DNA topoisomerase II, genotoxicity, and cancer

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 623, Issue 1-2, 2007, Pages 83-97

  McClendon, A Kathleen ^a   Osheroff, Neil ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anticancer drugs; Benzene; Bioflavonoid; DNA cleavage; DNA damage; DNA supercoiling; Topoisomerase; Topoisomerase II; Topoisomerase II poisons

Indexed keywords

DNA; DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME TRANSLOCATION; DNA CLEAVAGE; DNA DEGRADATION; DNA STRAND BREAKAGE; DNA SUPERCOILING; ENZYME ACTIVITY; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA, SUPERHELICAL; HUMANS; MODELS, MOLECULAR; MUTATION; NEOPLASMS;

EID: 34548391416     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2007.06.009     Document Type: Article

References (190)

1. Watson J.D., and Crick F.H.C. Molecular structure of nucleic acids. Nature 171 (1953) 737-738
2. Watson J.D., and Crick F.H.C. Genetical implications of the structure of deoxyribonucleic acid. Nature 171 (1953) 964-967
3. In: Cozzarelli N.R., and Wang J.C. (Eds). DNA Topology and its Biological Effects (1990), Cold Spring Harbor Laboratory Press, Cold Spring Harbor
4. Kanaar R., and Cozzarelli N.R. Roles of supercoiled DNA structure in DNA transactions. Curr. Opin. Struct. Biol. 2 (1992) 369-379
5. Wang J.C. DNA topoisomerases. Annu. Rev. Biochem. 65 (1996) 635-692
6. Schvartzman J.B., and Stasiak A. A topological view of the replicon. EMBO Rep. 5 (2004) 256-261
7. Wang J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3 (2002) 430-440
8. Brill S.J., DiNardo S., Voelkel-Meiman K., and Sternglanz R. DNA topoisomerase activity is required as a swivel for DNA replication and for ribosomal RNA transcription. NCI Monogr. 4 (1987) 11-15
9. Kim R.A., and Wang J.C. Function of DNA topoisomerases as replication swivels in Saccharomyces cerevisiae. J. Mol. Biol. 208 (1989) 257-267
10. Peter B.J., Ullsperger C., Hiasa H., Marians K.J., and Cozzarelli N.R. The structure of supercoiled intermediates in DNA replication. Cell 94 (1998) 819-827
11. Deibler R.W., Rahmati S., and Zechiedrich E.L. Topoisomerase IV, alone, unknots DNA in E. coli. Genes Dev. 15 (2001) 748-761
12. Osheroff N. DNA topoisomerases. Biochim. Biophys. Acta 1400 (1998) 1-2
13. Nitiss J.L. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta 1400 (1998) 63-81
14. Champoux J.J. DNA topisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70 (2001) 369-413
15. Fortune J.M., and Osheroff N. Topoisomerase II as a target for anticancer drugs: when enzymes stop being nice. Prog. Nucleic Acid Res. Mol. Biol. 64 (2000) 221-253
16. Wilstermann A.M., and Osheroff N. Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem. 3 (2003) 1349-1364
17. Sabourin M., and Osheroff N. Topoisomerases. Wiley Encyclopedia of Molecular Medicine (2002), John Wiley & Sons, Inc. pp. 3192-3197
18. Champoux J.J. DNA topoisomerases: type I. Encyclopedia of Biological Chemistry (2004), Elsevier Inc. pp. 798-805
19. Velez-Cruz R., and Osheroff N. DNA topoisomerases: type II. Encyclopedia of Biological Chemistry (2004), Elsevier Inc. pp. 806-811
20. Wang J.C. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys. 31 (1998) 107-144
21. Pommier Y., Pourquier P., Fan Y., and Strumberg D. Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400 (1998) 83-106
22. Leppard J.B., and Champoux J.J. Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma 114 (2005) 75-85
23. Wyckoff E., and Hsieh T.S. Functional expression of a Drosophila gene in yeast: genetic complementation of DNA topoisomerase II. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 6272-6276
24. Goto T., Laipis P., and Wang J.C. The purification and characterization of DNA topoisomerases I and II of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 259 (1984) 10422-10429
25. Drake F.H., Zimmerman J.P., McCabe F.L., Bartus H.F., Per S.R., Sullivan D.M., Ross W.E., Mattern M.R., Johnson R.K., and Crooke S.T. Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells. Evidence for two forms of the enzyme. J. Biol. Chem. 262 (1987) 16739-16747
26. Drake F.H., Hofmann G.A., Bartus H.F., Mattern M.R., Crooke S.T., and Mirabelli C.K. Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry 28 (1989) 8154-8160
