Cytochrome P450- and peroxidase-mediated oxidation of anticancer alkaloid ellipticine dictates its anti-tumor efficiency

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 1, 2011, Pages 175-185

  Stiborova M ^a   Rupertova M ^a   Frei, E ^b  

^a CHARLES UNIVERSITY   (Czech Republic)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Antitumor alkaloid ellipticine; Cytochrome P450 and peroxidase mediated prodrug activation; DNA adducts in target tumor; Mechanism of action

Indexed keywords

7 HYDROXYELLIPTICINE; 9 HYDROXYELLIPTICINE; CYTOCHROME P450 1A; CYTOCHROME P450 1B1; CYTOCHROME P450 3A4; DIMER; DRUG METABOLITE; ELLIPTICINE; ELLIPTICINE 12 YLIUM; ELLIPTICINE 13 YLIUM; ELLIPTICINE DERIVATIVE; PEROXIDASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; BREAST ADENOCARCINOMA; CANCER CELL CULTURE; COVALENT BOND; DNA ADDUCT; DRUG EFFICACY; DRUG OXIDATION; GENE TRANSFER; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL SURVIVAL; CYTOCHROME P-450 ENZYME SYSTEM; ELLIPTICINES; HUMANS; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; PEROXIDASE;

RATTUS;

EID: 78649447922     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.05.016     Document Type: Review

References (122)

1. P.H. Rooney, C. Telfer, M.C. McFadyen, W.T. Melvin, and G.I. Murray The role of cytochrome P450 in cytotoxic bioactivation: future therapeutic directions Curr. Cancer Drug Targets 4 2004 257 265
2. D.C. Lamb, M.R. Waterman, S.L. Kelly, and F.P. Guengerich Cytochromes P450 and drug discovery Curr. Opin. Biotechnol. 18 2007 504 512
3. L.H. Patterson, and G.I. Murray Tumor cytochrome P450 and drug activation Curr. Pharm. Des. 8 2002 1335 1347
4. L.H. Patterson, S.R. McKeown, T. Robson, R. Gallagher, S.M. Raleigh, and S. Orr Antitumor prodrug development using cytochrome P450 (CYP) mediated activation Anti-Cancer Drug Design 14 1999 473 486
5. M. Lubbert, C.W. Miller, and H.P. Koeffler Changes of DNA methylation and chromatin structure in the human myeloperoxidase gene during myeloid differentiation Blood 78 1991 345 356
6. K. Schmelz, N. Sattler, M. Wagner, M. Lubbert, B. Dorken, and I. Tamm Induction of gene expression by 5-aza-2′-deoxycytidine in acute myeloid leukemia (AML) and myelodysplastic syndrome (MDS) but not epithelial cells by DANN-methylation-dependent and -independent mechanisms Leukemia 19 2005 103 111
7. S. Yha, V. Yegnasubramanian, W.G. Nelson, W.B. Isaacs, and A.M. De Marzo Cyclooxygenases in cancer: progress and perspective Cancer Lett. 215 2004 1 20
8. A. Hoy, B. Leininger-Muller, C. Jolivalt, and G. Siest Effect of apolipoprotein E on cell viability in a human neuroblastoma cell line: influence of oxidation and lipid-association Neurosci. Lett. 285 2000 173 176
9. J.A. Williams, and D.H. Phillips Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer Cancer Res. 60 2000 4667 4677
10. R.A. Soslow, A.J. Dannenberg, D. Rush, B.M. Woemer, K.M. Khan, J. Masferrerer, and A.I. Koki COX-2 is expressed in human pulmonary, colonic, and mammary tumors Cancer 89 2000 2637 2645
11. M. Matsuo, N. Yonemitsu, M. Zaitsu, K. Ishii, Y. Hamasaki, K. Fukuyama, K. Tabuchi, and S. Miyazaki Expression of prostaglandin H synthase-2 in human brain tumors Acta Neuropathol. 102 2001 181 187
12. T. Shono, P.J. Tofilon, J.M. Bruner, O. Owolabi, and F.F. Lang Cyclooxygenase-2 expression in human gliomas: prognostic significance and molecular correlations Cancer Res. 61 2001 4375 4381
