Emodin triggers DNA double-strand breaks by stabilizing topoisomerase II-DNA cleavage complexes and by inhibiting ATP hydrolysis of topoisomerase II

Toxicological Sciences

Volumn 118, Issue 2, 2010, Pages 435-443

  Li, Yan ^a   Luan, Yang ^a   Qi, Xinming ^a   Li, Ming ^a   Gong, Likun ^a   Xue, Xiang ^a   Wu, Xiongfei ^a   Wu, Yuanfeng ^a   Chen, Min ^a   Xing, Guozhen ^a   Yao, Jun ^a   Ren, Jin ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

ATP hydrolysis; Cleavage complexes; DNA double strand breaks; Emodin; Topoisomerase II

Indexed keywords

ACLARUBICIN; ADENOSINE TRIPHOSPHATE; ATM PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); EMODIN; HISTONE H2AX; KINETOPLAST DNA; MITOXANTRONE; THYMIDINE KINASE;

ARTICLE; DNA CLEAVAGE; DNA PROTEIN COMPLEX; DOUBLE STRANDED DNA BREAK; ENZYME INHIBITION; GENE MUTATION; GENOTOXICITY; HUMAN; HUMAN CELL; MICRONUCLEUS TEST; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATE; CELL LINE, TUMOR; COMET ASSAY; DNA BREAKS, DOUBLE-STRANDED; DNA TOPOISOMERASES, TYPE II; EMODIN; HUMANS; HYDROLYSIS; MICRONUCLEUS TESTS; MUTAGENS; MUTATION; THYMIDINE KINASE; TOPOISOMERASE II INHIBITORS;

ATAXIA TELANGIECTASIA; FUNGI; SALMONELLA;

EID: 78549231954     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq282     Document Type: Article

References (48)

