Deoxidation rates play a critical role in DNA damage mediated by important synthetic drugs, quinoxaline 1,4-dioxides

Chemical Research in Toxicology

Volumn 28, Issue 3, 2015, Pages 470-481

  Wang, Xu ^a   Zhang, Huahai ^d   Huang, Lingli ^a   Pan, Yuanhu ^b   Li, Juan ^b   Chen, Dongmei ^b   Cheng, Guyue ^b   Hao, Haihong ^c   Tao, Yanfei ^c   Liu, Zhenli ^c   Yuan, Zonghui ^a,b,c  

^a National Reference Laboratory of Veterinary Drug Residues (HZAU)   (China)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^c Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety   (China)

^d NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARBADOX; CIADOX; OLAQUINDOX; QUINOXALINE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXYGEN;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL VIABILITY; CHEMICAL REACTION; CHEMICAL STRUCTURE; CONTROLLED STUDY; DEOXIDATION; DNA DAMAGE; EXPERIMENTAL PIG; GENOTOXICITY; HEPG2 CELL LINE; LIQUID CHROMATOGRAPHY; LIVER CELL; LIVER MICROSOME; MASS SPECTROMETRY; METABOLITE; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; RAT; ANIMAL; CELL CULTURE; CELL SURVIVAL; COMET ASSAY; DRUG EFFECTS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PIG; WISTAR RAT;

RATTUS; SUIDAE; SUS;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; COMET ASSAY; DNA DAMAGE; HEP G2 CELLS; HEPATOCYTES; HUMANS; MICROSOMES, LIVER; OXIDATION-REDUCTION; OXYGEN; QUINOXALINES; RATS, WISTAR; SWINE;

EID: 84924915127     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx5004326     Document Type: Article

References (50)

