Distinct mechanisms of site-specific oxidative DNA damage by doxorubicin in the presence of copper(II) and NADPH-cytochrome P450 reductase

Cancer Science

Volumn 94, Issue 8, 2003, Pages 686-691

  Mizutani, Hideki ^a,b   Oikawa, Shinji ^a   Hiraku, Yusuke ^a   Murata, Mariko ^a   Kojima, Michio ^b   Kawanishi, Shosuke ^a  

^a MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b MIE UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BENZOQUINONE; 8 HYDROXYDEOXYGUANOSINE; ADENINE; COPPER ION; DNA FRAGMENT; DOXORUBICIN; DRUG RESIDUE; GUANINE; HYDROGEN PEROXIDE; HYDROQUINONE; HYDROXIDE; PHOSPHORUS 32; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE FERRIHEMOPROTEIN REDUCTASE; SCAVENGER; THYMINE;

5' UNTRANSLATED REGION; ANTINEOPLASTIC ACTIVITY; CONTROLLED STUDY; DNA DAMAGE; DRUG OXIDATION; GENOTOXICITY; HUMAN; HUMAN CELL; ISOTOPE LABELING; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ANIMALS; CATTLE; COPPER; DEOXYGUANOSINE; DNA DAMAGE; DOXORUBICIN; GENES, P53; HL-60 CELLS; HUMANS; NADPH-FERRIHEMOPROTEIN REDUCTASE; TUMOR CELLS, CULTURED;

EID: 0141813521     PISSN: 13479032     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2003.tb01503.x     Document Type: Review

References (49)

