Ginkgo biloba leaf extract induces DNA damage by inhibiting topoisomerase II activity in human hepatic cells

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Zhang, Zhuhong ^a   Chen, Si ^a   Mei, Hu ^b   Xuan, Jiekun ^a   Guo, Xiaoqing ^a   Couch, Letha ^a   Dobrovolsky, Vasily N ^a   Guo, Lei ^a   Mei, Nan ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b CHONGQING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); GYRASE INHIBITOR; MUTAGENIC AGENT; PLANT EXTRACT; QUERCETIN;

CHEMISTRY; CONFORMATION; DNA DAMAGE; DRUG EFFECTS; ENZYME ACTIVATION; GENE SILENCING; GENETICS; GINKGO BILOBA; HEP-G2 CELL LINE; HUMAN; LIVER CELL; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; PLANT LEAF;

DNA DAMAGE; DNA TOPOISOMERASES, TYPE II; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GINKGO BILOBA; HEP G2 CELLS; HEPATOCYTES; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTAGENS; PLANT EXTRACTS; PLANT LEAVES; QUERCETIN; TOPOISOMERASE II INHIBITORS;

EID: 84942884282     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14633     Document Type: Article

References (54)

1. EGb. EGb 761: ginkgo biloba extract, Ginkor. Drugs R. D. 4, 188-193 (2003).
2. Van Beek, T. A., Montoro, P. Chemical analysis and quality control of Ginkgo biloba leaves, extracts, and phytopharmaceuticals. J. Chromatogr. A 1216, 2002-2032 (2009).
3. Lindstrom, A., Ooyen, C., Lynch, M. E., Bluementhal, M. Herb supplement sales increase 5.5% in 2012: Herbal supplement sales rise for 9th consecutive year; turmeric sales jump 40% in natural channel. HerbalGram 99, 60-65 (2013).
4. NBJ. Supplement business report (ed. Nutritional Business Journal) (Penton Media Inc, 2013).
5. NTP. Toxicology and carcinogenesis studies of Ginkgo biloba extract (CAS No. 90045-36-6) in F344/N rats and B6C3F1/N mice (Gavage studies). Natl. Toxicol. Program Tech. Rep. Ser. 578, 1-183 (2013).
6. Lin, H. et al. Mechanistic evaluation of Ginkgo biloba leaf extract-induced genotoxicity in L5178Y cells. Toxicol. Sci. 139, 338-349 (2014).
7. Ding, S. et al. Quantitative determination of major active components in Ginkgo biloba dietary supplements by liquid chromatography/mass spectrometry. Rapid Commun. Mass. Spectrom. 20, 2753-2760 (2006).
8. Russo, P., Del Bufalo, A., Cesario, A. Flavonoids acting on DNA topoisomerases: recent advances and future perspectives in cancer therapy. Curr. Med. Chem. 19, 5287-5293 (2012).
9. Champoux, J. J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413 (2001).
10. Vos, S. M., Tretter, E. M., Schmidt, B. H., Berger, J. M. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 12, 827-841 (2011).
11. McClendon, A. K., Osheroff, N. DNA topoisomerase II, genotoxicity, and cancer. Mutat. Res. 623, 83-97 (2007).
12. Bartek, J., Lukas, J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3, 421-429 (2003).
13. Larsen, A. K., Escargueil, A. E., Skladanowski, A. Catalytic topoisomerase II inhibitors in cancer therapy. Pharmacol. Ther. 99, 167-181 (2003).
14. Wilstermann, A. M., Osheroff, N. Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem. 3, 321-338 (2003).
15. Smart, D. J. Genotoxicity of topoisomerase II inhibitors: an anti-infective perspective. Toxicology 254, 192-198 (2008).
16. Boos, G., Stopper, H. Genotoxicity of several clinically used topoisomerase II inhibitors. Toxicol. Lett. 116, 7-16 (2000).
17. Pendleton, M., Lindsey, R. H., Jr., Felix, C. A., Grimwade, D., Osheroff, N. Topoisomerase II and leukemia. Ann. N. Y. Acad. Sci. 1310, 98-110 (2014).
