Redox activation of Fe(III)-thiosemicarbazones and Fe(III)-bleomycin by thioredoxin reductase: Specificity of enzymatic redox centers and analysis of reactive species formation by ESR spin trapping

Free Radical Biology and Medicine

Volumn 60, Issue , 2013, Pages 183-194

  Myers, Judith M ^a   Cheng, Qing ^b   Antholine, William E ^a,c   Kalyanaraman, Balaraman ^a,c   Filipovska, Aleksandra ^d   Arnér, Elias S J ^b   Myers, Charles R ^a,c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c FREE RADICAL RESEARCH CENTER   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Bleomycin; ESR; Free radicals; Glutathione reductase; Hydroxyl radical; Thioredoxin reductase; Thiosemicarbazones; Triapine

Indexed keywords

5 DIETHOXYPHOSPHORYL 5 METHYL 1 PYRROLINE 1 OXIDE; AMMONIUM FORMATE; BLEOMYCIN; CARBON DIOXIDE; FERRIC ION; GLUTATHIONE REDUCTASE; HYDROXYL RADICAL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SELENOCYSTEINE; THIOREDOXIN REDUCTASE; THIOREDOXIN REDUCTASE 1; THIOSEMICARBAZONE;

ANIMAL EXPERIMENT; ARTICLE; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOTOXICITY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; FENTON REACTION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RADICAL REACTION; RAT; SPIN TRAPPING;

ANTINEOPLASTIC AGENTS; BLEOMYCIN; GLUTATHIONE REDUCTASE; HUMANS; HYDROXYL RADICAL; IRON; IRON CHELATING AGENTS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SELENOCYSTEINE; SPIN TRAPPING; THIOREDOXIN REDUCTASE 1; THIOSEMICARBAZONES;

EID: 84875404357     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.02.016     Document Type: Article

References (83)

