Natural products as topoisomerase II poisons: Effects of thymoquinone on DNA cleavage mediated by human topoisomerase IIα

Chemical Research in Toxicology

Volumn 27, Issue 5, 2014, Pages 787-793

  Ashley, Rachel E ^a   Osheroff, Neil ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BLACK SEED EXTRACT; BLACK SEED OIL; DNA TOPOISOMERASE (ATP HYDROLYSING) A; ENZYME INHIBITOR; ETOPOSIDE; PLANT EXTRACT; POISON; QUINONE DERIVATIVE; THYMOQUINONE; UNCLASSIFIED DRUG; VEGETABLE OIL; BENZOQUINONE DERIVATIVE; BIOLOGICAL PRODUCT; DNA BINDING PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE II ALPHA; TUMOR ANTIGEN;

ACYLATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLACK CUMIN; CONFORMATIONAL TRANSITION; DNA CLEAVAGE; DNA STRAND; ELECTRON; ENZYME ACTIVITY; HUMAN; MUTAGENESIS; OXIDATION; PHYTOCHEMISTRY; PROTEIN CROSS LINKING; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; ISOLATION AND PURIFICATION; METABOLISM; PLANT SEED; TOXICITY;

ANTIGENS, NEOPLASM; BENZOQUINONES; BIOLOGICAL PRODUCTS; DNA CLEAVAGE; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; HUMANS; NIGELLA SATIVA; SEEDS;

EID: 84901047563     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx400453v     Document Type: Article

References (53)

