhauer, G., Marmé, F., Costa, J., & Altevogt, P. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.70 · Cited by 73 · see citing works
Self-citationRalBP1 is necessary for metastasis of human cancer cell lines
Wu, Z., Owens, C., Chandra, N., Popovic, K., Conaway, M., & Theodorescu, D. (2010) · Neoplasia · doi:10.1593/neo.101080 · Cited by 70 · see citing works
Self-citationWu, Y., McRoberts, K., Berr, S. S., Frierson, H. F., Conaway, M. R., & Theodorescu, D. (2006) · Oncogene · doi:10.1038/sj.onc.1209835 · Cited by 69 · see citing works
Self-citationUp-Regulation of Estrogen Responsive Genes in Hypospadias: Microarray Analysis
Wang, Z., Liu, B. C., Lin, G. T., Lin, C., Lue, T. F., Willingham, E. J., & Baskin, L. S. (2007) · The Journal of Urology · doi:10.1016/j.juro.2007.01.014 · Cited by 65 · see citing works
Estrogen‐mediated downregulation of CD24 in breast cancer cells
Kaipparettu, B. A., Malik, S., Konduri, S. D., Liu, W., Rokavec, M., van der Kuip, H., Hoppe, R., Hammerich‐Hille, S., Fritz, P., Schroth, W., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23480 · Cited by 55 · see citing works
Pre-B Cell Antigen Receptor-Mediated Signal Inhibits CD24-Induced Apoptosis in Human Pre-B Cells
Taguchi, T., Kiyokawa, N., Mimori, K., Suzuki, T., Sekino, T., Nakajima, H., Saito, M., Katagiri, Y. U., Matsuo, N., Matsuo, Y., et al. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.1.252 · Cited by 51 · see citing works
INFLUENCE OF HYPOXIA AND HYPOXIA-REOXYGENATION ON ENDOTHELIAL P-SELECTIN EXPRESSION
Closse, C., Seigneur, M., Renard, M., Pruvost, A., Dumain, P., Belloc, F., & Boisseau, M. (1997) · Thrombosis Research · doi:10.1016/s0049-3848(96)00233-2 · Cited by 50 · see citing works
Solomon, B., Binns, D., Roselt, P. D., Weibe, L. I., McArthur, G. A., Cullinane, C. M., & Hicks, R. J. (2005) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-05-0066 · Cited by 50 · see citing works
Tickoo, S. K., Milowsky, M. I., Dhar, N., Dudas, M. E., Gallagher, D. J., Al‐Ahmadie, H. A., Gopalan, A., Fine, S. W., Ishill, N. M., Bajorin, D. F., et al. (2010) · British Journal of Urology · doi:10.1111/j.1464-410x.2010.09517.x · Cited by 47 · see citing works
Target gene identification from expression array data by promoter analysis
Werner, T. (2001) · Biomolecular Engineering · doi:10.1016/s1389-0344(00)00071-x · Cited by 47 · see citing works
Smith, S. C., Baras, A. S., Owens, C. R., Dancik, G. M., & Theodorescu, D. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3966 · Cited by 41 · see citing works
Self-citationInvasion and Metastasis Models for Studying RhoGDI2 in Bladder Cancer
Nitz, M. D., Harding, M. A., & Theodorescu, D. (2008) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(07)00417-x · Cited by 27 · see citing works
Self-citationOxford, G., Smith, S. C., Hampton, G. M., & Theodorescu, D. (2007) · Oncogene · doi:10.1038/sj.onc.1210521 · Cited by 27 · see citing works
Self-citationInfluence Of Hypoxia And Hypoxia-Reoxygenation On Endothelial P-Selectin Expression
le Closse, C. E., Seigneur, M., Renard, M., Pruvost, A., Dumain, P., Belloc, F., & Boisseau, M. (2009) · Haemostasis · doi:10.1159/000217296 · Cited by 24 · see citing works
Partial pulmonary embolization disrupts alveolarization in fetal sheep
Filby, C. E., Hooper, S. B., & Wallace, M. J. (2010) · Respiratory Research · doi:10.1186/1465-9921-11-42 · Cited by 12 · see citing works
Flagged first, then by citations
2 of the 56 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Chen, H., Tian, J., He, W., & Guo, Z. (2015) · Journal of the American Chemical Society · doi:10.1021/ja511420n · Cited by 817 · see citing works
