Estrogen-dependent disruption of intracellular iron metabolism augments the cytotoxic effects of doxorubicin in select breast and ovarian cancer cells

References

• Tacar O, Sriamornsak P, Dass CR. Dox: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol. 2013;65:157–170. doi:10.1111/j.2042-7158.2012.01567.x23278683
   PubMed Web of Science ®Google Scholar
• Fornari FA, Randolph JK, Yalowich JC, Ritke MK, Gewirtz DA. Interference by Dox with DNA unwinding in MCF-7 breast tumor cells. Mol Pharmacol. 1994;45:649–656.8183243
   PubMed Web of Science ®Google Scholar
• Momparler RL, Karon M, Siegel SE, Avila F. Effect of adriamycin on DNA, RNA, and protein synthesis in cell-free systems and intact cells. Cancer Res. 1976;8:2891–2895.
   Google Scholar
• Pommier Y, Leo E, Zhang H, Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol. 2010;5:421–443. doi:10.1016/j.chembiol.2010.04.012
   Google Scholar
• May PM, Williams GK, Williams DR. Solution chemistry studies of adriamycin–iron complexes present in vivo. Eur J Cancer. 1980;16:1275–1276.7227451
   PubMed Web of Science ®Google Scholar
• Xu X, Persson HL, Richardson DR. Molecular pharmacology of the interaction of anthracyclines with iron. Mol Pharmacol. 2005;68:261–271. doi:10.1124/mol.105.01338315883202
   PubMed Web of Science ®Google Scholar
• Doroshow JH. Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Proc Natl Acad Sci USA. 1986;83:4514–4518.3086887
   PubMed Web of Science ®Google Scholar
• Gewirtz DA. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol. 1999;57:727–741.10075079
   PubMed Web of Science ®Google Scholar
• World Health Organization. Model list of essential medicines, 20th list, 2017. Available from: http\\:www.who.int/medicines/publications/essentialmedicines/20th. Accessed 321, 2018.
   Google Scholar
• Chatterjee K, Zhang J, Honbo N, Karliner JS. Dox cardiomyopathy. Cardiology. 2010;115:155–162. doi:10.1159/00026516620016174
   PubMed Web of Science ®Google Scholar
• Minotti G, Recalcati S, Menna P, Salvatorelli E, Corna G, Cairo G. Dox cardiotoxicity and the control of iron metabolism: quinone-dependent and independent mechanisms. Methods Enzymol. 2004;378:340–361. doi:10.1016/S0076-6879(04)78025-815038979
   PubMed Web of Science ®Google Scholar
• Gammella E, Maccarinelli F, Buratti P, Recalcati SS, Cairo G. The role of iron in anthracycline cardiotoxicity. Front Pharmacol. 2014;5:25. doi:10.3389/fphar.2014.0002524616701
   PubMed Web of Science ®Google Scholar
• Swain SM, Whaley FS, Gerber MC, et al. Cardio-protection with dexrazoxane for Dox-containing therapy in advanced breast cancer. J Clin Oncol. 1997;15:1318–1332. doi:10.1200/JCO.1997.15.4.13189193323
   PubMed Web of Science ®Google Scholar
• Hershko C, Link G, Tzahor M, et al. Anthracycline toxicity is potentiated by iron and inhibited by deferoxamine: studies in rat heart cells in culture. J Lab Clin Med. 1993;122:245–251.8409700
   PubMed Web of Science ®Google Scholar
• Link G, Tirosh R, Pinson A, Hershko C. Role of iron in the potentiation of anthracycline cardiotoxicity: identification of heart cell mitochondria as a major site of iron–anthracycline interaction. J Lab Clin Med. 1996;127:272–278.9273360
   PubMed Web of Science ®Google Scholar
• Panjrath GS, Patel V, Valdiviezo CI, Narula N, Narula J, Jain D. Potentiation of doxorubicin cardiotoxicity by iron loading in a rodent model. J Am Coll Cardiol. 2007;49:2457–2464. doi:10.1016/j.jacc.2007.02.06017599610
   PubMed Web of Science ®Google Scholar
