Tumor-initiating cells of breast and prostate origin show alterations in the expression of genes related to iron metabolism
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// Zuzana Rychtarcikova 1, 2, * , Sandra Lettlova 1, 3, * , Veronika Tomkova 1, 3 , Vlasta Korenkova 1 , Lucie Langerova 1 , Ekaterina Simonova 1 , Polina Zjablovskaja 4 , Meritxell Alberich-Jorda 4 , Jiri Neuzil 1, 5 , Jaroslav Truksa 1 1 Institute of Biotechnology, Czech Academy of Sciences, Prague, Czech Republic 2 Charles University in Prague, Faculty of Pharmacy in Hradec Kralove, Hradec Kralove, Czech Republic 3 Charles University in Prague, Faculty of Sciences, Prague, Czech Republic 4 Institute of Molecular Genetics, Czech Academy of Sciences, Prague, Czech Republic 5 School of Medical Science, Menzies Health Institute Queensland, Southport, Queensland, Australia * These authors contributed equally to this work Correspondence to: Jaroslav Truksa, email: jaroslav.truksa@ibt.cas.cz Keywords: tumor-initiating cells, breast cancer, iron metabolism, FeS cluster, stem cells Received: January 12, 2016 Accepted: November 30, 2016 Published: December 22, 2016 ABSTRACT The importance of iron in the growth and progression of tumors has been widely documented. In this report, we show that tumor-initiating cells (TICs), represented by spheres derived from the MCF7 cell line, exhibit higher intracellular labile iron pool, mitochondrial iron accumulation and are more susceptible to iron chelation. TICs also show activation of the IRP/IRE system, leading to higher iron uptake and decrease in iron storage, suggesting that level of properly assembled cytosolic iron-sulfur clusters (FeS) is reduced. This finding is confirmed by lower enzymatic activity of aconitase and FeS cluster biogenesis enzymes, as well as lower levels of reduced glutathione, implying reduced FeS clusters synthesis/utilization in TICs. Importantly, we have identified specific gene signature related to iron metabolism consisting of genes regulating iron uptake, mitochondrial FeS cluster biogenesis and hypoxic response ( ABCB10 , ACO1 , CYBRD1 , EPAS1 , GLRX5 , HEPH , HFE , IREB2 , QSOX1 and TFRC ). Principal component analysis based on this signature is able to distinguish TICs from cancer cells in vitro and also Leukemia-initiating cells (LICs) from non-LICs in the mouse model of acute promyelocytic leukemia (APL). Majority of the described changes were also recapitulated in an alternative model represented by MCF7 cells resistant to tamoxifen (TAMR) that exhibit features of TICs. Our findings point to the critical importance of redox balance and iron metabolism-related genes and proteins in the context of cancer and TICs that could be potentially used for cancer diagnostics or therapy.
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Several cancers, including breast, prostate and lymphoma, reprogram iron metabolism by increasing iron uptake or reducing iron export and storage.
“reprogramming of iron metabolism can occur via a variety of mechanisms, including the upregulation of several iron-intake pathways or downregulation of iron export and storage pathways in various types of cancer such as breast, prostate and lymphoma37,38.”
From Targeting cancer vulnerabilities with high-dose vitamin C (2019) · cites this paper as [37]
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Targeting Hypoxia-Inducible Factors for the Treatment of Anemia in Chronic Kidney Disease Patients
Locatelli, F., Fishbane, S. N., Block, G. A., & Macdougall, I. C. (2017) · American Journal of Nephrology · doi:10.1159/000455166 · Cited by 4,834 · see citing works
Cloning and characterization of a mammalian proton-coupled metal-ion transporter
Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., & Hediger, M. A. (1997) · Nature · doi:10.1038/41343 · Cited by 3,166 · see citing works
Tumour heterogeneity and cancer cell plasticity
Meacham, C., & Morrison, S. (2013) · Nature · doi:10.1038/nature12624 · Cited by 2,350 · see citing works
Hentze, M. W., Muckenthaler, M. U., & Andrews, N. C. (2004) · Cell · doi:10.1016/s0092-8674(04)00343-5 · Cited by 1,736 · see citing works
Iron and cancer: more ore to be mined
Torti, S. V., & Torti, F. M. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3495 · Cited by 1,621 · see citing works
Hentze, M. W., & Kühn, L. C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8175 · Cited by 1,292 · see citing works
A Novel Mammalian Iron-regulated Protein Involved in Intracellular Iron Metabolism
Abboud, S., & Haile, D. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000713200 · Cited by 1,267 · see citing works
Regulation of ferritin genes and protein
Torti, F. M., & Torti, S. V. (2002) · Blood · doi:10.1182/blood.v99.10.3505 · Cited by 1,173 · see citing works
An iron-regulated ferric reductase associated with the absorption of dietary iron
McKie, A. T., Barrow, D., Latunde-Dada, G. O., Rolfs, A., Sager, G., Mudaly, E., Mudaly, M., Richardson, C., Barlow, D., Bomford, A., et al. (2001) · Science · doi:10.1126/science.1057206 · Cited by 1,101 · see citing works
Vulpe, C. D., Kuo, Y.-M., Murphy, T. L., Cowley, L., Askwith, C., Libina, N., Gitschier, J., & Anderson, G. J. (1999) · Nature Genetics · doi:10.1038/5979 · Cited by 1,084 · see citing works
Brainson, C. F., & Kuperwasser, C. (2008) · Breast Cancer Research · doi:10.1186/bcr1982 · Cited by 1,035 · see citing works
Regulation of iron homeostasis by the hypoxia-inducible transcription factors (HIFs)
Peyssonnaux, C., Zinkernagel, A. S., Schuepbach, R. A., Rankin, E., Vaulont, S., Haase, V. H., Nizet, V., & Johnson, R. S. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31370 · Cited by 639 · see citing works
Oxidative damage during aging targets mitochondrial aconitase
Yan, L., Levine, R. L., & Sohal, R. S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11168 · Cited by 620 · see citing works
Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells
Liuzzi, J. P., Aydemir, F., Nam, H., Knutson, M. D., & Cousins, R. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606424103 · Cited by 577 · see citing works
The hypoxic tumor microenvironment: A driving force for breast cancer progression
Semenza, G. L. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.05.036 · Cited by 535 · see citing works
Ferritin and the response to oxidative stress
Orino, K., Lehman, L. J., Tsuji, Y., Ayaki, H., Torti, S. V., & Torti, F. M. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3570241 · Cited by 535 · see citing works
Ferritin and the response to oxidative stress
ORINO, K., LEHMAN, L., TSUJI, Y., AYAKI, H., TORTI, S. V., & TORTI, F. M. (2001) · Biochemical Journal · doi:10.1042/bj3570241 · Cited by 535 · see citing works
IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics
Sasaki, M., Knobbe, C. B., Munger, J. C., Lind, E. F., Brenner, D., Brüstle, A., Harris, I. S., Holmes, R., Wakeham, A., Haight, J., et al. (2012) · Nature · doi:10.1038/nature11323 · Cited by 513 · see citing works
Hypoxia inducible factors in cancer stem cells
Heddleston, J. M., Li, Z., Lathia, J. D., Bao, S., Hjelmeland, A. B., & Rich, J. N. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605551 · Cited by 453 · see citing works
Shah, Y. M., Matsubara, T., Ito, S., Yim, S.-H., & Gonzalez, F. J. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.12.012 · Cited by 431 · see citing works
Mutation Analysis in Hereditary Hemochromatosis
Beutler, E., Gelbart, T., West, C., Lee, P. L., Adams, M., Blackstone, R., Pockros, P. J., Kosty, M. P., Venditti, C. P., Phatak, P. D., et al. (1996) · Blood Cells Molecules and Diseases · doi:10.1006/bcmd.1996.0027 · Cited by 416 · see citing works
Cancer stem cell markers in common cancers – therapeutic implications
Klonisch, T. C., Wiecheć, E., Hombach‐Klonisch, S., Ande, S. R., Wesselborg, S., Schulze‐Osthoff, K., & Łoś, M. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.08.003 · Cited by 394 · see citing works
Fluorescence analysis of the labile iron pool of mammalian cells
Epsztejn, S., Kakhlon, O., Glickstein, H., Breuer, W., & Cabantchik, Z. I. (1997) · Analytical Biochemistry · doi:10.1006/abio.1997.2126 · Cited by 391 · see citing works
Iron–sulfur cluster biogenesis and human disease
Rouault, T. A., & Tong, W. H. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.05.008 · Cited by 387 · see citing works
Koh, M. Y., Lemos, R., Liu, X., & Powis, G. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4142 · Cited by 350 · see citing works
Sox2 promotes tamoxifen resistance in breast cancer cells
Piva, M., Domenici, G., Iriondo, O., Rábano, M., Simões, B. M., Comaills, V., Barredo, I., López‐Ruiz, J. A., Zabalza, I., Kypta, R. M., et al. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201303411 · Cited by 328 · see citing works
Hypoxia Enhances Tumor Stemness by Increasing the Invasive and Tumorigenic Side Population Fraction
Das, B., Tsuchida, R., Malkin, D. M., Koren, G., Baruchel, S., & Yeger, H. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0724 · Cited by 309 · see citing works
Iron regulatory proteins in pathobiology
Cairo, G., & Pietrangelo, A. (2000) · Biochemical Journal · doi:10.1042/bj3520241 · Cited by 299 · see citing works
Rouault, T. A., Stout, C. D., Kaptain, S., Harford, J. B., & Klausner, R. D. (1991) · Cell · doi:10.1016/0092-8674(91)90312-m · Cited by 296 · see citing works
Iron Regulates the Intracellular Degradation of Iron Regulatory Protein 2 by the Proteasome
Guo, B., Phillips, J. D., Yu, Y., & Leibold, E. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.37.21645 · Cited by 287 · see citing works
Delaby, C., Pilard, N., Gonçalves, A. S., Beaumont, C., & Canonne-Hergaux, F. (2005) · Blood · doi:10.1182/blood-2005-06-2398 · Cited by 283 · see citing works
Lange, H., Lisowsky, T., Gerber, J., Mühlenhoff, U., Kispál, G., & Lill, R. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve161 · Cited by 269 · see citing works
Hahn, P., Qian, Y., Dentchev, T., Chen, L., Beard, J., Harris, Z. L., & Dunaief, J. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405146101 · Cited by 264 · see citing works
Cancer cell iron metabolism and the development of potent iron chelators as anti-tumour agents
Richardson, D. R., Kalinowski, D. S., Lau, S. L., Jansson, P. J., & Lovejoy, D. B. (2008) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.04.003 · Cited by 260 · see citing works
Marie-Egyptienne, D. T., Lohse, I., & Hill, R. P. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.11.019 · Cited by 256 · see citing works
Prigione, A., Rohwer, N., Hoffmann, S., Mlody, B., Drews, K., Bukowiecki, R., Blümlein, K., Wanker, E. E., Ralser, M., Cramer, T., et al. (2013) · Stem Cells · doi:10.1002/stem.1552 · Cited by 252 · see citing works
Biogenesis of cytosolic and nuclear iron–sulfur proteins and their role in genome stability
Paul, V. D., & Lill, R. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.12.018 · Cited by 247 · see citing works
Jenkitkasemwong, S., Wang, C.-Y., Coffey, R., Zhang, W., Chan, A., Biel, T., Kim, J.-S., Hojyo, S., Fukada, T., & Knutson, M. D. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.05.002 · Cited by 245 · see citing works
Iron regulatory proteins and their role in controlling iron metabolism
Kühn, L. C. (2015) · Metallomics · doi:10.1039/c4mt00164h · Cited by 242 · see citing works
Xue, X., Ramakrishnan, S. K., Weisz, K. M., Triner, D. A., Xie, L., Attili, D., Pant, A., Győrffy, B., Zhan, M., Carter‐Su, C., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.07.015 · Cited by 242 · see citing works
Ye, H., Jeong, S. Y., Ghosh, M. C., Kovtunovych, G., Silvestri, L., Ortillo, D., Uchida, N., Tisdale, J. F., Camaschella, C., & Rouault, T. A. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40372 · Cited by 239 · see citing works
Habashy, H. O., Powe, D. G., Staka, C. M., Rakha, E. A., Ball, G., Green, A. R., Aleskandarany, M., Paish, E. C., Douglas Macmillan, R., Nicholson, R. I., et al. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0345-x · Cited by 236 · see citing works
The long history of iron in the Universe and in health and disease
Sheftel, A. D., Mason, A. B., & Ponka, P. (2011) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.08.002 · Cited by 234 · see citing works
Modulation of iron transport proteins in human colorectal carcinogenesis
Brookes, M. J., Hughes, S., Turner, F. E., Reynolds, G., Sharma, N., Ismail, T., Berx, G., McKie, A. T., Hotchin, N., Anderson, G. J., et al. (2006) · Gut · doi:10.1136/gut.2006.094060 · Cited by 226 · see citing works
Chen, W., Paradkar, P. N., Li, L., Pierce, E. L., Langer, N. B., Takahashi‐Makise, N., Hyde, B. B., Shirihai, O. S., Ward, D. M., Kaplan, J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904519106 · Cited by 220 · see citing works
An iron regulatory gene signature predicts outcome in breast cancer
Miller, L. D., Coffman, L. G., Chou, J. W., Black, M. A., Bergh, J., D'Agostino, R., Torti, S. V., & Torti, F. M. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1870 · Cited by 202 · see citing works
Rouault‐Pierre, K., López-Onieva, L., Foster, K., Anjos‐Afonso, F., Lamrissi‐Garcia, I., Serrano-Sanchez, M., Mitter, R., Ivanović, Z., de Verneuil, H., Gribben, J. G., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.08.011 · Cited by 187 · see citing works
Proto-Oncogenic Role of Mutant IDH2 in Leukemia Initiation and Maintenance
Kats, L. M., Reschke, M., Taulli, R., Pozdnyakova, O., Burgess, K., Bhargava, P., Straley, K. S., Karnik, R., Meissner, A., Small, D., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2013.12.016 · Cited by 187 · see citing works
Novel Chelators for Cancer Treatment: Where Are We Now?