Recent Advances in Tumor Targeting via EPR Effect for Cancer Treatment
Subhan, M. A., Yalamarty, S. S. K., Filipczak, N., Parveen, F., & Torchilin, V. P. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11060571 · Cited by 623 · see citing works
Hypoxia-inducible factors: master regulators of hypoxic tumor immune escape
Wu, Q., Li, Y., Nepovimová, E., Heger, Z., Wu, W., Kuča, K., & Adam, V. (2022) · Journal of Hematology & Oncology · doi:10.1186/s13045-022-01292-6 · Cited by 494 · see citing works
Catalase-Integrated Hyaluronic Acid as Nanocarriers for Enhanced Photodynamic Therapy in Solid Tumor
Phua, S. Z. F., Yang, G., Lim, W. Q., Verma, A., Chen, H., Thanabalu, T., & Zhao, Y. (2019) · ACS Nano · doi:10.1021/acsnano.9b01087 · Cited by 375 · see citing works
Cheng, H. B., Zhu, J., Li, S., Zeng, J., Lei, Q., Chen, K., Zhang, C., & Zhang, X. (2016) · Advanced Functional Materials · doi:10.1002/adfm.201603212 · Cited by 335 · see citing works
Emerging phagocytosis checkpoints in cancer immunotherapy
Liu, Y., Wang, Y., Yang, Y., Weng, L., Wu, Q., Zhang, J., Zhao, P., Fang, L., Shi, Y., & Wang, P. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01365-z · Cited by 287 · see citing works
Role of hypoxia-inducible factors in breast cancer metastasis
Gilkes, D. M., & Semenza, G. L. (2013) · Future Oncology · doi:10.2217/fon.13.92 · Cited by 274 · see citing works
Wei, J., Li, J., Sun, D., Li, Q., Ma, J., Chen, X., Zhu, X., & Zheng, N. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201706310 · Cited by 270 · see citing works
Liu, C., Wu, T., Liu, C., Chen, K., Chen, Y., Chen, G.-S., & Lin, S. (2017) · Small · doi:10.1002/smll.201700278 · Cited by 254 · see citing works
Novel insights into the function of CD24 : A driving force in cancer
Altevogt, P., Sammar, M., Hüser, L., & Kristiansen, G. (2020) · International Journal of Cancer · doi:10.1002/ijc.33249 · Cited by 215 · see citing works
Self-citationCui, C., Wong, C. C., Kai, A. K., Ho, D. W., Lau, E. Y.-T., Tsui, Y., Chan, L., Cheung, T. T., Chok, K., Chan, A. C. Y., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-313264 · Cited by 210 · see citing works
HIF-1α signaling: Essential roles in tumorigenesis and implications in targeted therapies
Zhao, Y., Xing, C., Deng, Y., Ye, C., & Peng, H. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2023.02.039 · Cited by 214 · see citing works
Semenza, G. L. (2012) · Oncogene · doi:10.1038/onc.2012.578 · Cited by 201 · see citing works
Brooks, D. L. P., Schwab, L. P., Krutilina, R. I., Parke, D. N., Sethuraman, A., Hoogewijs, D., Schörg, A., Gotwald, L., Fan, M., Wenger, R. H., et al. (2016) · Molecular Cancer · doi:10.1186/s12943-016-0510-x · Cited by 190 · see citing works
Hypoxia-regulated target genes implicated in tumor metastasis
Tsai, Y.-P., & Wu, K.-J. (2012) · Journal of Biomedical Science · doi:10.1186/1423-0127-19-102 · Cited by 190 · see citing works
Hypoxia-inducible factors and innate immunity in liver cancer
Yuen, V. W., & Wong, C. C. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137553 · Cited by 182 · see citing works
Nanomaterials to relieve tumor hypoxia for enhanced photodynamic therapy
Zhang, C., Qin, W., Bai, X., & Zhang, X.-Z. (2020) · Nano Today · doi:10.1016/j.nantod.2020.100960 · Cited by 143 · see citing works
Enhancing Photodynamic Therapy Efficacy by Using Fluorinated Nanoplatform
Que, Y., Liu, Y., Tan, W., Feng, C., Shi, P., Li, Y., & Huang, X. (2016) · ACS Macro Letters · doi:10.1021/acsmacrolett.5b00935 · Cited by 153 · see citing works
Hypoxia as a biomarker for radioresistant cancer stem cells