1. Antony, S., Agama, K. K., Miao, Z. H., Takagi, K., Wright, M. H., Robles, A. I., Varticovski, L., Nagarajan, M., Morrell, A., Cushman, M., et al. (2007). Novel indenoisoquinolines NSC 725776 and NSC 724998 produce persistent topoisomerase I cleavage complexes and overcome multidrug resistance. Cancer Res. 67, 10397-10405.
2. Bridgewater, L. C., Manning, F. C., Woo, E. S., and Patierno, S. R. (1994). DNA polymerase arrest by adducted trivalent chromium. Mol. Carcinog. 9, 122-133.
3. Cao, L., Alani, E., and Kleckner, N. (1990). A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61, 1089-1101.
4. Champoux, J. J. (2001). DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413.
5. Classen, S., Olland, S., and Berger, J. M. (2003). Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc. Natl. Acad. Sci. U.S.A. 100, 10629.
6. Ewing, T. J. A., and Kuntz, I. D. (1997). Critical evaluation of search algorithms for automated molecular docking and database screening. J. Comput. Chem. 18, 1175-1189.
7. Felix, C. A. (2001). Leukemias related to treatment with DNA topoisomerase II inhibitors. Med. Pediatr. Oncol. 36, 525-535.
8. Ferguson, L. R., and Baguley, B. C. (2006). Topoisomerase II enzymes and mutagenicity. Environ. Mol. Mutagen. 24, 245-261.
9. Gupta, R. S., Bromke, A., Bryant, D. W., Gupta, R., Singh, B., and McCalla, D. R. (1987). Etoposide (VP16) and teniposide (VM26): novel anticancer drugs, strongly mutagenic in mammalian but not prokaryotic test systems. Mutagenesis 2, 179-186.
10. Harker, W. G., Slade, D. L., Drake, F. H., and Parr, R. L. (1991). Mitoxantrone resistance in HL-60 leukemia cells: reduced nuclear topoisomerase II catalytic activity and drug-induced DNA cleavage in association with reduced expression of the topoisomerase II. beta. isoform. Biochemistry 30, 9953-9961.
11. Harkins, T. T., Lewis, T. J., and Lindsley, J. E. (1998). Pre-steady-state analysis of ATP hydrolysis by Saccharomyces cerevisiae DNA topoisomerase II. 2. Kinetic mechanism for the sequential hydrolysis of two ATP. Biochemistry 37, 7299-7312.
12. Hu, C. X., Zuo, Z. L., Xiong, B., Ma, J. G., Geng, M. Y., Lin, L. P., Jiang, H. L., and Ding, J. (2006). Salvicine functions as novel topoisomerase II poison by binding to ATP pocket. Mol. Pharmacol. 70, 1593.
13. Huang, K. C., Gao, H., Yamasaki, E. F., Grabowski, D. R., Liu, S., Shen, L. L., Chan, K. K., Ganapathi, R., and Snapka, R. M. (2001). Topoisomerase II poisoning by ICRF-193. J. Biol. Chem. 276, 44488.
14. Kingma, P. S., Fortune, J. M., and Osheroff, N. (2001). Topoisomerase II-catalyzed ATP hydrolysis as monitored by thin-layer chromatography. Methods Mol. Biol. 95, 51-56.
15. Kong, X. B., Rubin, L., Chen, L. I., Ciszewska, G., Watanabe, K. A., Tong, W. P., Sirotnak, F. M., and Chou, T. C. (1992). Topoisomerase II-mediated DNA cleavage activity and irreversibility of cleavable complex formation induced by DNA intercalator with alkylating capability. Mol. Pharmacol. 41, 237-244.
16. Krivobok, S., Seigle-Murandi, F., Steiman, R., Marzin, D. R., and Betina, V. (1992). Mutagenicity of substituted anthraquinones in the Ames/Salmonella microsome system. Mutat. Res. 279, 1-8.
17. Kuo, L. J., and Yang, L. X. (2008). Gamma-H2AX-a novel biomarker for DNA double-strand breaks. In Vivo 22, 305-309.
18. Lähdetie, J., Keiski, A., Suutari, A., and Toppari, J. (2006). Etoposide (VP-16) is a potent inducer of micronuclei in male rat meiosis: spermatid micronucleus test and DNA flow cytometry after etoposide treatment. Environ. Mol. Mutagen. 24, 192-202.
19. Lamartiniere, C. A. (2000). Protection against breast cancer with genistein: a component of soy. Am. J. Clin. Nutr. 71, 1705S-1707S; discussion 1708S-1709S.
20. McClendon, A. K., and Osheroff, N. (2007). DNA topoisomerase II, genotoxicity, and cancer. Mutat. Res. 623, 83-97.
21. Mengs, U., Grimminger, W., Krumbiegel, G., Schuler, D., Silber, W., and Völkner, W. (1999). No clastogenic activity of a senna extract in the mouse micronucleus assay. Mutat. Res. 444, 421-426.
22. Mori, H., Sugie, S., Niwa, K., Takahashi, M., and Kawai, K. (1985). Induction of intestinal tumours in rats by chrysazin. Br. J. Cancer. 52, 781-783.
23. Mori, H., Sugie, S., Niwa, K., Yoshimi, N., Tanaka, T., and Hirono, I. (1986). Carcinogenicity of chrysazin in large intestine and liver of mice. Jpn. J. Cancer Res. 77, 871.