Merlot, A. M., Kalinowski, D. S., & Richardson, D. R. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4540 · Cited by 186 · see citing works
Iron homeostasis: new tales from the crypt
Roy, C. N., & Enns, C. A. (2000) · Blood · doi:10.1182/blood.v96.13.4020 · Cited by 175 · see citing works
Nam, H., Wang, C., Zhang, L., Zhang, W., Hojyo, S., Fukada, T., & Knutson, M. D. (2013) · Haematologica · doi:10.3324/haematol.2012.072314 · Cited by 170 · see citing works
A Secreted Disulfide Catalyst Controls Extracellular Matrix Composition and Function
Ilani, T., Alon, A., Grossman, I., Horowitz, B., Kartvelishvily, E., Cohen, S., & Fass, D. (2013) · Science · doi:10.1126/science.1238279 · Cited by 169 · see citing works
Comino-Méndez, I., de Cubas, A. A., Bernal, C., Álvarez-Escolá, C., Sánchez-Malo, C., Ramírez-Tortosa, C. L., Pedrinaci, S., Rapizzi, E., Ercolino, T., Bernini, G., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt069 · Cited by 169 · see citing works
Targeting cancer by binding iron: Dissecting cellular signaling pathways
Lui, G. Y. L., Kovačević, Ž., Richardson, V., Merlot, A. M., Kalinowski, D. S., & Richardson, D. R. (2015) · Oncotarget · doi:10.18632/oncotarget.4349 · Cited by 163 · see citing works
Nonadhesive Culture System as a Model of Rapid Sphere Formation with Cancer Stem Cell Properties
Chen, S.-F., Chang, Y., Nieh, S., Liu, C., Yang, C., & Lin, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031864 · Cited by 159 · see citing works
Unexpected role of ceruloplasmin in intestinal iron absorption
Cherukuri, S., Potla, R., Sarkar, J., Nurko, S., Harris, Z. L., & Fox, P. L. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.10.003 · Cited by 158 · see citing works
Chen, W., Dailey, H. A., & Paw, B. H. (2010) · Blood · doi:10.1182/blood-2009-12-259614 · Cited by 157 · see citing works
ABC‐me: a novel mitochondrial transporter induced by GATA‐1 during erythroid differentiation
Shirihai, O. S., Gregory, T., Yu, C., Orkin, S. H., & Weiss, M. J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2492 · Cited by 154 · see citing works
Wnt Inhibitor Screen Reveals Iron Dependence of β-Catenin Signaling in Cancers
Song, S., Christova, T. Y., Perusini, S. J., Alizadeh, S., Bao, R.-Y., Miller, B. W., Hurren, R., Jitkova, Y., Gronda, M., Isaac, M. B., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-2745 · Cited by 151 · see citing works
Iron and hepatocellular carcinoma
Deugnier, Y., & Turlin, B. (2001) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.2001.02430.x · Cited by 145 · see citing works
[2Fe-2S] cluster transfer in iron–sulfur protein biogenesis
Banci, L., Brancaccio, D., Ciofi‐Baffoni, S., Conte, R. D., Gadepalli, R., Mikołajczyk, M., Neri, S., Piccioli, M., & Winkelmann, J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400102111 · Cited by 143 · 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
IRP2 Regulates Breast Tumor Growth
Wang, W., Deng, Z., Hatcher, H., Miller, L. D., Di, X., Tesfay, L., Sui, G., D'Agostino, R. B., Torti, F. M., & Torti, S. V. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1224 · Cited by 137 · see citing works
In vivo and in vitro oncogenic effects of HIF2A mutations in pheochromocytomas and paragangliomas
Toledo, R. A., Qin, Y., Srikantan, S., Morales, N. P., Li, Q., Deng, Y., Kim, S.-W., Pereira, M. A. A., Toledo, S. P. A., Su, X., et al. (2013) · Endocrine Related Cancer · doi:10.1530/erc-13-0101 · Cited by 133 · see citing works
Boult, J. K. R., Roberts, K., Brookes, M., Hughes, S., Bury, J. P., Cross, S. S., Anderson, G. J., Spychal, R., Iqbal, T. H., & Tselepis, C. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1054 · Cited by 132 · see citing works
Mitochondrial ABC proteins in health and disease
Zutz, A., Gompf, S., Schägger, H., & Tampé, R. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.02.009 · Cited by 132 · see citing works
Association Between Hemochromatosis (HFE) Gene Mutation Carrier Status and the Risk of Colon Cancer
Shaheen, N. J., Silverman, L. M., Keku, T. O., Lawrence, L. B., Rohlfs, E. M., Martin, C. F., Galanko, J., & Sandler, R. S. (2003) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/95.2.154 · Cited by 131 · see citing works
Lill, R., Srinivasan, V., & Mühlenhoff, U. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.09.015 · Cited by 130 · see citing works
Characterization and Expression of Iron Regulatory Protein 2 (IRP2)
Guo, B., Brown, F. M., Phillips, J. D., Yu, Y., & Leibold, E. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.28.16529 · Cited by 129 · see citing works
Guibal, F. C., Alberich-Jorda, M., Hirai, H., Ebralidze, A., Levantini, E., Di Ruscio, A., Zhang, P., Santana-Lemos, B. A., Neuberg, D., Wagers, A. J., et al. (2009) · Blood · doi:10.1182/blood-2008-10-182071 · Cited by 126 · see citing works
Hypoxia-inducible factors in cancer stem cells and inflammation
Peng, G., & Liu, Y. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.03.003 · Cited by 124 · see citing works
Mims, M. P., & Prchal, J. T. (2005) · Hematology · doi:10.1080/10245330500093419 · Cited by 123 · see citing works
Johansson, C., Roos, A. K., Montaño, S., Sengupta, R., Filippakopoulos, P., Guo, K., von Delft, F., Holmgren, A., Oppermann, U. C. T., & Kavanagh, K. L. (2010) · Biochemical Journal · doi:10.1042/bj20101286 · Cited by 123 · see citing works
Wang, J., Chen, G., Muckenthaler, M. U., Galy, B., Hentze, M. W., & Pantopoulos, K. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.954-965.2004 · Cited by 116 · see citing works
The gut in iron homeostasis: role of HIF-2 under normal and pathological conditions
Mastrogiannaki, M., Matak, P., & Peyssonnaux, C. (2013) · Blood · doi:10.1182/blood-2012-11-427765 · Cited by 116 · see citing works
Dubrovska, A., Hartung, A., Bouchez, L. C., Walker, J. R., Reddy, V. A., Cho, C. Y., & Schultz, P. G. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.105 · Cited by 115 · see citing works
The Ceruloplasmin Homolog Hephaestin and the Control of Intestinal Iron Absorption
