Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme

Biochimica et Biophysica Acta - Gene Structure and Expression

Volumn 1400, Issue 1-3, 1998, Pages 139-154

  Burden, D Andrew ^a   Osheroff, Neil ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anticancer drug; Catalytic cycle; DNA cleavage complex; Drug mechanism; Topoisomerase II

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE;

CELL KILLING; DNA BINDING; DNA CLEAVAGE; DNA METABOLISM; DNA STRAND BREAKAGE; DRUG MECHANISM; DRUG TARGETING; ENZYME MECHANISM; ENZYME SUBSTRATE; EUKARYOTE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANTINEOPLASTIC AGENTS; BINDING SITES; CATALYSIS; DNA; DNA TOPOISOMERASES, TYPE II; ENZYME INHIBITORS; EUKARYOTIC CELLS; HUMANS; MOLECULAR STRUCTURE; NUCLEIC ACID CONFORMATION;

EID: 0032190561     PISSN: 01674781     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4781(98)00132-8     Document Type: Review

References (166)

1. J.D. Watson, N.H. Hopkins, J.W. Roberts, J.A. Steitz, A.M. Weiner, Molecular Biology of the Gene, Benjamin/Cummings, Menlo Park, CA, 1987.
2. Osheroff N. Biochemical basis for the interactions of type I and type II topoisomerases with DNA. Pharmacol. Ther. 41:1989;223-241.
3. Osheroff N., Zechiedrich E.L., Gale K.C. Catalytic function of DNA topoisomerase II. BioEssays. 13:1991;269-273.
4. Berger J.M. Type II DNA topoisomerases. Curr. Opin. Sruct. Biol. 8:1998;26-32.
5. N.R. Cozzarelli, J.C. Wang, DNA Topology and its Biological Effects, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1990.
6. Wang J.C. DNA topoisomerases. Annu. Rev. Biochem. 65:1996;635-692.
7. Watt P.M., Hickson I.D. Structure and function of type II DNA topoisomerases. Biochem. J. 303:1994;681-695.
8. Hsieh T.-S., Brutlag D.L. ATP-dependent DNA topoisomerase from D. melanogaster reversibly catenates duplex DNA rings. Cell. 21:1980;115-121.
9. Liu L.F., Liu C.C., Alberts B.M. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell. 19:1980;697-707.
10. Liu L.F., Rowe T.C., Yang L., Tewey K.M., Chen G.L. Cleavage of DNA by mammalian DNA topoisomerase II. J. Biol. Chem. 258:1983;15365-15370.
11. Rowe T.C., Chen G.L., Hsiang Y.H., Liu L.F. DNA damage by antitumor acridines mediated by mammalian DNA topoisomerase II. Cancer Res. 46:1986;2021-2026.
12. Zechiedrich E.L., Christiansen K., Andersen A.H., Westergaard O., Osheroff N. Double-stranded DNA cleavage/religation reaction of eukaryotic topoisomerase II: evidence for a nicked DNA intermediate. Biochemistry. 28:1989;6229-6236.
13. Sander M., Hsieh T. Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258:1983;8421-8428.
14. Lindsley J.E., 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. USA. 88:1991;10485-10489.
15. Osheroff N., Shelton E.R., Brutlag D.L. DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258:1983;9536-9543.
16. Capranico G., Zunino F. DNA topoisomerase-trapping antitumour drugs. Eur. J. Cancer. 12:1992;2055-2060.
17. Corbett A.H., Osheroff N. When good enzymes go bad: conversion of topoisomerase II to a cellular toxin by antineoplastic drugs. Chem. Res. Toxicol. 6:1993;585-597.
18. Chen A.Y., Liu L.F. DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 34:1994;191-218.
19. L. Liu, DNA Topoisomerases: Topoisomerase-Targeted Drugs, Vol. 29, Academic Press, New York, 1994.
20. Froelich-Ammon S.J., Osheroff N. Topoisomerase poisons: harnessing the dark side of enzyme mechanism. J. Biol. Chem. 270:1995;21429-21432.