1. Y. Yu, D.S. Kalinowski, Z. Kovacevic, A.R. Siafakas, P.J. Jansson, C. Stefani, D.B. Lovejoy, P.C. Sharpe, P.V. Bernhardt, and D.R. Richardson Thiosemicarbazones from the old to new: iron chelators that are more than just ribonucleotide reductase inhibitors J. Med. Chem. 52 2009 5271 5294
2. D.H. Petering, W.E. Antholine, and L.A. Saryan Metal complexes as antitumor agents R.M. Ottenbrite, G.B. Butler, Anticancer and Interferon Agents 1984 Dekker New York 203 246
3. C.R. Chitambar, and W.E. Antholine Iron-targeting antitumor activity of gallium compounds and novel insights into Triapine((R))-metal complexes Antioxid. Redox Signaling 18 2013 956 972
4. D.S. Kalinowski, and D.R. Richardson Future of toxicology - iron chelators and differing modes of action and toxicity: the changing face of iron chelation therapy Chem. Res. Toxicol 20 2007 715 720
5. J. Shao, B. Zhou, A.J. Di Bilio, L. Zhu, T. Wang, C. Qi, J. Shih, and Y. Yen A ferrous-Triapine complex mediates formation of reactive oxygen species that inactivate human ribonucleotide reductase Mol. Cancer Ther 5 2006 586 592
6. A. Popovic-Bijelic, C.R. Kowol, M.E. Lind, J. Luo, F. Himo, É.A. Enyedy, V.B. Arion, and A. Gräslund Ribonucleotide reductase inhibition by metal complexes of Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone): a combined experimental and theoretical study J. Inorg. Biochem. 105 2011 1422 1431
7. R.A. Finch, M.C. Liu, A.H. Cory, J.G. Cory, and A.C. Sartorelli Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone; 3-AP): an inhibitor of ribonucleotide reductase with antineoplastic activity Adv. Enzyme Regul. 39 1999 3 12
8. P.J. Jansson, C.L. Hawkins, D.B. Lovejoy, and D.R. Richardson The iron complex of Dp44mT is redox-active and induces hydroxyl radical formation: an EPR study J. Inorg. Biochem. 104 2010 1224 1228
9. J.M. Myers, W.E. Antholine, and C.R. Myers The iron-chelating drug Triapine causes pronounced mitochondrial thiol redox stress Toxicol. Lett. 201 2011 130 136
10. 2 is not reflected in its reaction with other oxidants and thiol reagents J. Biol. Chem. 282 2007 11885 11892
11. M.H. Stipanuk, M. Londono, J.I. Lee, M. Hu, and A.F. Yu Enzymes and metabolites of cysteine metabolism in nonhepatic tissues of rats show little response to changes in dietary protein or sulfur amino acid levels J. Nutr 132 2002 3369 3378
12. J.I. Lee, M. Londono, L.L. Hirschberger, and M.H. Stipanuk Regulation of cysteine dioxygenase and gamma-glutamylcysteine synthetase is associated with hepatic cysteine level J. Nutr. Biochem. 15 2004 112 122
13. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med 30 2001 1191 1212
14. J. Yuan, D.B. Lovejoy, and D.R. Richardson Novel di-2-pyridyl-derived iron chelators with marked and selective antitumor activity: in vitro and in vivo assessment Blood 104 2004 1450 1458
15. J. Sigmond, J.A. Kamphuis, A.C. Laan, E.K. Hoebe, A.M. Bergman, and G.J. Peters The synergistic interaction of gemcitabine and cytosine arabinoside with the ribonucleotide reductase inhibitor Triapine is schedule dependent Biochem. Pharmacol. 73 2007 1548 1557
16. D.R. Richardson, P.C. Sharpe, D.B. Lovejoy, D. Senaratne, D.S. Kalinowski, M. Islam, and P.V. Bernhardt Dipyridyl thiosemicarbazone chelators with potent and selective antitumor activity form iron complexes with redox activity J. Med. Chem. 49 2006 6510 6521
17. A.B. Alvero, W. Chen, A.C. Sartorelli, P. Schwartz, T. Rutherford, and G. Mor Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone) induces apoptosis in ovarian cancer cells J. Soc. Gynecol. Invest 13 2006 145 152
18. M. Whitnall, J. Howard, P. Ponka, and D.R. Richardson A class of iron chelators with a wide spectrum of potent antitumor activity that overcomes resistance to chemotherapeutics Proc. Natl. Acad. Sci. USA 103 2006 14901 14906
19. T.B. Chaston, D.B. Lovejoy, R.N. Watts, and D.R. Richardson Examination of the antiproliferative activity of iron chelators: multiple cellular targets and the different mechanism of action of Triapine compared with desferrioxamine and the potent pyridoxal isonicotinoyl hydrazone analogue 311 Clin. Cancer Res 9 2003 402 414