Anderson, G. J., Frazer, D. M., McKie, A. T., & Vulpe, C. D. (2002) · Blood Cells Molecules and Diseases · doi:10.1006/bcmd.2002.0576 · Cited by 111 · see citing works
The Quiescin Q6 Gene (QSCN6) Is a Fusion of Two Ancient Gene Families: Thioredoxin and ERV1
Coppock, D. L., Cina-Poppe, D. A., & Gilleran, S. (1998) · Genomics · doi:10.1006/geno.1998.5605 · Cited by 107 · see citing works
Prognostic significance of HIF-2α/EPAS1 expression in hepatocellular carcinoma
Bangoura, G. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i23.3176 · Cited by 106 · see citing works
Iron transport by Nramp2/DMT1: pH regulation of transport by 2 histidines in transmembrane domain 6
Lam-Yuk-Tseung, S., Govoni, G. R., Forbes, J., & Gros, P. (2003) · Blood · doi:10.1182/blood-2002-07-2108 · Cited by 103 · see citing works
Beckman, L. E. (1999) · Carcinogenesis · doi:10.1093/carcin/20.7.1231 · Cited by 100 · see citing works
Multidomain Flavin-Dependent Sulfhydryl Oxidases
Coppock, D. L., & Thorpe, C. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.300 · Cited by 99 · see citing works
HIF and reactive oxygen species regulate oxidative phosphorylation in cancer
Hervouet, É., Vrbacká-Čížková, A., Demont, J., Pecinová, A., Pecina, P., Hal, N. L. W. F.-V., Keijer, J., Simonnet, H., Ivánek, R., Kmoch, S., et al. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn125 · Cited by 99 · see citing works
Hephaestin—a ferroxidase of cellular iron export
Petrák, J., & Vyoral, D. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.12.007 · Cited by 96 · see citing works
The mechanism of aconitase: 1.8 Å resolution crystal structure of the S642A:citrate complex
Lloyd, S. J., Lauble, H., Prasad, G. S., & Stout, C. D. (1999) · Protein Science · doi:10.1110/ps.8.12.2655 · Cited by 95 · see citing works
Cellular Iron Metabolism in Prognosis and Therapy of Breast Cancer
Torti, S. V., & Torti, F. M. (2013) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2013007784 · Cited by 93 · see citing works
Regulation of Protein S-Thiolation by Glutaredoxin 5 in the Yeast Saccharomyces cerevisiae
Shenton, D., Perrone, G. G., Quinn, K., Dawes, I. W., & Grant, C. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200559200 · Cited by 93 · see citing works
Human Quiescin-Sulfhydryl Oxidase, QSOX1: Probing Internal Redox Steps by Mutagenesis
Heckler, E. J., Alon, A., Fass, D., & Thorpe, C. (2008) · Biochemistry · doi:10.1021/bi702522q · Cited by 92 · see citing works
Hereditary Sideroblastic Anemias: Pathophysiology, Diagnosis, and Treatment
Camaschella, C. (2009) · Seminars in Hematology · doi:10.1053/j.seminhematol.2009.07.001 · Cited by 91 · see citing works
HIF1α Regulates mTOR Signaling and Viability of Prostate Cancer Stem Cells
Marhold, M., Tomasich, E., El‐Gazzar, A., Heller, G., Spittler, A., Horvat, R., Krainer, M., & Horak, P. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-14-0153-t · Cited by 90 · see citing works
SIRT3 regulates cellular iron metabolism and cancer growth by repressing iron regulatory protein 1
Jeong, S. M., Lee, J. J., Finley, L. W. S., Schmidt, P. J., Fleming, M. D., & Haigis, M. C. (2014) · Oncogene · doi:10.1038/onc.2014.124 · Cited by 84 · see citing works
Generating disulfides with the Quiescin-sulfhydryl oxidases
Heckler, E. J., Rancy, P. C., Kodali, V. K., & Thorpe, C. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.10.002 · Cited by 81 · see citing works
FRANKLIN, R. B., Levy, B. A., Zou, J., Hanna, N. N., Desouki, M. M., Bagasra, O., Johnson, L. A., & Costello, L. C. (2011) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-011-9269-x · Cited by 79 · see citing works
Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology
Silván, U., Díez-Torre, A., Arluzea, J., Andrade, R., Silió, M., & Aréchaga, J. (2009) · Differentiation · doi:10.1016/j.diff.2009.06.002 · Cited by 77 · see citing works
Lobello, N., Biamonte, F., Pisanu, M. E., Faniello, M. C., Jakopin, Ž., Chiarella, E., Giovannone, E. D., Mancini, R., Ciliberto, G., Cuda, G., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11495 · Cited by 77 · see citing works
Sox9 and Hif-2α regulate TUBB3 gene expression and affect ovarian cancer aggressiveness
Raspaglio, G., Petrillo, M., Martinelli, E., Puma, D. D. L., Mariani, M., Donato, M. D., Filippetti, F., Mozzetti, S., Prislei, S., Zannoni, G. F., et al. (2014) · Gene · doi:10.1016/j.gene.2014.03.037 · Cited by 75 · see citing works
Yan, B., Stantic, M., Zobalová, R., Bezawork‐Geleta, A., Stapelberg, M., Štursa, J., Rohlenová, K., Dong, L., & Neužil, J. (2015) · BMC Cancer · doi:10.1186/s12885-015-1394-7 · Cited by 72 · see citing works
The Emerging Role of QSOX1 in Cancer
Lake, D. F., & Faigel, D. O. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5572 · Cited by 69 · see citing works
Maffettone, C., Chen, G., Drozdov, I. A., Ouzounis, C. A., & Pantopoulos, K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010163 · Cited by 68 · see citing works
Increased Prevalence of theHFE C282YHemochromatosis Allele in Women with Breast Cancer
Kallianpur, A. R., Hall, L. D., Yadav, M., Christman, B. W., Dittus, R. S., Haines, J. L., Parl, F. F., & Summar, M. L. (2004) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-03-0188 · Cited by 67 · see citing works
Chitambar, C. R., & Antholine, W. E. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4880 · Cited by 65 · see citing works
Yamamoto, M., Arimura, H., Fukushige, T., Minami, K., Nishizawa, Y., Tanimoto, A., Kanekura, T., Nakagawa, M., Akiyama, S., & Furukawa, T. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00865-13 · Cited by 65 · see citing works
Ojo, D., Wei, F., Liu, Y., Wang, E., Zhang, H., Lin, X., Wong, N., Bane, A. L., & Tang, D. (2015) · Current Medicinal Chemistry · doi:10.2174/0929867322666150416095744 · Cited by 62 · see citing works
Katchman, B. A., Antwi, K., Hostetter, G. H., Demeure, M. J., Watanabe, A. T., Decker, G. A., Miller, L. J., Hoff, D. D. V., & Lake, D. F. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0018 · Cited by 61 · see citing works