27. Tsai-Pflugfelder M., Liu L.F., Liu A.A., Tewey K.M., Whang-Peng J., Knutsen T., Huebner K., Croce C.M., and Wang J.C. Cloning and sequencing of cDNA encoding human DNA topoisomerase II and localization of the gene to chromosome region 17q21-22. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 7177-7181
28. Jenkins J.R., Ayton P., Jones T., Davies S.L., Simmons D.L., Harris A.L., Sheer D., and Hickson I.D. Isolation of cDNA clones encoding the beta isozyme of human DNA topoisomerase II and localisation of the gene to chromosome 3p24. Nucleic Acids Res. 20 (1992) 5587-5592
29. Tan K.B., Dorman T.E., Falls K.M., Chung T.D., Mirabelli C.K., Crooke S.T., and Mao J. Topoisomerase II alpha and topoisomerase II beta genes: characterization and mapping to human chromosomes 17 and 3, respectively. Cancer Res. 52 (1992) 231-234
30. Austin C.A., and Marsh K.L. Eukaryotic DNA topoisomerase IIβ. Bioessays 20 (1998) 215-226
31. Wasserman R.A., Austin C.A., Fisher L.M., and Wang J.C. Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant human DNA topoisomerase II alpha in yeast. Cancer Res. 53 (1993) 3591-3596
32. Jensen S., Redwood C.S., Jenkins J.R., Andersen A.H., and Hickson I.D. Human DNA topoisomerases II alpha and II beta can functionally substitute for yeast TOP2 in chromosome segregation and recombination. Mol. Gen. Genet. 252 (1996) 79-86
33. Meczes E.L., Marsh K.L., Fisher L.M., Rogers M.P., and Austin C.A. Complementation of temperature-sensitive topoisomerase II mutations in Saccharomyces cerevisiae by a human TOP2 beta construct allows the study of topoisomerase II beta inhibitors in yeast. Cancer Chemother. Pharmacol. 39 (1997) 367-375
34. Heck M.M., and Earnshaw W.C. Topoisomerase II: a specific marker for cell proliferation. J. Cell. Biol. 103 (1986) 2569-2581
35. Hsiang Y.H., Wu H.Y., and Liu L.F. Proliferation-dependent regulation of DNA topoisomerase II in cultured human cells. Cancer Res. 48 (1988) 3230-3235
36. Woessner R.D., Mattern M.R., Mirabelli C.K., Johnson R.K., and Drake F.H. Proliferation- and cell cycle-dependent differences in expression of the 170 kD and 180 kD forms of topoisomerase II in NIH-3T3 cells. Cell Growth Differ. 2 (1991) 209-214
37. Heck M.M., Hittelman W.N., and Earnshaw W.C. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 1086-1090
38. Kimura K., Saijo M., Ui M., and Enomoto T. Growth state- and cell cycle-dependent fluctuation in the expression of two forms of DNA topoisomerase II and possible specific modification of the higher molecular weight form in the M phase. J. Biol. Chem. 269 (1994) 1173-1176
39. Bauman M.E., Holden J.A., Brown K.A., Harker W.G., and Perkins S.L. Differential immunohistochemical staining for DNA topoisomerase II alpha and beta in human tissues and for DNA topoisomerase II beta in non-Hodgkin's lymphomas. Mod. Pathol. 10 (1997) 168-175
40. Isaacs R.J., Davies S.L., Sandri M.I., Redwood C., Wells N.J., and Hickson I.D. Physiological regulation of eukaryotic topoisomerase II. Biochim. Biophys. Acta 1400 (1998) 121-137
41. Dereuddre S., Delaporte C., and Jacquemin-Sablon A. Role of topoisomerase II beta in the resistance of 9-OH-ellipticine-resistant Chinese hamster fibroblasts to topoisomerase II inhibitors. Cancer Res. 57 (1997) 4301-4308
42. Grue P., Grasser A., Sehested M., Jensen P.B., Uhse A., Straub T., Ness W., and Boege F. Essential mitotic functions of DNA topoisomerase IIα are not adopted by topoisomerase IIβ in human H69 cells. J. Biol. Chem. 273 (1998) 33660-33666
43. Yang X., Li W., Prescott E.D., Burden S.J., and Wang J.C. DNA topoisomerase IIb and neural development. Science 287 (2000) 131-134
44. Berger J.M., Gamblin S.J., Harrison S.C., and Wang J.C. Structure and mechanism of DNA topoisomerase II. Nature 379 (1996) 225-232
45. Berger J.M., Fass D., Wang J.C., and Harrison S.C. Structural similarities between topoisomerases that cleave one or both DNA strands. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 7876-7881
46. Classen S., Olland S., and Berger J.M. Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 10629-10634
47. Wei H., Ruthenburg A.J., Bechis S.K., and Verdine G.L. Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem. 280 (2005) 37041-37047
48. Worland S.T., and Wang J.C. Inducible overexpression, purification, and active site mapping of DNA topoisomerase II from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 264 (1989) 4412-4416