20. D.S. Kalinowski, and D.R. Richardson The evolution of iron chelators for the treatment of iron overload disease and cancer Pharmacol. Rev. 57 2005 547 583
21. Y. Soini, K. Kahlos, U. Napankangas, R. Kaarteenaho-Wiik, M. Saily, P. Koistinen, P. Paaakko, A. Holmgren, and V.L. Kinnula Widespread expression of thioredoxin and thioredoxin reductase in non-small cell lung carcinoma Clin. Cancer Res. 7 2001 1750 1757
22. D.T. Lincoln, E.M. Ali Emadi, K.F. Tonissen, and F.M. Clarke The thioredoxin-thioredoxin reductase system: over-expression in human cancer Anticancer Res. 23 2003 2425 2433
23. S.E. Eriksson, S. Prast-Nielsen, E. Flaberg, L. Szekely, and E.S. Arnér High levels of thioredoxin reductase 1 modulate drug-specific cytotoxic efficacy Free Radic. Biol. Med. 47 2009 1661 1671
24. S. Kumar, M. Bjornstedt, and A. Holmgren Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen Eur. J. Biochem 207 1992 435 439
25. J. Nordberg, and E.S. Arnér Reactive oxygen species, antioxidants, and the mammalian thioredoxin system Free Radic. Biol. Med. 31 2001 1287 1312
26. M. Bjornstedt, M. Hamberg, S. Kumar, J. Xue, and A. Holmgren Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols J. Biol. Chem. 270 1995 11761 11764
27. Q. Cheng, T. Sandalova, Y. Lindqvist, and E.S. Arnér Crystal structure and catalysis of the selenoprotein thioredoxin reductase 1 J. Biol. Chem. 284 2009 3998 4008
28. E.S. Arnér Focus on mammalian thioredoxin reductases - important selenoproteins with versatile functions Biochim. Biophys. Acta 1790 2009 495 526
29. G. Powis, and W.R. Montfort Properties and biological activities of thioredoxins Annu. Rev. Biophys. Biomol. Struct. 30 2001 421 455
30. L. Zhong, E.S. Arnér, and A. Holmgren Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence Proc. Natl. Acad. Sci. USA 97 2000 5854 5859
31. L. Zhong, and A. Holmgren Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations J. Biol. Chem 275 2000 18121 18128
32. J. Nordberg, L. Zhong, A. Holmgren, and E.S. Arnér Mammalian thioredoxin reductase is irreversibly inhibited by dinitrohalobenzenes by alkylation of both the redox active selenocysteine and its neighboring cysteine residue J. Biol. Chem 273 1998 10835 10842
33. A.B. Witte, K. Anestål, E. Jerremalm, H. Ehrsson, and E.S. Arnér Inhibition of thioredoxin reductase but not of glutathione reductase by the major classes of alkylating and platinum-containing anticancer compounds Free Radic. Biol. Med. 39 2005 696 703
34. S. Gromer, S. Urig, and K. Becker The thioredoxin system - from science to clinic Med. Res. Rev. 24 2004 40 89
35. S. Urig, and K. Becker On the potential of thioredoxin reductase inhibitors for cancer therapy Semin. Cancer Biol. 16 2006 452 465
36. A.P. Lothrop, E.L. Ruggles, and R.J. Hondal No selenium required: reactions catalyzed by mammalian thioredoxin reductase that are independent of a selenocysteine residue Biochemistry 48 2009 6213 6223
37. E.S. Arnér Recombinant expression of mammalian selenocysteine-containing thioredoxin reductase and other selenoproteins in Escherichia coli Methods Enzymol 347 2002 226 235
38. 11C Nat. Protoc 1 2006 604 613
39. L. Johansson, C. Chen, J.O. Thorell, A. Fredriksson, S. Stone-Elander, G. Gafvelin, and E.S. Arnér Exploiting the 21st amino acid-purifying and labeling proteins by selenolate targeting Nat. Methods 1 2004 61 66
40. O. Rengby, L. Johansson, L.A. Carlson, E. Serini, A. Vlamis-Gardikas, P. Karsnas, and E.S. Arnér Assessment of production conditions for efficient use of Escherichia coli in high-yield heterologous recombinant selenoprotein synthesis Appl. Environ. Microbiol. 70 2004 5159 5167
41. Q. Cheng, W.E. Antholine, J.M. Myers, B. Kalyanaraman, E.S. Arnér, and C.R. Myers The selenium-independent inherent pro-oxidant NADPH oxidase activity of mammalian thioredoxin reductase and its selenium-dependent direct peroxidase activities J. Biol. Chem. 285 2010 21708 21723
42. O. Rackham, A.M. Shearwood, R. Thyer, E. McNamara, S.M. Davies, B.A. Callus, A. Miranda-Vizuete, S.J. Berners-Price, Q. Cheng, E.S. Arnér, and A. Filipovska Substrate and inhibitor specificities differ between human cytosolic and mitochondrial thioredoxin reductases: implications for development of specific inhibitors Free Radic. Biol. Med. 50 2011 689 699