21. Sinha B.K. Topoisomerase inhibitors: a review of their therapeutic potential in cancer. Drugs. 49:1995;11-19.
22. Malonne H., Atassi G. DNA topoisomerase targeting drugs: mechanisms of action and perspectives. Anti-Cancer Drugs. 8:1997;811-822.
23. Y. Pommier, in: B.A. Teicher (Ed.), Cancer Therapeutics: Experimental and Clinical Agents, Vol. I, Humana Press, Totowa, NJ, 1997, pp. 153-174.
24. Nelson E.M., Tewey K.M., Liu L.F. Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4′-(9-acridinylamino)-methanesulfon-m-anisidide. Proc. Natl. Acad. Sci. USA. 81:1984;1361-1365.
25. Chen G.L., Yang L., Rowe T.C., Halligan B.D., Tewey K.M., Liu L.F. Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259:1984;13560-13566.
26. Ross W., Rowe T., Glisson B., Yalowich J., Liu L. Role of topoisomerase II in mediating epipodophyllotoxin-induced DNA cleavage. Cancer Res. 44:1984;5857-5860.
27. Robinson M.J., Martin B.A., Gootz T.D., McGuirk P.R., Moynihan M., Sutcliffe J.A., 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.
28. Elsea S.H., McGuirk P.R., Gootz T.D., Moynihan M., 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.
29. Miller K.G., Liu L.F., Englund P.T. A homogeneous type II DNA topoisomerase from HeLa cell nuclei. J. Biol. Chem. 256:1981;9334-9339.
30. Shelton E.R., Osheroff N., Brutlag D.L. DNA topoisomerase II from Drosophila melanogaster. Purification and physical characterization. J. Biol. Chem. 258:1983;9530-9535.
31. Goto T., Laipis P., 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.
32. Halligan B.D., Edwards K.A., Liu L.F. Purification and characterization of a type II DNA topoisomerase from bovine calf thymus. J. Biol. Chem. 260:1985;2475-2482.
33. 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., Crooke S.T., et al. Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells. Evidence for two forms of the enzyme. J. Biol. Chem. 262:1987;16739-16747.
34. Sullivan D.M., Latham M.D., Rowe T.C., Ross W.E. Purification and characterization of an altered topoisomerase II from a drugresistant Chinese hamster ovary cell line. Biochemistry. 28:1989;5680-5687.
35. Saijo M., Enomoto T., Hanaoka F., Ui M. Purification and characterization of type II DNA topoisomerase from mouse FM3A cells: phosphorylation of topoisomerase II and modification of its activity. Biochemistry. 29:1990;583-590.
36. Shiozaki K., Yanagida M. A functional 125-kDa core polypeptide of fission yeast DNA topoisomerase II. Mol. Cell. Biol. 11:1991;6093-6102.
37. Lynn R., Giaever G., Swanberg S.L., Wang J.C. Tandem regions of yeast DNA topoisomerase II share homology with different subunits of bacterial gyrase. Science. 233:1986;647-649.
38. Wyckoff E., Natalie D., Nolan J.M., Lee M., Hsieh T. Structure of the Drosophila DNA topoisomerase II gene. Nucleotide sequence and homology among topoisomerases II. J. Mol. Biol. 205:1989;1-13.
39. Worland S.T., 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.
40. Shiozaki K., Yanagida M. Functional dissection of the phosphorylated termini of fission yeast DNA topoisomerase II. J. Cell Biol. 119:1992;1023-1036.
41. Crenshaw D.G., Hsieh T. Function of the hydrophilic carboxyl terminus of type II DNA topoisomerase from Drosophila melanogaster. II. In vivo studies. J. Biol. Chem. 268:1993;21335-21343.
42. Mirski S.E., 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.
43. Cardenas M.E., Dang Q., Glover C.V., Gasser S.M. Casein kinase II phosphorylates the eukaryote-specific C-terminal domain of topoisomerase II in vivo. EMBO J. 11:1992;1785-1796.
44. Wells N.J., Addison C.M., Fry A.M., Ganapathi R., 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.
45. Caron P.R., Watt P., Wang J.C. The C-terminal domain of Saccharomyces cerevisiae DNA topoisomerase II. Mol. Cell. Biol. 14:1994;3197-3207.