49. Shiozaki K., and Yanagida M. Functional dissection of the phosphorylated termini of fission yeast DNA topoisomerase II. J. Cell. Biol. 119 (1992) 1023-1036
50. Crenshaw D.G., and Hsieh T. Function of the hydrophilic carboxyl terminus of type II DNA topoisomerase from Drosophila melanogaster. I. In vitro studies. J. Biol. Chem. 268 (1993) 21328-21334
51. Mirski S.E., and Cole S.P. Cytoplasmic localization of a mutant M(r) 160,000 topoisomerase II alpha is associated with the loss of putative bipartite nuclear localization signals in a drug-resistant human lung cancer cell line. Cancer Res. 55 (1995) 2129-2134
52. Wessel I., Jensen P.B., Falck J., Mirski S.E., Cole S.P., and Sehested M. Loss of amino acids 1490Lys-Ser-Lys1492 in the COOH-terminal region of topoisomerase IIalpha in human small cell lung cancer cells selected for resistance to etoposide results in an extranuclear enzyme localization. Cancer Res. 57 (1997) 4451-4454
53. Adachi N., Miyaike M., Kato S., Kanamaru R., Koyama H., and Kikuchi A. Cellular distribution of mammalian DNA topoisomerase II is determined by its catalytically dispensable C-terminal domain. Nucleic Acids Res. 25 (1997) 3135-3142
54. Mirski S.E., Gerlach J.H., Cummings H.J., Zirngibl R., Greer P.A., and Cole S.P. Bipartite nuclear localization signals in the C terminus of human topoisomerase II alpha. Exp. Cell Res. 237 (1997) 452-455
55. Cowell I.G., Willmore E., Chalton D., Marsh K.L., Jazrawi E., Fisher L.M., and Austin C.A. Nuclear distribution of human DNA topoisomerase IIbeta: a nuclear targeting signal resides in the 116-residue C-terminal tail. Exp. Cell Res. 243 (1998) 232-240
56. DeVore R.F., Corbett A.H., and Osheroff N. Phosphorylation of topoisomerase II by casein kinase II and protein kinase C: effects on enzyme-mediated DNA cleavage/religation and sensitivity to the antineoplastic drugs etoposide and 4′-(9-acridinylamino)methane-sulfon-m-anisidide. Cancer Res. 52 (1992) 2156-2161
57. Cardenas M.E., Dang Q., Glover C.V., and Gasser S.M. Casein kinase II phosphorylates the eukaryote-specific C-terminal domain of topoisomerase II in vivo. EMBO J. 11 (1992) 1785-1796
58. Wells N.J., Addison C.M., Fry A.M., Ganapathi R., and Hickson I.D. Serine 1524 is a major site of phosphorylation on human topoisomerase II alpha protein in vivo and is a substrate for casein kinase II in vitro. J. Biol. Chem. 269 (1994) 29746-29751
59. Corbett K.D., Shultzaberger R.K., and Berger J.M. The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 7293-7298
60. Hsieh T.J., Farh L., Huang W.M., and Chan N.L. Structure of the topoisomerase IV C-terminal domain: a broken beta-propeller implies a role as geometry facilitator in catalysis. J. Biol. Chem. 279 (2004) 55587-55593
61. Corbett K.D., Schoeffler A.J., Thomsen N.D., and Berger J.M. The structural basis for substrate specificity in DNA topoisomerase IV. J. Mol. Biol. 351 (2005) 545-561
62. McClendon A.K., Rodriguez A.C., and Osheroff N. Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J. Biol. Chem. 280 (2005) 39337-39345
63. Dickey J.S., and Osheroff N. Impact of the C-terminal domain of topoisomerase IIa on the DNA cleavage activity of the human enzyme. Biochemistry 44 (2005) 11546-11554
64. McClendon A.K., and Osheroff N. The Geometry of DNA supercoils modulates topoisomerase-mediated DNA cleavage and enzyme response to anticancer drugs. Biochemistry 45 (2006) 3040-3050
65. McClendon A.K., Dickey J.S., and Osheroff N. Ability of viral topoisomerase II to discern the handedness of supercoiled DNA: bimodal recognition of DNA geometry by type II enzymes. Biochemistry 45 (2006) 11674-11680
66. Osheroff N. Eukaryotic topoisomerase II. Characterization of enzyme turnover. J. Biol. Chem. 261 (1986) 9944-9950
67. Osheroff N. Role of the divalent cation in topoisomerase II mediated reactions. Biochemistry 26 (1987) 6402-6406
68. Roca J., and Wang J.C. The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell 71 (1992) 833-840
69. Lindsley J.E., and Wang J.C. On the coupling between ATP usage and DNA transport by yeast DNA topoisomerase II. J. Biol. Chem. 268 (1993) 8096-8104
70. Wilstermann A.M., and Osheroff N. Positioning the 3′-DNA terminus for topoisomerase II-mediated religation. J. Biol. Chem. 276 (2001) 17727-17731
71. Liu L.F. DNA topoisomerases-enzymes that catalyse the breaking and rejoining of DNA. CRC Crit. Rev. Biochem. 15 (1983) 1-24 [Review]
