The mechanism of cytotoxicity and DNA adduct formation by the anticancer drug ellipticine in human neuroblastoma cells

Biochemical Pharmacology

Volumn 77, Issue 9, 2009, Pages 1466-1479

  Poljaková, Jitka ^a   Eckschlager, Tomáš ^a   Hraběta, Jan ^a   Hřebačková, Jana ^a   Smutný, Svatopluk ^a   Frei, Eva ^b   Martínek, Václav ^a   Kizek, René ^c   Stiborová, Marie ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MENDEL UNIVERSITY IN BRNO   (Czech Republic)

Author keywords

Anticancer drug; Cytotoxicity; DNA adduct; Ellipticine; Neuroblastoma

Indexed keywords

12 HYDROXYELLIPTICINE; 13 HYDROXYELLIPTICINE; CISPLATIN; CYTOCHROME P450; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); DOXORUBICIN; ELLIPTICINE; ELLIPTICINE DERIVATIVE; MESSENGER RNA; PEROXIDASE; PROTEIN; UNCLASSIFIED DRUG; VINCRISTINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL HYPOXIA; DNA ADDUCT; DNA FRAGMENTATION; DNA REPLICATION; DRUG CYTOTOXICITY; DRUG DNA BINDING; DRUG INHIBITION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; NITROBLUE TETRAZOLIUM TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME P-450 ENZYME SYSTEM; DNA ADDUCTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELLIPTICINES; HUMANS; PEROXIDASE;

EID: 63149114184     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.01.021     Document Type: Article

References (55)