1. Wu, Y., Yu, H., Wang, Y., Huang, L., Tao, Y., Chen, D., Peng, D., Liu, Z., and Yuan, Z. (2007) Development of a high-performance liquid chromatography method for the simultaneous quantification of quinoxaline-2-carboxylic acid and methyl-3-quinoxaline-2-carboxylic acid in animal tissues J. Chromatogr. A 1146, 1-7
2. Wang, X., Fang, G. J., Wang, Y. L., Ihsan, A., Huang, L. L., Zhou, W., Liu, Z. L., and Yuan, Z. H. (2011) Two generation reproduction and teratogenicity studies of feeding cyadox in Wistar rats Food Chem. Toxicol. 49, 1068-1079
3. Carta, A., Corona, P., and Loriga, M. (2005) Quinoxaline 1,4-dioxide: a versatile scaffold endowed with manifold activities Curr. Med. Chem. 12, 2259-2272
4. Vicente, E., Perez-Silanes, S., Lima, L. M., Ancizu, S., Burguete, A., Solano, B., Villar, R., Aldana, I., and Monge, A. (2009) Selective activity against Mycobacterium tuberculosis of new quinoxaline 1,4-di- N -oxides Bioorg. Med. Chem. 17, 385-389
5. Cohen, E. E., Rosine, D., Haraf, D. J., Loh, E., Shen, L., Lusinchi, A., Vokes, E. E., and Bourhis, J. (2007) Phase I trial of tirapazamine, cisplatin, and concurrent accelerated boost reirradiation in patients with recurrent head and neck cancer Int. J. Radiat. Oncol., Biol., Phys. 67, 678-684
6. Covens, A., Blessing, J., Bender, D., Mannel, R., Morgan, M., and Gynecologic Oncology, G. (2006) A phase II evaluation of tirapazamine plus cisplatin in the treatment of recurrent platinum-sensitive ovarian or primary peritoneal cancer: a Gynecologic Oncology Group study Gynecol. Oncol. 100, 586-590
7. Maluf, F. C., Leiser, A. L., Aghajanian, C., Sabbatini, P., Pezzulli, S., Chi, D. S., Wolf, J. K., Levenback, C., Loh, E., and Spriggs, D. R. (2006) Phase II study of tirapazamine plus cisplatin in patients with advanced or recurrent cervical cancer Int. J. Gynecol. Cancer 16, 1165-1171
8. Ihsan, A., Wang, X., Tu, H. G., Zhang, W., Dai, M. H., Peng, D. P., Wang, Y. L., Huang, L. L., Chen, D. M., Mannan, S., Tao, Y. F., Liu, Z. L., and Yuan, Z. H. (2013) Genotoxicity evaluation of mequindox in different short-term tests Food Chem. Toxicol. 51, 330-336
9. Ihsan, A., Wang, X., Zhang, W., Tu, H., Wang, Y., Huang, L., Iqbal, Z., Cheng, G., Pan, Y., Liu, Z., Tan, Z., Zhang, Y., and Yuan, Z. (2013) Genotoxicity of quinocetone, cyadox and olaquindox in vitro and in vivo Food Chem. Toxicol. 59C, 207-214
10. Wang, X., Zhang, W., Wang, Y., Peng, D., Ihsan, A., Huang, X., Huang, L., Liu, Z., Dai, M., Zhou, W., and Yuan, Z. H. (2010) Acute and sub-chronic oral toxicological evaluations of quinocetone in Wistar rats Regul. Toxicol. Pharmacol. 58, 421-427
11. Ihsan, A., Wang, X., Huang, X. J., Liu, Y., Liu, Q., Zhou, W., and Yuan, Z. H. (2010) Acute and subchronic toxicological evaluation of mequindox in Wistar rats Regul. Toxicol. Pharmacol. 57, 307-314
12. Chen, Q., Tang, S., Jin, X., Zou, J., Chen, K., Zhang, T., and Xiao, X. (2009) Investigation of the genotoxicity of quinocetone, carbadox and olaquindox in vitro using Vero cells Food Chem. Toxicol. 47, 328-334
13. Fang, G., He, Q., Zhou, S., Wang, D., Zhang, Y., and Yuan, Z. (2006) Subchronic oral toxicity study with cyadox in Wistar rats Food Chem. Toxicol. 44, 36-41
14. Wang, X., He, Q. H., Wang, Y. L., Ihsan, A., Huang, L. L., Zhou, W., Su, S. J., Liu, Z. L., and Yuan, Z. H. (2011) A chronic toxicity study of cyadox in Wistar rats Regul. Toxicol. Pharmacol. 59, 324-333
15. Nunoshiba, T. and Nishioka, H. (1989) Genotoxicity of quinoxaline 1,4-dioxide derivatives in Escherichia coli and Salmonella typhimurium Mutat. Res. 217, 203-209
16. Scheutwinkel-Reich, M. and Hude, W. v. d. (1984) Sister-chromatid exchange in Chinese hamster V79 cells exposed to quindoxin, carbadox and olaquindox Mutat. Res. 139, 199-202