72. Sander M., and Hsieh T. Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258 (1983) 8421-8428
73. Zechiedrich E.L., Christiansen K., Andersen A.H., Westergaard O., and Osheroff N. Double-stranded DNA cleavage/religation reaction of eukaryotic topoisomerase II: evidence for a nicked DNA intermediate. Biochemistry 28 (1989) 6229-6236
74. Osheroff N., and Zechiedrich E.L. Calcium-promoted DNA cleavage by eukaryotic topoisomerase II: trapping the covalent enzyme-DNA complex in an active form. Biochemistry 26 (1987) 4303-4309
75. Osheroff N., Shelton E.R., and Brutlag D.L. DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258 (1983) 9536-9543
76. Lindsley J.E., and Wang J.C. Proteolysis patterns of epitopically labeled yeast DNA topoisomerase II suggest an allosteric transition in the enzyme induced by ATP binding. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 10485-10489
77. Baird C.L., Harkins T.T., Morris S.K., and Lindsley J.E. Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13685-13690
78. Liu L.F., and D'Arpa P. Topoisomerase-targeting antitumor drugs: mechanisms of cytotoxicity and resistance. Important Adv. Oncol. (1992) 79-89
79. Li T.K., and Liu L.F. Tumor cell death induced by topoisomerase-targeting drugs. Annu. Rev. Pharmacol. Toxicol. 41 (2001) 53-77
80. Walker J.V., and Nitiss J.L. DNA topoisomerase II as a target for cancer chemotherapy. Cancer Invest. 20 (2002) 570-589
81. Baldwin E.L., and Osheroff N. Etoposide, topoisomerase II and cancer. Curr. Med. Chem. Anti-Cancer Agents 5 (2005) 363-372
82. Baguley B.C., and Ferguson L.R. Mutagenic properties of topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400 (1998) 213-222
83. Kaufmann S.H. Cell death induced by topoisomerase-targeted drugs: more questions than answers. Biochim. Biophys. Acta 1400 (1998) 195-211
84. Felix C.A. Secondary leukemias induced by topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400 (1998) 233-255
85. Burden D.A., and Osheroff N. Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400 (1998) 139-154
86. Felix C.A. Leukemias related to treatment with DNA topoisomerase II inhibitors. Med. Pediatr. Oncol. 36 (2001) 525-535
87. DeVore R., Whitlock J., Hainsworth J.D., and Johnson D.H. Therapy-related acute nonlymphocytic leukemia with monocytic features and rearrangement of chromosome 11q. Ann. Intern. Med. 110 (1989) 740-742
88. Pedersen-Bjergaard J., and Philip P. 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 (1991) 1147-1148
89. Pedersen-Bjergaard J. Radiotherapy- and chemotherapy-induced myelodysplasia and acute myeloid leukemia. A review. Leuk. Res. 16 (1992) 61-65
90. Felix C.A., Winick N.J., Negrini M., Bowman W.P., Croce C.M., and Lange B.J. Common region of ALL-1 gene disrupted in epipodophyllotoxin-related secondary acute myeloid leukemia. Cancer Res. 53 (1993) 2954-2956
91. Felix C.A., Lange B.J., Hosler M.R., Fertala J., and Bjornsti M.-A. Chromosome band 11q23 translocation breakpoints are DNA topoisomerase II cleavage sites. Cancer Res. 55 (1995) 4287-4292
92. Broeker P.L., Super H.G., Thirman M.J., Pomykala H., Yonebayashi Y., Tanabe S., Zeleznik-Le N., and Rowley J.D. Distribution of 11q23 breakpoints within the MLL breakpoint cluster region in de novo acute leukemia and in treatment-related acute myeloid leukemia: correlation with scaffold attachment regions and topoisomerase II consensus binding sites. Blood 87 (1996) 1912-1922
93. Sung P.A., Libura J., and Richardson C. Etoposide and illegitimate DNA double-strand break repair in the generation of MLL translocations: new insights and new questions. DNA Rep. (Amst.) 5 (2006) 1109-1118
94. Felix C.A., Kolaris C.P., and Osheroff N. Topoisomerase II and the etiology of chromosomal translocations. DNA Rep. (Amst.) 5 (2006) 1093-1108
95. Hess J.L. MLL: a histone methyltransferase disrupted in leukemia. Trends Mol. Med. 10 (2004) 500-507
96. Hess J.L. Mechanisms of transformation by MLL. Crit. Rev. Eukaryot. Gene Expr. 14 (2004) 235-254
97. Tenney K., and Shilatifard A. A COMPASS in the voyage of defining the role of trithorax/MLL-containing complexes: linking leukemogensis to covalent modifications of chromatin. J. Cell. Biochem. 95 (2005) 429-436
98. Lappin T.R., Grier D.G., Thompson A., and Halliday H.L. HOX genes: seductive science, mysterious mechanisms. Ulster Med. J. 75 (2006) 23-31