Peitzsch, C., Perrin, R. L., Hill, R. P., Dubrovska, A., & Kurth, I. (2014) · International Journal of Radiation Biology · doi:10.3109/09553002.2014.916841 · Cited by 142 · see citing works
Shi, S., Du, Y., Zou, Y., Niu, J., Cai, Z., Wang, X., Qiu, F., Ding, Y., Yang, G., Wu, Y., et al. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c02221 · Cited by 137 · see citing works
CD24 regulates sorafenib resistance via activating autophagy in hepatocellular carcinoma
Lü, S., Yao, Y., Xu, G., Chao Hui, Z. H. O. U., Zhang, Y., Sun, J., Jiang, R., Shao, Q., & Chen, Y. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0681-z · Cited by 129 · see citing works
The potential role of HIF on tumour progression and dissemination
Unwith, S., Zhao, H., Hennah, L., & Ma, D. (2014) · International Journal of Cancer · doi:10.1002/ijc.28889 · Cited by 126 · see citing works
Chen, H., He, W., & Guo, Z. (2014) · Chemical Communications · doi:10.1039/c4cc03385j · Cited by 111 · see citing works
Molecular Mechanism of Tumor Cell Immune Escape Mediated by CD24/Siglec-10
Yin, S.-S., & Gao, F. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01324 · Cited by 106 · see citing works
Targeting Hypoxia-Inducible Factor-1-Mediated Metastasis for Cancer Therapy
Ma, Z., Wang, L. Z., Cheng, J.-T., Lam, S. T., Ma, X., Xiang, X., Wong, A. L., Goh, B. C., Gong, Q., Sethi, G., et al. (2020) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7935 · Cited by 102 · see citing works
Overdevest, J. B., Knubel, K. H., Duex, J. E., Thomas, S., Nitz, M. D., Harding, M. A., Smith, S. C., Frierson, H. F., Conaway, M. R., & Theodorescu, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113960109 · Cited by 95 · see citing works
Self-citationTian, X., Zhu, Y., Zhang, M., Luo, L., Wu, J., Zhou, H., Guan, L., Battaglia, G., & Tian, Y. (2017) · Chemical Communications · doi:10.1039/c6cc09470h · Cited by 94 · see citing works
CD24: A Novel Target for Cancer Immunotherapy
Panagiotou, Ε., Syrigos, N. K., Charpidou, A. G., Kotteas, E. A., & Vathiotis, I. A. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12081235 · Cited by 90 · see citing works
Hypoxia and Regulation of Cancer Cell Stemness
Yun, Z., & Lin, Q. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5915-6_2 · Cited by 89 · see citing works
CD24 Overexpression Is Associated with Poor Prognosis in Luminal A and Triple-Negative Breast Cancer
Kwon, M. J., Han, J., Seo, J., Song, K., Jeong, H. M., Choi, J., Kim, Y. J., Lee, S. H., Choi, Y., & Shin, Y. K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139112 · Cited by 90 · see citing works
Role of hypoxia inducible factor-1 in cancer stem cells (Review)
Zhang, Q., Han, Z., Zhu, Y., Chen, J., & Li, W. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11655 · Cited by 86 · see citing works
Targeted therapies in bladder cancer: an overview of in vivo research
van Kessel, K. E. M., Zuiverloon, T. C. M., Alberts, A. R., Boormans, J. L., & Zwarthoff, E. C. (2015) · Nature Reviews Urology · doi:10.1038/nrurol.2015.231 · Cited by 84 · see citing works
Peroxidase Mimetic Nanozymes in Cancer Phototherapy: Progress and Perspectives
Thangudu, S., & Su, C. (2021) · Biomolecules · doi:10.3390/biom11071015 · Cited by 82 · see citing works
Wei, X., Zhao, L., Ren, R., Ji, F., Xue, S., Zhang, J., Liu, Z., Ma, Z., Wang, X. W., Wong, L. L., et al. (2020) · Hepatology · doi:10.1002/hep.31448 · Cited by 79 · see citing works
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 · see citing works
Targets in small cell lung cancer
Teicher, B. A. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.09.014 · Cited by 77 · see citing works
Highly specific role of the insulin receptor in breast cancer progression
