Etoposide quinone is a redox-dependent topoisomerase II poison

Biochemistry

Volumn 50, Issue 25, 2011, Pages 5660-5667

  Jacob, David A ^a   Mercer, Susan L ^a,b   Osheroff, Neil ^c,d   Deweese, Joseph E ^a,c  

^a LIPSCOMB UNIVERSITY   (United States)

^b LIPSCOMB UNIVERSITY   (United States)

^c Biochemistry   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMAL REARRANGEMENT; DITHIOTHREITOL; DNA CLEAVAGE; DOUBLE-STRANDED DNA BREAKS; ETOPOSIDE; HUMAN CANCER; HUMAN TOPOISOMERASE; LEUKEMOGENESIS; MOLECULAR BASIS; TOPOISOMERASE II;

DNA; ENZYMES; METABOLISM; METABOLITES; PATIENT MONITORING; PATIENT TREATMENT; PHENOLS;

REDUCING AGENTS;

DNA TOPOISOMERASE (ATP HYDROLYSING); DRUG METABOLITE; ETOPOSIDE; ETOPOSIDE DERIVATIVE; ETOPOSIDE QUINONE; PLASMID DNA; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION RESPONSE; DNA ADDUCT; DNA CLEAVAGE; DRUG EFFECT; DRUG MECHANISM; DRUG SYNTHESIS; HUMAN; LEUKEMOGENESIS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ANTIGENS, NEOPLASM; BENZOQUINONES; CATECHOLS; DITHIOTHREITOL; DNA ADDUCTS; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; ENZYME STABILITY; ETOPOSIDE; HUMANS; LEUKEMIA, MYELOID, ACUTE; OXIDATION-REDUCTION; REDUCING AGENTS;

EID: 79959464133     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200438m     Document Type: Article

References (55)