Kuo, Y., Su, T., Chen, H., Attieh, Z., Syed, B. A., McKie, A. T., Anderson, G. J., Gitschier, J. M., & Vulpe, C. D. (2004) · Gut · doi:10.1136/gut.2003.019026 · Cited by 60 · see citing works
Katchman, B. A., Ocal, I. T., Cunliffe, H. E., Chang, Y.-H. H., Hostetter, G. H., Watanabe, A. T., Lobello, J. R., & Lake, D. F. (2013) · Breast Cancer Research · doi:10.1186/bcr3407 · Cited by 58 · see citing works
Ogawara, Y., Katsumoto, T., Aikawa, Y., Shima, Y., Kagiyama, Y., Soga, T., Matsunaga, H., Seki, T., Araki, K., & Kitabayashi, I. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2200 · Cited by 58 · see citing works
Iron homeostasis and anemia markers in early breast cancer
Lamy, P., Durigova, A., & Jacot, W. (2014) · Clinica Chimica Acta · doi:10.1016/j.cca.2014.04.011 · Cited by 57 · see citing works
Iron regulatory proteins 1 and 2
Henderson, B. R. (1996) · BioEssays · doi:10.1002/bies.950180909 · Cited by 57 · see citing works
Schmitt, S., Saathoff, F., Meissner, L., Schropp, E.-M., Lichtmannegger, J., Schulz, S., Eberhagen, C., Borchard, S., Aichler, M., Adamski, J., et al. (2013) · Analytical Biochemistry · doi:10.1016/j.ab.2013.08.007 · Cited by 55 · see citing works
Tan, M. G. K., Kumarasinghe, P. M., Wang, S. M., Ooi, L. L., Aw, S. E., & Hui, K. M. (2009) · Experimental Biology and Medicine · doi:10.3181/0807-rm-227 · Cited by 55 · see citing works
Overexpression of iron regulatory protein 1 suppresses growth of tumor xenografts
Chen, G., Fillebeen, C., Wang, J., & Pantopoulos, K. (2006) · Carcinogenesis · doi:10.1093/carcin/bgl210 · Cited by 55 · see citing works
Down-regulation of iron regulatory protein 1 gene expression by nitric oxide
Oliveira, L., & Drapier, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120571797 · Cited by 51 · see citing works
Gottschling, S., Granzow, M., Kuner, R., Jauch, A. S., Herpel, E., Xu, E. C., Muley, T., Schnabel, P. A., Herth, F. J. F., & Meister, M. A. (2013) · Lung Cancer · doi:10.1016/j.lungcan.2012.12.015 · Cited by 49 · see citing works
Therapeutic Uses of Gallium Nitrate
Apseloff, G. (1999) · American Journal of Therapeutics · doi:10.1097/00045391-199911000-00008 · Cited by 49 · see citing works
Gallium nitrate in the treatment of bladder cancer
Einhorn, L. H. (2003) · Seminars in Oncology · doi:10.1016/s0093-7754(03)00174-x · Cited by 49 · see citing works
Treatment with gallium nitrate: Evidence for interference with iron metabolism in vivo
Seligman, P. A., Moran, P. L., Schleicher, R. B., & Crawford, E. D. (1992) · American Journal of Hematology · doi:10.1002/ajh.2830410403 · Cited by 49 · see citing works
Mollbrink, A., Jawad, R., Vlamis-Gardikas, A., Edenvik, P., Isaksson, B., Danielsson, O., Stål, P., & Fernandes, A. (2014) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463201402700204 · Cited by 48 · see citing works
Ferroportin/IREG-1/MTP-1/SLC40A1 modulates the uptake of iron at the apical membrane of enterocytes
Thomas, C. (2003) · Gut · doi:10.1136/gut.53.1.44 · Cited by 47 · see citing works
HIF1 Contributes to Hypoxia-Induced Pancreatic Cancer Cells Invasion via Promoting QSOX1 Expression
Shi, C., Fan, Y., Liu, B., & Lou, W. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000354460 · Cited by 46 · see citing works
Erythropoiesis and Iron Sulfur Cluster Biogenesis
Ye, H., & Rouault, T. A. (2010) · Advances in Hematology · doi:10.1155/2010/329394 · Cited by 44 · see citing works
Functional Analysis of GLRX5 Mutants Reveals Distinct Functionalities of GLRX5 Protein
Liu, G., Wang, Y., Anderson, G. J., Camaschella, C., Chang, Y., & Nie, G. (2015) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25267 · Cited by 43 · see citing works
Elevated Transcription of the Gene QSOX1 Encoding Quiescin Q6 Sulfhydryl Oxidase 1 in Breast Cancer
Soloviev, M., Esteves, M. P., Amiri, F., Crompton, M. R., & Rider, C. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057327 · Cited by 39 · see citing works
HIF2α reduces growth rate but promotes angiogenesis in a mouse model of neuroblastoma
Favier, J., Lapointe, S., Maliba, R., & Sirois, M. G. (2007) · BMC Cancer · doi:10.1186/1471-2407-7-139 · Cited by 38 · see citing works
Alterations in expression profile of iron-related genes in colorectal cancer
Hamara, K., Bielecka-Kowalska, A., Przybyłowska-Sygut, K., Sygut, A., Dziki, A. J., & Szemraj, J. (2013) · Molecular Biology Reports · doi:10.1007/s11033-013-2659-3 · Cited by 34 · see citing works
Agudo, A., Bonet, C., Sala, N., Muñoz, X., Aranda, N., Fonseca‐Nunes, A., Clavel‐Chapelon, F., Boutron‐Ruault, M., Vineis, P., Panico, S., et al. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt045 · Cited by 34 · see citing works
Effect of hypoxia on the binding and subcellular distribution of iron regulatory proteins
Christova, T. Y., & Templeton, D. M. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-006-9393-2 · Cited by 32 · see citing works
Redox control of iron regulatory protein 2 stability
Hausmann, A., Lee, J., & Pantopoulos, K. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.01.036 · Cited by 29 · see citing works
Luo, X., Hill, M., Johnson, A. A., & Latunde-Dada, G. O. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.08.012 · Cited by 24 · see citing works
QSOX1 Inhibits Autophagic Flux in Breast Cancer Cells
Poillet-Perez, L., Pernodet, N., Boyer‐Guittaut, M., Adami, P., Borg, C., Jouvenot, M., Delage-Mourroux, R., & Despouy, G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086641 · Cited by 21 · see citing works
Fehringer, G., Liu, G., Pintilie, M., Sykes, J. R., Cheng, D., Liu, G., Chen, Z., Seymour, L., Der, S. D., Shepherd, F. A., et al. (2012) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-1123-t · Cited by 21 · see citing works
Isocitrate dehydrogenase (IDH)2 R140Q mutation induces myeloid and lymphoid neoplasms in mice
Mylonas, E., Janin, M., Bawa, O., Opolon, P., David, M. D., Quivoron, C., Bernard, O., Ottolenghi, C., Debotton, S., & Penard‐Lacronique, V. (2014) · Leukemia · doi:10.1038/leu.2014.18 · Cited by 20 · see citing works
Haro, K. J., Sheth, A., & Scheinberg, D. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048841 · Cited by 19 · see citing works
