Interactions between doxorubicin and the human iron regulatory system

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1593, Issue 2-3, 2003, Pages 209-218

  Brazzolotto, Xavier ^a   Andriollo, Maud ^b   Guiraud, Pascale ^b   Favier, Alain ^b   Moulis, Jean Marc ^a  

^a CEA GRENOBLE   (France)

^b UNIV GRENOBLE ALPES   (France)

Author keywords

Anthracycline; Formaldehyde; Glutathione; Iron chelation; Iron regulation; Resistance mechanism

Indexed keywords

DOXORUBICIN; IRON; IRON REGULATORY FACTOR; RNA;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CONTROLLED STUDY; CYTOSOLIC FRACTION; DRUG EFFECT; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; IRON METABOLISM; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING;

EID: 1342335858     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4889(02)00391-9     Document Type: Article

References (53)

1. Olson R.D., Mushlin P.S. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 4:1990;3076-3086.
2. Gewirth D.A. A critical evaluation of the mechanism of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57:1999;727-741.
3. Kang Y.J., Zhou Z.-X., Wang G.-W., Buridi A., Klein J.B. Suppression by metallothionein of doxorubicin-induced cardiomyocyte apoptosis through inhibition of p38 mitogen-activated protein kinases. J. Biol. Chem. 275:2000;13690-13698.
4. Singal P.K., Li T., Kumar D., Danelisen I., Iliskovic N. Adriamycin-induced heart failure: mechanism and modulation. Mol. Cell. Biochem. 207:2000;77-85.
5. Weiss G., Loyevsky M., Gordeuk V.R. Dexrazoxane. Gen. Pharmacol. 32:1999;155-158.
6. Minotti G., Cairo G., Monti E. Role of iron in anthracycline cardiotoxicity: new tunes for an old song? FASEB J. 13:1999;199-212.
7. Minotti G., Ronchi R., Salvatorelli E., Menna P., Cairo G. Doxorubicin irreversibly inactivates Iron Regulatory Proteins 1 and 2 in cardiomyocytes: evidence for distinct metabolic pathways and implications for iron-mediated cardiotoxicity of antitumor therapy. Cancer Res. 61:2001;8422-8428.
8. Taatjes D.J., Gaudiano G., Koch T.H. Production of formaldehyde and DNA-adriamycin or DNA-daunomycin adducts, initiated through redox chemistry of dithiothreitol/iron, xanthine oxidase/NADH/iron, or glutathione/iron. Chem. Res. Toxicol. 10:1997;953-961.
9. Taatjes D.J., Koch T.H. Nuclear targeting and retention of anthracycline antitumor drugs in sensitive and resistant tumor cells. Curr. Med. Chem. 8:2001;15-29.
10. Hentze M.W., Kühn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 93:1996;8175-8182.
11. Theil E.C., Eisenstein R.S. Combinatorial mRNA regulation: iron regulatory proteins and iso-iron-responsive elements (iso-IREs). J. Biol. Chem. 275:2000;40659-40662.
12. Theil E.C. Targeting mRNA to regulate iron and oxygen metabolism. Biochem. Pharmacol. 59:1999;87-93.
13. Cairo G., Pietrangelo A. Iron regulatory proteins in pathobiology. Biochem. J. 352:2000;241-250.
14. Chénais B., Andriollo M., Guiraud P., Belhoussine R., Jeannesson P. Oxidative stress involvement in chemically induced differentiation of K562 cells. Free Radic. Biol. Med. 29:2000;18-27.
15. Hansen M.B., Nielsen S.E., Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119:1989;203-210.
16. Versantvoort C.H.M., Withoff S., Broxterman H.J., Kuiper C.M., Scheper R.J., Mulder N.H., de Vries E.G.E. Resistance-associated factors in human small-cell lung-carcinoma GLC4 sub-lines with increasing adriamycin resistance. Int. J. Cancer. 61:1995;375-380.