1. Chabner BA, Allegra CJ, Curt GA, Calabresi P. Antineoplastic agents. In: Hardman JG, Limbird LE, editors. Goodman & Gilman's the pharmacological basis of therapeutics. 9th ed. New York: McGraw-Hill; 1996. p. 1233-87.
2. 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: 727-41.
3. Jung K, Reszka R. Mitochondria as subcellular targets for clinically useful anthracyclines. Adv Drug Deliv Rev 2001; 49: 87-105.
4. Hurley LH. DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer 2002; 2: 188-200.
5. Blasiak J, Gloc E, Wozniak K, Mlynarski W, Stolarska M, Skorski T, Majsterek I. Genotoxicity of idarubicin and its modulation by vitamins C and E and amifostine. Chem Biol Interact 2002; 140: 1-18.
6. Powis G. Free radical formation by antitumor quinones. Free Radic Biol Med 1989; 6: 63-101.
7. Handa K, Sato S. Stimulation of microsomal NADPH oxidation by quinone group-containing anticancer chemicals. Gann 1976; 67: 523-8.
8. Bachur NR, Gordon SL, Gee MV, Kon H. NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proc Natl Acad Sci USA 1979; 76: 954-7.
9. Kalyanaraman B, Perez-Reyes E, Mason RP. Spin-trapping and direct electron spin resonance investigations of the redox metabolism of quinone anti-cancer drugs. Biochim Biophys Acta 1980; 630: 119-30.
10. Doroshow JH. Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinines. Proc Natl Acad Sci USA 1986; 83: 4514-8.
11. Gille L, Nohl H. Analyses of the molecular mechanism of adriamycin-induced cardiotoxicity. Free Radic Biol Med 1997; 23: 775-82.
12. Kotamraju S, Chitambar CR, Kalivendi SV Joseph J, Kalyanaraman B. Transferrin receptor-dependent iron uptake is responsible for doxorubicin-mediated apoptosis in endothelial cells: role of oxidant-induced iron signaling in apoptosis. J Biol Chem 2002; 277: 17179-87.
13. Berlin V, Haseltine WA. Reduction of adriamycin to a semiquinone-free radical by NADPH cytochrome P-450 reductase produces DNA cleavage in a reaction mediated by molecular oxygen. J Biol Chem 1981; 256: 4747-56.
14. Davies KJ, Doroshow JH. Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem 1986; 261: 3060-7.
15. Tada-Oikawa S, Oikawa S, Kawanishi M, Yamada M, Kawanishi S. Generation of hydrogen peroxide precedes loss of mitochondrial membrane potential during DNA alkylation-induced apoptosis. FEBS Lett 1999; 442: 65-9.
16. Mizutani H, Tada-Oikawa S, Hiraku Y, Oikawa S, Kojima M, Kawanishi S. Mechanism of apoptosis induced by a new topoisomerase inhibitor through the generation of hydrogen peroxide. J Biol Chem 2002; 277: 30684-9.
17. Pietronigro DD, McGinness JE, Koren MJ, Crippa R, Seligman ML, Demopoulos HB. Spontaneous generation of adriamycin semiquinone radicals at physiologic pH. Physiol Chem Phys 1979; 11: 405-14.
18. Chinami M, Kato T, Ogura R, Shingu M. Semiquinone formation of adriamycin by oxidation at para-OH residue. Biochem Int 1984; 8: 299-304.
19. Reszka KJ, McCormick ML, Britigan BE. Peroxidase- and nitrite-dependent metabolism of the anthracycline anticancer agents daunorubicin and doxorubicin. Biochemistry 2001; 40: 15349-61.
20. Kasugai I, Yamada M. High production of catalase in hydrogen peroxide-resistant human leukemia HL-60 cell lines. Leuk Res 1992; 16: 173-9.
21. Ito K, Inoue S, Yamamoto K, Kawanishi S. 8-Hydroxydeoxyguanosine formation at the 5′ site of 5′-GG-3′ sequences in double-stranded DNA by UV radiation with riboflavin. J Biol Chem 1993; 268: 13221-7.
22. Chumakov P. EMBL Data Library accession number X54156, 1990.
23. Yamashita N, Murata M, Inoue S, Hiraku Y, Yoshinaga T, Kawanishi S. Superoxide formation and DNA damage induced by a fragrant furanone in the presence of copper(II). Mutat Res 1998; 397: 191-201.
24. Capon DJ, Chen EY, Levinson AD, Seeburg PH, Goeddel DV. Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature 1983; 302: 33-7.
25. Yamamoto K, Kawanishi S. Site-specific DNA damage induced by hydrazine in the presence of manganese and copper ions. The role of hydroxyl radical and hydrogen atom. J Biol Chem 1991; 266: 1509-15.
26. Kawanishi S, Yamamoto K. Mechanism of site-specific DNA damage induced by methylhydrazines in the presence of copper(II) or manganese(III). Biochemistry 1991; 30: 3069-75.
27. Kawanishi S, Oikawa S, Kawanishi M, Sugiyama H, Saito I, Strekowski L, Wilson WD. Amplification of pepleomycin-mediated DNA cleavage and apoptosis by unfused aromatic cations. Biochemistry 2000; 39: 13210-5.
28. Maxam AM, Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 1980; 65: 499-560.
29. Kasai H, Crain PF, Kucnino Y, Nishimura S, Ootsuyama A, Tanooka H. Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis 1986; 7: 1849-51.
30. Faure H, Coudray C, Mousseau M, Ducros V, Douki T, Bianchini F, Cadet J, Favier A. 5-Hydroxymethyluracil excretion, plasma TBARS and plasma antioxidant vitamins in adriamycin-treated patients. Free Radic Biol Med 1996; 20: 979-83.
31. Olinski R, Jaruga P, Foksinski M, Bialkowski K, Tujakowski J. Epirubicin-induced oxidative DNA damage and evidence for its repair in lymphocytes of cancer patients who are undergoing chemotherapy. Mol Pharmacol 1997; 52: 882-5.
32. Burkitt MJ. A critical overview of the chemistry of copper-dependent low density lipoprotein oxidation: roles of lipid hydroperoxides, alpha-tocopherol, thiols, and ceruloplasmin. Arch Biochem Biophys 2001; 394: 117-35.
33. 2. Free Radic Biol Med 1999; 26: 905-18.
34. Pryor WA, Tang RH. Ethylene formation from methional. Biochem Biophys Res Commun 1978; 81: 498-503.
35. Dizdaroglu M, Aruoma OI, Halliwell B. Modification of bases in DNA by copper ion-1,10-phenanthroline complexes. Biochemistry 1990; 29: 8447-51.
36. Yourtee DM, Elkins LL, Nalvarte EL, Smith RE. Amplification of doxorubicin mutagenicity by cupric ion. Toxicol Appl Pharmacol 1992; 116: 57-65.
37. Coates RJ, Weiss NS, Daling JR, Rettmer RL, Warnick GR. Cancer risk in relation to serum copper levels. Cancer Res 1989; 49: 4353-6.
38. Zowczak M, Iskra M, Torlinski L, Cofta S. Analysis of serum copper and zinc concentrations in cancer patients. Biol Trace Elem Res 2001; 82: 1-8.
39. Sakano K, Oikawa S, Hasegawa K, Kawanishi S. Hydroxyurea induces site-specific DNA damage via formation of hydrogen peroxide and nitric oxide. Jpn J Cancer Res 2001; 92: 1166-74.
40. Ogawa K, Hiraku Y, Oikawa S, Murata M, Sugimura Y, Kawamura J, Kawanishi S. Molecular mechanisms of DNA damage induced by procarbazine in the presence of Cu(II). Mutat Res in press.
41. Kawanishi S, Hiraku Y, Murata M, Oikawa S. The role of metals in site-specific DNA damage with reference to carcinogenesis. Free Radic Biol Med 2002; 32: 822-32.
42. Dijkwel PA, Wenink PW. Structural integrity of the nuclear matrix: differential effects of thiol agents and metal chelators. J Cell Sci 1986; 84: 53-67.
43. Saucier MA, Wang X, Re RN, Brown J, Bryan SE. Effects of ionic strength on endogenous nuclease activity in chelated and nonchelated chromatin. J Inorg Biochem 1991; 41: 117-24.
44. Someya A, Tanaka N. DNA strand scission induced by adriamycin and aclacinomycin A. J Antibiot (Tokyo) 1979; 32: 839-45.
45. Cova D, Sassano M, Monti E, Piccinini F. DNA damage induced by doxorubicin, 4′-epidoxorubicin and their copper(II) complexes. Arch Toxicol 1990; 64: 597-8.
46. Kawanishi S, Inoue S, Sano S. Mechanism of DNA cleavage induced by sodium chromate(VI) in the presence of hydrogen peroxide. J Biol Chem 1986; 261: 5952-8.
47. Celander DW, Cech TR. Iron(II)-ethylenediaminetetraacetic acid catalyzed cleavage of RNA and DNA oligonucleotides: similar reactivity toward single- and double-stranded forms. Biochemistry 1990; 29: 1355-61.
48. Brenner DE, Galloway S, Cooper J, Noone R, Hande KR. Improved high-performance liquid chromatography assay of doxorubicin: detection of circulating aglycones in human plasma and comparison with thin-layer chromatography. Cancer Chemother Pharmacol 1985; 14: 139-45.
49. Benet LZ, Kroetz DL, Sheiner LB. Pharmacokinetics: the dynamics of drug absorption, distribution and elimination. In: Hardman JG, Limbird LE, editors. Goodman & Gilman's the pharmacological basis of therapeutics. 9th ed. New York: McGraw-Hill; 1996. p. 3-27.