13. J.P. Peng, C.Y. Su, H.C. Chang, C.Y. Chai, and W.C. Hung Overexpression of cyclo-oxygenase 2 in squamous cell carcinoma of the hypopharynx Hum. Pathol. 33 2002 100 104
14. F.W. Wiese, P.A. Thompson, and F.F. Kadlubar Carcinogen substrate specificity of human COX-1 and COX-2 Carcinogenesis 22 2001 5 10
15. K.M. Gorlewska-Roberts, C.H. Teitel, J.O. Lay, D.W. Roberts, and F.F. Kadlubar Lactoperoxidase-catalyzed activation of carcinogenic aromatic and heterocyclic amines Chem. Res. Toxicol. 17 2004 1659 1666
16. T. Shimada Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons Drug Metab. Pharmacokinet. 21 2006 257 276
17. S. Goodwin, A.F. Smith, and E.C. Horning Alkaloids of Ochrosia elliptica Labill J. Am. Chem. Soc. 81 1959 1903 1908
18. J.G. Rouesse, T. Le Chevalier, F. Caille, J.M. Mondesir, H. Sancho-Gamier, F. May-Levin, M. Spielman, R. DeJager, and J.L. Amiel Phase II study of ellipticinium in advanced breast cancer Cancer Treat. Rep. 69 1985 707 708
19. G. Mathe, K. Triana, P. Pontiggia, D. Blanquet, M. Hallard, and C. Morette Data of pre-clinical and early clinical trials of acriflavine and hydroxy-methyl-ellipticine reviewed, enriched by the experience of their use for 18 months to 6 years in combination with other HIV1 virostatic Biomed. Pharmacother. 52 1998 391 396
20. C. Auclair Multimodal action of antitumor agents on DNA: the ellipticine series Arch. Biochem. Biophys. 259 1987 1 14
21. M.R. Boyd Status of the NCI preclinical antitumor drug discovery screen: implications for selection of new agents for clinical trials V.T. DeVita Jr. S. Hellman, S. Rosenburg, Cancer: Principles and Practice of Oncology Updates vol. 3 1989 Lippincott Philadelphia 1 12
22. M.R. Boyd The future of drug development J.E. Niederhuber, Current Therapy in Oncology 1993 B.C. Decker Philadelphia 11 22
23. E.M. Acton, V.L. Narayanan, P.A. Risbood, P.H. Shoemaker, D.T. Vistica, and M.R. Boyd Anticancer specificity of some ellipticinium salts against human brain tumors in vitro J. Med. Chem. 37 1994 2185 2189
24. M. Ohashi, E. Sugikawa, and N. Nakanishi Inhibition of p53 protein phosphorylation by 9-hydroxyellipticine: a possible anticancer mechanism Jpn. J. Cancer Res. 86 1995 819 829
25. F. Arguello, M.A. Alexander, J.F. Greene Jr, S.F. Stinson, J.L. Jorden, E.M. Smith, N.T. Kalavar, W.G. Alvord, R.L. Klabansky, and E.A. Sausville Preclinical evaluation of 9-chloro-2-methylellipticinium acetate alone and in combination with conventional anticancer drugs to treatment of human brain tumor xenografts J. Cancer Res. Clin. Oncol. 124 1998 19 26
26. L.M. Shi, T.G. Myers, Y. Fan, P.M. O'Connor, K.D. Paull, S.H. Friend, and J.N. Weinstein Mining the National Cancer Institute Anticancer Drug Discovery Database: cluster analysis of ellipticine analogs with p53-inverse and central nervous system-selective patterns of activity Mol. Pharmacol. 53 1998 241 251
27. M. Stiborová, C.A. Bieler, M. Wiessler, and E. Frei The anticancer agent ellipticine on activation by cytochrome P450 forms covalent DNA adducts Biochem. Pharmacol. 62 2001 675 684
28. M. Stiborová, M. Rupertová, H.H. Schmeiser, and E. Frei Molecular mechanism of antineoplastic action of an anticancer drug ellipticine Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 150 2006 13 23
29. L. Bořek-Dohalská, E. Frei, and M. Stiborová 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
30. N.C. Garbett, and D.E. Graves Extending nature's leads: the anticancer agent ellipticine Curr. Med. Chem. Anti-Cancer Agents 4 2004 149 172