43. Y. Wang, M. Qiao, J.J. Mieyal, L.M. Asmis, and R. Asmis Molecular mechanism of glutathione-mediated protection from oxidized low-density lipoprotein-induced cell injury in human macrophages: role of glutathione reductase and glutaredoxin Free Radic. Biol. Med. 41 2006 775 785
44. C.R. Myers, and J.M. Myers Iron stimulates the rate of reduction of hexavalent chromium by human microsomes Carcinogenesis 19 1998 1029 1038
45. 5: generation of hydroxyl radical and superoxide Free Radic. Biol. Med. 42 2007 738 755
46. C. Frejaville, H. Karoui, B. Tuccio, F. Le Moigne, M. Culcasi, S. Pietri, R. Lauricella, and P. Tordo 5-(Diethoxyphosphoryl)-5-methyl-1-pyrroline N-oxide: a new efficient phosphorylated nitrone for the in vitro and in vivo spin trapping of oxygen-centered radicals J. Med. Chem. 38 1995 258 265
47. Tordo, P. Spin-trapping: recent developments and applications. In: Gilbert, B. C.; Atherton, N. M.; Davies, M. J., Eds. Electron Paramagnetic Resonance: Specialist Periodical Reports. Cambridge (UK): Royal Chem. Soc.; 1998:116-144.
48. D.R. Duling Simulation of multiple isotropic spin-trap EPR spectra J. Magn. Reson. B 104 1994 105 110
49. W. Li, W.E. Antholine, and D.H. Petering Kinetics of reaction of DNA-bound Fe(III)bleomycin with ascorbate: interplay of specific and non-specific binding J. Inorg. Biochem. 90 2002 8 17
50. W.E. Antholine, and D.H. Petering On the reaction of iron bleomycin with thiols and oxygen Biochem. Biophys. Res. Commun. 90 1979 384 389
51. J. Vásquez-Vivar, N. Hogg, P. Martásek, H. Karoui, P. Tordo, K.A.J. Pritchard, and B. Kalyanaraman Effect of redox-active drugs on superoxide generation from nitric oxide synthases: biological and toxicological implications Free Radic. Res. 31 1999 607 617
52. 2 Proc. Natl. Acad. Sci. USA 95 1998 6675 6680
53. •OH? Photochem. Photobiol. 77 2003 165 170
54. S. Mitroka, S. Zimmeck, D. Troya, and J.M. Tanko How solvent modulates hydroxyl radical reactivity in hydrogen atom abstractions J. Am. Chem. Soc. 132 2010 2907 2913
55. H. Karoui, N. Hogg, C. Fréjaville, P. Tordo, and B. Kalyanaraman Characterization of sulfur-centered radical intermediates formed during the oxidation of thiols and sulfite by peroxynitrite J. Biol. Chem. 271 1996 6000 6009
56. K. Anestål, S. Prast-Nielsen, N. Cénas, and E.S. Arnér Cell death by SecTRAPs: thioredoxin reductase as a prooxidant killer of cells PLoS ONE 3 2008 e1846
57. J.M. Myers, and C.R. Myers The effects of hexavalent chromium on thioredoxin reductase and peroxiredoxins in human bronchial epithelial cells Free Radic. Biol. Med 47 2009 1477 1485
58. C.R. Myers The effects of chromium(VI) on the thioredoxin system: implications for redox regulation Free Radic. Biol. Med. 52 2012 2091 2107
59. M. Takizawa, K. Komori, Y. Tampo, and M. Yonaha Paraquat-induced oxidative stress and dysfunction of cellular redox systems including antioxidative defense enzymes glutathione peroxidase and thioredoxin reductase Toxicol. In Vitro 21 2007 355 363
60. T. Sandalova, L. Zhong, Y. Lindqvist, A. Holmgren, and G. Schneider Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme Proc. Natl. Acad. Sci. USA 98 2001 9533 9538
61. S. Wadler, D. Makower, C. Clairmont, P. Lambert, K. Fehn, M. Sznol, and I Phase and pharmacokinetic study of the ribonucleotide reductase inhibitor, 3-aminopyridine-2-carboxaldehyde thiosemicarbazone, administered by 96-hour intravenous continuous infusion J. Clin. Oncol. 22 2004 1553 1563
62. J. Kolesar, R.C. Brundage, M. Pomplun, D. Alberti, K. Holen, A. Traynor, P. Ivy, and G. Wilding Population pharmacokinetics of 3-aminopyridine-2- carboxaldehyde thiosemicarbazone (Triapine®) in cancer patients Cancer Chemother. Pharmacol. 67 2011 393 400
63. C.A. Kunos, S. Waggoner, V. von Gruenigen, E. Eldermire, J. Pink, A. Dowlati, and T.J. Kinsella Phase I trial of pelvic radiation, weekly cisplatin, and 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (3-AP, NSC #663249) for locally advanced cervical cancer Clin. Cancer Res. 16 2010 1298 1306
64. Z.D. Liu, and R.C. Hider Design of iron chelators with therapeutic application Coord. Chem. Rev. 232 2002 151 171