Rostoker, R., Abelson, S., Bitton-Worms, K., Genkin, I., Ben-Shmuel, S., Dakwar, M., Orr, Z. S., Caspi, A., Tzukerman, M., & LeRoith, D. (2015) · Endocrine Related Cancer · doi:10.1530/erc-14-0490 · Cited by 72 · see citing works
Hypoxia-Induced Phenotypes that Mediate Tumor Heterogeneity
Qian, J., & Rankin, E. B. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-12734-3_3 · Cited by 71 · see citing works
Zhang, Y., Shen, T., Kirillov, A. M., Liu, W., & Tang, Y. (2016) · Chemical Communications · doi:10.1039/c6cc02571d · Cited by 69 · see citing works
A redox-activated theranostic nanoagent: toward multi-mode imaging guided chemo-photothermal therapy
Zhang, T., Xu, C.-H., Zhao, W., Gu, Y., Li, X., Xu, J., & Chen, H. (2018) · Chemical Science · doi:10.1039/c8sc02446d · Cited by 69 · see citing works
Targeting Hypoxia-Driven Metabolic Reprogramming to Constrain Tumor Progression and Metastasis
Galvis, M. M., & Teng, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155487 · Cited by 69 · see citing works
Teo, W. W., Merino, V. F., Cho, S., Korangath, P. C., Liang, X., Wu, R., Neumann, N. M., Ewald, A. J., & Sukumar, S. V. (2016) · Oncogene · doi:10.1038/onc.2016.95 · Cited by 67 · see citing works
Hypoxia: syndicating triple negative breast cancer against various therapeutic regimens
Srivastava, N., Usmani, S. S., Subbarayan, R., Saini, R., & Pandey, P. K. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1199105 · Cited by 64 · see citing works
Engineered Breast Cancer Cell Spheroids Reproduce Biologic Properties of Solid Tumors
Ham, S. L., Joshi, R., Luker, G. D., & Tavana, H. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600644 · Cited by 64 · see citing works
Implications of Hypoxia in Breast Cancer Metastasis to Bone
Gilkes, D. M. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17101669 · Cited by 63 · see citing works
Li, X., Tian, W., Jiang, Z., Song, Y., Leng, X., & Yu, J. (2024) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-023-03606-0 · Cited by 65 · see citing works
Yamada, S., Utsunomiya, T., Morine, Y., Imura, S., Ikemoto, T., Arakawa, Y., Kanamoto, M., Iwahashi, S., Saito, Y., Takasu, C., et al. (2014) · Annals of Surgical Oncology · doi:10.1245/s10434-014-3575-z · Cited by 63 · see citing works
Cholangiocarcinoma: Correlation between Molecular Profiling and Imaging Phenotypes
Sadot, E., Simpson, A. L., Gian, R. K., Gönen, M., Shia, J., Allen, P. J., D'Angelica, M. I., DeMatteo, R. P., Kingham, T. P., & Jarnagin, W. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132953 · Cited by 59 · see citing works
H2O2-responsive theranostic nanomedicine
Yu, L., Chen, Y., & Chen, H. (2017) · Chinese Chemical Letters · doi:10.1016/j.cclet.2017.05.023 · Cited by 56 · see citing works
The role of tumor microenvironment on cancer stem cell fate in solid tumors
Razi, S., Haghparast, A., Khameneh, S. C., Sadrabadi, A. E., Aziziyan, F., Bakhtiyari, M., Nabi‐Afjadi, M., Tarhriz, V., Jalili, A., & Zalpoor, H. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01129-w · Cited by 56 · see citing works
Zhang, C., Liu, W., Bai, X., Cheng, S., Zhong, Z., & Zhang, X. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.01.041 · Cited by 52 · see citing works
Fujikuni, N., Yamamoto, H., Tanabe, K., Naito, Y., Sakamoto, N., Tanaka, Y., Yanagihara, K., Oue, N., Yasui, W., & Ohdan, H. (2014) · Cancer Science · doi:10.1111/cas.12522 · Cited by 51 · see citing works
Endocrine-disrupting effects of bisphenols on urological cancers
Pellerin, È., Caneparo, C., Chabaud, S., Bolduc, S., & Pelletier, M. (2020) · Environmental Research · doi:10.1016/j.envres.2020.110485 · Cited by 50 · see citing works