31. P.L. Kuo, Y.C. Kuo, Y.L. Hsu, C.Y. Cho, and C.C. Lin Ellipticine induced apoptosis through p53-dependent pathway in human hepatocellular carcinoma HepG2 cells Life Sci. 78 2006 2550 2557
32. J. Poljaková, E. Frei, J.E. Gomez, D. Aimová, T. Eckschlager, J. Hraběta, and M. Stiborová DNA adduct formation by the anticancer drug ellipticine in human leukemia HL-60 and CCRF-CEM cells Cancer Lett. 252 2007 270 279
33. J. Poljaková, T. Eckschlager, J. Hraběta, J. Hřebačková, S. Smutný, E. Frei, V. Martínek, R. Kizek, and M. Stiborová The mechanism of cytotoxicity and DNA adduct formation by the anticancer drug ellipticine in human neuroblastoma cells Biochem. Pharmacol. 77 2009 1466 1479
34. E. Tian, T.H. Landowski, O.W. Stephens, S. Yaccoby, B. Barlogie, and J.D. Shaughnessy Jr. Ellipticine derivative NSC 338258 represents a potential new antineoplastic agent for the treatment of multiple myeloma Mol. Cancer Ther. 7 2008 500 509
35. K. Fang, S.P. Chen, C.W. Lin, W.C. Cheng, and H.T. Huang Ellipticine-induced apoptosis depends on Akt translocation and signaling in lung epithelial cancer cells Lung Cancer 63 2009 227 234
36. E. Martinkova, M. Dontenwill, E. Frei, and M. Stiborová Cytotoxicity of and DNA adduct formation by ellipticine in human U87MG glioblastoma cancer cells Neuro Endocrinol. Lett. 30 Suppl.1 2009 60 66
37. E. Martinkova, A. Maglott, D.Y. Leger, D. Bonnet, M. Stiborova, K. Takeda, S. Martin, and M. Dontenwill α5β1 integrin antagonists reduce chemotherapy-induced premature senescence and facilitate apoptosis in human glioblastoma cells Int. J. Cancer 2010 10.1002/ijc.25187
38. P. Dodion, M. Rozencweig, C. Nicaise, M. Piccart, E. Cumps, N. Crespeigne, D. Kisner, and Y. Kenis Phase I clinical study of 9-hydroxy-2N-methyl-ellipticinium acetate (NSC-264137) administered on a 5-day i.v. schedule Eur. J. Cancer Clin. Oncol. 18 1982 519 522
39. C. Paoletti, J.B. Le Pecq, N. Dat-Xuong, P. Juret, H. Garnier, J.L. Amiel, and J. Rouesse Antitumor activity, pharmacology, and toxicity of ellipticines, ellipticinium, and 9-hydroxy derivatives: preliminary clinical trials of 2-methyl-9-hydroxy ellipticinium (NSC 264-137) Recent Results Cancer Res. 74 1980 107 123
40. P. Juret, A. Tanguy, A. Girard, J.Y. Le Talaer, J.S. Abbatucci, Dat-Yuong, J.B. Le Pecq, and C. Paoletti Hydroxy 9-methyl 2-ellipticinium acetate (NSC 264-137). Toxicologic study and therapeutic effect in 100 cancers Nouv. Presse Med. 8 1979 1495 1498
41. P. Juret, J.E. Couette, T. Delozier, and J.Y. Le Talaer Hydroxy-9-methyl-2-ellipticinium (NSC 264-137) for osseous metastases from breast cancer. A 4 year experience Bull. Cancer 68 1981 224 231
42. P. Juret, J.F. Heron, J.E. Couette, T. Delozier, and J.Y. Le Talaer Hydroxy-9-methyl-2-ellipticinium for osseous metastases from breast cancer: a 5-year experience Cancer Treat. Rep. 66 1982 1909 1916
43. M.M. Moore, K.H. Brock, C.L. Doerr, and D.M. DeMarini Mutagenesis of L5178Y/TK(+/-)-3.7.2C mouse lymphoma cells by the clastogen ellipticine Environ. Mutagen. 9 1987 161 170
44. D.M. DeMarini, S. Cros, C. Paoletti, P. Lecointe, and A.W. Hsie Mutagenicity and cytotoxicity of five antitumor ellipticines in mammalian cells and their structure-activity relationships in Salmonella Cancer Res. 43 1983 3544 3552
45. E.T. Sakamoto-Hojo, and C.S. Takahashi Clastogenic action of ellipticine over the cell cycle of human lymphocytes and influence of posttreatments with caffeine and ara-C at G2 Mutat. Res. 248 1991 195 202