17. Beutin, L., Preller, E., and Kowalski, B. (1981) Mutagenicity of quindoxin, its metabolites, and two substituted quinoxaline-di- N -oxides Antimicrob. Agents Chemother. 20, 336-343
18. Yoshimura, H., Nakamura, M., Koeda, T., and Yoshikawa, K. (1981) Mutagenicities of carbadox and olaquindox-growth promoters for pigs Mutat. Res. 90, 49-55
19. Cerna, M. and Angelis, K. (1986) Mutagenic action of the quinoxaline-type growth promotors on microorganisms Biol. Chem. Zivocisne Vyroby-Vet. 22, 9-15
20. Wang, X., Huang, X. J., Ihsan, A., Liu, Z. Y., Huang, L. L., Zhang, H. H., Zhang, H. F., Zhou, W., Liu, Q., Xue, X. J., and Yuan, Z. H. (2011) Metabolites and JAK/STAT pathway were involved in the liver and spleen damage in male Wistar rats fed with mequindox Toxicology 280, 126-134
21. Liu, Z., Huang, L., Dai, M., Chen, D., Tao, Y., Wang, Y., and Yuan, Z. (2009) Metabolism of cyadox in rat, chicken and pig liver microsomes and identification of metabolites by accurate mass measurements using electrospray ionization hybrid ion trap/time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 23, 2026-2034
22. Liu, Z., Huang, L., Dai, M., Chen, D., Wang, Y., Tao, Y., and Yuan, Z. (2008) Metabolism of olaquindox in rat liver microsomes: structural elucidation of metabolites by high-performance liquid chromatography combined with ion trap/time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 22, 1009-1016
23. Liu, Z. Y., Huang, L. L., Chen, D. M., Dai, M. H., Tao, Y. F., Wang, Y. L., and Yuan, Z. H. (2010) Application of electrospray ionization hybrid ion trap/time-of-flight mass spectrometry in the rapid characterization of quinocetone metabolites formed in vitro Anal. Bioanal. Chem. 396, 1259-1271
24. Liu, Z. Y., Huang, L. L., Chen, D. M., Dai, M. H., Tao, Y. F., and Yuan, Z. H. (2010) The metabolism and N-oxide reduction of olaquindox in liver preparations of rats, pigs and chicken Toxicol. Lett. 195, 51-59
25. Liu, Z. Y., Huang, L. L., Chen, D. M., and Yuan, Z. H. (2010) Metabolism of mequindox in liver microsomes of rats, chicken and pigs Rapid Commun. Mass Spectrom. 24, 909-918
26. Liu, Z. Y., Tao, Y. F., Chen, D. M., Wang, X., and Yuan, Z. H. (2011) Identification of carbadox metabolites formed by liver microsomes from rats, pigs and chickens using high-performance liquid chromatography combined with hybrid ion trap/time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 25, 341-348
27. Huang, X. J., Wang, X., Ihsan, A., Liu, Q., Xue, X. J., Su, S. J., Yang, C. H., Zhou, W., and Yuan, Z. H. (2010) Interactions of NADPH oxidase, renin-angiotensin-aldosterone system and reactive oxygen species in mequindox-mediated aldosterone secretion in Wistar rats Toxicol. Lett. 198, 112-118
28. Amin, K. M., Ismail, M. M., Noaman, E., Soliman, D. H., and Ammar, Y. A. (2006) New quinoxaline 1,4-di- N -oxides. Part 1: Hypoxia-selective cytotoxins and anticancer agents derived from quinoxaline 1,4-di- N -oxides Bioorg. Med. Chem. 14, 6917-6923
29. Ganley, B., Chowdhury, G., Bhansali, J., Daniels, J. S., and Gates, K. S. (2001) Redox-activated, hypoxia-selective DNA cleavage by quinoxaline 1,4-di- N -oxide Bioorg. Med. Chem. 9, 2395-2401
30. Ismail, M. M., Amin, K. M., Noaman, E., Soliman, D. H., and Ammar, Y. A. (2010) New quinoxaline 1, 4-di- N -oxides: anticancer and hypoxia-selective therapeutic agents Eur. J. Med. Chem. 45, 2733-2738
31. Voogd, C. E., van der Stel, J. J., and Jacobs, J. J. (1980) The mutagenic action of quindoxin, carbadox, olaquindox and some other N-oxides on bacteria and yeast Mutat. Res. 78, 233-242
32. Azqueta, A., Arbillaga, L., Pachon, G., Cascante, M., Creppy, E. E., and Lopez de Cerain, A. (2007) A quinoxaline 1,4-di- N -oxide derivative induces DNA oxidative damage not attenuated by vitamin C and E treatment Chem.-Biol. Interact. 168, 95-105