46. Crenshaw D.G., 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.
47. Goto T., Wang J.C. Yeast DNA topoisomerase II is encoded by a single-copy, essential gene. Cell. 36:1984;1073-1080.
48. Drake F.H., Hofmann G.A., Bartus H.F., Mattern M.R., Crooke S.T., Mirabelli C.K. Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry. 28:1989;8154-8160.
49. Jenkins J.R., Ayton P., Jones T., Davies S.L., Simmons D.L., Harris A.L., Sheer D., 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.
50. Austin C.A., Sng J.H., Patel S., Fisher L.M. Novel HeLa topoisomerase II is the II beta isoform: complete coding sequence and homology with other type II topoisomerases. Biochim. Biophys. Acta. 1172:1993;283-291.
51. Capranico G., Tinelli S., Austin C.A., Fisher M.L., Zunino F. Different patterns of gene expression of topoisomerase II isoforms in differentiated tissues during murine development. Biochim. Biophys. Acta. 1132:1992;43-48.
52. Burden D.A., Sullivan D.M. Phosphorylation of the alpha- and beta-isoforms of DNA topoisomerase II is qualitatively different in interphase and mitosis in Chinese hamster ovary cells. Biochemistry. 33:1994;14651-14655.
53. Watanabe M., Tsutsui K., Tsutsui K., Inoue Y. Differential expressions of the topoisomerase II alpha and II beta mRNAs in developing rat brain. Neurosci. Res. 19:1994;51-57.
54. Jensen S., Redwood C.S., Jenkins J.R., Andersen A.H., 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.
55. Meczes E.L., Marsh K.L., Fisher L.M., Rogers M.P., 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.
56. Heck M.M., Hittelman W.N., Earnshaw W.C. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc. Natl. Acad. Sci. USA. 85:1988;1086-1090.
57. Woessner R.D., Mattern M.R., Mirabelli C.K., Johnson R.K., Drake F.H. Proliferation- and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. Cell Growth Differ. 2:1991;209-214.
58. Saijo M., Ui M., Enomoto T. Growth state and cell cycle dependent phosphorylation of DNA topoisomerase II in Swiss 3T3 cells. Biochemistry. 31:1992;359-363.
59. Burden D.A., Goldsmith L.J., Sullivan D.M. Cell-cycle-dependent phosphorylation and activity of Chinese-hamster ovary topoisomerase II. Biochem. J. 293:1993;297-304.
60. Kimura K., Saijo M., Ui M., 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.
61. Heck M.M., Earnshaw W.C. Topoisomerase II: A specific marker or cell proliferation. J. Cell Biol. 103:1986;2569-2581.
62. Sullivan D.M., Chow K.C., Glisson B.S., Ross W.E. Role of proliferation in determining sensitivity to topoisomerase II-active chemotherapy agents. Natl. Cancer Inst. Monogr. 4:1987;73-78.
63. Sullivan D.M., Latham M.D., Ross W.E. Proliferation-dependent topoisomerase II content as a determinant of antineoplastic drug action in human, mouse, and Chinese hamster ovary cells. Cancer Res. 47:1987;3973-3979.
64. Hsiang Y.H., Wu H.Y., Liu L.F. Proliferation-dependent regulation of DNA topoisomerase II in cultured human cells. Cancer Res. 48:1988;3230-3235.
65. Biersack H., Jensen S., Gromova I., Nielsen I., Westergaard O., Andersen A. Active heterodimers are formed from human DNA topoisomerase IIα and IIβ isoforms. Proc. Natl. Acad. Sci. USA. 93:1996;8288-8293.
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. Sander M., Hsieh T., Udvardy A., Schedl P. Sequence dependence of Drosophila topoisomerase II in plasmid relaxation and DNA binding. J. Mol. Biol. 194:1987;219-229.
69. Lee M.P., Sander M., Hsieh T. Nuclease protection by Drosophila DNA topoisomerase II. Enzyme/DNA contacts at the strong topoisomerase II cleavage sites. J. Biol. Chem. 264:1989;21779-21787.