46. E. Noviello, M.G. Aluigi, G. Cimoli, E. Rovini, A. Mazzoni, S. Parodi, F. De Sessa, and P. Russo Sister-chromatid exchanges, chromosomal aberrations and cytotoxicity produced by topoisomerase II-targeted drugs in sensitive (A2780) and resistant (A2780-DX3) human ovarian cancer cells: correlations with the formation of DNA double-strand breaks Mutat. Res. 311 1994 21 29
47. P.L. Kuo, Y.L. Hsu, C.H. Chang, and C.C. Lin The mechanism of ellipticine-induced apoptosis and cell cycle arrest in human breast MCF-7 cancer cells Cancer Lett. 223 2005 293 301
48. P.L. Kuo, Y.L. Hsu, C.H. Chang, and C.C. Lin 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
49. P. Kovacic, J.R. Ames, P. Lumme, H. Elo, O. Cox, H. Jacson, L.A. Rivera, L. Ramirez, and M.D. Ryan Change transfer-oxy radical mechanism for anti-cancer agents Anti-Cancer Drug Design 1 1986 197 214
50. M.A. Schwaller, B. Allard, E. Lescot, and F. Moreau Protonophoric activity of ellipticine and isomers across the energy-transducing membrane of mitochondria J. Biol. Chem. 270 1995 22709 22713
51. M. Hägg, M. Berndtsson, A. Mandic, R. Zhou, M.C. Shoshan, and S. Linder Induction of endoplasmic reticulum stress by ellipticine plant alkaloids Mol. Cancer Ther. 3 2004 489 497
52. E. Sugikawa, T. Hosoi, N. Yazaki, N. Gamanuma, N. Nakanishi, and M. Ohashi Mutant p53 mediated induction of cell cycle arrest and apoptosis at G1 phase by 9-hydroxyellipticine Anticancer Res. 19 1999 3099 3108
53. Y. Peng, C. Li, L. Chen, S. Sebti, and J. Chen Rescue of mutant p53 transcription function by ellipticine Oncogene 22 2003 4478 4487
54. G.W. Xu, I.A. Mawji, C.J. Macrae, C.A. Koch, A. Datti, J.L. Wrana, J.W. Dennis, and A.D. Schimmer A high-content chemical screen identifies ellipticine as a modulator of p53 nuclear localization Apoptosis 13 2008 413 422
55. M.P. Singh, G.C. Hill, D. Peoch, B. Rayner, J.L. Inabach, and J.W. Lown 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
56. M. Monnot, O. Mauffret, V. Simon, E. Lescot, B. Psaume, J.M. Saucier, M. Charra, J. Belehradek Jr., and S. Fermandjian DNA-drug recognition and effects on topoisomerase II-mediated cytotoxicity. A three-mode binding model for ellipticine derivatives J. Biol. Chem. 25 1991 1820 9182
57. P. Fossé, B. René, M. Charra, C. Paoletti, and J.M. Saucier Stimulation of topoisomerase II-mediated DNA cleavage by ellipticine derivatives: structure-activity relationships Mol. Pharmacol. 42 1992 590 595
58. S.J. Froelich-Ammon, M.W. Patchan, N. Osheroff, and R.B. Thompson 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
59. Y. Chu, and M.T. Hsu Ellipticine increases the superhelical density of intracellular SV40 DNA by intercalation Nucleic Acids Res. 20 1992 4033 4038
60. 32P-postlabeling Int. J. Cancer 107 2003 885 890
61. M. Stiborová, M. Stiborová-Rupertová, L. Bořek-Dohalská, M. Wiessler, and E. Frei 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
62. 2-oxide Cancer Res. 64 2004 8374 8380
63. M. Stiborová, J. Poljaková, H. Ryšlavá, M. Dračínský, T. Eckschlager, and E. Frei 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
64. M. Stiborová, M. Rupertová, D. Aimová, H. Ryšlavá, and E. Frei Formation and persistence of DNA adducts of anticancer drug ellipticine in rats Toxicology 236 2007 50 60 (Pubitemid 46777068)
65. M. Stiborová, V.M. Arlt, C.J. Henderson, C.R. Wolf, V. Kotrbová, M. Moserová, J. Hudecek, D.H. Phillips, and E. Frei 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