99. Li Z.Y., Liu D.P., and Liang C.C. New insight into the molecular mechanisms of MLL-associated leukemia. Leukemia 19 (2005) 183-190
100. Osheroff N. Effect of antineoplastic agents on the DNA cleavage/religation reaction of eukaryotic topoisomerase II: inhibition of DNA religation by etoposide. Biochemistry 28 (1989) 6157-6160
101. Robinson M.J., Martin B.A., Gootz T.D., McGuirk P.R., Moynihan M., Sutcliffe J.A., and Osheroff N. Effects of quinolone derivatives on eukaryotic topoisomerase II. A novel mechanism for enhancement of enzyme-mediated DNA cleavage. J. Biol. Chem. 266 (1991) 14585-14592
102. Hande K.R. Clinical applications of anticancer drugs targeted to topoisomerase II. Biochim. Biophys. Acta 1400 (1998) 173-184
103. Hande K.R. Etoposide: four decades of development of a topoisomerase II inhibitor. Eur. J. Cancer 34 (1998) 1514-1521
104. Pommier Y., and Marchand C. Interfacial inhibitors of protein-nucleic acid interactions. Curr. Med. Chem. Anti-Cancer Agents 5 (2005) 421-429
105. Kurzer M.S., and Xu X. Dietary phytoestrogens. Annu. Rev. Nutr. 17 (1997) 353-381
106. Scalbert A., and Williamson G. Dietary intake and bioavailability of polyphenols. J. Nutr. 130 (2000) 2073S-2085S
107. Yao L.H., Jiang Y.M., Shi J., Tomas-Barberan F.A., Datta N., Singanusong R., and Chen S.S. Flavonoids in food and their health benefits. Plant Foods Hum. Nutr. 59 (2004) 113-122
108. Kanadaswami C., Lee L.T., Lee P.P., Hwang J.J., Ke F.C., Huang Y.T., and Lee M.T. The antitumor activities of flavonoids. In Vivo 19 (2005) 895-909
109. Siddiqui I.A., Adhami V.M., Saleem M., and Mukhtar H. Beneficial effects of tea and its polyphenols against prostate cancer. Mol. Nutr. Food Res. 50 (2006) 130-143
110. Barnes S., Peterson T.G., and Coward L. Rationale for the use of genistein-containing soy matrices in chemoprevention trials for breast and prostate cancer. J. Cell. Biochem. Suppl. 22 (1995) 181-187
111. Stoll B.A. Eating to beat breast cancer: potential role for soy supplements. Ann. Oncol. 8 (1997) 223-225
112. Lamartiniere C.A. Protection against breast cancer with genistein: a component of soy. Am. J. Clin. Nutr. 71 (2000) 1705S-1707S discussion 1708S-1709S
113. Dragsted L.O. Antioxidant actions of polyphenols in humans. Int. J. Vitam. Nutr. Res. 73 (2003) 112-119
114. Sang S., Hou Z., Lambert J.D., and Yang C.S. Redox properties of tea polyphenols and related biological activities. Antioxid. Redox Signal 7 (2005) 1704-1714
115. Adlercreutz H., Markkanen H., and Watanabe S. Plasma concentrations of phyto-oestrogens in Japanese men. Lancet 342 (1993) 1209-1210
116. Sarkar F.H., Adsule S., Padhye S., Kulkarni S., and Li Y. The role of genistein and synthetic derivatives of isoflavone in cancer prevention and therapy. Mini Rev. Med. Chem. 6 (2006) 401-407
117. Strick R., Strissel P.L., Borgers S., Smith S.L., and Rowley J.D. Dietary bioflavonoids induce cleavage in the MLL gene and may contribute to infant leukemia. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4790-4795
118. Austin C.A., Patel S., Ono K., Nakane H., and Fisher L.M. Site-specific DNA cleavage by mammalian DNA topoisomerase II induced by novel flavone and catechin derivatives. Biochem. J. 282 Pt 3 (1992) 883-889
119. Markovits J., Junqua S., Goldwasser F., Venuat A.M., Luccioni C., Beaumatin J., Saucier J.M., Bernheim A., and Jacquemin-Sablon A. Genistein resistance in human leukaemic CCRF-CEM cells: selection of a diploid cell line with reduced DNA topoisomerase II beta isoform. Biochem. Pharmacol. 50 (1995) 177-186
120. Bandele O.J., and Osheroff N. Bioflavonoids as poisons of human topoisomerase IIalpha and IIbeta. Biochemistry 46 (2007) 6097-6108
121. Lopez-Lazaro M., Willmore E., and Austin C.A. Cells lacking DNA topoisomerase IIbeta are resistant to genistein. J. Nat. Prod. 70 (2007) 763-767
122. Elsea S.H., McGuirk P.R., Gootz T.D., Moynihan M., and Osheroff N. Drug features that contribute to the activity of quinolones against mammalian topoisomerase II and cultured cells: correlation between enhancement of enzyme-mediated DNA cleavage in vitro and cytotoxic potential. Antimicrob. Agents Chemother. 37 (1993) 2179-2186
123. Spitzner J.R., Chung I.K., Gootz T.D., McGuirk P.R., and Muller M.T. Analysis of eukaryotic topoisomerase II cleavage sites in the presence of the quinolone CP-115,953 reveals drug-dependent and -independent recognition elements. Mol. Pharmacol. 48 (1995) 238-249