33. Chowdhury, G., Kotandeniya, D., Daniels, J. S., Barnes, C. L., and Gates, K. S. (2004) Enzyme-activated, hypoxia-selective DNA damage by 3-amino-2-quinoxalinecarbonitrile 1,4-di- N -oxide Chem. Res. Toxicol. 17, 1399-1405
34. Lam, W. and Ramanathan, R. (2002) In electrospray ionization source hydrogen/deuterium exchange LC-MS and LC-MS/MS for characterization of metabolites J. Am. Soc. Mass Spectrom. 13, 345-353
35. Durand, S., Legeret, B., Martin, A. S., Sancelme, M., Delort, A. M., Besse-Hoggan, P., and Combourieu, B. (2006) Biotransformation of the triketone herbicide mesotrione by a Bacillus strain. Metabolite profiling using liquid chromatography/electrospray ionization quadrupole time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 20, 2603-2613
36. - (1996) Guide for the Care and Use of Laboratory Animals, National Research Council, National Academy Press, Washington, DC.
37. Liu, X. L., Li, L. J., and Chen, Z. (2002) Isolation and primary culture of rat hepatocytes Hepatobiliary Pancreatic Dis. Int. 1, 77-79
38. Krishnaswamy, R., Devaraj, S. N., and Padma, V. V. (2010) Lutein protects HT-29 cells against deoxynivalenol-induced oxidative stress and apoptosis: prevention of NF-kappaB nuclear localization and down regulation of NF-kappaB and cyclo-oxygenase-2 expression Free Radical Biol. Med. 49, 50-60
39. 2 availability to ARPE-19 cultures in models of oxidative stress Free Radical Biol. Med. 48, 1064-1070
40. Selvendiran, K., Ahmed, S., Dayton, A., Kuppusamy, M. L., Tazi, M., Bratasz, A., Tong, L., Rivera, B. K., Kalai, T., Hideg, K., and Kuppusamy, P. (2010) Safe and targeted anticancer efficacy of a novel class of antioxidant-conjugated difluorodiarylidenyl piperidones: differential cytotoxicity in healthy and cancer cells Free Radical Biol. Med. 48, 1228-1235
41. Jain, S., Jain, A. K., Pohekar, M., and Thanki, K. (2013) Novel self-emulsifying formulation of quercetin for improved in vivo antioxidant potential: Implications for drug-induced cardiotoxicity and nephrotoxicity Free Radical Biol. Med. 65C, 117-130
42. Lee, K. K., Fujimoto, K., Zhang, C., Schwall, C. T., Alder, N. N., Pinkert, C. A., Krueger, W., Rasmussen, T., and Boelsterli, U. A. (2013) Isoniazid-induced cell death is precipitated by underlying mitochondrial complex I dysfunction in mouse hepatocytes Free Radical Biol. Med. 65, 584-594
43. Singh, N. P., McCoy, M. T., Tice, R. R., and Schneider, E. L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells Exp. Cell Res. 175, 184-191
44. Duez, P., Dehon, G., Kumps, A., and Dubois, J. (2003) Statistics of the comet assay: a key to discriminate between genotoxic effects Mutagenesis. 18, 159-166
45. Brown, J. M. (2000) Exploiting the hypoxic cancer cell: mechanisms and therapeutic strategies Mol. Med. Today 6, 157-162
46. Evans, J. W., Yudoh, K., Delahoussaye, Y. M., and Brown, J. M. (1998) Tirapazamine is metabolized to its DNA-damaging radical by intranuclear enzymes Cancer Res. 58, 2098-2101
47. Jin, X., Chen, Q., Tang, S. S., Zou, J. J., Chen, K. P., Zhang, T., and Xiao, X. L. (2009) Investigation of quinocetone-induced genotoxicity in HepG2 cells using the comet assay, cytokinesis-block micronucleus test and RAPD analysis Toxicol. In Vitro 23, 1209-1214
48. Zou, J., Chen, Q., Tang, S., Jin, X., Chen, K., Zhang, T., and Xiao, X. (2009) Olaquindox-induced genotoxicity and oxidative DNA damage in human hepatoma G2 (HepG2) cells Mutat. Res. 676, 27-33
49. Nonaka, Y., Fujii, S., and Yamano, T. (1986) The semiquinone state of NADPH-adrenodoxin oxidoreductase in the course of anaerobic reduction with NADPH J. Biochem. 99, 803-814
50. Fotakis, G. and Timbrell, J. A. (2006) In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride Toxicol. Lett. 160, 171-177