1. Maris J.M., and Mathay K.K. Molecular biology of neuroblastomas. J Clin Oncol 17 (1999) 2264-2279
2. Brodeur G.M. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3 (2003) 203-216
3. Stiborová M., Bieler C.A., Wiessler M., and Frei E. The anticancer agent ellipticine on activation by cytochrome P450 forms covalent DNA adducts. Biochem Pharmacol 62 (2001) 675-684
4. Auclair C. Multimodal action of antitumor agents on DNA: the ellipticine series. Arch Biochem Biophys 259 (1987) 1-14
5. Kuo P.L., Hsu Y.L., Kuo Y.C., Chang C.H., and Lin C.C. The antiproliferative inhibition of ellipticine in human breast mda-mb-231 cancer cells is through cell cycle arrest and apoptosis induction. Anti-Cancer Drugs 16 (2005) 789-795
6. Kuo P.L., Hsu Y.L., Chang C.H., and Lin C.C. The mechanism of ellipticine-induced apoptosis and cell cycle arrest in human breast MCF-7 cancer cells. Cancer Lett 223 (2005) 293-301
7. Kovacic P., Ames J.R., Lumme P., Elo H., Cox O., Jacson H., et al. Change transfer-oxy radical mechanism for anti-cancer agents. Anti-Cancer Drug Design 1 (1986) 197-214
8. Kuo P.L., Kuo Y.C., Hsu Y.L., Cho C.Y., and Lin C.C. Ellipticine induced apoptosis through p53-dependent pathway in human hepatocellular carcinoma HepG2 cells. Life Sci 78 (2006) 2550-2557
9. Garbett N.C., and Graves D.E. Extenting nature's leads: the anticancer agent ellipticine. Curr Med Chem Anti-Cancer Agents 4 (2004) 149-172
10. Schwaller M.A., Allard B., Lescot E., and Moreau F. Protonophoric activity of ellipticine and isomers across the energy-transducing membrane of mitochondria. J Biol Chem 270 (1995) 22709-22713
11. Ohashi M., Sugikawa E., and Nakanishi N. Inhibition of p53 protein phosphorylation by 9-hydroxyellipticine: a possible anticancer mechanism. Jpn J Cancer Res 86 (1995) 819-829
12. Sugikawa E., Hosoi T., Yazaki N., Gamanuma N., Nakanishi N., and Ohashi M. Mutant p53 mediated induction of cell cycle arrest and apoptosis at G1 phase by 9-hydroxyellipticine. Anticancer Res 19 (1999) 3099-3108
13. Singh M.P., Hill G.C., Peoch D., Rayner B., Inabach J.L., and Lown J.W. High-field NMR and restrained molecular modeling studies on a DNA heteroduplex containing a modified apurinic abasic site in the form of covalently linked 9-aminoellipticine. Biochemistry 33 (1994) 10271-10285
14. Monnot M., Mauffret O., Simon V., Lescot E., Psaume B., Saucier J.M., et al. DNA-drug recognition and effects on topoisomerase II-mediated cytotoxicity. A three-mode binding model for ellipticine derivatives. J Biol Chem 25 (1991) 1820-1829
15. Fossé P., René B., Charra M., Paoletti C., and Saucier J.M. Stimulation of topoisomerase II-mediated DNA cleavage by ellipticine derivatives: structure-activity relationships. Mol Pharmacol 42 (1992) 590-595
16. Froelich-Ammon S.J., Patchan M.W., Osheroff N., and Thompson R.B. Topoisomerase II binds to ellipticine in the absence or presence of DNA. Characterization of enzyme-drug interactions by fluorescence spectroscopy. J Biol Chem 270 (1995) 14998-15004
17. 32P-postlabeling. Int J Cancer 107 (2003) 885-890
18. Stiborová M., Stiborová-Rupertová M., Bořek-Dohalská L., Wiessler M., and Frei E. Rat microsomes activating the anticancer drug ellipticine to species covalently binding to deoxyguanosine in DNA are a suitable model mimicking ellipticine bioactivation in humans. Chem Res Toxicol 16 (2003) 38-47
19. 2-oxide. Cancer Res 64 (2004) 8374-8380
20. Stiborová M., Bořek-Dohalská L., Aimová D., Kotrbová V., Kukačková K., Janouchová K., et al. Oxidation pattern of the anticancer drug ellipticine by hepatic microsomes-similarity between human and rat systems. Gen Physiol Biophys 25 (2006) 245-261
21. Stiborová M., Poljaková J., Ryšlavá H., Dračínský M., Eckschlager T., and Frei E. Mammalian peroxidases activate anticancer drug ellipticine to intermediates forming deoxyguanosine adducts in DNA identical to those found in vivo and generated from 12-hydroxyellipticine and 13-hydroxyellipticine. Int J Cancer 120 (2007) 243-251
22. Stiborová M., Rupertová M., Aimová D., Ryšlavá H., and Frei E. Formation and persistence of DNA adducts of anticancer drug ellipticine in rats. Toxicology 236 (2007) 50-60
23. Poljaková J., Dračínský M., Frei E., Hudeček J., and Stiborová M. The effect of pH on peroxidase-mediated oxidation of and DNA-adduct formation by ellipticine. Collect Czech Chem Commun 71 (2006) 1169-1185
24. Stiborová M., Arlt V.M., Henderson C.J., Wolf C.R., Kotrbová V., Moserová M., et al. Role of hepatic cytochromes P450 in bioactivation of the anticancer drug ellipticine: studies with the hepatic NADPH:cytochrome P450 reductase null mouse. Toxicol Appl Pharmacol 226 (2008) 318-327
25. Bořek-Dohalská L., Frei E., and Stiborová M. DNA adduct formation by the anticancer drug ellipticine and its hydroxy derivatives in human breast adenocarcinoma MCF-7 cells. Collect Czech Chem Commun 69 (2004) 603-615
26. Poljaková J., Frei E., Gomez J.E., Aimová D., Eckschlager T., Hraběta J., et al. DNA adduct formation by the anticancer drug ellipticine in human leukemia HL-60 and CCRF-CEM cells. Cancer Lett 252 (2007) 270-279
27. Frei E., Bieler C.A., Arlt V.M., Wiessler M., and Stiborová M. Covalent binding of the anticancer drug ellipticine to DNA in V79 cells transfected with human cytochrome P450 enzymes. Biochem Pharmacol 64 (2002) 289-295
28. Schwab M. Human neuroblastoma: from basic science to clinical debut of cellular oncogenes. Naturwissenschaften 86 (1999) 71-78
29. Bedrnicek J., Vicha A., Jarosova M., Holzerova M., Cinatl Jr. J., Michaelis M., et al. Characterization of drug-resistant neuroblastoma cell lines by comparative genomic hybridization. Neoplasma 52 (2005) 415-419