124. Anderson V.E., and Osheroff N. Type II topoisomerases as targets for quinolone antibacterials: turning Dr. Jekyll into Mr. Hyde. Curr. Pharm. Des. 7 (2001) 337-353
125. Bromberg K.D., Burgin A.B., and Osheroff N. Quinolone action against human topoisomerase IIa: stimulation of enzyme-mediated double-stranded DNA cleavage. Biochemistry 42 (2003) 3393-3398
126. Hooper D.C., and Wolfson J.S. Fluoroquinolone antimicrobial agents. N. Engl. J. Med. 324 (1991) 384-394
127. In: Hooper D.C., and Wolfson J.S. (Eds). Qunolone Antimicrobial Agents (1993), American Society for Microbiology, Washington, DC
128. Chow K.C., Macdonald T.L., and Ross W.E. DNA binding by epipodophyllotoxins and N-acyl anthracyclines: implications for mechanism of topoisomerase II inhibition. Mol. Pharmacol. 34 (1988) 467-473
129. Capranico G., Palumbo M., Tinelli S., and Zunino F. Unique sequence specificity of topoisomerase II DNA cleavage stimulation and DNA binding mode of streptonigrin. J. Biol. Chem. 269 (1994) 25004-25009
130. Waring M.J. Drugs and DNA: uncoiling of the DNA double helix as evidence of intercalation. Humangenetik 9 (1970) 234-236
131. Graves D.E. Targeting DNA through-covalent interactions of reversible binding drugs. Methods Enzymol. 340 (2001) 377-395
132. Graves D.E. Drug-DNA interactions. Methods Mol. Biol. 95 (2001) 161-169
133. Beck W.T., Danks M.K., Wolverton J.S., Kim R., and Chen M. Drug resistance associated with altered DNA topoisomerase II. Adv. Enzyme Reg. 33 (1993) 113-127
134. Vassetzky Y.S., Alghisi G.C., and Gasser S.M. DNA topoisomerase II mutations and resistance to anti-tumor drugs. Bioessays 17 (1995) 767-774
135. Burden D.A., Kingma P.S., Froelich-Ammon S.J., Bjornsti M.-A., Patchan M.W., Thompson R.B., and Osheroff N. Topoisomerase II-etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J. Biol. Chem. 271 (1996) 29238-29244
136. Kingma P.S., Burden D.A., and Osheroff N. Binding of etoposide to topoisomerase II in the absence of DNA: decreased affinity as a mechanism of drug resistance. Biochemistry 38 (1999) 3457-3461
137. Leroy D., Kajava A.V., Frei C., and Gasser S.M. Analysis of etoposide binding to subdomains of human DNA topoisomerase II alpha in the absence of DNA. Biochemistry 40 (2001) 1624-1634
138. Wilstermann A.M., Bender R.P., Godfrey M., Choi S., Anklin C., Berkowitz D.B., Osheroff N., and Graves D.E. Topoisomerase II-drug interaction domains: identification of substituents on etoposide that interact with the enzyme. Biochemistry 46 (2007) 8217-8225
139. 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. Secondary leukemia or myelodysplastic syndrome after treatment with epipodophyllotoxins. J. Clin. Oncol. 17 (1999) 569-577
140. Andersen M.K., Christiansen D.H., Jensen B.A., Ernst P., Hauge G., and Pedersen-Bjergaard J. Therapy-related acute lymphoblastic leukaemia with MLL rearrangements following DNA topoisomerase II inhibitors, an increasing problem: report on two new cases and review of the literature since 1992. Br. J. Haematol. 114 (2001) 539-543
141. Libura J., Slater D.J., Felix C.A., and Richardson C. Therapy-related acute myeloid leukemia-like MLL rearrangements are induced by etoposide in primary human CD34+ cells and remain stable after clonal expansion. Blood 105 (2005) 2124-2131
142. 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. DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N. Engl. J. Med. 352 (2005) 1529-1538
143. Rowley J.D. 1993 Robert R. de Villiers lecture. Chromosome translocations: dangerous liaisons. Leukemia 8 Suppl. 1 (1994) S1-S6
144. Felix C.A., Lange B.J., Hosler M.R., Fertala J., and Bjornsti M.A. Chromosome band 11q23 translocation breakpoints are DNA topoisomerase II cleavage sites. Cancer Res. 55 (1995) 4287-4492
145. Lovett B.D., Lo Nigro L., Rappaport E.F., Blair I.A., Osheroff N., Zheng N., Megonigal M.D., Williams W.R., Nowell P.C., and Felix C.A. Near-precise interchromosomal recombination and functional DNA topoisomerase II cleavage sites at MLL and AF-4 genomic breakpoints in treatment-related acute lymphoblastic leukemia with t(4;11) translocation. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 9802-9807
146. 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. Etoposide metabolites enhance DNA topoisomerase II cleavage near leukemia-associated MLL translocation breakpoints. Biochemistry 40 (2001) 1159-1170