1. Gali-Muhtasib, H., Roessner, A., and Schneider-Stock, R. (2006) Thymoquinone: A promising anti-cancer drug from natural sources Int. J. Biochem. Cell Biol. 38, 1249-1253
2. Burits, M. and Bucar, F. (2000) Antioxidant activity of Nigella sativa essential oil Phytother. Res. 14, 323-328 (Pubitemid 30655515)
3. Hajhashemi, V., Ghannadi, A., and Jafarabadi, H. (2004) Black cumin seed essential oil, as a potent analgesic and antiinflammatory drug Phytother. Res. 18, 195-199 (Pubitemid 38568744)
4. Zohary, D. and Hopf, M. (2000) Domestication of Plants in the Old World: The Origin and Spread of Cultivated Plants in West Asia, Europe, and the Nile Valley, 3 rd ed., Oxford University Press, New York.
5. Badary, O. A., Taha, R. A., Gamal el-Din, A. M., and Abdel-Wahab, M. H. (2003) Thymoquinone is a potent superoxide anion scavenger Drug Chem. Toxicol. 26, 87-98 (Pubitemid 36597385)
6. Sayed, M. D. (1980) Traditional medicine in health care J. Ethnopharmacol. 2, 19-22 (Pubitemid 10075654)
7. Khader, M., Bresgen, N., and Eckl, P. M. (2009) In vitro toxicological properties of thymoquinone Food Chem. Toxicol. 47, 129-133
8. Salomi, M. J., Nair, S. C., and Panikkar, K. R. (1991) Inhibitory effects of Nigella sativa and saffron (Crocus sativus) on chemical carcinogenesis in mice Nutr. Cancer 16, 67-72
9. Swamy, S. M. and Tan, B. K. (2000) Cytotoxic and immunopotentiating effects of ethanolic extract of Nigella sativa L. seeds J. Ethnopharmacol. 70, 1-7 (Pubitemid 30138064)
10. Mabrouk, G. M., Moselhy, S. S., Zohny, S. F., Ali, E. M., Helal, T. E., Amin, A. A., and Khalifa, A. A. (2002) Inhibition of methylnitrosourea (MNU) induced oxidative stress and carcinogenesis by orally administered bee honey and Nigella grains in Sprague Dawely rats J. Exp. Clin. Cancer Res. 21, 341-346
11. 2 Int. J. Environ. Res. Public Health 2, 411-419 (Pubitemid 47618950)
12. Farah, I. O. and Begum, R. A. (2003) Effect of Nigella sativa (N. sativa L.) and oxidative stress on the survival pattern of MCF-7 breast cancer cells Biomed. Sci. Instrum. 39, 359-364 (Pubitemid 36433453)
13. Hasan, T. N., Shafi, G., Syed, N. A., Alfawaz, M. A., Alsaif, M. A., Munshi, A., Lei, K. Y., and Alshatwi, A. A. (2013) Methanolic extract of Nigella sativa seed inhibits SiHa human cervical cancer cell proliferation through apoptosis Nat. Prod. Commun. 8, 213-216
14. Woo, C. C., Kumar, A. P., Sethi, G., and Tan, K. H. (2012) Thymoquinone: Potential cure for inflammatory disorders and cancer Biochem. Pharmacol. 83, 443-451
15. Badary, O. A., Al-Shabanah, O. A., Nagi, M. N., Al-Rikabi, A. C., and Elmazar, M. M. (1999) Inhibition of benzo(a)pyrene-induced forestomach carcinogenesis in mice by thymoquinone Eur. J. Cancer Prev. 8, 435-440 (Pubitemid 30048073)
16. Badary, O. A. and Gamal El-Din, A. M. (2001) Inhibitory effects of thymoquinone against 20-methylcholanthrene-induced fibrosarcoma tumorigenesis Cancer Detect. Prev. 25, 362-368
17. Banerjee, S., Padhye, S., Azmi, A., Wang, Z., Philip, P. A., Kucuk, O., Sarkar, F. H., and Mohammad, R. M. (2010) Review on molecular and therapeutic potential of thymoquinone in cancer Nutr. Cancer 62, 938-946
18. Lindsey, R. H., Jr., Bromberg, K. D., Felix, C. A., and Osheroff, N. (2004) 1,4-Benzoquinone is a topoisomerase II poison Biochemistry 43, 7563-7574 (Pubitemid 38745772)
19. Deweese, J. E. and Osheroff, N. (2009) The DNA cleavage reaction of topoisomerase II: Wolf in sheep's clothing Nucleic Acids Res. 37, 738-749
20. Champoux, J. J. (2001) DNA topoisomerases: Structure, function, and mechanism Annu. Rev. Biochem. 70, 369-413 (Pubitemid 32662215)
21. Nitiss, J. L. (2009) DNA topoisomerase II and its growing repertoire of biological functions Nat. Rev. Cancer 9, 327-337
22. Pommier, Y., Leo, E., Zhang, H., and Marchand, C. (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs Chem. Biol. 17, 421-433
23. Vos, S. M., Tretter, E. M., Schmidt, B. H., and Berger, J. M. (2011) All tangled up: How cells direct, manage and exploit topoisomerase function Nat. Rev. Mol. Cell Biol. 12, 827-841
24. Wang, J. C. (2002) Cellular roles of DNA topoisomerases: A molecular perspective Nat. Rev. Mol. Cell Biol. 3, 430-440 (Pubitemid 34685700)
25. Liu, Z., Deibler, R. W., Chan, H. S., and Zechiedrich, L. (2009) The why and how of DNA unlinking Nucleic Acids Res. 37, 661-671
26. Nitiss, J. L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy Nat. Rev. Cancer 9, 338-350
27. Austin, C. A., Patel, S., Ono, K., Nakane, H., and Fisher, L. M. (1992) Site-specific DNA cleavage by mammalian DNA topoisomerase II induced by novel flavone and catechin derivatives Biochem. J. 282, 883-889
28. Bandele, O. J. and Osheroff, N. (2007) Bioflavonoids as poisons of human topoisomerase IIα and IIβ Biochemistry 46, 6097-6108
29. Bandele, O. J. and Osheroff, N. (2008) (-)-Epigallocatechin gallate, a major constituent of green tea, poisons human type II topoisomerases Chem. Res. Toxicol. 21, 936-943 (Pubitemid 351644572)