66. V. Kotrbová, D. Aimová, A. Březinová, K. Janouchová, J. Poljaková, P. Hodek, E. Frei, and M. Stiborová Cytochromes P450 reconstituted with NADPH:P450 reductase mimic the activating and detoxicating metabolism of the anticancer drug ellipticine in microsomes Neuro Endocrinol. Lett. 27 Suppl. 2 2006 18 20
67. J. Poljaková, M. Dračínský, E. Frei, J. Hudeček, and M. Stiborová The effect of pH on peroxidase-mediated oxidation of and DNA-adduct formation by ellipticine Collect. Czech. Chem. Commun. 71 2006 1169 1185
68. M. Stiborová, L. Bořek-Dohalská, D. Aimová, V. Kotrbová, K. Kukačková, K. Janouchová, M. Rupertová, H. Ryšlavá, J. Hudeček, and E. Frei Oxidation pattern of the anticancer drug ellipticine by hepatic microsomes-similarity between human and rat systems Gen. Physiol. Biophys. 25 2006 245 261
69. M. Chadwick, D.M. Silveira, B.R. Platz, and D. Hayes Comparative physiological disposition of ellipticine in several animal species after intravenous administration Drug Metab. Dispos. 6 1978 528 541
70. A.R. Branfam, R.J. Bruni, V.N. Reihold, D.M. Silveira, M. Chadwick, and D.W. Yesair Characterization of metabolites of ellipticine in rat bile Drug Metab. Dispos. 6 1978 542 548
71. S. Rendic, and F.J. DiCarlo Human cytochrome P450 enzymes: a status report summarizing their reactions, substrates, inducers, and inhibitors Drug Metab. Rev. 29 1997 413 480
72. G. Hofle, N. Glase, T. Leibold, and M. Sefkow Epothilone A-D and their thiazole-modified analogs as novel anticancer agents Pure Appl. Chem. 71 1999 2019 2024
73. M. Moserová, V. Kotrbová, M. Rupertová, K. Naiman, J. Hudeček, P. Hodek, E. Frei, and M. Stiborová Isolation and partial characterization of the adduct formed by 13-hydroxyellipticine with deoxyguanosine in DNA Neuro Endocrinol. Lett. 29 2008 728 732
74. M. Dračínský, J. Sejbal, B. Rygerová, and M. Stiborová An efficient modification of ellipticine synthesis and preparation of 13-hydroxyellipticine Tetrahetron Lett. 48 2007 6893 6895
75. A. Dipple, Q.A. Khan, J.E. Page, I. Pontén, and J. Szeliga DNA reactions, mutagenic action and stealth properties of polycyclic aromatic hydrocarbon carcinogens (review) Int. J. Oncol. 14 1999 103 111
76. Q.A. Khan, K.H. Vousden, and A. Dipple Lack of p53-mediated G1 arrest in response to an environmental carcinogen Oncology 57 1999 258 264
77. M.L. Simões, S.L. Hockley, T. Schwerdtle, G.G. da Costa, H.H. Schmeiser, D.H. Phillips, and V.M. Arlt 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
78. T.H. Broschard, M. Wiessler, C.W. von der Lieth, and H.H. Schmeiser 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
79. W.P. Ross, and B. Kaina DNA damage-induced cell death by apoptosis Trends Mol. Med. 12 2006 440 450
80. S.P. Ivy, A. Tulpule, C.R. Fairchild, S.D. Averbuch, C.E. Myers, D.W. Nebert, W.M. Baird, and K.H. Cowan Altered regulation of P-450IA1 expression in a multidrug-resistant MCF-7 human breast cancer cell line J. Biol. Chem. 263 1988 19119 19125
81. E. Frei, C.A. Bieler, V.M. Arlt, M. Wiessler, and M. Stiborová Covalent binding of the anticancer drug ellipticine to DNA in V79 cells transfected with human cytochrome P450 enzymes Biochem. Pharmacol. 64 2002 289 295
82. D.L. McCormick, C.B. Adamowski, A. Fiks, and R.C. Moon Lifetime dose-response relationships for mammary tumor induction by a single administration of N-methyl-N-nitrosourea Cancer Res. 41 1981 1690 1694