17. Gauchez A.-S., Lunardi J., Pernin C., Marti-Battle D., Fagret D. Detection of chemoresistance profile of cell lines K562, KB, GLC4 and HL60 through characterization of the hmdr1, mrp and lrp transcripts. In Vivo. 21:2001;101-104.
18. Brazzolotto X., Gaillard J., Pantopoulos K., Hentze M.W., Moulis J.-M. Human cytoplasmic aconitase (Iron Regulatory Protein 1) is converted into its [3Fe-4S] form by hydrogen peroxide in vitro but is not activated for iron-responsive element binding. J. Biol. Chem. 274:1999;21625-21630.
19. Brazzolotto X., Timmins P., Dupont Y., Moulis J.-M. Structural changes associated with switching activities of human Iron Regulatory Protein 1. J. Biol. Chem. 277:2002;11995-12000.
20. Zhu K., Henning D., Iwakuma T., Valdez B.C., Busch H. Adriamycin inhibits human RHII/Gu RNA helicase activity by binding to its substrate. Biochem. Biophys. Res. Commun. 266:1999;361-365.
21. Myers C.E., Gianni L., Simone C.B., Klecker R., Greene R. Oxidative destruction of erythrocyte ghost membranes catalyzed by the doxorubicin-iron complex. Biochemistry. 21:1982;1707-1713.
22. Fiallo M.M.L., Drechsel H., Garnier-Suillerot A., Matzanke B.F., Kozlowski H. Solution structure of iron(III)-anthracycline complexes. J. Med. Chem. 42:1999;2844-2851.
23. Naylor S., Mason R.P., Sanders J.K.M., Williams D.H., Monetti G. Formaldehyde adducts of glutathione. Biochem. J. 249:1988;573-579.
24. Recalcati S., Conte D., Cairo G. Preferential activation of iron regulatory protein-2 in cell lines as a result of higher sensitivity to iron. Eur. J. Biochem. 259:1999;304-309.
25. Torti F.M., Torti S.V. Regulation of ferritin genes and protein. Blood. 99:2002;3505-3516.
26. Takanashi S., Bachur N.R. Adriamycin metabolism in man. Evidence from urinary metabolites. Drug Metab. Dispos. 4:1976;79-87.
27. Wang A.H.J., Gao Y.G., Liaw Y.C., Li Y.K. Formaldehyde cross-links daunorubicin and DNA efficiently: HPLC and X-ray diffraction studies. Biochemistry. 30:1991;3812-3815.
28. Zeman S.M., Phillips D.R., Crothers D.M. Characterization of covalent adriamycine-DNA adducts. Proc. Natl. Acad. Sci. U. S. A. 95:1998;11561-11565.
29. Fenick D.J., Taatjes D.J., Koch T.H. Doxoform and daunoform: anthracycline-formaldehyde conjugates toxic to resistant tumor cells. J. Med. Chem. 40:1997;2452-2461.
30. Taatjes D.J., Koch T.H. Growth inhibition, nuclear uptake, and retention of anthracycline-formalhehyde conjugates in prostate cancer cells relative to clinical anthracyclines. Anticancer Res. 19:1999;1201-1208.
31. Deltour L., Foglio M.H., Duester G. Metabolic deficiencies in alcohol dehydrogenase Adh1, Adh3, and Adh4 null mutant mice. J. Biol. Chem. 274:1999;16796-16801.
32. Edenberg H.J. Regulation of the mammalian alcohol dehydrogenase genes. Prog. Nucleic Acid Res. Mol. Biol. 64:2000;295-341.
33. Liu L., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature. 410:2001;490-494.
34. Thomas C.E., Aust S.D. Release of iron from ferritin by cardiotoxic anthracycline antibiotics. Arch. Biochem. Biophys. 248:1986;684-689.
35. Denis-Gay M., Petit J.-M., Mazat J.-P., Ratineaud M.-H. Modification of oxido-reductase activities in adriamycin-resistant leukaemia K562 cells. Biochem. Pharmacol. 56:1998;451-457.
36. Kudoh K., Ramanna M., Ravatn R., Elkahloun A.G., Bittner M.L., Meltzer P.S., Trent J.M., Dalton W.S., Chin K.-V. Monitoring the expression profiles of doxorubicin-induced and doxorubicin-resistant cancer cells by cDNA microarray. Cancer Res. 60:2000;4161-4166.