18. Ross, J. A., Potter, J. D., Reaman, G. H., Pendergrass, T. W., Robison, L. L. Maternal exposure to potential inhibitors of DNA topoisomerase II and infant leukemia (United States): a report from the Children's Cancer Group. Cancer Causes & Control. CCC 7, 581-590 (1996).
19. Strick, R., Strissel, P. L., Borgers, S., Smith, S. L., Rowley, J. D. Dietary bioflavonoids induce cleavage in the MLL gene and may contribute to infant leukemia. Proc. Natl. Acad. Sci. USA. 97, 4790-4795 (2000).
20. Ferguson, L. R. Inhibitors of topoisomerase II enzymes: a unique group of environmental mutagens and carcinogens. Mutat. Res. 400, 271-278 (1998).
21. Ferguson, L. R., Baguley, B. C. Topoisomerase II enzymes and mutagenicity. Environ. Mol. Mutagen. 24, 245-261 (1994).
22. Walmsley, R. M., Tate, M. The GADD45a-GFP GreenScreen HC assay. Methods Mol. Biol. 817, 231-250 (2012).
23. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
24. Bensasson, R. V. et al. Potency of inhibition of human DNA topoisomerase I by flavones assessed through physicochemical parameters. Free Radic. Biol. Med. 51, 1406-1410 (2011).
25. Jang, S. Y. et al. Caffeic acid and quercitrin purified from Houttuynia cordata inhibit DNA topoisomerase I activity. Nat. Prod. Res. 25, 222-231 (2011).
26. Webb, M. R., Ebeler, S. E. Comparative analysis of topoisomerase IB inhibition and DNA intercalation by flavonoids and similar compounds: structural determinates of activity. Biochem. J. 384, 527-541 (2004).
27. Chen, S. et al. Mechanism study of goldenseal-associated DNA damage. Toxicol. Lett. 221, 64-72 (2013).
28. Resende, F. A., Vilegas, W., Dos Santos, L. C., Varanda, E. A. Mutagenicity of flavonoids assayed by bacterial reverse mutation (Ames) test. Molecules 17, 5255-5268 (2012).
29. Caria, H., Chaveca, T., Laires, A., Rueff, J. Genotoxicity of quercetin in the micronucleus assay in mouse bone marrow erythrocytes, human lymphocytes, V79 cell line and identification of kinetochore-containing (CREST staining) micronuclei in human lymphocytes. Mutat. Res. 343, 85-94 (1995).
30. Meltz, M. L., MacGregor, J. T. Activity of the plant flavanol quercetin in the mouse lymphoma L5178Y TK+/- mutation, DNA single-strand break, and Balb/c 3T3 chemical transformation assays. Mutat. Res. 88, 317-324 (1981).
31. Kressmann, S., Muller, W. E., Blume, H. H. Pharmaceutical quality of different Ginkgo biloba brands. J. Pharm. Pharmacol. 54, 661-669 (2002).
32. Lopez-Lazaro, M., Willmore, E., Austin, C. A. The dietary flavonoids myricetin and fisetin act as dual inhibitors of DNA topoisomerases I and II in cells. Mutat. Res. 696, 41-47 (2010).
33. Yamashita, Y. et al. Induction of mammalian DNA topoisomerase I mediated DNA cleavage by antitumor indolocarbazole derivatives. Biochemistry 31, 12069-12075 (1992).
34. Kanakis, C. D., Tarantilis, P. A., Polissiou, M. G., Diamantoglou, S., Tajmir-Riahi, H. A. An overview of DNA and RNA bindings to antioxidant flavonoids. Cell Biochem. Biophys. 49, 29-36 (2007).
35. Ando, M., Yoshikawa, K., Iwase, Y., Ishiura, S. Usefulness of Monitoring gamma-H2AX and Cell Cycle Arrest in HepG2 Cells for Estimating Genotoxicity Using a High-Content Analysis System. J. Biomol. Screen. 19, 1246-1254 (2014).
36. Nikoloff, N., Larramendy, M. L., Soloneski, S. Assessment of DNA damage, cytotoxicity, and apoptosis in human hepatoma (HepG2) cells after flurochloridone herbicide exposure. Food Chem. Toxicol. 65, 233-241 (2014).
