Topoisomerase inhibitors as anticancer agents: A patent update

Expert Opinion on Therapeutic Patents

Volumn 23, Issue 8, 2013, Pages 1033-1056

  Khadka, Daulat B ^a   Cho, Won Jea ^a  

^a Chonnam National University   (South Korea)

Author keywords

COMPARE analysis; Dibenzonaphthyridine; Evodiamine; Indenoisoquinoline; Molecular modeling; Structure activity relationship; Topo poison; Topoisomerase; Virtual screening

Indexed keywords

ANTINEOPLASTIC AGENT; ARSENIC TRIOXIDE; BELOTECAN; BENZACRIDINE; BENZO[A]PHENAZIN 11 CARBOXAMIDE; BENZO[C]PHENANTHRIDINE DERIVATIVE; CAMPTOTHECIN; DIBENZO[C,H][1,6]NAPHTHYRIDINONE DERIVATIVE; DNA TOPOISOMERASE INHIBITOR; EDOTECARIN; EVODIAMINE; GYRASE INHIBITOR; INDENO[1,2 C]ISOQUINOLINE; IRINOTECAN; ISOQUINOL[4,3 C]CINNOLIN 12 ONE; KR 0006033; LAMELLARIN; NAPHTHYRIDINE DERIVATIVE; NITIDINE; NITROINDENOISOQUINOLINE; PIBENZIMOL; PROTOBERBERINE; PYRIDINE DERIVATIVE; STAUROSPORINE; TOPOTECAN; UNCLASSIFIED DRUG; US 0139409; VINBLASTINE; WO 041653; WO 041660; WO 140467;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; CANCER CELL; CANCER CHEMOTHERAPY; CELL CYCLE ARREST; CELL DEATH; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; COMPUTER AIDED DESIGN; CRYSTAL STRUCTURE; CYTOTOXICITY; DNA CLEAVAGE; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG SCREENING; ENZYME ACTIVITY; HEREDITY; HUMAN; IC 50; LIGAND BINDING; LUNG CANCER; MOLECULAR DOCKING; MOLECULAR MODEL; NONHUMAN; OVARY CANCER; PATENT; REVIEW; SOLID TUMOR; STEREOSPECIFICITY; STRUCTURE ACTIVITY RELATION; TRANSESTERIFICATION;

ANIMALS; ANTINEOPLASTIC AGENTS; COMPUTER-AIDED DESIGN; DNA TOPOISOMERASES, TYPE I; DNA TOPOISOMERASES, TYPE II; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; NEOPLASMS; PATENTS AS TOPIC; STRUCTURE-ACTIVITY RELATIONSHIP; TOPOISOMERASE I INHIBITORS; TOPOISOMERASE II INHIBITORS;

EID: 84880670468     PISSN: 13543776     EISSN: 17447674     Source Type: Journal    
DOI: 10.1517/13543776.2013.790958     Document Type: Review

References (122)