• Gehl J, Boesgaard M, Paaske T, Vittrup Jensen B, Dombernowsky P. Combined Dox and paclitaxel in advanced breast cancer: effective and cardiotoxic. Ann Oncol. 1996;7:687–693.8905026
   PubMed Web of Science ®Google Scholar
• Richly H, Schultheis B, Adamietz IA, et al. Combination of sorafenib and Dox in patients with advanced hepatocellular carcinoma: results from a phase I extension trial. Eur J Cancer. 2009;45:579–587. doi:10.1016/j.ejca.2008.10.03919101137
   PubMed Web of Science ®Google Scholar
• Wendel H, De Stanchina E, Fridman J, et al. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature. 2004;428:332–337. doi:10.1038/nature0236915029198
   PubMed Web of Science ®Google Scholar
• Xiong W, Wang L, Yu F. Regulation of cellular iron metabolism and its implications in lung cancer progression. Med Oncol. 2014;31:28. doi:10.1007/s12032-014-0028-224861923
   PubMed Web of Science ®Google Scholar
• Kalousová M, Krechler T, Jáchymová M, Kuběna AA, Žák A, Zima T. Ferritin as an independent mortality predictor in patients with pancreas cancer. Results of a pilot study. Tumour Biol. 2012;33:1695–1700. doi:10.1007/s13277-012-0426-z22875781
   PubMed Web of Science ®Google Scholar
• Osborne NJ, Gurrin LC, Allen KJ, et al. HFE C282Y homozygotes are at increased risk of breast and colorectal cancer. Hepatology. 2010;51:1311–1318. doi:10.1002/hep.2344820099304
   PubMed Web of Science ®Google Scholar
• Xue X, Taylor M, Anderson E, et al. Hypoxia-inducible factor-2alpha activation promotes colorectal cancer progression by dysregulating iron homeostasis. Cancer Res. 2012;72:2285–2293. doi:10.1158/0008-5472.CAN-11-383622419665
   PubMed Web of Science ®Google Scholar
• Pinnix ZK, Miller LD, Wang W, et al. Ferroportin and iron regulation in breast cancer progression and prognosis. Sci Transl Med. 2010;2:43ra56 3001127. doi:10.1126/scisignal.3001127
   Web of Science ®Google Scholar
• Shpyleva SI, Tryndyak VP, Kovalchuk O, et al. Role of ferritin alterations in human breast cancer cells. Breast Cancer Res Treat. 2011;126:63–71. doi:10.1007/s10549-010-0849-420390345
   PubMedGoogle Scholar
• Torti SV, Torti FM. Cellular iron metabolism in prognosis and therapy of breast cancer. Crit Rev Oncog. 2013;18:435–448.23879588
   PubMedGoogle Scholar
• Torti SV, Torti FM. Iron and cancer: more ore to be mined. Nat Rev Cancer. 2013;13:342–355. doi:10.1038/nrc349523594855
   PubMed Web of Science ®Google Scholar
• Richardson DR, Kalinowski DS, Lau S, Jansson PJ, Lovejoy DB. Cancer cell iron metabolism and the development of potent iron chelators as anti-tumour agents. Biochim Biophys Acta. 2009;1790:702–717. doi:10.1016/j.bbagen.2008.04.00318485918
   PubMed Web of Science ®Google Scholar
• Yalovenko TM, Todor IM, Lukianova NY, Chekhun VF. Hepcidin as a possible marker in determination of malignancy degree and sensitivity of breast cancer cells to cytostatic drugs. Exp Oncol. 2016;38:84–88.27356575
   PubMedGoogle Scholar
• Chekhun VF, Lukyanova NY, Burlaka AP, et al. Iron metabolism disturbances in the MCF-7 human breast cancer cells with acquired resistance to doxorubicin and cisplatin. Int J Oncol. 2013;43:1481–1486. doi:10.3892/ijo.2013.206323969999
   PubMed Web of Science ®Google Scholar
• Bajbouj K, Shafarin J, Allam H, et al. Elevated levels of estrogen suppress hepcidin synthesis and enhance serum iron availability in premenopausal women. Exp Clin Endocrinol Diabetes. 2018;126:453–459. doi:10.1055/s-0043-12407729396964
   PubMed Web of Science ®Google Scholar
• Bajbouj K, Shafarin J, Abdalla MY, Ahmad IM, Hamad M. Estrogen-induced disruption of intracellular iron metabolism leads to oxidative stress, membrane damage, and cell cycle arrest in MCF-7 cells. Tumour Biol. 2017;39:1010428317726184. doi:10.1177/101042831772618429022497