37. Yoshitomi, S. et al. Establishment of the transformants expressing human cytochrome P450 subtypes in HepG2, and their applications on drug metabolism and toxicology. Toxicol. In Vitro 15, 245-256 (2001).
38. Hashizume, T. et al. Advantages of human hepatocyte-derived transformants expressing a series of human cytochrome p450 isoforms for genotoxicity examination. Toxicol. Sci. 116, 488-497 (2010).
39. Tolosa, L., Gomez-Lechon, M. J., Perez-Cataldo, G., Castell, J. V., Donato, M. T. HepG2 cells simultaneously expressing five P450 enzymes for the screening of hepatotoxicity: identification of bioactivable drugs and the potential mechanism of toxicity involved. Arch. Toxicol. 87, 1115-1127 (2013).
40. Chen, S. et al. Sertraline induces endoplasmic reticulum stress in hepatic cells. Toxicology 322, 78-88 (2014).
41. Egert, S. et al. Daily quercetin supplementation dose-dependently increases plasma quercetin concentrations in healthy humans. J. Nutr. 138, 1615-1621 (2008).
42. Mix, J. A., Crews, W. D., Jr. A double-blind, placebo-controlled, randomized trial of Ginkgo biloba extract EGb 761 in a sample of cognitively intact older adults: neuropsychological findings. Hum. Psychopharmacol. 17, 267-277 (2002).
43. Lovera, J. F. et al. Ginkgo biloba does not improve cognitive function in MS: a randomized placebo-controlled trial. Neurology 79, 1278-1284 (2012).
44. Vellas, B. et al. Long-term use of standardised Ginkgo biloba extract for the prevention of Alzheimer's disease (GuidAge): a randomised placebo-controlled trial. Lancet Neurol. 11, 851-859 (2012).
45. Gavrilova, S. I. et al. Efficacy and safety of Ginkgo biloba extract EGb 761((R)) in mild cognitive impairment with neuropsychiatric symptoms: a randomized, placebo-controlled, double-blind, multi-center trial. Int. J. Geriatr. Psychiatry 29, 1087-1095 (2014).
46. Rangel-Ordonez, L., Noldner, M., Schubert-Zsilavecz, M., Wurglics, M. Plasma levels and distribution of flavonoids in rat brain after single and repeated doses of standardized Ginkgo biloba extract EGb 761(R). Planta Med. 76, 1683-1690 (2010).
47. Tang, J. et al. Herb-drug interactions: Effect of Ginkgo biloba extract on the pharmacokinetics of theophylline in rats. Food Chem. Toxicol. 45, 2441-2445 (2007).
48. Uchida, S. et al. Effects of Ginkgo biloba extract on pharmacokinetics and pharmacodynamics of tolbutamide and midazolam in healthy volunteers. J. Clin. Pharmacol. 46, 1290-1298 (2006).
49. Yin, O. Q., Tomlinson, B., Waye, M. M., Chow, A. H., Chow, M. S. Pharmacogenetics and herb-drug interactions: experience with Ginkgo biloba and omeprazole. Pharmacogenetics 14, 841-850 (2004).
50. Zadoyan, G. et al. Effect of Ginkgo biloba special extract EGb 761(R) on human cytochrome P450 activity: a cocktail interaction study in healthy volunteers. Eur. J. Clin. Pharmacol. 68, 553-560 (2012).
51. Zuo, X. C. et al. Effects of Ginkgo biloba extracts on diazepam metabolism: a pharmacokinetic study in healthy Chinese male subjects. Eur. J. Clin. Pharmacol. 66, 503-509 (2010).
52. Chen, S. et al. Sertraline, an antidepressant, induces apoptosis in hepatic cells through the mitogen-activated protein kinase pathway. Toxicol. Sci. 137, 404-415 (2014).
53. Li, Y., Couch, L., Higuchi, M., Fang, J. L., Guo, L. Mitochondrial dysfunction induced by sertraline, an antidepressant agent. Toxicol. Sci. 127, 582-591 (2012).
54. Li, Y. et al. Methysticin and 7,8-dihydromethysticin are two major kavalactones in kava extract to induce CYP1A1. Toxicol. Sci. 124, 388-399 (2011).