Mechanism of the cytotoxicity of the diazoparaquinone antitumor antibiotic kinamycin F

Free Radical Biology and Medicine

Volumn 43, Issue 8, 2007, Pages 1132-1144

  O'Hara, Kimberley A ^a   Wu, Xing ^a   Patel, Daywin ^a   Liang, Hong ^a   Yalowich, Jack C ^b   Chen, Nan ^c   Goodfellow, Valerie ^c   Adedayo, Otunola ^c   Dmitrienko, Gary I ^c   Hasinoff, Brian B ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Anticancer drug; Cytotoxicity; Diazo; Electron paramagnetic resonance spectroscopy; Kinamycin F; Phenoxyl radical; Quinone; Semiquinone radical; Topoisomerase II

Indexed keywords

ANTINEOPLASTIC AGENT; BUTHIONINE SULFOXIMINE; CATALASE; DEFEROXAMINE; DIMETHYL SULFOXIDE; DNA; GLUTATHIONE; HYDROGEN PEROXIDE; IRON; KINAMYCIN F; PEROXIDASE; PEROXIDE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; ELECTRON SPIN RESONANCE; HUMAN; HUMAN CELL; LEUKEMIA CELL; PEROXIDATION; PRIORITY JOURNAL;

AMITROLE; ANTIGENS, NEOPLASM; CELL SURVIVAL; DITHIOTHREITOL; DNA; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; DRUG SYNERGISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLUORESCEINS; GLUTATHIONE; HORSERADISH PEROXIDASE; HUMANS; HYDROGEN PEROXIDE; K562 CELLS; QUINONES;

BACTERIA (MICROORGANISMS);

EID: 34548491837     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.07.005     Document Type: Article

References (41)