83. G.I. Murray, R.J. Weaver, P.J. Paterson, S.W. Ewen, W.T. Melvin, and M.D. Burke Expression of xenobiotic metabolizing enzymes in breast cancer J. Pathol. 169 1993 347 353
84. G.I. Murray, W.T. Melvin, and M. Burke Cytochrome P450 expression in tumors J. Pathol. 176 1995 323 324
85. B.F. El-Rayes, S. Ali, L.K. Heilbrun, S. Lababidi, S. Bouwman, D. Vischer, and P.A. Philip Cytochrome P450 and glutathione transferase expression in human breast cancer Clin. Cancer Res. 9 2003 1705 1709
86. C.J. Henderson, and C.R. Wolf Transgenic analysis of human drug-metabolizing enzymes: preclinical drug development and toxicology Mol. Interv. 3 2003 331 343
87. S.T. Saarikoski, S.P. Rivera SP, O. Hankinson, and K. Husgafvel-Pursiainen CYP2S1: a short review Toxicol. Appl. Pharmacol. 207 Suppl. 2 2005 62 69
88. D. Downie, M.C. McFadyen, P.H. Rooney, M.E. Cruickshank, D.E. Parkin, I.D. Miller, C. Telfer, W.T. Melvin, and G.I. Murray Profiling cytochrome P450 expression in ovarian cancer: identification of prognostic markers Clin. Cancer Res. 11 2005 7369 7735
89. P.H. Bui, and O. Hankinson Functional characterization of human cytochrome P450 2S1 using a synthetic gene-expressed protein in Escherichia coli Mol. Pharmacol. 76 2009 1031 1043
90. P.H. Bui PH, E.L. Hsu, and O. Hankinson Fatty acid hydroperoxides support cytochrome P450 2S1-mediated bioactivation of benzo[a]pyrene-7, 8-dihydrodiol Mol. Pharmacol. 76 2009 1044 1052
91. R.W.L. Godschalk, E.J.C. Moonen, P.A.E.L. Schilderman, W.M.R. Broekmans, J.C.S. Kleinjans, and F.J. van Schooten Exposure-route-dependent DNA adduct formation by polycyclic aromatic hydrocarbons Carcinogenesis 21 2000 87 92
92. M.C. Poirier Chemical-induced DNA damage and human cancer risk Nat. Rev. 4 2004 630 637
93. 32P-post-labelling analysis of DNA adducts formed in the livers of animals treated with safrole, estragole and other naturally-occurring alkenylbenzenes. I. Adult female CD-1 mice Carcinogenesis 5 1984 1613 1622 (Pubitemid 15127027)
94. J.A. Ross, G.B. Nelson, K.H. Wilson, J.R. Rabinowitz, A. Galati, G.D. Stoner, S. Nesnow, and M.J. Mass Adenomas induced by polycyclic aromatic hydrocarbons in strain A/J mouse lung correlate with time-integrated DNA adduct levels Cancer Res. 55 1995 1039 1044
95. B.A. Smith, N.F. Fullerton, R.H. Heflich, and F.A. Beland DNA adduct formation and T-lymphocyte mutation induction in F344 rats implanted with tumorigenic doses of 1, 6-dinitropyrene Cancer Res. 55 1995 2316 2324
96. D. Aimová, L. Svobodová, V. Kotrbová, B. Mrázová, P. Hodek, J. Hudeček, R. Václaví ková, E. Frei, and M. Stiborová The anticancer drug ellipticine is a potent inducer of rat cytochromes P450 1A1 and 1A2, thereby modulating its own metabolism Drug Metab. Dispos. 35 2007 1926 1934
97. N. Fernandez, M. Roy, and P. Lesca Binding characteristics of Ah receptors from rats and mice before and after separation from hepatic cytosols. 7-Hydroxyellipticine as a competitive antagonist of cytochrome P-450 induction Eur. J. Biochem. 172 1988 585 592
98. T.A. Gasiewicz, R.S. Kende, G. Rucci, B. Whitney, and J.J. Willey Analysis of structural requirements for Ah receptor antagonist activity: ellipticines, flavones, and related compounds Biochem. Pharmacol. 52 1996 1787 1830
99. D. Aimová, and M. Stiborová Antitumor drug ellipticine inhibits the activities of rat hepatic cytochromes P450 Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 149 2005 437 440
100. C.Y. Chang, and A. Puga Constitutive activation of the aromatic hydrocarbon receptor Mol. Cell. Biol. 18 1998 525 535