Illuminating luminal B: QSOX1 as a subtype-specific biomarker
Das, P., Siegers, G. M., & Postovit, L.-M. M. (2013) · Breast Cancer Research · doi:10.1186/bcr3417 · Cited by 18 · see citing works
Kida, A., & Kahn, M. (2014) · Current Molecular Pharmacology · doi:10.2174/1874467207666140219121219 · Cited by 17 · see citing works
Zhen, Q., Liu, J., Liu, J.-B., Wang, R., Chu, W.-W., Zhang, Y.-X., Tan, G.-L., Zhao, X.-J., & Lv, B. (2015) · Cancer Biology & Therapy · doi:10.1080/15384047.2015.1016689 · Cited by 16 · see citing works
Expression level of quiescin sulfhydryl oxidase 1 (QSOX1) in neuroblastomas
Araújo, D. G. B., Nakao, L. S., Gozzo, P. D. C., Souza, C. D. A., Balderrama-Brondani, V., Gugelmin, E. S., Bom, A. P. K. P., Olandoski, M., & de Noronha, L. (2014) · European Journal of Histochemistry · doi:10.4081/ejh.2014.2228 · Cited by 16 · see citing works
Positive expression of HIF-2α/EPAS1 in invasive bladder cancer
Xia, G., Kageyama, Y., Hayashi, T., Hyochi, N., Kawakami, S., & Kihara, K. (2002) · Urology · doi:10.1016/s0090-4295(01)01607-7 · Cited by 15 · see citing works
Stimulation of non-transferrin iron uptake by iron deprivation in K562 cells
Kovár̆, J., Neubauerová, J., Cimburová, M., Truksa, J., Balušíková, K., & Horák, J. (2006) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2006.06.004 · Cited by 14 · see citing works
Self-citationIron and neoplasia: Serum transferrin receptor and ferritin in prostate cancer
Richardson, D. R. (2004) · Journal of Laboratory and Clinical Medicine · doi:10.1016/j.lab.2004.05.016 · Cited by 12 · see citing works
Zhao, Z., Li, C., Hu, M., Li, J., & Liu, R. (2014) · Tumor Biology · doi:10.1007/s13277-014-1978-x · Cited by 10 · see citing works
Sempos, C. T. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.2001.tb06961.x · Cited by 4 · see citing works
Molecular Diagnosis of Hereditary Hemochromatosis
Huber, S., & Voelkerding, K. V. (2003) · Humana Press eBooks · doi:10.1385/1-59259-081-0:439 · Cited by 1 · see citing works
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- [126]Kuhn LC Iron regulatory proteins and their role in controlling iron metabolism Metallomics 2015 7 232 243 25306858
- [131]Liuzzi JP Aydemir F Nam H Knutson MD Cousins RJ Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells Proc Natl Acad Sci USA 2006 103 13612 13617 16950869 PMC1564235
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Ngo, B., Van Riper, J. M., Cantley, L. C., & Yun, J. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0135-7 · Cited by 423 · see citing works
Transferrin receptor 1 in cancer: a new sight for cancer therapy.
Shen, Y., Li, X., Dong, D., Zhang, B., Xue, Y., & Shang, P. (2018) · Europe PMC (PubMed Central) · Cited by 357 · see citing works
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Roemhild, K., von Maltzahn, F., Weiskirchen, R., Knüchel, R., von Stillfried, S. F., & Lammers, T. (2021) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2021.05.001 · Cited by 315 · see citing works
Hong, X., Roh, W., Sullivan, R. J., Wong, K. H. K., Wittner, B. S., Guo, H., Dubash, T. D., Sade-Feldman, M., Wesley, B., Horwitz, E. P., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-1500 · Cited by 237 · see citing works
Torti, S. V., & Torti, F. M. (2020) · Cancer Research · doi:10.1158/0008-5472.can-20-2017 · Cited by 176 · see citing works
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El-Hout, M., Santos, L. D., Hamaï, A., & Mehrpour, M. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.07.009 · Cited by 170 · see citing works
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Boretti, A. A., & Banik, B. K. (2020) · PharmaNutrition · doi:10.1016/j.phanu.2020.100190 · Cited by 168 · see citing works
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Wu, X., Liu, H., Han, D., Peng, B., Zhang, H., Zhang, L., Li, J., Liu, J., Cui, C., Fang, S., et al. (2019) · Journal of the American Chemical Society · doi:10.1021/jacs.9b03720 · Cited by 158 · see citing works
Sandoval-Acuña, C., Torrealba, N., Tomková, V., Jadhav, S. B., Blažková, K., Merta, L., Lettlová, S., Adamcova, M. K., Rösel, D., Brábek, J., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-1628 · Cited by 158 · see citing works
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Recalcati, S., Gammella, E., & Cairo, G. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.07.015 · Cited by 107 · see citing works
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Drozdov, A. S., Nikitin, P. I., & Rozenberg, J. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222313011 · Cited by 62 · see citing works
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Neiveyans, M., Melhem, R., Arnoult, C., Bourquard, T., Jarlier, M., Busson, M., Laroche, A., Cérutti, M., Pugnière, M., Ternant, D., et al. (2019) · mAbs · doi:10.1080/19420862.2018.1564510 · Cited by 28 · see citing works
Isola, S., Gammeri, L., Furci, F., Gangemi, S., Pioggia, G., & Allegra, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137284 · Cited by 27 · see citing works
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Yu, R., Hang, Y., Tsai, H., Wang, D., & Zhu, H. (2024) · Cancer Cell International · doi:10.1186/s12935-024-03329-x · Cited by 25 · see citing works
Engineered stem cells targeting multiple cell surface receptors in tumors
Kavari, S. L., & Shah, K. (2019) · Stem Cells · doi:10.1002/stem.3069 · Cited by 22 · see citing works
Abuzaid, H., Abdelrazig, S., Ferreira, L., Collins, H. M., Kim, D., Lim, K., Kam, T., Turyanska, L., & Bradshaw, T. D. (2022) · ACS Omega · doi:10.1021/acsomega.2c00997 · Cited by 22 · see citing works
Wang, F., Wu, W., Hsiu, W.-S., Liu, Y.-J., & Chuang, K.-W. (2019) · Metabolites · doi:10.3390/metabo10010016 · Cited by 20 · see citing works
Hsu, T., Su, Y., Chen, H., Liao, P., Shen, S. C., Tsai, K., Wang, T.-H., Chen, A., Huang, C., Shibu, M. A., et al. (2023) · Aging · doi:10.18632/aging.204867 · Cited by 19 · see citing works
Characterization of human frataxin missense variants in cancer tissues