   PubMedGoogle Scholar
• Shafarin J, Bajbouj K, El-Serafy A, Sandeep S, Hamad M. Estrogen-dependent downregulation of hepcidin synthesis induces intracellular iron efflux in cancer cells in vitro. Biol Med. 2016;8:356–363. doi:10.4172/0974-8369.1000356
   Google Scholar
• Prus E, Fibach E. Flow cytometry measurement of the labile iron pool in human hematopoietic cells. Cytometry A. 2008;73:22–27. doi:10.1002/cyto.a.2049118044720
   PubMed Web of Science ®Google Scholar
• Ingle JN, Ahmann DL, Green SJ, et al. Randomized clinical trial of diethylstilbestrol versus tamoxifen in postmenopausal women with advanced breast cancer. N Engl J Med. 1981;304:16–21. doi:10.1056/NEJM1981010130401047001242
   PubMed Web of Science ®Google Scholar
• LaCroix AZ, Chlebowski RT, Manson JE, et al. Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial. JAMA. 2011;305:1305–1314. doi:10.1001/jama.2011.38221467283
   PubMed Web of Science ®Google Scholar
• Jordan CV. The new biology of estrogen-induced apoptosis applied to treat and prevent breast cancer. Endocr Relat Cancer. 2015;22:R1–R31. doi:10.1530/ERC-14-044825339261
   PubMed Web of Science ®Google Scholar
• Mobley JA, Brueggemeier RW. Estrogen receptor-mediated regulation of oxidative stress and DNA damage in breast cancer. Carcinogenesis. 2004;25:3–9. doi:10.1093/carcin/bgg17514514655
   PubMed Web of Science ®Google Scholar
• Kuo LJ, Yang L. γ-H2A: a novel biomarker for DNA double-strand breaks. In Vivo. 2008;22:305–310.18610740
   PubMed Web of Science ®Google Scholar
• Tarasewicz E, Hamdan R, Straehla J, et al. CDK4 inhibition and doxorubicin mediate breast cancer cell apoptosis through Smad3 and survivin. Cancer Biol Ther. 2014;15:1301–1311. doi:10.4161/cbt.2969325006666
   PubMed Web of Science ®Google Scholar
• Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther. 2006;5:1087–1098. doi:10.1158/1535-7163.MCT-05-037516731740
   PubMed Web of Science ®Google Scholar
• Zhang Y, Hunter T. Roles of Chk1 in cell biology and cancer therapy. Int J Cancer. 2014;134:1013–1023. doi:10.1002/ijc.2822623613359
   PubMed Web of Science ®Google Scholar
• Patil M, Pabla N, Dong Z. Checkpoint kinase 1 in DNA damage response and cell cycle regulation. Cell Mol Life Sci. 2013;70:4009–4021. doi:10.1007/s00018-013-1307-323508805
   PubMed Web of Science ®Google Scholar
• Meuth M. Chk1 suppressed cell death. Cell Div. 2010;5:21. doi:10.1186/1747-1028-5-2120813042
   PubMed Web of Science ®Google Scholar
• Liu Q, Guntuku S, Cui XS, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Develop. 2000;14:1448–1459.10859164
   PubMed Web of Science ®Google Scholar
• Goto H, Izawa I, Li P, Inagaki M. Novel regulation of checkpoint kinase 1: is checkpoint kinase 1 a good candidate for anti-cancer therapy? Cancer Sci. 2012;103:1195–1200. doi:10.1111/j.1349-7006.2012.02280.x22435685
   PubMed Web of Science ®Google Scholar
• Gergely P, Niland B, Gonchoroff N, Pullmann R Jr, Phillips PE, Perl A. Persistent mitochondrial hyperpolarization, increased reactive oxygen intermediate production, and cytoplasmic alkalinization characterize altered IL-10 signaling in patients with systemic lupus erythematosus. J Immunol. 2002;169:1092–1100.12097418
   PubMed Web of Science ®Google Scholar
• Hua K, Din J, Cao Q, et al. Estrogen and progestin regulate HIF-1alpha expression in ovarian cancer cell lines via the activation of Akt signaling transduction pathway. Oncol Report. 2009;21:893–898.