147. Felix C.A., and Lange B.J. Leukemia in infants. Oncologist 4 (1999) 225-240
148. Spector L.G., Xie Y., Robison L.L., Heerema N.A., Hilden J.M., Lange B., Felix C.A., Davies S.M., Slavin J., Potter J.D., Blair C.K., Reaman G.H., and Ross J.A. Maternal diet and infant leukemia: the DNA topoisomerase II inhibitor hypothesis: a report from the children's oncology group. Cancer Epidemiol. Biomarkers Prev. 14 (2005) 651-655
149. Slater D.J., Hilgenfeld E., Rappaport E.F., Shah N., Meek R.G., Williams W.R., Lovett B.D., Osheroff N., Autar R.S., Ried T., and Felix C.A. MLL-SEPTIN6 fusion recurs in novel translocation of chromosomes 3, X, and 11 in infant acute myelomonocytic leukaemia and in t(X;11) in infant acute myeloid leukaemia, and MLL genomic breakpoint in complex MLL-SEPTIN6 rearrangement is a DNA topoisomerase II cleavage site. Oncogene 21 (2002) 4706-4714
150. Rowley J.D. The critical role of chromosome translocations in human leukemias. Ann. Rev. Genet. 32 (1998) 495-519
151. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic triggers initiate translocations within the MLL gene involving the nonhomologous end joining repair system. Cancer Res. 61 (2001) 4550-4555
152. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic stimuli initiate MLL-AF9 translocations that are transcribed in cells capable of division. Cancer Res. 63 (2003) 1377-1381
153. Vaughan A.T., Betti C.J., Villalobos M.J., Premkumar K., Cline E., Jiang Q., and Diaz M.O. Surviving apoptosis: a possible mechanism of benzene-induced leukemia. Chem. Biol. Interact. 153-154 (2005) 179-185
154. Wang H., Mao Y., Chen A.Y., Zhou N., LaVoie E.J., and Liu L.F. Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation. Biochemistry 40 (2001) 3316-3323
155. Bender R.P., Lindsey Jr. R.H., Burden D.A., and Osheroff N. N-acetyl-p-benzoquinone imine, the toxic metabolite of acetaminophen, is a topoisomerase II poison. Biochemistry 43 (2004) 3731-3739
156. Lindsey Jr. R.H., Bromberg K.D., Felix C.A., and Osheroff N. 1,4-Benzoquinone is a topoisomerase II poison. Biochemistry 43 (2004) 7563-7574
157. Bender R.P., Lehmler H.J., Robertson L.W., Ludewig G., and Osheroff N. Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIalpha: altering enzyme function by blocking the N-terminal protein gate. Biochemistry 45 (2006) 10140-10152
158. Chen H., and Eastmond D.A. Topoisomerase inhibition by phenolic metabolites: a potential mechanism for benzene's clastogenic effects. Carcinogenesis 16 (1995) 2301-2307
159. Baker R.K., Kurz E.U., Pyatt D.W., Irons R.D., and Kroll D.J. Benzene metabolites antagonize etoposide-stabilized cleavable complexes of DNA topoisomerase IIalpha. Blood 98 (2001) 830-833
160. Lindsey Jr. R.H., Bender R.P., and Osheroff N. Effects of benzene metabolites on DNA cleavage mediated by human topoisomerase II alpha: 1,4-hydroquinone is a topoisomerase II poison. Chem. Res. Toxicol. 18 (2005) 761-770
161. Eastmond D.A., Mondrala S.T., and Hasegawa L. Topoisomerase II inhibition by myeloperoxidase-activated hydroquinone: a potential mechanism underlying the genotoxic and carcinogenic effects of benzene. Chem. Biol. Interact. 153-154 (2005) 207-216
162. Snyder R., and Kalf G.F. A perspective on benzene leukemogenesis. Crit. Rev. Toxicol. 24 (1994) 177-209
163. Hayes R.B., Yin S.N., Dosemeci M., Li G.L., Wacholder S., Travis L.B., Li C.Y., Rothman N., Hoover R.N., and Linet M.S. Benzene and the dose-related incidence of hematologic neoplasms in China. Chinese Academy of Preventive Medicine-National Cancer Institute Benzene Study Group. J. Natl. Cancer Inst. 89 (1997) 1065-1071
164. Irons R.D. Molecular models of benzene leukemogenesis. J. Toxicol. Environ. Health A 61 (2000) 391-397
165. Smith M.T., Zhang L., Wang Y., Hayes R.B., Li G., Wiemels J., Dosemeci M., Titenko-Holland N., Xi L., Kolachana P., Yin S., and Rothman N. Increased translocations and aneusomy in chromosomes 8 and 21 among workers exposed to benzene. Cancer Res. 58 (1998) 2176-2181
166. Smith M.T. Benzene, NQO1, and genetic susceptibility to cancer. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7624-7626
167. Smith M.T., Wang Y., Skibola C.F., Slater D.J., Lo Nigro L., Nowell P.C., Lange B.J., and Felix C.A. Low NAD(P)H:quinone oxidoreductase activity is associated with increased risk of leukemia with MLL translocations in infants and children. Blood 100 (2002) 4590-4593