Pathophysiology of recurrent hepatocellular carcinoma after radiofrequency ablation
Ikemoto, T., Shimada, M., & Yamada, S. (2016) · Hepatology Research · doi:10.1111/hepr.12705 · Cited by 47 · see citing works
Hypoxia in bone metastasis and osteolysis
Todd, V. M., & Johnson, R. W. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.06.004 · Cited by 48 · see citing works
Song, W., He, Y., Feng, Y., Wang, Y. Y., Li, X., Wu, Y., Zhang, S., Zhong, L., Yan, F., & Sun, L. (2024) · Small · doi:10.1002/smll.202305764 · Cited by 41 · see citing works
Wang, J., Zhang, K., Wang, J., Wu, X., Liu, X., Li, B., Zhu, Y., Yu, Y., Cheng, Q., Hu, Z., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4305 · Cited by 41 · see citing works
Nanozyme’s catalytic activity at neutral pH: reaction substrates and application in sensing
Chen, X., Liao, J., Lin, Y., Zhang, J., & Zheng, C. (2023) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-023-04525-w · Cited by 39 · see citing works
CD24, A Review of its Role in Tumor Diagnosis, Progression and Therapy
Ni, Y., Zhao, X., & Wang, W. (2020) · Current Gene Therapy · doi:10.2174/1566523220666200623170738 · Cited by 39 · see citing works
Global Gene Repression by the Steroid Receptor Coactivator SRC-1 Promotes Oncogenesis
Walsh, C. A., Bolger, J. C., Byrne, C., Cocchiglia, S., Yuan, H., Fagan, A., Qin, L., Cahalin, A., McCartan, D. P., McIlroy, M., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2133 · Cited by 38 · see citing works
Physical view on migration modes
Mierke, C. T. (2015) · Cell Adhesion & Migration · doi:10.1080/19336918.2015.1066958 · Cited by 34 · see citing works
CD24: A Rheostat That Modulates Cell Surface Receptor Signaling of Diverse Receptors
Ayre, D. C., & Christian, S. L. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00146 · Cited by 34 · see citing works
The biological roles of CD24 in ovarian cancer: old story, but new tales
Gu, Y., Zhou, G., Tang, X., Shen, F., Ding, J., & Hua, K. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1183285 · Cited by 32 · see citing works
Silencing of CD24 Enhances the PRIMA-1–Induced Restoration of Mutant p53 in Prostate Cancer Cells
Zhang, W., Yi, B., Wang, C., Chen, D., Bae, S., Wei, S., Guo, R., Lu, C., Nguyen, L. L. H., Yang, W., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-1927 · Cited by 32 · see citing works
Priming of the Cells: Hypoxic Preconditioning for Stem Cell Therapy.
Wei, Z. Z., Zhu, Y., Zhang, J. Y., McCrary, M. R., Wang, S., Zhang, Y., Yu, S., & Wei, L. (2017) · PubMed Central · doi:10.4103/0366-6999.215324 · Cited by 32 · see citing works
Nuclear CD24 Drives Tumor Growth and Is Predictive of Poor Patient Prognosis
Duex, J. E., Owens, C. R., Chauca-Diaz, A., Dancik, G. M., Vanderlinden, L. A., Ghosh, D., Leivo, M. Z., Hansel, D. E., & Theodorescu, D. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0367 · Cited by 31 · see citing works
Self-citationBiomedical engineered nanomaterials to alleviate tumor hypoxia for enhanced photodynamic therapy
Lai, C., Luo, B.-Y., Shen, J., & Shao, J. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106551 · Cited by 31 · see citing works
Downregulation of CD 24 suppresses bone metastasis of lung cancer
Okabe, H., Aoki, K., Yogosawa, S., Saito, M., Marumo, K., & Yoshida, K. (2017) · Cancer Science · doi:10.1111/cas.13435 · Cited by 30 · see citing works
Checkpoint CD24 function on tumor and immunotherapy
Huang, S., Zhang, X., Wei, Y., & Xiao, Y. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1367959 · Cited by 29 · see citing works
Androgen receptor activation: a prospective therapeutic target for bladder cancer?