1. Schoeffler AJ, Berger JM DNA topoisomerases: harnessing and constraining energy to govern chromosome topology Q Rev Biophys 2008;41:41-101
2. Pommier Y, Leo E, Zhang H, Marchand C DNA topoisomerases and their poisoning by anticancer and antibacterial drugs Chem Biol 2010;17:421-33
3. Pommier Y Topoisomerase I inhibitors: camptothecins and beyond Nat Rev Cancer 2006;6:789-802
4. Sordet O, Khan QA, Plo I, et al Apoptotic topoisomerase I-DNA complexes induced by staurosporine-mediated oxygen radicals J Biol Chem 2004;279:50499-504
5. Pourquier P, Pilon AA, Kohlhagen G, et al Trapping of mammalian topoisomerase I and recombinations induced by damaged DNA containing nicks or gaps Importance of DNA end phosphorylation and camptothecin effects J Biol Chem 1997;272:26441-7
6. Pourquier P, Ueng LM, Kohlhagen G, et al Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I J Biol Chem 1997;272:7792-6
7. Lesher DT, Pommier Y, Stewart L, Redinbo MR 8-Oxoguanine rearranges the active site of human topoisomerase I Proc Natl Acad Sci USA 2002;99:12102-7
8. Chrencik JE, Burgin AB, Pommier Y, et al Structural impact of the leukemia drug 1-beta-D-arabinofuranosylcytosine (Ara-C) on the covalent human topoisomerase I-DNA complex J Biol Chem 2003;278:12461-6
9. Chowdhury AR, Mandal S, Mittra B, et al Betulinic acid, a potent inhibitor of eukaryotic topoisomerase I: identification of the inhibitory step, the major functional group responsible and development of more potent derivatives Med Sci Monit 2002;8:BR254-65
10. Sehested M, Jensen PB Mapping of DNA topoisomerase II poisons (etoposide, clerocidin) and catalytic inhibitors (aclarubicin, ICRF-187) to four distinct steps in the topoisomerase II catalytic cycle Biochem Pharmacol 1996;51:879-86
11. Gormley NA, Orphanides G, Meyer A, et al The interaction of coumarin antibiotics with fragments of DNA gyrase B protein Biochemistry 1996;35:5083-92
12. Drake FH, Hofmann GA, Mong SM, et al In vitro and intracellular inhibition of topoisomerase II by the antitumor agent merbarone Cancer Res 1989;49:2578-83
13. Roca J, Ishida R, Berger JM, et al Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp Proc Natl Acad Sci USA 1994;91:1781-5
14. Giovanella BC, Stehlin JS, Wall ME, et al DNA topoisomerase I-targeted chemotherapy of human colon cancer in xenografts Science 1989;246:1046-8
15. Kohlhagen G, Paull KD, Cushman M, et al Protein-linked DNA strand breaks induced by NSC 314622, a novel noncamptothecin topoisomerase I poison Mol Pharmacol 1998;54:50-8
16. Staker BL, Hjerrild K, Feese MD, et al The mechanism of topoisomerase I poisoning by a camptothecin analog Proc Natl Acad Sci USA 2002;99:15387-92
17. Staker BL, Feese MD, Cushman M, et al Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex J Med Chem 2005;48:2336-45
18. Ioanoviciu A, Antony S, Pommier Y, et al Synthesis and mechanism of action studies of a series of norindenoisoquinoline topoisomerase I poisons reveal an inhibitor with a flipped orientation in the ternary DNA-enzyme-inhibitor complex as determined by X-ray crystallographic analysis J Med Chem 2005;48:4803-14
19. Song Y, Shao Z, Dexheimer TS, et al Structure-based design, synthesis, and biological studies of new anticancer norindenoisoquinoline topoisomerase I inhibitors J Med Chem 2010;53:1979-89
20. Dong G, Sheng C, Wang S, et al Selection of evodiamine as a novel topoisomerase I inhibitor by structure-based virtual screening and hit optimization of evodiamine derivatives as antitumor agents J Med Chem 2010;53:7521-31
21. Dong G, Wang S, Miao Z, et al New tricks for an old natural product: discovery of highly potent evodiamine derivatives as novel antitumor agents by systemic structure-activity relationship analysis and biological evaluations J Med Chem 2012;55:7593-613
22. Versace RW The silatecans, a novel class of lipophilic camptothecins Expert Opin Ther Patent 2003;13:751-60
23. Basili S, Moro S Novel camptothecin derivatives as topoisomerase I inhibitors Expert Opin Ther Patent 2009;19:555-74