24. Mueller, S. O., Schmitt, M., Dekant, W., Stopper, H., Schlatter, J., Schreier, P., and Lutz, W. K. (1999). Occurrence of emodin, chrysophanol and physcion in vegetables, herbs and liquors. Genotoxicity and antigenotoxicity of the anthraquinones and of the whole plants. Food Chem. Toxicol. 37, 481-491.
25. Mueller, S. O., and Stopper, H. (1999). Characterization of the genotoxicity of anthraquinones in mammalian cells. Biochim. Biophys. Acta. 1428, 406-414.
26. Müller, S. O., Eckert, I., Lutz, W. K., and Stopper, H. (1996). Genotoxicity of the laxative drug components emodin, aloe-emodin and danthron in mammalian cells: topoisomerase II mediated? Mutat. Res. 371, 165-173.
27. National Toxicology Program (NTP). (2001). NTP toxicology and, carcinogenesis studies of EMODIN (CAS NO. 518-82-1) feed studies in F344/N rats and B6C3F1 mice. Natl. Toxicol. Program Tech. Rep. Ser. 493, 1-278.
28. Nusko, G., Schneider, B., Muller, G., Kusche, J., and Hahn, E. G. (1993). Retrospective study on laxative use and melanosis coli as risk factors for colorectal neoplasma. Pharmacology 47(Suppl. 1), 234-241.
29. Olive, P. L. (1999). DNA damage and repair in individual cells: applications of the comet assay in radiobiology. Int. J. Radiat. Biol. 75, 395-405.
30. Osheroff, N., Shelton, E. R., and Brutlag, D. L. (1983). DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258, 9536.
31. Raghunand, N., He, X., Van Sluis, R., Mahoney, B., Baggett, B., Taylor, C. W., Paine-Murrieta, G., Roe, D., Bhujwalla, Z. M., and Gillies, R. J. (1999). Enhancement of chemotherapy by manipulation of tumour pH. Br. J. Cancer. 80, 1005.
32. Resnick, M. A. (1976). The repair of double-strand breaks in DNA: a model involving recombination+. J. Theor. Biol. 59, 97-106.
33. Roca, J., Ishida, R., Berger, J. M., Andoh, T., and Wang, J. C. (1994). Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. U.S.A. 91, 1781.
34. Sahai, B. M., and Kaplan, J. G. (1986). A quantitative decatenation assay for type II topoisomerases. Anal. Biochem. 156, 364-379.
35. Singer, S., Souza, K., and Thilly, W. G. (1995). Pyruvate utilization, phosphocholine and adenosine triphosphate (ATP) are markers of human breast tumor progression: a 31P-and 13C-nuclear magnetic resonance (NMR) spectroscopy study. Cancer Res. 55, 5140.
36. 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.
37. Smart, D. J., Halicka, H. D., Schmuck, G., Traganos, F., Darzynkiewicz, Z., and Williams, G. M. (2008). Assessment of DNA double-strand breaks and gammaH2AX induced by the topoisomerase II poisons etoposide and mitoxantrone. Mutat. Res. 641, 43-47.
38. Takahashi, A., Mori, E., and Ohnishi, T. (2010). The foci of DNA double strand break-recognition proteins localize with gammaH2AX after heat treatment. J. Radiat. Res. (Tokyo) 51, 91-95.
39. Tikkanen, L., Matsushima, T., and Natori, S. (1983). Mutagenicity of anthraquinones in the Salmonella preincubation test. Mutat. Res. 116, 297-304.
40. Velez-Cruz, R., and Osheroff, N. (2004). Topoisomerases: eukaryotic and prokaryotic type II. In Encyclopedia of Molecular Biology (W. Lennarz and M. D. Lane, Eds.), pp. 806-811. Elsevier Science, San Diego, CA.
41. Wada, S., Kurahayashi, H., Kobayashi, Y., Funayama, T., Yamamoto, K., Natsuhori, M., and Ito, N. (2003). The relationship between cellular radiosensitivity and radiation-induced DNA damage measured by the comet assay. J. Vet. Med. Sci. 65, 471-477.
42. Wei, H., Ruthenburg, A. J., Bechis, S. K., and Verdine, G. L. (2005). Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem. 280, 37041.
43. Westendorf, J., Marquardt, H., Poginsky, B., Dominiak, M., Schmidt, J., and Marquardt, H. (1990). Genotoxicity of naturally occurring hydroxyanthraquinones. Mutat. Res. 240, 1-12.
44. Wilstermann, A. M., and Osheroff, N. (2003). Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem. 3, 321-338.
45. Yamashita, Y., Fujii, N., Murakata, C., Ashizawa, T., Okabe, M., and Nakano, H. (1992). Induction of mammalian DNA topoisomerase I mediated DNA cleavage by antitumor indolocarbazole derivatives. Biochemistry 31, 12069-12075.
46. Zhan, L., Sakamoto, H., Sakuraba, M., Wu, D. S., Zhang, L. S., Suzuki, T., Hayashi, M., and Honma, M. (2004). Genotoxicity of microcystin-LR in human lymphoblastoid TK6 cells. Mutat. Res. 557, 1-6.
47. Zhou, S. F., Xue, C. C., Yu, X. Q., and Wang, G. (2007). Metabolic activation of herbal and dietary constituents and its clinical and toxicological implications: an update. Curr. Drug Metab. 8, 526-553.
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.