Mizushima, T., Tirador, K. A., & Miyamoto, H. (2017) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2017.1280468 · Cited by 28 · see citing works
Li, L., Chen, J., Ge, C., Zhao, F., Chen, T., Tian, H., Li, J., & Li, H. (2019) · OncoTargets and Therapy · doi:10.2147/ott.s196506 · Cited by 26 · see citing works
Zaarour, R. F., Ribeiro, M., Azzarone, B. G., Kapoor, S., & Chouaı̈b, S. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1222575 · Cited by 24 · see citing works
Cui, Y., Cho, I.-H., Chowdhury, B., & Irudayaraj, J. (2013) · Epigenetics · doi:10.4161/epi.25958 · Cited by 25 · see citing works
Amplification of the CD24 Gene Is an Independent Predictor for Poor Prognosis of Breast Cancer
Zhang, P., Zheng, P., & Liu, Y. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00560 · Cited by 25 · see citing works
Mittal, K., Choi, D. H., Ogden, A., Donthamsetty, S., Melton, B. D., Gupta, M. V., Pannu, V., Cantuaria, G. H., Varambally, S., Reid, M. D., et al. (2017) · Scientific Reports · doi:10.1038/srep43984 · Cited by 24 · see citing works
Raddum, A. M., Evensen, L., Hollås, H., Grindheim, A. K., Lorens, J. B., & Vedeler, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060281 · Cited by 24 · see citing works
Luo, Z., Li, M., Zhou, M., Li, H., Chen, Y., Ren, X., & Dai, Y. (2019) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2019.03.007 · Cited by 24 · see citing works
Nagare, R. P., Sneha, S., Sidhanth, C., Roopa, S., Murhekar, K. M., Shirley, S., Swaminathan, R., Velusamy, S., & Ganesan, T. S. (2020) · Cancer Biomarkers · doi:10.3233/cbm-201463 · Cited by 24 · see citing works
Cao, X., Cao, D., Jin, M., Jia, Z., Kong, F., Ma, H., Wang, Y., & Jiang, J. (2014) · BMC Gastroenterology · doi:10.1186/1471-230x-14-157 · Cited by 22 · see citing works
He, J., Hu, Y., Hu, M., Zhang, S., & Li, B. (2016) · Scientific Reports · doi:10.1038/srep20586 · Cited by 22 · see citing works
Kokate, S. B., Dixit, P., Das, L., Rath, S., Roy, A. D., Poirah, I., Chakraborty, D., Rout, N., Singh, S. P., & Bhattacharyya, A. (2018) · The FASEB Journal · doi:10.1096/fj.201701344rrr · Cited by 22 · see citing works
Sunil, V., Mozhi, A., Zhan, W., Teoh, J. H., & Wang, C. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120974 · Cited by 21 · see citing works
Chen, H., He, C., Chen, T., & Xue, X. (2020) · Biomaterials Science · doi:10.1039/d0bm00500b · Cited by 21 · see citing works
Review Hypoxia-shaped vascular niche for cancer stem cells
Collet, G., Hafny‐Rahbi, B. E., Nadim, M., Tejchman, A., Klimkiewicz, K., & Kiéda, C. (2015) · Współczesna Onkologia · doi:10.5114/wo.2014.47130 · Cited by 20 · see citing works
Su, P., Zhu, Z., Fan, Q., Cao, J., Wang, Y., Yang, X., Cheng, B., Liu, W., & Tang, Y. (2018) · Inorganic Chemistry Frontiers · doi:10.1039/c8qi00777b · Cited by 20 · see citing works
Söhngen, C., Thomas, D. J., Skowron, M. A., Bremmer, F., Eckstein, M., Stefanski, A., Driessen, M. D., Wakileh, G. A., Stühler, K., Altevogt, P., et al. (2023) · The FEBS Journal · doi:10.1111/febs.16880 · Cited by 19 · see citing works
Self-citationJana, B., Thomas, A. P., Kim, S., Lee, I. S., Choi, H., Jin, S., Park, S. A., Min, S. K., Kim, C., & Ryu, J. (2020) · Chemistry - A European Journal · doi:10.1002/chem.202001366 · Cited by 19 · see citing works
Phenotypic and molecular states of IDH1 mutation-induced CD24-positive glioma stem-like cells
Haddock, S., Alban, T. J., Turcan, Ş., Husic, H., Rosiek, E., Ma, X., Wang, Y., Bale, T., Desrichard, A., Makarov, V., et al. (2022) · Neoplasia · doi:10.1016/j.neo.2022.100790 · Cited by 19 · see citing works
A mathematical model of tumor hypoxia targeting in cancer treatment and its numerical simulation
Sabir, M., Shah, A., Muhammad, W., Ali, I., & Bastian, P. (2017) · Computers & Mathematics with Applications · doi:10.1016/j.camwa.2017.08.019 · Cited by 19 · see citing works