24. Long BH, Balasubramanian BN Non-camptothecin topoisomerase I active compounds as potential anticancer agents Expert Opin Ther Patent 2000;10:635-66
25. Fox BM, Xiao X, Antony S, et al Design, synthesis, and biological evaluation of cytotoxic 11-alkenylindenoisoquinoline topoisomerase I inhibitors and indenoisoquinoline-camptothecin hybrids J Med Chem 2003;46:3275-82
26. Xiao X, Antony S, Pommier Y, Cushman M Total synthesis and biological evaluation of 22-hydroxyacuminatine J Med Chem 2006;49:1408-12
27. Grillet F, Baumlova B, Prevost G, et al Synthesis and bioevaluation of 22-hydroxyacuminatine analogs Bioorg Med Chem Lett 2008;18:2143-6
28. Purdue Research Foundation Cytotoxic indeno and isoindoloisoquinolones WO100891; 2004
29. Cinelli MA, Morrell A, Dexheimer TS, et al Design, synthesis, and biological evaluation of 14-substituted aromathecins as topoisomerase I inhibitors J Med Chem 2008;51:4609-19
30. Cinelli MA, Cordero B, Dexheimer TS, et al Synthesis and biological evaluation of 14-(aminoalkyl-aminomethyl) aromathecins as topoisomerase I inhibitors: investigating the hypothesis of shared structure-activity relationships Bioorg Med Chem 2009;17:7145-55
31. Purdue Research Foundation Oxobenzindolizinoquinolines and uses thereof WO140467; 2009
32. Cinelli MA, Morrell AE, Dexheimer TS, et al The structure-activity relationships of A-ring-substituted aromathecin topoisomerase I inhibitors strongly support a camptothecin-like binding mode Bioorg Med Chem 2010;18:5535-52
33. Industry foundation of Chonnam National University Novel isoindolo[2,1-b]isoquinolinone derivatives and anti-cancer agents including them KR0006033; 2011
34. Van HT, Cho WJ Structural modification of 3-arylisoquinolines to isoindolo[2,1-b]isoquinolinones for the development of novel topoisomerase 1 inhibitors with molecular docking study Bioorg Med Chem Lett 2009;19:2551-4
35. Van HT, Le QM, Lee KY, et al Convenient synthesis of indeno[1,2-c] isoquinolines as constrained forms of 3-arylisoquinolines and docking study of a topoisomerase I inhibitor into DNA-topoisomerase I complex Bioorg Med Chem Lett 2007;17:5763-7
36. Zhang Y, Wu LJ, Tashiro S, et al Intracellular regulation of evodiamine-induced A375-S2 cell death Biol Pharm Bull 2003;26:1543-7
37. Zhang Y, Zhang QH, Wu LJ, et al Atypical apoptosis in L929 cells induced by evodiamine isolated from Evodia rutaecarpa J Asian Nat Prod Res 2004;6:19-27
38. Huang DM, Guh JH, Huang YT, et al Induction of mitotic arrest and apoptosis in human prostate cancer pc-3 cells by evodiamine J Urol 2005;173:256-61
39. Chan AL, Chang WS, Chen LM, et al Evodiamine stabilizes topoisomerase I-DNA cleavable complex to inhibit topoisomerase I activity Molecules 2009;14:1342-52
40. Taipei Medical University Pharmaceutical composition for inhibiting topoisomerase I and method for exploiting drug US0144763; 2010
41. Pan X, Hartley JM, Hartley JA, et al Evodiamine, a dual catalytic inhibitor of type I and II topoisomerases, exhibits enhanced inhibition against camptothecin resistant cells Phytomedicine 2012;19:618-24
42. The Second Military Medical University Evodiamine compounds, preparation method thereof and application thereof CN102311434; 2012
43. Fang SD, Wang LK, Hecht SM Inhibitors of DNA topoisomerase I isolated from the roots of Zanthoxylum nitidum J Org Chem 1993;58:5025-7
44. Wang LK, Johnson RK, Hecht SM Inhibition of topoisomerase I function by nitidine and fagaronine Chem Res Toxicol 1993;6:813-18
45. Janin YL, Croisy A, Riou JF, Bisagni E Synthesis and evaluation of new 6-amino-substituted benzo[c] phenanthridine derivatives J Med Chem 1993;36:3686-92
46. Rutgers, The State university of New Jersey Heterocyclic cytotoxic agents WO31067; 1999
47. Makhey D, Li D, Zhao B, et al Substituted benzo[i]phenanthridines as mammalian topoisomerase-targeting agents Bioorg Med Chem 2003;11:1809-20
48. Li D, Zhao B, Sim SP, et al 2,3-Dimethoxybenzo[i]phenanthridines: topoisomerase I-targeting anticancer agents Bioorg Med Chem 2003;11:521-8
49. Li D, Zhao B, Sim SP, et al 8,9-methylenedioxybenzo[i]phenanthridines: topoisomerase I-targeting activity and cytotoxicity Bioorg Med Chem 2003;11:3795-805