70. Thomsen B., Bendixen C., Lund K., Andersen A.H., Sørenson B.S., Westergaard O. Characterization of the interaction between topoisomerase II and DNA by transcriptional footprinting. J. Mol. Biol. 215:1990;237-244.
71. Howard M.T., Lee M.P., Hsieh T.S., Griffith J.D. Drosophila topoisomerase II-DNA interactions are affected by DNA structure. J. Mol. Biol. 217:1991;53-62.
72. Bechert T., Diekmann S., Arndt-Jovin D.J. Human 170 kDa and 180 kDa topoisomerases II bind preferentially to curved and left-handed linear DNA. J. Biomol. Struct. Dynam. 12:1994;605-623.
73. Zechiedrich E.L., Osheroff N. Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 9:1990;4555-4562.
74. Roca J., Berger J.M., Wang J.C. On the simultaneous binding of eukaryotic DNA topoisomerase II to a pair of double-stranded DNA helices. J. Biol. Chem. 268:1993;14250-14255.
75. Roca J., 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.
76. Madden K.R., Stewart L., Champoux J.J. Preferential binding of human topoisomerase I to superhelical DNA. EMBO J. 14:1995;5399-5409.
77. Corbett A.H., DeVore R.F., Osheroff N. Effect of casein kinase IImediated phosphorylation on the catalytic cycle of topoisomerase II. Regulation of enzyme activity by enhancement of ATP hydrolysis. J. Biol. Chem. 267:1992;20513-20518.
78. Dang Q., Alghisi G.C., Gasser S.M. Phosphorylation of the C-terminal domain of yeast topoisomerase II by casein kinase II affects DNA-protein interaction. J. Mol. Biol. 243:1994;10-24.
79. Osheroff N., 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.
80. Andersen A.H., Christiansen K., Zechiedrich E.L., Jensen P.S., Osheroff N., Westergaard O. Strand specificity of the topoisomerase II mediated double-stranded DNA cleavage reaction. Biochemistry. 28:1989;6237-6244.
81. Muller M.T., Spitzner J.R., DiDonato J.A., Mehta V.B., Tsutsui K., Tsutsui K. Single-strand DNA cleavages by eukaryotic topoisomerase II. Biochemistry. 27:1988;8369-8379.
82. Sander M., Hsieh T.S. Drosophila topoisomerase II double-strand DNA cleavage: analysis of DNA sequence homology at the cleavage site. Nucleic Acids Res. 13:1985;1057-1072.
83. Spitzner J.R., Muller M.T. A consensus sequence for cleavage by vertebrate DNA topoisomerase II. Nucleic Acids Res. 16:1988;5533-5556.
84. Pommier Y., Capranico G., Orr A., Kohn K.W. Distribution of topoisomerase II cleavage sites in simian virus 40 DNA and the effects of drugs. J. Mol. Biol. 222:1991;909-924.
85. Sperry A.O., Blasquez V.C., Garrard W.T. Dysfunction of chromosomal loop attachment sites: illegitimate recombination linked to matrix association regions and topoisomerase II. Proc. Natl. Acad. Sci. USA. 86:1989;5497-5501.
86. Cornarotti M., Tinelli S., Willmore E., Zunino F., Fisher L.M., Austin C.A., Capranico G. Drug sensitivity and sequence specificity of human recombinant DNA topoisomerases IIα (p170) and IIβ (p180). Mol. Pharmacol. 50:1996;1463-1471.
87. Capranico G., Kohn K.W., Pommier Y. Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin. Nucleic Acids Res. 18:1990;6611-6619.
88. Spitzner J.R., Chung I.K., Muller M.T. Eukaryotic topoisomerase II preferentially cleaves alternating purine-pyrimidine repeats. Nucleic Acids Res. 18:1990;1-11.
89. Froelich-Ammon S.J., Gale K.C., Osheroff N. Site-specific cleavage of a DNA hairpin by topoisomerase II. DNA secondary structure as a determinant of enzyme recognition/cleavage. J. Biol. Chem. 269:1994;7719-7725.