Petrosino, M., Pasquo, A., Novak, L., Toto, A., Gianni, S., Mantuano, E., Veneziano, L., Minicozzi, V., Pastore, A., Puglisi, R., et al. (2019) · Human Mutation · doi:10.1002/humu.23789 · Cited by 19 · see citing works
Agrawal, P., Chen, S., de Pablos, A. D., Vadlamudi, Y., Vand-Rajabpour, F., Jame-Chenarboo, F., Kar, S., Yanke, A., Berico, P., de Vega, E. M. S., et al. (2025) · Science Advances · doi:10.1126/sciadv.adg3481 · Cited by 12 · see citing works
Iron Metabolism in Cancer and Senescence: A Cellular Perspective
Crescenzi, E., Leonardi, A., & Pacifico, F. (2023) · Biology · doi:10.3390/biology12070989 · Cited by 18 · see citing works
Wang, F., Xu, W., Zhang, W., Xu, R.-C., Sun, J., Zhang, G., Liu, Z., Qi, Z., Dong, L., Weng, S., et al. (2023) · Hepatology International · doi:10.1007/s12072-023-10607-9 · Cited by 15 · see citing works
Moon, S. J., Kim, J. H., Kong, S. H., & Shin, C. S. (2020) · Endocrinology and Metabolism · doi:10.3803/enm.2020.35.1.132 · Cited by 15 · see citing works
Therapy-resistant nature of cancer stem cells in view of iron metabolism
Wang, W., Tabu, K., Aimaitijiang, A., & Taga, T. (2022) · Inflammation and Regeneration · doi:10.1186/s41232-022-00220-y · Cited by 14 · see citing works
Upregulated Expression of CYBRD1 Predicts Poor Prognosis of Patients with Ovarian Cancer
Chen, R., Cao, J., Jiang, W., Wang, S., & Cheng, J. (2021) · Journal of Oncology · doi:10.1155/2021/7548406 · Cited by 14 · see citing works
Cao, J., Hu, C., Xu, J., Han, J., Zhang, R., Cao, M., Li, Y., & Xu, Z. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/4257342 · Cited by 13 · see citing works
Article review: Brazilin as potential anticancer agent
Raptania, C. N., Zakia, S., Fahira, A. I., & Amalia, R. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1355533 · Cited by 13 · see citing works
Role of the human cytochrome b561 family in iron metabolism and tumors (Review)
Zhou, X., An, Z., Lei, H., Liao, H., & Guo, X. (2024) · Oncology Letters · doi:10.3892/ol.2024.14857 · Cited by 12 · see citing works
Tran, T. T., Gunathilake, M. N., Lee, J., Choi, I. J., Kim, Y., & Kim, J. (2021) · Nutrients · doi:10.3390/nu13082600 · Cited by 12 · see citing works
Yang, Y., Ning, Y., Chen, Y., Tian, T., Gao, X., Kong, Y., Lei, K., & Cui, Z. (2025) · Cancer Science · doi:10.1111/cas.70015 · Cited by 11 · see citing works
Iron chelators as mitophagy agents: Potential and limitations
Brogyányi, T., Kejík, Z., Veselá, K., Dytrych, P., Hoskovec, D., Masařík, M., Babula, P., Kaplánek, R., Přibyl, T., Zelenka, J., et al. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117407 · Cited by 10 · see citing works
Greenshields, A. L., Coombs, M. R. P., Fernando, W., Holbein, B. E., & Hoskin, D. W. (2019) · BioMetals · doi:10.1007/s10534-019-00222-3 · Cited by 9 · see citing works
Ren, G., Zhou, J., Su, Y., Yang, Q., & Li, J. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1567216 · Cited by 9 · see citing works
Puzzling out iron complications in cancer drug resistance
Abedi, M., & Rahgozar, S. (2022) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2022.103772 · Cited by 8 · see citing works
Hema Naveena, A., & Bhatia, D. D. (2023) · ChemBioChem · doi:10.1002/cbic.202300506 · Cited by 7 · see citing works
Gong, H., Li, Z., Wu, Z., Lian, G., & Su, Z. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.155042 · Cited by 7 · see citing works
Wang, W., Hua, S., Li, J., Zhao, J., Zhang, Y., Jiang, J., & Han, B. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1081091 · Cited by 7 · see citing works
Ramberg, S., & Andreassen, R. (2021) · Non-Coding RNA · doi:10.3390/ncrna7040061 · Cited by 6 · see citing works
Qing, M., Zhou, J., Chen, W., & Cheng, L. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/2793222 · Cited by 5 · see citing works
Decoding iron deficiency in cancer: mechanisms, immune modulation, and therapeutic potential
Lin, L., Yin, X., & Guan, Y. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1650929 · Cited by 7 · see citing works
Transmetalation in Cancer Pharmacology
Dharmasivam, M., & Kaya, B. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262211008 · Cited by 5 · see citing works
Protein-Decorated Microbubbles for Ultrasound-Mediated Cell Surface Manipulation
Brans, V. A., Gray, M. D., Sezgin, E., & Stride, E. (2023) · ACS Applied Bio Materials · doi:10.1021/acsabm.3c00861 · Cited by 4 · see citing works
Release of a novel peptide from ferritin nanocages: A new tool for therapeutic applications
Canè, C., Lucignano, R., Somma, A. D., Liccardo, M., Iannuzzi, C., Duilio, A., & Picone, D. (2023) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2023.130525 · Cited by 4 · see citing works
Jadhav, S. B., Sandoval-Acuña, C., Pacior, Y., Potomova, P., Klanicová, K., Blažková, K., Sedláček, R., Štursa, J., Werner, L., & Truksa, J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.17.575692 · Cited by 4 · see citing works
Self-citationProgress and potential of ferritin nanocages for cancer drug delivery
Giacobbo, V., Gorgoglione, F., Sevieri, M., Bignami, B., Tagliolini, I., Corsi, F., & Mazzucchelli, S. (2025) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2025.2584632 · Cited by 3 · see citing works
A fistful of iron: ferritin as a vulnerability point of the brain cancers
Segui, F., Parks, S. K., Vučetić, M., & Picco, V. (2026) · Cell Death and Disease · doi:10.1038/s41419-026-08564-w · Cited by 3 · see citing works
Bhat, A. A., Thapa, R., Fuloria, S., Karupiah, S., Veerasamy, R., Perveen, N., & Fuloria, N. K. (2026) · Critical Reviews in Analytical Chemistry · doi:10.1080/10408347.2026.2680160 · Cited by 3 · see citing works
Singh, R., Parchwani, D. N., Sharma, G., & Sharma, P. (2025) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-025-01341-0 · Cited by 3 · see citing works
Sultan, G., & Zubair, S. (2023) · Computational Biology and Chemistry · doi:10.1016/j.compbiolchem.2023.107999 · Cited by 3 · see citing works
Transferrin Receptor and Targeting Strategies
Joshi, H. A., Attar, E. S., Dandekar, P. P., & Devarajan, P. V. (2019) · AAPS advances in the pharmaceutical sciences series · doi:10.1007/978-3-030-29168-6_16 · Cited by 3 · see citing works