50. Rutgers, The State university of New Jersey Cytotoxic agents WO041653; 2003
51. Rutgers, The State university of New Jersey Solubilized topoisomerase poisons WO041660; 2003
52. Ruchelman AL, Singh SK, Wu X, et al Diaza-and triazachrysenes: potent topoisomerase-targeting agents with exceptional antitumor activity against the human tumor xenograft, MDA-MB-435 Bioorg Med Chem Lett 2002;12:3333-6
53. Ruchelman AL, Singh SK, Ray A, et al 5H-Dibenzo[c,h]1,6-naphthyridin-6- ones: novel topoisomerase I-targeting anticancer agents with potent cytotoxic activity Bioorg Med Chem 2003;11:2061-73
54. Rutgers, The State university of New Jersey Nitro and amino substituted topoisomerase agents WO014918; 2004
55. Singh SK, Ruchelman AL, Li TK, et al Nitro and amino substitution in the D-ring of 5-(2-dimethylaminoethyl)-2,3-methylenedioxy-5H-dibenzo[c,h][1,6] naphthyridin-6-ones: effect on topoisomerase-I targeting activity and cytotoxicity J Med Chem 2003;46:2254-7
56. Ruchelman AL, Kerrigan JE, Li TK, et al Nitro and amino substitution within the A-ring of 5H-8,9-dimethoxy-5-(2-N,N-dimethylaminoethyl)dibenzo[c, h][1,6]naphthyridin-6-ones : influence on topoisomerase I-targeting activity and cytotoxicity Bioorg Med Chem 2004;12:3731-42
57. Rutgers, The State university of New Jersey Nitro and amino substituted topoisomerase agents WO014906; 2004
58. Ruchelman AL, Zhu S, Zhou N, et al Dimethoxybenzo[i]phenanthridine-12- carboxylic acid derivatives and 6Hdibenzo[ c,h][2,6]naphthyridin-5-ones with potent topoisomerase I-targeting activity and cytotoxicity Bioorg Med Chem Lett 2004;14:5585-9
59. Zhu S, Ruchelman AL, Zhou N, et al 6-Substituted 6H-dibenzo[c,h][2,6] naphthyridin-5-ones: reversed lactam analogues of ARC-111 with potent topoisomerase I-targeting activity and cytotoxicity Bioorg Med Chem 2006;14:3131-43
60. Rutgers, The State university of New Jersey Solubilized topoisomerase poison agents WO051289; 2003
61. Rutgers, The State university of New Jersey Topoisomerase poison agents WO047505; 2003
62. Purdue Research Foundation Substituted dibenzonaphthyridines, pharmaceuticaluses thereof and processes thereof WO024437; 2012
63. Morrell A, Antony S, Kohlhagen G, et al Synthesis of benz[d]indeno[1,2-b] pyran-5,11-diones: versatile intermediates for the design and synthesis of topoisomerase I inhibitors Bioorg Med Chem Lett 2006;16:1846-9
64. Kiselev E, Dexheimer TS, Pommier Y, Cushman M Design, synthesis, and evaluation of dibenzo[c,h][1,6] naphthyridines as topoisomerase I inhibitors and potential anticancer agents J Med Chem 2010;53:8716-26
65. Kiselev E, Empey N, Agama K, et al Dibenzo[c,h][1,5]naphthyridinediones as topoisomerase I inhibitors: design, synthesis, and biological evaluation J Org Chem 2012;77:5167-72
66. Industry foundation of Chonnam National University Novel isoquinolinone-based derivatives and anti-cancer agents including them KR0022951; 2011
67. Lee SH, Van HT, Yang SH, et al Molecular design, synthesis and docking study of benz[b]oxepines and 12-oxobenzo[c]phenanthridinones as topoisomerase 1 inhibitors Bioorg Med Chem Lett 2009;19:2444-7
68. Rutgers, The State university of New Jersey Heterocyclic cytotoxic agents WO32631; 2001
69. Yu Y, Singh SK, Liu A, et al Substituted dibenzo[c,h]cinnolines: topoisomerase I-targeting anticancer agents Bioorg Med Chem 2003;11:1475-91
70. Ruchelman AL, Singh SK, Ray A, et al 11H-Isoquino[4,3-c]cinnolin-12-ones; novel anticancer agents with potent topoisomerase I-targeting activity and cytotoxicity Bioorg Med Chem 2004;12:795-806
71. Kobayashi Y, Yamashita Y, Fujii N, et al Inhibitors of DNA topoisomerase I and II isolated from the Coptis rhizomes Planta Med 1995;61:414-18
72. Zee-Cheng KY, Paull KD, Cheng CC Experimental antileukemic agents Coralyne, analogs, and related compounds J Med Chem 1974;17:347-51
73. Wang LK, Rogers BD, Hecht SM Inhibition of topoisomerase I function by coralyne and 5,6-dihydrocoralyne Chem Res Toxicol 1996;9:75-83