90. Arndt-Jovin D.J., Udvardy A., Garner M.M., Ritter S., Jovin T.M. Z-DNA binding and inhibition by GTP of Drosophila topoisomerase II. Biochemistry. 32:1993;4862-4872.
91. Chung I.K., Mehta V.B., Spitzner J.R., Muller M.T. Eukaryotic topoisomerase II cleavage of parallel stranded DNA tetraplexes. Nucleic Acids Res. 20:1992;1973-1977.
92. Corbett A.H., Zechiedrich E.L., Osheroff N. A role for the passage helix in the DNA cleavage reaction of eukaryotic topoisomerase II. A two-site model for enzyme-mediated DNA cleavage. J. Biol. Chem. 267:1992;683-686.
93. Wigley D.B., Davies G.J., Dodson E.J., Maxwell A., Dodson G. Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature. 351:1991;624-629.
94. Ali J.A., Orphanides G., Maxwell A. Nucleotide binding to the 43-kilodalton N-terminal fragment of the DNA gyrase B protein. Biochemistry. 34:1995;9801-9808.
95. Berger J.M., Gamblin S.J., Harrison S.C., Wang J.C. Structure and mechanism of DNA topoisomerase II. Nature. 379:1996;225-232.
96. Berger J.M., Wang J.C. Recent developments in DNA topoisomerase II structure and mechanism. Curr. Opin. Struct. Biol. 6:1996;84-90.
97. Benedetti P., Baldi M.I., Mattoccia E., Tocchini-Valentini G.P. Purification and characterization of Xenopus laevis topoisomerase II. EMBO J. 2:1983;1303-1308.
98. Schomburg U., Grosse F. Purification and characterization of DNA topoisomerase II from calf thymus associated with polypeptides of 175 and 150 kDa. Eur. J. Biochem. 160:1986;451-457.
99. Roca J., Berger J.M., Harrison S.C., Wang J.C. DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl. Acad. Sci. USA. 93:1996;4057-4062.
100. Lindsley J.E. Intradimerically tethered DNA topoisomerase II is catalytically active in DNA transport. Proc. Natl. Acad. Sci. USA. 93:1996;2975-2980.
101. E.L. Zechiedrich, Doctoral Dissertation in Biochemistry, Vanderbilt University, Nashville, TN, 1990.
102. Roca J., Wang J.C. DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell. 77:1994;609-616.
103. Robinson M.J., Osheroff N. Effects of antineoplastic drugs on the post-strand-passage DNA cleavage/religation equilibrium of topoisomerase II. Biochemistry. 30:1991;1807-1813.
104. Lindsley J.E., Wang J.C. On the coupling between ATP usage and DNA transport by yeast DNA topoisomerase II. J. Biol. Chem. 268:1993;8096-8104.
105. Corbett A.H., Fernald A.W., Osheroff N. Protein kinase C modulates the catalytic activity of topoisomerase II by enhancing the rate of ATP hydrolysis: evidence for a common mechanism of regulation by phosphorylation. Biochemistry. 32:1993;2090-2097.
106. R.L. Stevenson, The Strange Case of Dr. Jekyll and Mr. Hyde, Longmans, Greene, and Co., London, 1886.
107. Kohn K.W. DNA filter elution: a window on DNA damage in mammalian cells. BioEssays. 18:1996;505-513.
108. Ferguson L.R., Baguley B.C. Topoisomerase II enzymes and mutagenicity. Environ. Mol. Mutagen. 24:1994;245-261.
109. Holm C., Covey J.M., Kerrigan D., Pommier Y. Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res. 49:1989;6365-6368.
110. D'Arpa P., Beardmore C., Liu L.F. Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res. 50:1990;6919-6924.
111. Howard M.T., Neece S.H., Matson S.W., Kreuzer K.N. Disruption of a topoisomerase-DNA cleavage complex by a DNA helicase. Proc. Natl. Acad. Sci. USA. 91:1994;12031-12035.
112. Bae Y.S., Kawasaki I., Ikeda H., Liu L.F. Illegitimate recombination mediated by calf thymus DNA topoisomerase II in vitro. Proc. Natl. Acad. Sci. USA. 85:1988;2076-2080.