168. Kim S.Y., Choi J.K., Cho Y.H., Chung E.J., Paek D., and Chung H.W. Chromosomal aberrations in workers exposed to low levels of benzene: association with genetic polymorphisms. Pharmacogenetics 14 (2004) 453-463
169. Sole F., Caballin M.R., Coll M.D., Woessner S., and Egozcue J. Acute lymphoblastic leukemia with t(4;11) in a patient previously exposed to a carcinogen. Cancer Genet. Cytogenet. 49 (1990) 133-136
170. de la Chica R.A., Ribas I., Giraldo J., Egozcue J., and Fuster C. Chromosomal instability in amniocytes from fetuses of mothers who smoke. JAMA 293 (2005) 1212-1222
171. Snyder R., and Hedli C.C. An overview of benzene metabolism. Environ. Health Perspect. 104 Suppl. 6 (1996) 1165-1171
172. Larson R.A., Wang Y., Banerjee M., Wiemels J., Hartford C., Le Beau M.M., and Smith M.T. Prevalence of the inactivating 609C → T polymorphism in the NAD(P)H:quinone oxidoreductase (NQO1) gene in patients with primary and therapy-related myeloid leukemia. Blood 94 (1999) 803-807
173. Kingma P.S., Greider C.A., and Osheroff N. Spontaneous DNA lesions poison human topoisomerase IIα and stimulate cleavage proximal to leukemic 11q23 chromosomal breakpoints. Biochemistry 36 (1997) 5934-5939
174. Kingma P.S., and Osheroff N. The response of eukaryotic topoisomerases to DNA damage. Biochim. Biophys. Acta 1400 (1998) 223-232
175. Cline S.D., and Osheroff N. Cytosine arabinoside lesions are position-specific topoisomerase II poisons and stimulate DNA cleavage mediated by the human type II enzymes. J. Biol. Chem. 274 (1999) 29740-29743
176. Cline S.D., Jones W.R., Stone M.P., and Osheroff N. DNA abasic lesions in a different light: solution structure of an endogenous topoisomerase II poison. Biochemistry 38 (1999) 15500-15507
177. Sabourin M., and Osheroff N. 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 (2000) 1947-1954
178. Khan Q.A., Kohlhagen G., Marshall R., Austin C.A., Kalena G.P., Kroth H., Sayer J.M., Jerina D.M., and Pommier Y. Position-specific trapping of topoisomerase II by benzo[a]pyrene diol epoxide adducts: implications for interactions with intercalating anticancer agents. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 12498-12503
179. Velez-Cruz R., Riggins J.N., Daniels J.S., Cai H., Guengerich F.P., Marnett L.J., and Osheroff N. Exocyclic DNA lesions stimulate DNA cleavage mediated by human topoisomerase II alpha in vitro and in cultured cells. Biochemistry 44 (2005) 3972-3981
180. Lindahl T., and Nyberg B. Rate of depurination of native deoxyribonucleic acid. Biochemistry 11 (1972) 3610-3618
181. Lindahl T., and Karlstrom O. Heat-induced depyrimidination of deoxyribonucleic acid in neutral solution. Biochemistry 12 (1973) 5151-5154
182. Nakamura J., and Swenberg J.A. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues. Cancer Res. 59 (1999) 2522-2526
183. Swenberg J.A., Fedtke N., Ciroussel F., Barbin A., and Bartsch H. Etheno adducts formed in DNA of vinyl chloride-exposed rats are highly persistent in liver. Carcinogenesis 13 (1992) 727-729
184. Lee S.H., Oe T., and Blair I.A. 4,5-Epoxy-2(E)-decenal-induced formation of 1,N(6)-etheno-2′-deoxyadenosine and 1,N(2)-etheno-2′-deoxyguanosine adducts. Chem. Res. Toxicol. 15 (2002) 300-304
185. Solovyan V.T., Bezvenyuk Z.A., Salminen A., Austin C.A., and Courtney M.J. The role of topoisomerase II in the excision of DNA loop domains during apoptosis. J. Biol. Chem. 277 (2002) 21458-21467
186. Belyaev I.Y. DNA loop organization and DNA fragmentation during radiation-induced apoptosis in human lymphocytes. Radiats. Biol. Radioecol. 45 (2005) 541-548
187. Crisona N.J., Strick T.R., Bensimon D., Croquette V., and Cozzarelli N.R. Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. Genes Dev. 14 (2000) 2881-2892
188. Stone M.D., Bryant Z., Crisona N.J., Smith S.B., Vologodskii A., Bustamante C., and Cozzarelli N.R. Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 8654-8659
189. Waring M. Variation of the supercoils in closed circular DNA by binding of antibiotics and drugs: evidence for molecular models involving intercalation. J. Mol. Biol. 54 (1970) 247-279
190. Eastmond D.A., Schuler M., Frantz C., Chen H., Parks R., Wang L., and Hawegawa L. Characterization and mechanisms of chromosomal alterations induced by benzene in mice and humans. Res. Rep. Health Eff. Inst. 103 (2001) 1-80