Cömertpay, B., Gülfidan, G., Arğa, K. Y., & Göv, E. (2021) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2021.0021 · Cited by 3 · see citing works
Winnberg, J. S., Vermani, L., Liu, W., Soller, V., Thutkawkorapin, J., Lindblad, M., & Lindblom, A. (2024) · Hereditary Cancer in Clinical Practice · doi:10.1186/s13053-024-00299-z · Cited by 2 · see citing works
Iron Vulnerability of Cancer Stem Cells
Nengroo, M. A., Sinha, A., & Datta, D. B. (2022) · Handbook of Oxidative Stress in Cancer: Therapeutic Aspects · doi:10.1007/978-981-16-5422-0_235 · Cited by 2 · see citing works
Radak, M., Ghamari, N., & Fallahi, H. (2023) · Biosystems · doi:10.1016/j.biosystems.2023.105093 · Cited by 2 · see citing works
Balligand, T., Carpenet, C., Olive-Palau, S., Jaspers, T., Suresh, P., Liu, X., Medhi, H., Lee, Y. H., Rashidian, M., Strooper, B. D., et al. (2025) · eLife · doi:10.7554/elife.104302 · Cited by 2 · see citing works
Metal Ion Binding in Wild-Type and Mutated Frataxin: A Stability Study
Morante, S., Botticelli, S., Chiaraluce, R., Consalvi, V., Penna, G. L., Novak, L., Pasquo, A., Petrosino, M., Proux, O., Rossi, G. C., et al. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.878017 · Cited by 1 · see citing works
ROS Modulation by Iron Chelators and Lipids: A Developing Anticancer Strategy
Kakhlon, O. (2021) · Springer eBooks · doi:10.1007/978-981-15-4501-6_129-1
Iron Vulnerability of Cancer Stem Cells
Nengroo, M. A., Sinha, A., & Datta, D. B. (2021) · Handbook of Oxidative Stress in Cancer: Therapeutic Aspects · doi:10.1007/978-981-16-1247-3_235-1
ROS Modulation by Iron Chelators and Lipids: A Developing Anticancer Strategy
Kakhlon, O. (2022) · Springer eBooks · doi:10.1007/978-981-15-9411-3_129
Yang, Y., Fu, X., & Yang, Y. (2022) · Research Square · doi:10.21203/rs.3.rs-1478458/v1
Yang, Y., Fu, X., & Yang, Y. (2022) · Research Square · doi:10.21203/rs.3.rs-1478458/v2
Lipid Nanocarriers for Breast Cancer Treatment
Lopes, L. B., Apolinário, A. C., Salata, G. C., Malagó, I. D., & Passos, J. S. (2022) · Springer eBooks · doi:10.1007/978-3-031-17831-3_1
Folia Pharmaceutica Universitatis Carolinae LI
Opletalová, V., Vojtíšek, T., & Doležal, M. (2024) · Karolinum Press eBooks · doi:10.14712/9788024656663
Feng, G., Arima, Y., Midorikawa, K., Kobayashi, H., Oikawa, S., Zhao, W., Zhang, Z., Takeuchi, K., & Murata, M. (2023) · Figshare · doi:10.6084/m9.figshare.24054390
Feng, G., Arima, Y., Midorikawa, K., Kobayashi, H., Oikawa, S., Zhao, W., Zhang, Z., Takeuchi, K., & Murata, M. (2023) · Figshare · doi:10.6084/m9.figshare.24054384
Balligand, T., Carpenet, C., Olive-Palau, S., Jaspers, T., Suresh, P., Liu, X., Medhi, H., Lee, Y. H., Rashidian, M., Strooper, B. D., et al. (2025) · eLife · doi:10.7554/elife.104302.3
Balligand, T., Carpenet, C., Olive-Palau, S., Jaspers, T., Suresh, P., Liu, X., Medhi, H., Lee, Y. H., Rashidian, M., Strooper, B. D., et al. (2025) · eLife · doi:10.7554/elife.104302.1
TFRC Expression in Endometrial Cancer Tissues and Its Prognostic Value
米, 婷. (2025) · Advances in Clinical Medicine · doi:10.12677/acm.2025.152329
Balligand, T., Carpenet, C., Olive-Palau, S., Jaspers, T., Suresh, P., Liu, X., Medhi, H., Lee, Y. H., Rashidian, M., Strooper, B. D., et al. (2025) · eLife · doi:10.7554/elife.104302.2
Feng, G., Arima, Y., Midorikawa, K., Kobayashi, H., Oikawa, S., Zhao, W., Zhang, Z., Takeuchi, K., & Murata, M. (2023) · Figshare · doi:10.6084/m9.figshare.24054387
Feng, G., Arima, Y., Midorikawa, K., Kobayashi, H., Oikawa, S., Zhao, W., Zhang, Z., Takeuchi, K., & Murata, M. (2023) · Figshare · doi:10.6084/m9.figshare.24054393
Rôle de l'autophagie dans l'émergence des cellules souches cancéreuses : implication du métabolisme
El-Hout, M. (2019) · theses.fr (ABES) · doi:10.70675/881cf980z01caz4a56z8a81zdcebe1247536
Liu, C., Peng, Q., Zhang, X., Li, Z., Wu, Y., Wen, Y., Zheng, R., Wu, S.-Z., Zhou, C., Hu, Z., et al. (2026) · Advanced Science · doi:10.1002/advs.202520109
- Authors
- Rychtarcikova, Z., Lettlova, S., Tomkova, V., Korenkova, V., Langerova, L., Simonova, E., Zjablovskaja, P., Alberich-Jorda, M., Neuzil, J., & Truksa, J.
- Affiliations
- Institute of Biotechnology, Czech Academy of Sciences, Prague, Czech Republic
- Czech Academy of Sciences (CZ)
- Institute of Molecular Genetics, Czech Academy of Sciences, Prague, Czech Republic
- ORCID
- Truksa, Jaroslav
- Venue
- Oncotarget
- Publisher
- Impact Journals, LLC
- Published
- 2016-12-22
- Volume
- 8
- Issue
- 4
- Pages
- 6376-6398
- ISSN
- 1949-2553 (ISSN-L)
- PMC
- PMC5351639
- OpenAlex
- W2561157023
- Cited by
- 100
- References
- 142
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 10 · 2023: 13 · 2022: 14 · 2021: 13 · 2020: 10 · 2019: 15 · 2018: 6 · 2017: 2
- FWCI
- 7.29
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- cc-by
- Locations
- Oncotarget (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Griffith Research Online (submittedVersion, cc-by)
- Funders
- Grantová Agentura České Republiky (GA13-28830S, GA15-03796S)
- Kellner Family Foundation
- Topics
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Ferroptosis and cancer prognosis
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- cancer stem cells, breast cancer, prostate cancer, iron metabolism, iron-sulfur clusters, labile iron pool, mitochondrial iron accumulation, iron chelation, aconitase, glutathione, hypoxia response, ABCB10, EPAS1, gene expression signatures, iron absorption, iron storage
- MeSH terms
- Animals, Antineoplastic Agents, Biological Transport, Breast Neoplasms, Dose-Response Relationship, Drug, Female, Humans, Iron, Iron Chelating Agents, Male, Mice, Transgenic, Mitochondria, Phenotype, Prostatic Neoplasms, Tamoxifen, Neoplastic Stem Cells, Leukemia, Promyelocytic, Acute, Gene Expression Regulation, Enzymologic, Gene Expression Regulation, Neoplastic, Spheroids, Cellular, Drug Resistance, Neoplasm, Gene Expression Profiling, Principal Component Analysis, Transcriptome, MCF-7 Cells
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