30. Cinatl Jr. J., Cinatl J., Driever P.H., Kotchetkov R., Pouckova P., Kornhuber B., et al. Sodium valproate inhibits in vivo growth of human neuroblastoma cells. Anti-Cancer Drugs 8 (1997) 958-963
31. Kotchetkov R., Cinatl J., Blaheta R., Vogel J.U., Karaskova J., et al. Development of resistance to vincristine and doxorubicin in neuroblastoma alters malignant properties and induces additional karyotype changes: a preclinical model. Int J Cancer 104 (2003) 36-43
32. Hakura A., Suzuki S., Sawada S., Sugihara T., Hori Y., Uchida K., et al. Use of human liver S9 in the Ames test: assay of three procarcinogens using human S9 derived from multiple donors. Regul Toxicol Pharmacol 37 (2003) 20-27
33. Eling T.E., Thompson D.C., Foureman G.L., Curtis J.F., and Hughes M.F. Prostaglandin H synthase and xenobiotic oxidation. Annu Re Pharmacol Toxicol 30 (1990) 1-45
34. Stiborová M., Frei E., Hodek P., Wiessler M., and Schmeiser H.H. Human hepatic and renal microsomes, cytochromes P450 1A1/2, NADPH:cytochrome P450 reductase and prostaglandin H synthase mediate the formation of aristolochic acid-DNA adducts found in patients with urothelial cancer. Int J Cancer 113 (2005) 189-197
35. Arlt V.M., Hewer A., Sorg B.L., Schmeiser H.H., Phillips D.H., and Stiborová M. 3-Aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone, forms DNA adducts after metabolic activation by human and rat liver microsomes: evidence for activation by cytochrome P450 1A1 and P450 1A2. Chem Res Toxicol 17 (2004) 1092-1101
36. Rendic S., and DiCarlo F.J. Human cytochrome P450 enzymes: a status report summarizing their reactions, substrates, inducers, and inhibitors. Drug Metab Rev 29 (1997) 413-480
37. Stiborová M., Martínek V., Rýdlová H., Hodek P., and Frei E. Sudan I is a potential carcinogen for humans: evidence for its metabolic activation and detoxication by human recombinant cytochrome P450 1A1 and liver microsomes. Cancer Res 62 (2002) 5678-5684
38. Stiborová M., Martínek V., Rýdlová H., Koblas T., and Hodek P. Expression of cytochrome P450 1A1 and its contribution to oxidation of a potential human carcinogen 1-phenylazo-2-naphthol (Sudan I) in human livers. Cancer Lett 220 (2005) 145-154
39. Stiborová M., Dračínská H., Hájková J., Kadeřábková P., Frei E., Schmeiser H.H., et al. The environmental pollutant and carcinogen 3-nitrobenzanthrone and its human metabolite 3-aminobenzanthrone are potent inducers of rat hepatic cytochromes P450 1A1 and -1A2 and NAD(P)H:quinone oxidoreductase. Drug Metab Dispos 34 (2006) 1398-1405
40. Lanza F., Latorraca A., Moretti S., Castagnari B., Ferrari L., and Castoldi G. Comparative analysis of different permeabilization methods for the flow cytometry measurement of cytoplasmic myeloperoxidase and lysozyme in normal and leukemic cells. Cytometry 30 (1997) 134-144
41. Moserová M., Kotrbová V., Rupertová M., Naiman K., Hudeček J., Hodek P., et al. Isolation and partial characterization of the adduct formed by 13-hydroxyellipticine with deoxyguanosine in DNA. Neuro Endocrinol Lett 29 (2008) 728-732
42. Ueng Y.-F., Kuwabara T., Chun Y.-J., and Guengerich F.P. Cooperativity in oxidation catalyzed by cytochrome P450 3A4. Biochemistry 36 (1997) 370-381
43. Arlt V.M., Henderson C.J., Wolf C.R., Schmeiser H.H., Phillips D.H., and Stiborová M. Bioactivation of 3-aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone: evidence for DNA adduct formation mediated by cytochrome P450 enzymes and peroxidases. Cancer Lett 234 (2006) 220-231
44. Chu Y., and Hsu M.T. Ellipticine increases the superhelical density of intracellular SV40 DNA by intercalation. Nucleic Acids Res 20 (1992) 4033-4038
45. Stiborová M., Rupertová M., Schmeiser H.H., and Frei E. Molecular mechanism of antineoplastic action of an anticancer drug ellipticine. Biomed Pap 150 (2006) 13-23
46. Dračínský M., Sejbal J., Rygerová B., and Stiborová M. An efficient modification of ellipticine synthesis and preparation of 13-hydroxyellipticine. Tetrahetron Lett 48 (2007) 6893-6895
47. Dipple A., Khan Q.A., Page J.E., Pontén I., and Szeliga J. DNA reactions, mutagenic action and stealth properties of polycyclic aromatic hydrocarbon carcinogens (review). Int J Oncol 14 (1999) 103-111
48. Khan Q.A., Vousden K.H., and Dipple A. Lack of p53-mediated G1 arrest in response to an environmental carcinogen. Oncology 57 (1999) 258-264
49. Simões M.L., Hockley S.L., Schwerdtle T., da Costa G.G., Schmeiser H.H., Phillips D.H., and Arlt V.M. Gene expression profiles modulated by the human carcinogen aristolochic acid I in human cancer cells and their dependence on TP53. Toxicol Appl Pharmacol 232 (2008) 86-98
50. Ross W.P., and Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol Med 12 (2006) 440-450
51. Broschard T.H., Wiessler M., von der Lieth C.W., and Schmeiser H.H. Translesional synthesis on DNA templates containing site-specifically placed deoxyadenosine and deoxyguanosine adducts formed by the plant carcinogen aristolochic acid. Carcinogenesis 15 (1994) 2331-2340
52. Rekha G.K., and Sladek N.E. Multienzyme-mediated stable and transient multidrug resistance and collateral sensitivity induced by xenobiotics. Cancer Chemother Pharmacol 40 (1997) 215-224
53. Aimová D., and Stiborová M. Antitumor drug ellipticine inhibits the activities of rat hepatic cytochromes P450. Biomed Pap 149 (2005) 437-440
54. Chang C.-Y., and Puga A. Constitutive activation of the aromatic hydrocarbon receptor. Mol Cell Biol 18 (1998) 525-535
55. Hardesty C.T., Chaney N.A., and Mead J.A. The effect of route of administration on the distribution of ellipticine in mice. Cancer Res 32 (1972) 1884-1889