Kleinmanns, K., Fosse, V., Bjørge, L., & McCormack, E. (2020) · Journal of Personalized Medicine · doi:10.3390/jpm10040255 · Cited by 19 · see citing works
Paříková, A., Hrubá, P., Krejčík, Z., Stránecký, V., Franeková, J., Krediet, R. T., & Viklický, O. (2019) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00274.2019 · Cited by 17 · see citing works
Stremitzer, S., Sunakawa, Y., Zhang, W. Y., Yang, D., Ning, Y., Stintzing, S., Sebio, A., Yamauchi, S., Matsusaka, S., El-Khoueiry, R. E., et al. (2015) · The Pharmacogenomics Journal · doi:10.1038/tpj.2015.14 · Cited by 17 · see citing works
Wu, X. Y., Wu, H., Liu, L., Qiang, G.-H., & Zhu, J. (2020) · Translational Cancer Research · doi:10.21037/tcr-20-2571 · Cited by 16 · see citing works
Yin, H., Cao, P., Wang, X., Li, Y., & Yin, X. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.0c00244 · Cited by 14 · see citing works
Metronidazole conjugated bismuth sulfide nanoparticles for enhanced X-ray radiation therapy
Javani, S., Barsbay, M., Ghaffarlou, M., Mousazadeh, N., Mohammadi, A., Mozafari, F., Rezaeejam, H., Nasehi, L., Nosrati, H., Kavetskyy, T. S., et al. (2022) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2022.103336 · Cited by 14 · see citing works
Hong, P., Xu, T., Xu, J., Chen, W., Xu, J., Chen, J., Li, L., Zheng, C., Li, L., Liu, J., et al. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216994 · Cited by 13 · see citing works
DNA Promoter Methylation and ERG Regulate the Expression of CD24 in Prostate Cancer
Tolkach, Y., Zarbl, R., Bauer, S., Ritter, M., Ellinger, J., Hauser, S., Hüser, L., Klauck, S. M., Altevogt, P., Sültmann, H., et al. (2021) · American Journal Of Pathology · doi:10.1016/j.ajpath.2020.12.014 · Cited by 13 · see citing works
Self-citationShakib, P. A., Ensani, F., Abdirad, A., Valizadeh, B., Seyedmajidi, M., & Sum, S. (2015) · PubMed Central · Cited by 13 · see citing works
Takashima, K., Fujii, S., Komatsuzaki, R., Komatsu, M., Takahashi, M., Kojima, T., Daiko, H., Minashi, K., Chiwaki, F., Muto, M., et al. (2020) · International Journal of Oncology · doi:10.3892/ijo.2020.4963 · Cited by 13 · see citing works
Liu, J., Yan, C., & Xu, S. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06704-8 · Cited by 12 · see citing works
- Authors
- Thomas, S., Harding, M. A., Smith, S. C., Overdevest, J. B., Nitz, M. D., Frierson, H. F., Tomlins, S. A., Kristiansen, G., & Theodorescu, D.
- Affiliations
- University of Bonn (DE)
- ORCID
- Venue
- Cancer Research
- Published
- 2012-10-31
- Volume
- 72
- Issue
- 21
- Pages
- 5600-5612
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC3488144
- OpenAlex
- W2114076439
- Cited by
- 128
- References
- 56
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 11 · 2023: 8 · 2022: 8 · 2021: 9 · 2020: 19 · 2019: 7 · 2018: 7 · 2017: 11 · 2016: 11 · 2015: 12 · 2014: 9 · 2013: 6 · 2012: 4
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Virginia
- National Institutes of Health
- National Cancer Institute (CA 075115, P01CA104106, R01CA075115, CA 104106, R29CA075115, P30CA044579)
- 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 › Mechanisms of cancer metastasis
- Keywords
- CD24, HIF-1α, hypoxia, tumor growth, metastasis, hypoxia response element, transcriptional regulation, cancer stem cells, tumor cell survival, patient survival
- MeSH terms
- Animals, Humans, Immunohistochemistry, Mice, Nude, Neoplasm Invasiveness, Neoplasms, Promoter Regions, Genetic, RNA, Messenger, Transplantation, Heterologous, Blotting, Western, Cell Hypoxia, Gene Expression Regulation, Neoplastic, Disease Progression, Cell Line, Tumor, Chromatin Immunoprecipitation, Mice, Hypoxia-Inducible Factor 1, alpha Subunit, CD24 Antigen, Real-Time Polymerase Chain Reaction
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