1. Hande, K. R. (1998) Etoposide: four decades of development of a topoisomerase II inhibitor Eur. J. Cancer 34, 1514-1521 (Pubitemid 28446331)
2. Baldwin, E. L. and Osheroff, N. (2005) Etoposide, topoisomerase II and cancer Curr. Med. Chem. Anticancer Agents 5, 363-372 (Pubitemid 40974810)
3. Nitiss, J. L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy Nat. Rev. Cancer 9, 338-350
4. 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
5. 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
6. Bromberg, K. D., Burgin, A. B., and Osheroff, N. (2003) A two-drug model for etoposide action against human topoisomerase IIα J. Biol. Chem. 278, 7406-7412 (Pubitemid 36800745)
7. Deweese, J. E., Burgin, A. B., and Osheroff, N. (2008) Using 3′-bridging phosphorothiolates to isolate the forward DNA cleavage reaction of human topoisomerase IIα Biochemistry 47, 4129-4140 (Pubitemid 351458127)
8. Pedersen-Bjergaard, J. and Philip, P. (1991) Balanced translocations involving chromosome bands 11q23 and 21q22 are highly characteristic of myelodysplasia and leukemia following therapy with cytostatic agents targeting at DNA-topoisomerase II Blood 78, 1147-1148
9. Pedersen-Bjergaard, J. and Rowley, J. D. (1994) The balanced and the unbalanced chromosome aberrations of acute myeloid leukemia may develop in different ways and may contribute differently to malignant transformation Blood 83, 2780-2786 (Pubitemid 24142706)
10. Mistry, A. R., Felix, C. A., Whitmarsh, R. J., Mason, A., Reiter, A., Cassinat, B., Parry, A., Walz, C., Wiemels, J. L., Segal, M. R., Ades, L., Blair, I. A., Osheroff, N., Peniket, A. J., Lafage-Pochitaloff, M., Cross, N. C., Chomienne, C., Solomon, E., Fenaux, P., and Grimwade, D. (2005) DNA topoisomerase II in therapy-related acute promyelocytic leukemia N. Engl. J. Med. 352, 1529-1538 (Pubitemid 40517093)
11. Pui, C.-H., Ribeiro, R. C., Hancock, M. L., Rivera, G. K., Evans, W. E., Raimondi, S. C., Head, D. R., Behm, F. G., Mahmoud, M. H., Sandlund, J. T., and Crist, W. M. (1991) Acute myeloid leukemia in children treated with epipodophyllotoxins for acute lymphoblastic leukemia N. Engl. J. Med. 325, 1682-1687
12. Smith, M. A., Rubinstein, L., and Ungerleider, R. S. (1994) Therapy-related acute myeloid leukemia following treatment with epipodophyllotoxins: estimating the risks Med. Ped. Oncol. 23, 86-98 (Pubitemid 24213321)
13. Relling, M. V., Yanishevski, Y., Nemec, J., Evans, W. E., Boyett, J. M., Behm, F. G., and Pui, C. H. (1998) Etoposide and antimetabolite pharmacology in patients who develop secondary acute myeloid leukemia Leukemia 12, 346-352 (Pubitemid 28138219)
14. Smith, M. A., Rubinstein, L., Anderson, J. R., Arthur, D., Catalano, P. J., Freidlin, B., Heyn, R., Khayat, A., Krailo, M., Land, V. J., Miser, J., Shuster, J., and Vena, D. (1999) Secondary leukemia or myelodysplastic syndrome after treatment with epipodophyllotoxins J. Clin. Oncol. 17, 569-577 (Pubitemid 29075244)
15. Lovett, B. D., Strumberg, D., Blair, I. A., Pang, S., Burden, D. A., Megonigal, M. D., Rappaport, E. F., Rebbeck, T. R., Osheroff, N., Pommier, Y. G., and Felix, C. A. (2001) Etoposide metabolites enhance DNA topoisomerase II cleavage near leukemia-associated MLL translocation breakpoints Biochemistry 40, 1159-1170 (Pubitemid 32142877)
16. Felix, C. A., Kolaris, C. P., and Osheroff, N. (2006) Topoisomerase II and the etiology of chromosomal translocations DNA Repair 5, 1093-1108 (Pubitemid 44291622)
17. Stanulla, M., Wang, J., Chervinsky, D. S., Thandla, S., and Aplan, P. D. (1997) DNA cleavage within the MLL breakpoint cluster region is a specific event which occurs as part of higher-order chromatin fragmentation during the initial stages of apoptosis Mol. Cell. Biol. 17, 4070-4079 (Pubitemid 27281883)
18. Betti, C. J., Villalobos, M. J., Jiang, Q., Cline, E., Diaz, M. O., Loredo, G., and Vaughan, A. T. (2005) Cleavage of the MLL gene by activators of apoptosis is independent of topoisomerase II activity Leukemia 19, 2289-2295 (Pubitemid 41741626)
19. van Maanen, J. M., Retel, J., de Vries, J., and Pinedo, H. M. (1988) Mechanism of action of antitumor drug etoposide: a review J. Natl. Cancer Inst. 80, 1526-1533 (Pubitemid 19009648)
20. Roche, V. F. (2007) Cancer and Chemotherapy in Foye's Principles of Medicinal Chemistry (Foye, W. O., Lemke, T. L., and Williams, D. A., Eds.) 6 th ed., Lippincott Williams & Wilkins, Baltimore, MD.
21. Relling, M. V., Evans, R., Dass, C., Desiderio, D. M., and Nemec, J. (1992) Human cytochrome P450 metabolism of teniposide and etoposide J. Pharmacol. Exp. Ther. 261, 491-496
22. Relling, M. V., Nemec, J., Schuetz, E. G., Schuetz, J. D., Gonzalez, F. J., and Korzekwa, K. R. (1994) O-demethylation of epipodophyllotoxins is catalyzed by human cytochrome P450 3A4 Mol. Pharmacol. 45, 352-358 (Pubitemid 24063092)
23. Zhuo, X., Zheng, N., Felix, C. A., and Blair, I. A. (2004) Kinetics and regulation of cytochrome P450-mediated etoposide metabolism Drug Metab. Dispos. 32, 993-1000 (Pubitemid 39096060)
24. Stremetzne, S., Jaehde, U., Kasper, R., Beyer, J., Siegert, W., and Schunack, W. (1997) Considerable plasma levels of a cytotoxic etoposide metabolite in patients undergoing high-dose chemotherapy Eur. J. Cancer 33, 978-979 (Pubitemid 27287055)
25. Stremetzne, S., Jaehde, U., and Schunack, W. (1997) Determination of the cytotoxic catechol metabolite of etoposide (3′O-demethyletoposide) in human plasma by high-performance liquid chromatography J. Chromatogr., B: Biomed. Sci. Appl. 703, 209-215 (Pubitemid 28011260)