30. Bandele, O. J., Clawson, S. J., and Osheroff, N. (2008) Dietary polyphenols as topoisomerase II poisons: B ring and C ring substituents determine the mechanism of enzyme-mediated DNA cleavage enhancement Chem. Res. Toxicol. 21, 1253-1260 (Pubitemid 351967390)
31. Lopez-Lazaro, M., Willmore, E., and Austin, C. A. (2010) The dietary flavonoids myricetin and fisetin act as dual inhibitors of DNA topoisomerases I and II in cells Mutat. Res. 696, 41-47
32. Lopez-Lazaro, M., Willmore, E., Jobson, A., Gilroy, K. L., Curtis, H., Padget, K., and Austin, C. A. (2007) Curcumin induces high levels of topoisomerase I- and II-DNA complexes in K562 leukemia cells J. Nat. Prod. 70, 1884-1888
33. Lin, R. K., Zhou, N., Lyu, Y. L., Tsai, Y. C., Lu, C. H., Kerrigan, J., Chen, Y. T., Guan, Z., Hsieh, T. S., and Liu, L. F. (2011) Dietary isothiocyanate-induced apoptosis via thiol modification of DNA topoisomerase IIα J. Biol. Chem. 286, 33591-33600
34. Ketron, A. C., Gordon, O. N., Schneider, C., and Osheroff, N. (2012) Oxidative metabolites of curcumin poison human type II topoisomerases Biochemistry 52, 221-227
35. Timmel, M. A., Byl, J. A., and Osheroff, N. (2013) Epimerization of green tea catechins during brewing does not affect the ability to poison human type II topoisomerases Chem. Res. Toxicol. 26, 622-628
36. Ketron, A. and Osheroff, N. (2014) Phytochemicals as anticancer and chemopreventive topoisomerase II poisons Phytochem. Rev. 13, 19-35
37. Kingma, P. S., Greider, C. A., and Osheroff, N. (1997) Spontaneous DNA lesions poison human topoisomerase IIα and stimulate cleavage proximal to leukemic 11q23 chromosomal breakpoints Biochemistry 36, 5934-5939 (Pubitemid 27257858)
38. Worland, S. T. and Wang, J. C. (1989) Inducible overexpression, purification, and active site mapping of DNA topoisomerase II from the yeast Saccharomyces cerevisiae J. Biol. Chem. 264, 4412-4416 (Pubitemid 19081341)
39. Bender, R. P., Ham, A. J., and Osheroff, N. (2007) Quinone-induced enhancement of DNA cleavage by human topoisomerase IIα: Adduction of cysteine residues 392 and 405 Biochemistry 46, 2856-2864 (Pubitemid 46420241)
40. Fortune, J. M. and Osheroff, N. (1998) Merbarone inhibits the catalytic activity of human topoisomerase IIα by blocking DNA cleavage J. Biol. Chem. 273, 17643-17650 (Pubitemid 28355102)
41. Byl, J. A., Fortune, J. M., Burden, D. A., Nitiss, J. L., Utsugi, T., Yamada, Y., and Osheroff, N. (1999) DNA topoisomerases as targets for the anticancer drug TAS-103: Primary cellular target and DNA cleavage enhancement Biochemistry 38, 15573-15579 (Pubitemid 129503599)
42. Gentry, A. C., Pitts, S. L., Jablonsky, M. J., Bailly, C., Graves, D. E., and Osheroff, N. (2011) Interactions between the etoposide derivative F14512 and human type II topoisomerases: Implications for the C4 spermine moiety in promoting enzyme-mediated DNA cleavage Biochemistry 50, 3240-3249
43. Osheroff, N. (1986) Eukaryotic topoisomerase II. Characterization of enzyme turnover J. Biol. Chem. 261, 9944-9950 (Pubitemid 17214132)
44. Osheroff, N., Shelton, E. R., and Brutlag, D. L. (1983) DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA J. Biol. Chem. 258, 9536-9543
45. Bender, R. P., Jablonksy, M. J., Shadid, M., Romaine, I., Dunlap, N., Anklin, C., Graves, D. E., and Osheroff, N. (2008) Substituents on etoposide that interact with human topoisomerase IIα in the binary enzyme-drug complex: Contributions to etoposide binding and activity Biochemistry 47, 4501-4509 (Pubitemid 351522100)
46. Pommier, Y. and Marchand, C. (2012) Interfacial inhibitors: Targeting macromolecular complexes Nat. Rev. Drug Discovery 11, 25-36
47. Lindsey, R. H., Bender, R. P., and Osheroff, N. (2005) Stimulation of topoisomerase II-mediated DNA cleavage by benzene metabolites Chem.-Biol. Interact. 153-154, 197-205 (Pubitemid 40797811)
48. Bender, R. P. and Osheroff, N. (2007) Mutation of cysteine residue 455 to alanine in human topoisomerase IIα confers hypersensitivity to quinones: Enhancing DNA scission by closing the N-terminal protein gate Chem. Res. Toxicol. 20, 975-981 (Pubitemid 47035352)
49. Wang, H., Mao, Y., Chen, A. Y., Zhou, N., LaVoie, E. J., and Liu, L. F. (2001) Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation Biochemistry 40, 3316-3323 (Pubitemid 32221633)
50. Bender, R. P., Lehmler, H. J., Robertson, L. W., Ludewig, G., and Osheroff, N. (2006) Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIα: Altering enzyme function by blocking the N-terminal protein gate Biochemistry 45, 10140-10152 (Pubitemid 44257408)
51. Mondrala, S. and Eastmond, D. A. (2010) Topoisomerase II inhibition by the bioactivated benzene metabolite hydroquinone involves multiple mechanisms Chem.-Biol. Interact. 184, 259-268
52. Jacob, D. A., Mercer, S. L., Osheroff, N., and Deweese, J. E. (2011) Etoposide quinone is a redox-dependent topoisomerase II poison Biochemistry 50, 5660-5667
53. Bender, R. P., Lindsey, R. H., Jr., Burden, D. A., and Osheroff, N. (2004) N -Acetyl- p -benzoquinone imine, the toxic metabolite of acetaminophen, is a topoisomerase II poison Biochemistry 43, 3731-3739 (Pubitemid 38391728)