113. Nitiss J., Wang J.C. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl. Acad. Sci. USA. 85:1988;7501-7505.
114. Andersson H.C., Kihlman B.A. The production of chromosomal alterations in human lymphocytes by drugs known to interfere with the activity of DNA topoisomerase II. I. m-AMSA. Carcinogenesis. 10:1989;123-130.
115. DeVore R., Whitlock J., Hainsworth T., Johnson D. Therapy-related acute nonlymphocytic leukemia with monocytic features and rearrangement of chromosome 11q. Ann. Intern. Med. 110:1989;740-742.
116. Lonn U., Lonn S., Nylen U., Winblad G. Altered formation of DNA in human cells treated with inhibitors of DNA topoisomerase II (etoposide and teniposide). Cancer Res. 49:1989;6202-6207.
117. Charron M., Hancock R. DNA topoisomerase II is required for formation of mitotic chromosomes in Chinese hamster ovary cells: studies using the inhibitor 4′-demethylepipodophyllotoxin 9-(4,6-O-thenylidene-beta-D-glucopyranoside). Biochemistry. 29:1990;9531-9537.
118. Han Y.H., Austin M.J., Pommier Y., Povirk L.F. Small deletion and insertion mutations induced by the topoisomerase II inhibitor teniposide in CHO cells and comparison with sites of drug-stimulated DNA cleavage in vitro. J. Mol. Biol. 229:1993;52-66.
119. Solary E., Bertrand R., Pommier Y. Apoptosis induced by DNA topoisomerase I and II inhibitors in human leukemic HL-60 cells. [Review]. Leuk. Lymph. 15:1994;21-32.
120. Chen A.Y., Liu L.F. Mechanisms of resistance to topoisomerase inhibitors. Cancer Treat. Res. 73:1994;263-281.
121. DeVore R., Hainsworth J., Greco F.A., Hande K., Johnson D. Chronic oral etoposide in the treatment of small cell lung cancer. Semin. Oncol. 19:1992;40-44.
122. Belani C.P., Doyle L.A., Aisner J. Etoposide: current status and future perspectives in the management of malignant neoplasms. Cancer Chemother. Pharmacol. 34:1994;S118-126.
123. Y. Pommier, M.R. Fesen, F. Goldwasser, in: B.A. Chabner, D.L. Longo (Eds.), Cancer Chemotherapy and Biotherapy: Principles and Practice, 2nd edn., Lippincott-Raven, Philadelphia, PA, 1996, pp. 435-461.
124. B.A. Chabner, in: V.T. DeVita, S. Hellman, S.A. Rosenberg (Eds.), Cancer: Principles and Practice of Oncology, 4th edn., J.B. Lippincott Co., Philadelphia, PA, 1993, pp. 325-417.
125. Barnes S., Peterson T.G., 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.
126. Stoll B.A. Eating to beat breast cancer: Potential role for soy supplements. Ann. Oncol. 8:1997;223-225.
127. Maxwell A. The molecular basis of quinolone action. [Review]. J. Antimicrob. Chemother. 30:1992;409-414.
128. Robinson M.J., Martin B.A., Gootz T.D., McGuirk P.R., Osheroff N. Effects of novel fluoroquinolones on the catalytic activities of eukaryotic topoisomerase II: Influence of the C-8 fluorine group. Antimicrob. Agents Chemother. 36:1992;751-756.
129. T. Gootz, N. Osheroff, in: D.C. Hooper, J.S. Wolfson (Eds.), Quinolone Antimicrobial Agents, American Society of Microbiology, Washington, DC, 1993, pp. 139-160.
130. Hooper D.C., Wolfson J.S. Fluoroquinolone antimicrobial agents. New Engl. J. Med. 324:1991;384-394.
131. D.C. Hooper, J.S. Wolfson (Eds.), Quinolone Antimicrobial Agents, American Society of Microbiology, Washington, DC, 1993.
132. L.F. Liu, P. D'Arpa, Topoisomerase-targeting antitumor drugs: mechanisms of cytotoxicity and resistance, Important Adv. Oncol. (1992) 79-89.