26. Pang, S., Zheng, N., Felix, C. A., Scavuzzo, J., Boston, R., and Blair, I. A. (2001) Simultaneous determination of etoposide and its catechol metabolite in the plasma of pediatric patients by liquid chromatography/tandem mass spectrometry J. Mass Spectrom. 36, 771-781 (Pubitemid 32737419)
27. Zheng, N., Felix, C. A., Pang, S., Boston, R., Moate, P., Scavuzzo, J., and Blair, I. A. (2004) Plasma etoposide catechol increases in pediatric patients undergoing multiple-day chemotherapy with etoposide Clin. Cancer Res. 10, 2977-2985 (Pubitemid 38619673)
28. Haim, N., Roman, J., Nemec, J., and Sinha, B. K. (1986) Peroxidative free radical formation and O-demethylation of etoposide(VP-16) and teniposide(VM-26) Biochem. Biophys. Res. Commun. 135, 215-220 (Pubitemid 16063992)
29. Gantchev, T. G. and Hunting, D. J. (1997) Inhibition of the topoisomerase II-DNA cleavable complex by the ortho-quinone derivative of the antitumor drug etoposide (VP-16) Biochem. Biophys. Res. Commun. 237, 24-27 (Pubitemid 27390316)
30. Gantchev, T. G. and Hunting, D. J. (1998) The ortho-quinone metabolite of the anticancer drug etoposide (VP-16) is a potent inhibitor of the topoisomerase II/DNA cleavable complex Mol. Pharmacol. 53, 422-428 (Pubitemid 28162863)
31. Kagan, V. E., Yalowich, J. C., Borisenko, G. G., Tyurina, Y. Y., Tyurin, V. A., Thampatty, P., and Fabisiak, J. P. (1999) Mechanism-based chemopreventive strategies against etoposide-induced acute myeloid leukemia: free radical/antioxidant approach Mol. Pharmacol. 56, 494-506 (Pubitemid 29406876)
32. Kagan, V. E., Kuzmenko, A. I., Tyurina, Y. Y., Shvedova, A. A., Matsura, T., and Yalowich, J. C. (2001) Pro-oxidant and antioxidant mechanisms of etoposide in HL-60 cells: role of myeloperoxidase Cancer Res. 61, 7777-7784 (Pubitemid 33049364)
33. Felix, C. A., Walker, A. H., Lange, B. J., Williams, T. M., Winick, N. J., Cheung, N. K., Lovett, B. D., Nowell, P. C., Blair, I. A., and Rebbeck, T. R. (1998) Association of CYP3A4 genotype with treatment-related leukemia Proc. Natl. Acad. Sci. U.S.A. 95, 13176-13181 (Pubitemid 28509544)
34. Decker, H. and Tuczek, F. (2000) Tyrosinase/catecholoxidase activity of hemocyanins: structural basis and molecular mechanism Trends Biochem. Sci. 25, 392-397 (Pubitemid 30497251)
35. 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)
36. 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)
37. Lindsey, R. H., Jr., Bender, R. P., and Osheroff, N. (2005) Effects of benzene metabolites on DNA cleavage mediated by human topoisomerase IIα: 1,4-hydroquinone is a topoisomerase II poison Chem. Res. Toxicol. 18, 761-770 (Pubitemid 40563291)
38. 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)
39. 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)
40. 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)
41. Elsea, S. H., Hsiung, Y., Nitiss, J. L., and Osheroff, N. (1995) A yeast type II topoisomerase selected for resistance to quinolones. Mutation of histidine 1012 to tyrosine confers resistance to nonintercalative drugs but hypersensitivity to ellipticine J. Biol. Chem. 270, 1913-1920
42. 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)
43. 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)
44. Nemec, J. (1986) Epipodophyllotoxinquinone glucoside derivatives, method of production and use, U.S. Patent, 4,609,644.
45. 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)
46. Wilstermann, A. M., Bender, R. P., Godfrey, M., Choi, S., Anklin, C., Berkowitz, D. B., Osheroff, N., and Graves, D. E. (2007) Topoisomerase II-drug interaction domains: identification of substituents on etoposide that interact with the enzyme Biochemistry 46, 8217-8225 (Pubitemid 47075961)
47. 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)
48. Saulnier, M. G., Vyas, D. M., Langley, D. R., Doyle, T. W., Rose, W. C., Crosswell, A. R., and Long, B. H. (1989) E-ring desoxy analogues of etoposide J. Med. Chem. 32, 1418-1420 (Pubitemid 19205342)
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. Wang, H., Mao, Y., Zhou, N., Hu, T., Hsieh, T. S., and Liu, L. F. (2001) ATP-bound topoisomerase II as a target for antitumor drugs J. Biol. Chem. 276, 15990-15995
51. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L., and Rogan, E. G. (1997) Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators Proc. Natl. Acad. Sci. U.S.A. 94, 10937-10942 (Pubitemid 27430839)
52. Sabourin, M. and Osheroff, N. (2000) Sensitivity of human type II topoisomerases to DNA damage: stimulation of enzyme-mediated DNA cleavage by abasic, oxidized and alkylated lesions Nucleic Acids Res. 28, 1947-1954 (Pubitemid 30229661)
53. Velez-Cruz, R., Riggins, J. N., Daniels, J. S., Cai, H., Guengerich, F. P., Marnett, L. J., and Osheroff, N. (2005) Exocyclic DNA lesions stimulate DNA cleavage mediated by human topoisomerase IIα in vitro and in cultured cells Biochemistry 44, 3972-3981 (Pubitemid 40358049)
54. van Maanen, J. M., Lafleur, M. V., Mans, D. R., van den Akker, E., de Ruiter, C., Kootstra, P. R., Pappie, D., de Vries, J., Retel, J., and Pinedo, H. M. (1988) Effects of the ortho-quinone and catechol of the antitumor drug VP-16-213 on the biological activity of single-stranded and double-stranded phi X174 DNA Biochem. Pharmacol. 37, 3579-3589
55. Bandele, O. 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)