   PubMed Web of Science ®Google Scholar
• Kazi AA, Molitoris KH, Koos RD. Estrogen rapidly activates the PI3K/AKT pathway and hypoxia-inducible factor 1 and induces vascular endothelial growth factor A expression in luminal epithelial cells of the rat uterus. Biol Reprod. 2009;81: 378–378. doi:10.1095/biolreprod.109.076117
   PubMed Web of Science ®Google Scholar
• Yang Q, Jian J, Katz S, Abramson SB, Huang X. 17β-estradiol inhibits iron hormone hepcidin through an estrogen responsive element half-site. Endocrinol. 2012;153:3170–3178. doi:10.1210/en.2011-2045
   PubMed Web of Science ®Google Scholar
• Hou Y, Zhang S, Wang L, et al. Estrogen regulates iron homeostasis through governing hepatic hepcidin expression via an estrogen response element. Genetics. 2012;511:398–403.
   Google Scholar
• Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL. Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol. 2012;52:1213–1225. doi:10.1016/j.yjmcc.2012.03.00622465037
   PubMed Web of Science ®Google Scholar
• Canzoneri JC, Oyelere AK. Interaction of anthracyclines with iron responsive element mRNAs. Nucleic Acids Res. 2008;36:6825–6834. doi:10.1093/nar/gkn77418953029
   PubMed Web of Science ®Google Scholar
• Brazzolott X, Andriollo M, Guiraud P, Favier A, Moulis JM. Interactions between doxorubicin and the human iron regulatory system. Biochim Biophys Acta. 2003;1593:209–218. doi:10.1016/S0167-4889(02)00391-912581865
   PubMed Web of Science ®Google Scholar
• Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: molecular control of mammalian iron metabolism. Cell. 2004;117:285–297.15109490
   PubMed Web of Science ®Google Scholar
• Barabas K, Faulk WP. Transferrin receptors associate with drug resistance in cancer cells. Biochem Biophys Res Commun. 1993;197:702–708. doi:10.1006/bbrc.1993.25367903529
   PubMed Web of Science ®Google Scholar
• Rahbar AM, Fenselau C. Unbiased examination of changes in plasma membrane proteins in drug resistant cancer cells. J Proteome Res. 2005;4:2148–2153. doi:10.1021/pr050237016335961
   PubMed Web of Science ®Google Scholar
• Habashy HO, Powe DG, Staka CM, et al. Transferrin receptor (CD71) is a marker of poor prognosis in breast cancer and can predict response to tamoxifen. Breast Cancer Res Treat. 2010;119:283–293. doi:10.1007/s10549-009-0345-x19238537
   PubMed Web of Science ®Google Scholar
• Chitambar CR. Gallium nitrate for the treatment of non-Hodgkin’s lymphoma. Drugs. 2004;13:531–541.
   Web of Science ®Google Scholar
• Kang HC. Identification of genes with differential expression in acquired drug-resistant gastric cancer cells using high-density oligonucleotide microarrays. Clin Cancer Res. 2004;10:272–284.14734480
   PubMed Web of Science ®Google Scholar
• Chitambar CR, Wereley JP. Resistance to the antitumor agent gallium nitrate in human leukemic cells is associated with decreased gallium/iron uptake, increased activity of iron regulatory protein-1, and decreased ferritin production. J Biol Chem. 1997;272:12151–12157.9115286
   PubMed Web of Science ®Google Scholar
• O’Donnell AJM, Macleod KG, Burns DJ, Smyth JF, Langdon SP. Estrogen receptor-α mediates gene expression changes and growth response in ovarian cancer cells exposed to estrogen. Endo Relat Cancer. 2005;12:851–866. doi:10.1677/erc.1.01039
   PubMed Web of Science ®Google Scholar
• Li L, Li X, Han X, et al. An ovarian cancer model with positive ER: reversion of ER antagonist resistance by Src blockade. Oncol Rep. 2014;32:943–950. doi:10.3892/or.2014.328424968896
   PubMed Web of Science ®Google Scholar
• Ford CH, Al-Bader M, Al-Ayadhi B, Francis I. Reassessment of estrogen receptor expression in human breast cancer cell lines. Anticancer Res. 2011;31:521–527.21378333
   PubMed Web of Science ®Google Scholar
• Moggs JG, Murphy TC, Lim FL, et al. Anti-proliferative effect of estrogen in breast cancer cells that re-express ERα is mediated by aberrant regulation of cell cycle genes. J Mol Endocrinol. 2005;34:535–551. doi:10.1677/jme.1.0177015821115
   PubMed Web of Science ®Google Scholar
• Prossnitz ER, Arterburn JB, Sklar LA. GPR30: a G protein-coupled receptor for estrogen. Mol Cell Endocrinol. 2007;265–266:138–142. doi:10.1016/j.mce.2006.12.010
   PubMed Web of Science ®Google Scholar