101. 5 Pharmacol. Ther. 97 2003 139 152
102. 5 Neuro Endocrinol. Lett. 27 Supp. 2 2006 35 39
103. G.K. Rekha, and N.E. Sladek Multienzyme-mediated stable and transient multidrug resistance and collateral sensitivity induced by xenobiotics Cancer Chemother. Pharmacol. 40 1997 215 224
104. D. Schlaifer, K. Meyer, C. Muller, M. Attal, M.T. Smith, S. Tamaki, J. Weimels, J. Pris, J.P. Jaffrezou, G. Laurent, and C.E. Myers Antisense inhibition of myeloperoxidase increases the sensitivity of the HL-60 cell line to vincristine Leukemia 8 1994 289 291
105. A. Kirschenbaum, A.P. Klausner, R. Lee, P. Unger, S. Yao, X.H. Kiu, and A.C. Levine Expression of cyclooxygenase-1 and cyclooxygenase-2 in the human prostate Urology 56 2000 671 676
106. E.A. Castilla, R.A. Prayson, A.A. Kanner, L.A. Rybicky, R.R. Tubbs, M.A. Vogelbaum, and G.H. Barnett Cyclooxygenase-2 in oligodendroglial neoplasms Cancer 8 2003 1465 1472
107. J. Ludwig-Muller, S.V. Tokalov, A. Franz, and H.O. Gutzeit Quercetin metabolism in vital and apoptotic human leukaemia cells Biol. Chem. 386 2005 279 283
108. 2-methyl-9-hydroxy-ellipticinium acetate (NSC 264137) on RNA and poly A in vitro Biochem. Biophys. Res. Commun. 12 1984 416 422
109. B. Dugué, C. Auclair, and B. Meunier Covalent binding of elliptinium acetate (NSC 264137) to nucleic acids of L1210 cells in culture Cancer Res. 46 1986 3828 3833
110. 2-methyl-9-hydroxyellipticinium to DNA in vitro Biochemistry 25 1986 1240 1245
111. 2-methyl-9-hydroxyellipticinium acetate J. Med. Chem. 26 1983 574 579
112. J. Bernadou, M. Bonnafous, G. Labat, P. Loiseau, and B. Meunier Model systems for metabolism studies-biomimetic oxidation of acetaminophen and ellipticine derivatives with water-soluble metalloporphyrins associated to potassium monopersulfate Drug Metab. Dispos. 19 1991 360 365
113. G. Meunier, and B. Meunier Peroxidase-catalyzed O-demethylation reactions-quinone-imine formation from 9-methoxyellipticine derivatives J. Biol. Chem. 260 1985 10576 10582
114. G. Meunier, D. Demontauzon, J. Bernandou, G. Grassy, M. Bonnafous, S. Cros, and B. Meunier The biooxidation of cyto-toxic ellipticine derivatives-a key to structure-activity relationship studies Mol. Pharmacol. 33 1988 93 102
115. 2-methylolivacinium acetate Tetrahedron 41 1985 5107 5120
116. 2-methyl-9- hydroxyellipticinium acetate-an antitumor agent Tetrahedron Lett. 26 1985 2891 2894
117. G. Pratviel, J. Bernadou, T. Ha, G. Meunier, S. Cros, B. Meunier, B. Gillet, and E. Guitret Ribose as the preferential target for the oxidized form of elliptinium acetate in ribonucleos(t)ides-biological-activities of the resulting adducts J. Med. Chem. 20 1986 1350 1355
118. J. Poljaková, K. Forsterová, M. Šulc, E. Frei, and M. Stiborová Oxidation of ellipticine by peroxidases Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 149 2005 449 453
119. M.J. Donaghy, and S.P. Stanforch Nucleophilic addition of fused benzimidazole N-oxide Tetrahedron 55 1999 1441 1448
120. P.D. Josephy The role of peroxidase-catalyzed activation of aromatic amines in breast cancer Mutagenesis 11 1996 3 7
121. J. Ma, and D.J. Waxman Collaboration between hepatic and intratumoral prodrug activation in a P450 prodrug-activation gene therapy model for cancer treatment Mol. Cancer Ther. 6 2007 2879 2890
122. H. Lu, C.S. Chen, and D.J. Waxman Potentiation of methoxymorpholinyl doxorubicin antitumor activity by P450 3A4 gene transfer Cancer Gene Ther. 16 2009 393 404