65. J.M. Kolesar, W.R. Schelman, P.G. Geiger, K.D. Holen, A.M. Traynor, D.B. Alberti, J.P. Thomas, C.R. Chitambar, G. Wilding, and W.E. Antholine Electron paramagnetic resonance study of peripheral blood mononuclear cells from patients with refractory solid tumors treated with Triapine J. Inorg. Biochem. 102 2008 693 698
66. A.G. Cox, C.C. Winterbourn, and M.B. Hampton Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling Biochem. J. 425 2010 313 325
67. R.A. Walker, and S.J. Day Transferrin receptor expression in non-malignant and malignant human breast tissue J. Pathol. 148 1986 217 224
68. D. Hogemann-Savellano, E. Bos, C. Blondet, F. Sato, T. Abe, L. Josephson, R. Weissleder, J. Gaudet, D. Sgroi, P.J. Peters, and J.P. Basilion The transferrin receptor: a potential molecular imaging marker for human cancer Neoplasia 5 2003 495 506
69. T.R. Daniels, T. Delgado, J.A. Rodriguez, G. Helguera, and M.L. Penichet The transferrin receptor. Part I. Biology and targeting with cytotoxic antibodies for the treatment of cancer Clin. Immunol. 121 2006 144 158
70. W.H. Watson, J.M. Heilman, L.L. Hughes, and J.C. Spielberger Thioredoxin reductase-1 knock down does not result in thioredoxin-1 oxidation Biochem. Biophys. Res. Commun. 368 2008 832 836
71. S.V. Singh, S.R. Brunnert, B. Roberts, and A. Krishan Differential expression of glutathione S-transferase, glutathione peroxidase and glutathione reductase in normal and malignant human breast tissues Cancer Lett. 51 1990 43 48
72. J. Xu, and E.S. Arnér Pyrroloquinoline quinone modulates the kinetic parameters of the mammalian selenoprotein thioredoxin reductase 1 and is an inhibitor of glutathione reductase Biochem. Pharmacol 83 2012 815 820
73. N. Cénas, H. Nivinskas, Z. Anusevicius, J. Sarlauskas, F. Lederer, and E.S. Arnér Interactions of quinones with thioredoxin reductase: a challenge to the antioxidant role of the mammalian selenoprotein J. Biol. Chem. 279 2004 2583 2592
74. E.S. Arnér, H. Nakamura, T. Sasada, J. Yodoi, A. Holmgren, and G. Spyrou Analysis of the inhibition of mammalian thioredoxin, thioredoxin reductase, and glutaredoxin by cis-diamminedichloroplatinum(II) and its major metabolite, the glutathione-platinum complex Free Radic. Biol. Med. 31 2001 1170 1178
75. R.A. Finch, M. Liu, S.P. Grill, W.C. Rose, R. Loomis, K.M. Vasquez, Y. Cheng, and A.C. Sartorelli Triapine (3-aminopyridine-2-carboxaldehyde- thiosemicarbazone): a potent inhibitor of ribonucleotide reductase activity with broad spectrum antitumor activity Biochem. Pharmacol. 59 2000 983 991
76. S. Urig, J. Lieske, K. Fritz-Wolf, A. Irmler, and K. Becker Truncated mutants of human thioredoxin reductase 1 do not exhibit glutathione reductase activity FEBS Lett. 580 2006 3595 3600
77. C.C. Böhme, L.D. Arscott, K. Becker, R.H. Schirmer, and C.H. Williams Jr. Kinetic characterization of glutathione reductase from the malarial parasite Plasmodium falciparum: comparison with the human enzyme J. Biol. Chem. 275 2000 37317 37323
78. P. Quach, E. Gutierrez, M.T. Basha, D.S. Kalinowski, P.C. Sharpe, D.B. Lovejoy, P.V. Bernhardt, P.J. Jansson, and D.R. Richardson Methemoglobin formation by Triapine, di-2-pyridylketone-4,4-dimethyl-3-thiosemicarbazone (Dp44mT), and other anticancer thiosemicarbazones: identification of novel thiosemicarbazones and therapeutics that prevent this effect Mol. Pharmacol. 82 2012 105 114
79. D.L. Melnyk, S.B. Horwitz, and J. Peisach Redox potential of iron-bleomycin Biochemistry 20 1981 5327 5331
80. G.R. Buettner The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate Arch. Biochem. Biophys. 300 1993 535 543
81. B.B. Hasinoff NADPH-cytochrome-P450 reductase promotes hydroxyl radical production by the iron complex of ADR-925, the hydrolysis product of ICRF-187 (dexrazoxane) Free Radic. Res 22 1995 319 325
82. L.A. Morehouse, C.E. Thomas, and S.D. Aust Superoxide generation by NADPH-cytochrome P-450 reductase: the effect of iron chelators and the role of superoxide in microsomal lipid peroxidation Arch. Biochem. Biophys 232 1984 366 377
83. M.H. Bilimoria, and H. Kamin The effect of high salt concentrations upon cytochrome c, cytochrome b5, and iron-EDTA reductase activities of liver microsomal NADPH-cytochrome c reductase Ann. N. Y. Acad. Sci 212 1973 428 448