133. Pommier Y., Leteurtre F., Fesen M.R., Fujimori A., Bertrand R., Solary E., Kohlhagen G., Kohn K.W. Cellular determinants of sensitivity and resistance to DNA topoisomerase inhibitors. Cancer Invest. 12:1994;530-542.
134. Kreuzer K.N., Cozzarelli N.R. Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J. Bacteriol. 140:1979;424-435.
135. Webb C.D., Latham M.D., Lock R.B., Sullivan D.M. Attenuated topoisomerase II content directly correlates with a low level of drug resistance in a Chinese hamster ovary cell line. Cancer Res. 51:1991;6543-6549.
136. Nitiss J.L., Liu Y.X., Harbury P., Jannatipour M., Wasserman R., Wang J.C. Amsacrine and etoposide hypersensitivity of yeast cells overexpressing DNA topoisomerase II. Cancer Res. 52:1992;4467-4472.
137. Qiu J., Catapano C.V., Fernandes D.J. Formation of topoisomerase IIα complexes with nascent DNA is related to VM-26-induced cytotoxicity. Biochemistry. 35:1996;16354-16360.
138. Brown G.A., McPherson J.P., Gu L., Hedley D.W., Toso R., Deuchars K.L., Freedman M.H., Goldenberg G.J. Relationship of DNA topoisomerase II alpha and beta expression to cytotoxicity of antineoplastic agents in human acute lymphoblastic leukemia cell lines. Cancer Res. 55:1995;78-82.
139. Beck W.T., Danks M.K., Wolverton J.S., Kim R., Chen M. Drug resistance associated with altered DNA topoisomerase II. Adv. Enzyme Regul. 33:1993;113-127.
140. Vassetzky Y.S., Alghisi G.-C., Gasser S.M. DNA topoisomerase II mutations and resistance to anti-tumor drugs. BioEssays. 17:1995;767-774.
141. Nitiss J.L., Beck W.T. Antitopoisomerase drug action and resistance. Eur. J. Cancer. 32a:1996;958-966.
142. Hsiung Y., Elsea S.H., Osheroff N., Nitiss J.L. A mutation in yeast TOP2 homologous to a quinolone-resistant mutation in bacteria. J. Biol. Chem. 270:1995;20359-20364.
143. Zwelling L.A., Hinds M., Chan D., Mayes J., Sie K.L., Parker E., Silberman L., Radcliffe A., Beran M., Blick M. Characterization of an amsacrine-resistant line of human leukemia cells. Evidence for a drugresistant form of topoisomerase II. J. Biol. Chem. 264:1989;16411-16420.
144. Bugg B.Y., Danks M.K., Beck W.T., Suttle D.P. Expression of a mutant DNA topoisomerase II in CCRF-CEM human leukemic cells selected for resistance to teniposide. Proc. Natl. Acad. Sci. USA. 88:1991;7654-7658.
145. Mayes J., Hinds M., Soares L., Altschuler E., Kim P., Zwelling L.A. Further characterization of an amsacrine-resistant line of HL-60 human leukemia cells and its topoisomerase II. Effects of ATP concentration, anion concentration, and the three-dimensional structure of the DNA target. Biochem. Pharmacol. 46:1993;699-707.
146. Elsea S.H., Hsiung Y., Nitiss J.L., Osheroff N. 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. 270:1995;1913-1920.
147. Corbett A.H., Hong D., Osheroff N. Exploiting mechanistic differences between drug classes to define functional drug interaction domains on topoisomerase II. Evidence that several diverse DNA cleavage-enhancing agents share a common site of action on the enzyme. J. Biol. Chem. 268:1993;14394-14398.
148. Osheroff N., Corbett A.H., Elsea S.H., Westergaard M. Defining functional drug-interaction domains on topoisomerase II by exploiting mechanistic differences between drug classes. Cancer Chemother. Pharmacol. 34:1994;S19-25.
149. Elsea S.H., Westergaard M., Osheroff N. Quinolones share a common interaction domain on topoisomerase II with other DNA cleavage-enhancing antineoplastic drugs. Biochemistry. 36:1997;2919-2924.