1. Omura S., Nakagawa A., Yamada H., Hata T., Furusaki A., and Watanabe T. Structure of kinamycin C, and the structural relation among kinamycin A, B, C, and D. Chem. Pharm. Bull. 19 (1971) 2428-2430
2. Omura S., Nakagawa A., Yamada H., Hata T., Furukawa A., and Watanabe T. Structures and biological properties of kinamycin A, B, C, and D. Chem. Pharm. Bull. 21 (1973) 931-940
3. Seaton P.J., and Gould S.J. New products related to kinamycin from Streptomyces murayamaensis. II. Structures of pre-kinamycin, keto-anhydrokinamycin, and kinamycins E and F. J. Antibiot. (Tokyo) 42 (1989) 189-197
4. Mithani S., Weeratunga G., Taylor J., and Dmitrienko G.I. The kinamycins are diazofluorenes and not cyanocarbazoles. J. Am. Chem. Soc. 116 (1994) 2209-2210
5. Gould S.J., Tamayo N., Melville C.R., and Cone M.C. Revised structures for the kinamycin antibiotics: 5-diazobenzo[b]fluorenes rather than benzo[b]carbazole cyanamides. J. Am. Chem. Soc. 116 (1994) 2207-2208
6. He H., Ding W.D., Bernan V.S., Richardson A.D., Ireland C.M., Greenstein M., Ellestad G.A., and Carter G.T. Lomaiviticins A and B, potent antitumor antibiotics from Micromonospora lomaivitiensis. J. Am. Chem. Soc. 123 (2001) 5362-5363
7. Lei X., and Porco Jr. J.A. Total synthesis of the diazobenzofluorene antibiotic (-)-kinamycin C. J. Am. Chem. Soc. 128 (2006) 14790-14791
8. 2 radical and orthoquinonemethide intermediates. J. Am. Chem. Soc. 128 (2006) 12562-12573
9. Feldman K.S., and Eastman K.J. A proposal for the mechanism-of-action of diazoparaquinone natural products. J. Am. Chem. Soc. 127 (2005) 15344-15345
10. Zeng W., Eric Ballard T., Tkachenko A.G., Burns V.A., Feldheim D.L., and Melander C. Mimicking the biological activity of diazobenzo[b]fluorene natural products with electronically tuned diazofluorene analogs. Bioorg. Med. Chem. Lett. 16 (2006) 5148-5151
11. Arya D.P., and Jebaratnam D.J. DNA cleaving ability of 9-diazofluorenes and diaryl diazomethanes: Implications for the mode of action of the kinamycin antibiotics. J. Org. Chem. 60 (1995) 3268-3269
12. Laufer R.S., and Dmitrienko G.I. Diazo group electrophilicity in kinamycins and lomaiviticin A: potential insights into the molecular mechanism of antibacterial and antitumor activity. J. Am. Chem. Soc. 124 (2002) 1854-1855
13. Hasinoff B.B., Wu X., Yalowich J.C., Goodfellow V., Laufer R.S., Adedayo O., and Dmitrienko G.I. Kinamycins A and C, bacterial metabolites that contain an unusual diazo group, as potential new anticancer agents: antiproliferative and cell cycle effects. Anticancer Drugs 17 (2006) 825-837
14. Cone M.C., Seaton P.J., Halley K.A., and Gould S.J. New products related to kinamycin from Streptomyces murayamaensis. I. Taxonomy, production, isolation and biological properties. J. Antibiot. (Tokyo) 42 (1989) 179-188
15. Ritke M.K., and Yalowich J.C. Altered gene expression in human leukemia K562 cells selected for resistance to etoposide. Biochem. Pharmacol. 46 (1993) 2007-2020
16. Ritke M.K., Roberts D., Allan W.P., Raymond J., Bergoltz V.V., and Yalowich J.C. Altered stability of etoposide-induced topoisomerase II-DNA complexes in resistant human leukemia K562 cells. Br. J. Cancer 69 (1994) 687-697
17. Hasinoff B.B., Kozlowska H., Creighton A.M., Allan W.P., Thampatty P., and Yalowich J.C. Mitindomide is a catalytic inhibitor of DNA topoisomerase II that acts at the bisdioxopiperazine binding site. Mol. Pharmacol. 52 (1997) 839-845
18. Liang H., Wu X., Guziec L.J., Guziec F.S.J., Larson K.K., Lang J., Yalowich J.C., and Hasinoff B.B. A structure-based 3D-QSAR study of anthrapyrazole analogs of the anticancer agents losoxantrone and piroxantrone. J. Chem. Inf. Model. 46 (2006) 1827-1835
19. Chaires J.B., Satyanarayana S., Suh D., Fokt I., Przewloka T., and Priebe W. Parsing the free energy of anthracycline antibiotic binding to DNA. Biochemistry 35 (1996) 2047-2053
20. Jenkins T.C. Optical absorbance and fluorescence techniques for measuring DNA-drug interactions. Methods Mol. Biol. 90 (1997) 195-218