37. Hipfner D.R., Deeley R.G., Cole S.P.C. Structural, mechanistic and clinical aspects of MRP1. Biochim. Biophys. Acta. 1461:1999;359-376.
38. Borst P., Evers R., Kool M., Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J. Natl. Cancer Inst. 92:2000;1295-1302.
39. van Tellingen O. The importance of drug-transporting P-glycoproteins in toxicology. Toxicol. Lett. 120:2001;31-41.
40. Praet M., Stryckmans P., Ruysschaert J.-M. Cellular uptake, cytotoxicity, and transport kinetics of anthracyclines in human sensitive and multidrug-resistant K562 cells. Biochem. Pharmacol. 51:1996;1341-1348.
41. Marbeuf-Gaye C., Ettori D., Priebe W., Koslowski H., Garnier-Suillerot A. Correlation between the kinetics of anthracycline uptake and the resistance factor in cancer cells expressing the multidrug resistance protein or the P-glycoprotein. Biochim. Biophys. Acta. 1450:1999;374-384.
42. Van Luyn M.J.A., Müller M., Renes J., Meijer C., Scheper R.J., Nienhuis E.F., Mulder N.H., Jansen P.L.M., de Vries E.G.E. Transport of glutathione conjugates into secretory vesicles is mediated by the multidrug-resistance protein 1. Int. J. Cancer. 76:1998;55-62.
43. Loetchutinat C., Priebe W., Garnier-Suillerot A. Drug sequestration in cytoplasmic organelles does not contribute to the diminished sensitivity of anthracyclines in multidrug resistant K562 cells. Eur. J. Biochem. 268:2001;4459-4467.
44. Minotti G., Cavaliere A.F., Mordente A., Rossi M., Schiavello R., Zamparelli R., Possati G.F. Secondary alcohol metabolites mediate iron delocalization in cytosolic fractions of myocardial biopsies exposed to anticancer anthracyclines. J. Clin. Invest. 95:1995;1595-1605.
45. Minotti G., Recalcati S., Mordente A., Liberi G., Calafiore A.M., Mancuso C., Preciozi P., Cairo G. The secondary alcohol metabolite of doxorubicin irreversibly inactivates aconitase/iron regulatory protein-1 in cytosolic fractions from human myocardium. FASEB J. 12:1998;541-552.
46. Licata S., Saponiero A., Mordente A., Minotti G. Doxorubicin metabolism and toxicity in human myocardium: role of cytoplasmic deglycosidation and carbonyl reduction. Chem. Res. Toxicol. 13:2000;414-420.
47. Behnia K., Boroujerdi M. Inhibition of aldo-keto reductases by phenobarbital alters metabolism, pharmacokinetics and toxicity of doxorubicin in rats. J. Pharm. Pharmacol. 51:1999;1275-1282.
48. Gonzalez B., Akman S., Doroshow J., Rivera H., Kaplan W.D., Forrest G.L. Protection against daunorubicin cytotoxicity by expression of a cloned human carbonyl reductase cDNA in K562 leukemia cells. Cancer Res. 55:1995;4646-4650.
49. Ax W., Soldan M., Koch L., Maser E. Development of daunorubicin resistance in tumor cells by induction of carbonyl reduction. Biochem. Pharmacol. 59:2000;293-300.
50. Minotti G., Parlani M., Salvatorelli E., Menna P., Cipollone A., Animati F., Maggi C.A., Manzini S. Impairment of myocardial contractility by anticancer anthracyclines: role of secondary alcohol metabolites and evidence of reduced toxicity by a novel disaccharide analogue. Br. J. Pharmacol. 134:2001;1271-1278.
51. Laurent G., Jaffrézou J.-P. Signaling pathways activated by daunorubicin. Blood. 98:2001;913-924.
52. Pantopoulos K., Mueller S., Atzberger A., Ansorge W., Stremmel W., Hentze M.W. Differences in the regulation of iron regulatory protein-1 (IRP-1) by extra- and intracellular oxidative stress. J. Biol. Chem. 272:1997;9802-9808.
53. Weinberg E.D. The role of iron in cancer. Eur. J. Cancer Prev. 5:1996;19-36.