150. Estey E.H., Silberman L., Beran M., Andersson B.S., Zwelling L.A. The interaction between nuclear topoisomerase II activity from human leukemia cells, exogenous DNA, and 4′-(9-acridinylamino)methanesulfon-m-anisidide (m-AMSA) or 4-(4,6-O-ethylidene-beta-D-glucopyranoside) (VP-16) indicates the sensitivity of the cells to the drugs. Biochem. Biophys. Res. Commun. 144:1987;787-793.
151. Freudenreich C.H., Kreuzer K.N. Localization of an aminoacridine antitumor agent in a type II topoisomerase-DNA complex. Proc. Natl. Acad. Sci. USA. 91:1994;11007-11011.
152. Pommier Y., Capranico G., Orr A., Kohn K.W. Local base sequence preferences for DNA cleavage by mammalian topoisomerase II in the presence of amsacrine or teniposide. Nucleic Acids Res. 19:1991;5973-5980.
153. Capranico G., De Isabella P., Tinelli S., Bigioni M., Zunino F. Similar sequence specificity of mitoxantrone and VM-26 stimulation of in vitro DNA cleavage by mammalian DNA topoisomerase II. Biochemistry. 32:1993;3038-3046.
154. 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.
155. Robinson M.J., Osheroff N. Stabilization of the topoisomerase II-DNA cleavage complex by antineoplastic drugs: inhibition of enzyme-mediated DNA religation by 4′-(9-acridinylamino)methanesulfon-m-anisidide. Biochemistry. 29:1990;2511-2515.
156. Sørensen B.S., Sinding J., Andersen A.H., Alsner J., Jensen P.B., Westergaard O. Mode of action of topoisomerase II-targeting agents at a specific DNA sequence. Uncoupling the DNA binding, cleavage and religation events. J. Mol. Biol. 228:1992;778-786.
157. Burden D.A., Kingma P.S., Froelich-Ammon S.J., Bjornsti M.-A., Patchan M.W., Thompson R.B., Osheroff N. Topoisomerase II·etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J. Biol. Chem. 271:1996;29238-29244.
158. Froelich-Ammon S.J., Patchan M.W., Osheroff N., 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;14998-15005.
159. Cline S.D., Macdonald T.L., Osheroff N. Azatoxin is a mechanistic hybrid of the topoisomerase II-targeted anticancer drugs etoposide and ellipticine. Biochemistry. 36:1997;13095-13101.
160. Kingma P.S., Osheroff N. Spontaneous DNA damage stimulates topoisomerase II-mediated DNA cleavage. J. Biol. Chem. 272:1997;7488-7493.
161. Kingma P.S., Osheroff N. Apurinic sites are position-specific topoisomerase II-poisons. J. Biol. Chem. 272:1997;1148-1155.
162. Hertzberg R.P., Caranfa M.J., Hecht S.M. On the mechanism of topoisomerase I inhibition by camptothecin: evidence for binding to an enzyme-DNA complex. Biochemistry. 28:1989;4629-4638.
163. Shen L.L., Kohlbrenner W.E., Weigl D., Baranowski J. Mechanism of quinolone inhibition of DNA gyrase. Appearance of unique norfloxacin binding sites in enzyme-DNA complexes. J. Biol. Chem. 264:1989;2973-2978.
164. Willmott C.J., Maxwell A. A single point mutation in the DNA gyrase A protein greatly reduces binding of fluoroquinolones to the gyrase-DNA complex. Antimicrob. Agents Chemother. 37:1993;126-127.
165. Yoshida H., Nakamura M., Bogaki M., Ito H., Kojima T., Hattori H., Nakamura S. Mechanism of action of quinolones against Escherichia coli DNA gyrase. Antimicrob. Agents Chemother. 37:1993;839-845.
166. Froelich-Ammon S.J., Burden D.A., Patchan M.W., Elsea S.H., Thompson R.B., Osheroff N. Increased drug affinity as the mechanistic basis for drug hypersensitivity of a mutant type II topoisomerase. J. Biol. Chem. 270:1995;28018-28021.