21. Hasinoff B.B., Wu X., Krokhin O.V., Ens W., Standing K.G., Nitiss J.L., Sivaram T., Giorgianni A., Yang S., Jiang Y., and Yalowich J.C. Biochemical and proteomics approaches to characterize topoisomerase IIα cysteines and DNA as targets responsible for cisplatin-induced inhibition of topoisomerase IIα. Mol. Pharmacol. 67 (2005) 937-947
22. Schroder H.C., Batel R., Schwertner H., Boreiko O., and Muller W.E. Fast micromethod DNA single-strand-break assay. Methods Mol. Biol. 314 (2006) 287-305
23. O'Malley Y.Q., Reszka K.J., and Britigan B.E. Direct oxidation of 2′,7′-dichlorodihydrofluorescein by pyocyanin and other redox-active compounds independent of reactive oxygen species production. Free Radic. Biol. Med. 36 (2004) 90-100
24. Maresca M., Colao C., and Leoncini G. Generation of hydrogen peroxide in resting and activated platelets. Cell Biochem. Funct. 10 (1992) 79-85
25. Barnabé N., Zastre J., Venkataram S., and Hasinoff B.B. Deferiprone protects against doxorubicin-induced myocyte cytotoxicity. Free Radic. Biol. Med. 33 (2002) 266-275
26. Leonard G.A., Hambley T.W., McAuley-Hecht K., Brown T., and Hunter W.N. Anthracycline-DNA interactions at unfavourable base-pair triplet-binding sites: structures of d(CGGCCG)/daunomycin and d(TGGCCA)/adriamycin complexes. Acta Crystallogr., D Biol. Crystallogr. 49 (1993) 458-467
27. GOLD 3.1, CCDC Software Ltd., Cambridge, UK.
28. Verdonk M.L., Cole J.C., Hartshorn M.J., Murray C.W., and Taylor R.D. Improved protein-ligand docking using GOLD. Proteins 52 (2003) 609-623
29. Price C.C., and Tsunawa S. Polycondensation of mercaptobenzenediazonium salts. J. Am. Chem. Soc. 28 (1963) 1867-1868
30. Bolton J.L., Trush M.A., Penning T.M., Dryhurst G., and Monks T.J. Role of quinones in toxicology. Chem. Res. Toxicol. 13 (2000) 135-160
31. Schafer F.Q., and Buettner G.R. 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
32. Kagan V.E., Kuzmenko A.I., Tyurina Y.Y., Shvedova A.A., Matsura T., and Yalowich J.C. Pro-oxidant and antioxidant mechanisms of etoposide in HL-60 cells: role of myeloperoxidase. Cancer Res. 61 (2001) 7777-7784
33. Brandt R., and Keston A.S. Synthesis of diacetyldichlorofluorescin: A stable reagent for fluorometric Analysis. Anal. Biochem. 11 (1965) 6-9
34. Kagan V.E., Yalowich J.C., Borisenko G.G., Tyurina Y.Y., Tyurin V.A., Thampatty P., and Fabisiak J.P. Mechanism-based chemopreventive strategies against etoposide-induced acute myeloid leukemia: free radical/antioxidant approach. Mol. Pharmacol. 56 (1999) 494-506
35. Hasinoff B.B., Wu X., Begleiter A., Guziec L., Guziec F., Giorgianni A., Yang S., Jiang Y., and Yalowich J.C. Structure-activity study of the interaction of bioreductive benzoquinone alkylating agents with DNA topoisomerase II. Cancer Chemother. Pharmacol. 57 (2006) 221-233
36. Bender R.P., Lehmler H.J., Robertson L.W., Ludewig G., and Osheroff N. Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIα: altering enzyme function by blocking the N-terminal protein gate. Biochemistry 45 (2006) 10140-10152
37. Paz M.M., and Tomasz M. Reductive activation of mitomycin A by thiols. Org. Lett. 3 (2001) 2789-2792
38. Rush J.D., and Koppenol W.H. Oxidizing intermediates in the reaction of ferrous EDTA with hydrogen peroxide. Reactions with organic molecules and ferricytochrome c. J. Biol. Chem. 261 (1986) 6730-6733
39. Swallow A.J. Physical chemistry of semiquinones. In: Trumower B.L. (Ed). Function of Quinones in Energy Conserving Systems (1982), Academic Press, New York 59-72
40. Ollinger K., and Brunmark A. Effect of hydroxy substituent position on 1,4-naphthoquinone toxicity to rat hepatocytes. J. Biol. Chem. 266 (1991) 21496-21503
41. Tyurina Y.Y., Tyurin V.A., Yalowich J.C., Quinn P.J., Claycamp H.G., Schor N.F., Pitt B.R., and Kagan V.E. Phenoxyl radicals of etoposide (VP-16) can directly oxidize intracellular thiols: protective versus damaging effects of phenolic antioxidants. Toxicol. Appl. Pharmacol. 131 (1995) 277-2788