74. Makhey D, Gatto B, Yu C, et al Coralyne and related compounds as mammalian topoisomerase I and topoisomerase II poisons Bioorg Med Chem 1996;4:781-91
75. Rutgers, The State university of New Jersey Coralyne analogs as topoisomerase inhibitors WO29106; 1997
76. Rutgers, The State university of New Jersey Substituted heterocycles as anti-tumor agents WO12181; 1998
77. Makhey D, Yu C, Liu A, et al Substituted benz[a]acridines and benz[c] acridines as mammalian topoisomerase poisons Bioorg Med Chem 2000;8:1171-82
78. Xenova Limited Benzo[a]phenazin-11-carboxamide derivatives and their use as joint inhibitors of topoisomerase I and II WO46157; 2001
79. Vicker N, Burgess L, Chuckowree IS, et al Novel angular benzophenazines: dual topoisomerase I and topoisomerase II inhibitors as potential anticancer agents J Med Chem 2002;45:721-39
80. Finlay GJ, Riou JF, Baguley BC From amsacrine to DACA (N-[2-(dimethylamino)ethyl]acridine-4-carboxamide): selectivity for topoisomerases I and II among acridine derivatives Eur J Cancer 1996;32A:708-14
81. Purdue Research Foundation Novel indenoisoquinolines as antineoplastic agents WO21537; 2000
82. Strumberg D, Pommier Y, Paull K, et al Synthesis of cytotoxic indenoisoquinoline topoisomerase I poisons J Med Chem 1999;42:446-57
83. Jayaraman M, Fox BM, Hollingshead M, et al Synthesis of new dihydroindeno [1,2-c]isoquinoline and indenoisoquinolinium chloride topoisomerase I inhibitors having high in vivo anticancer activity in the hollow fiber animal model J Med Chem 2002;45:242-9
84. Cushman M, Alexandra I, Pommier Y Synthesis of indenoisoquinoliniums and methods of use WO089294; 2005
85. Purdue Research Foundation The substituted norindenoisoquinolines, synthesis thereof, and methods of use WO094416; 2011
86. Purdue Research Foundation Synthesis of indenoisoquinolines US0025595; 2006
87. Morrell A, Antony S, Kohlhagen G, et al Synthesis of nitrated indenoisoquinolines as topoisomerase I inhibitors Bioorg Med Chem Lett 2004;14:3659-63
88. Morrell A, Antony S, Kohlhagen G, et al A systematic study of nitrated indenoisoquinolines reveals a potent topoisomerase I inhibitor J Med Chem 2006;49:7740-53
89. Rutgers, The State university of New Jersey Nitro and amino substituted heterocycles as topoisomerase I targeting agents WO014862; 2004
90. Purdue Research Foundation Alcohol-, diol-, and carbohydrate-substituted indenoisoquinolines as topoisomerase I inhibitors WO162513; 2012
91. Peterson KE, Cinelli MA, Morrell AE, et al Alcohol-, diol-, and carbohydrate-substituted indenoisoquinolines as topoisomerase I inhibitors: investigating the relationships involving stereochemistry, hydrogen bonding, and biological activity J Med Chem 2011;54:4937-53
92. Yeungnam University, Industry-academic Cooperation Foundation Novel 2,4-diphenyl-6-aryl pyridine compound as a potent topoisomerase I and II inhibitor, the preparation method thereof and a composition containing the same KR0109028; 2011
93. Zhao LX, Kim TS, Ahn SH, et al Synthesis, topoisomerase I inhibition and antitumor cytotoxicity of 2,2':6',2"-, 2,2':6',3"-and 2,2':6',4"-terpyridine derivatives Bioorg Med Chem Lett 2001;11:2659-62
94. Zhao LX, Moon YS, Basnet A, et al Synthesis, topoisomerase I inhibition and structure-activity relationship study of 2,4,6-trisubstituted pyridine derivatives Bioorg Med Chem Lett 2004;14:1333-7
95. Zhao LX, Sherchan J, Park JK, et al Synthesis, cytotoxicity and structure-activity relationship study of terpyridines Arch Pharm Res 2006;29:1091-5
96. Basnet A, Thapa P, Karki R, et al 2,4,6-Trisubstituted pyridines: synthesis, topoisomerase I and II inhibitory activity, cytotoxicity, and structure-activity relationship Bioorg Med Chem 2007;15:4351-9
97. Karki R, Thapa P, Kang MJ, et al Synthesis, topoisomerase I and IIinhibitory activity, cytotoxicity, and structure-activity relationship study of hydroxylated 2,4-diphenyl-6-aryl pyridines Bioorg Med Chem 2010;18:3066-77
98. Andersen RJ, Faulkner DJ, Cun-heng H, et al Metabolites of the marine prosobranch mollusc Lamellaria sp J Am Chem Soc 1985;107:5492-5
99. Quesada AR, Garcia Gravalos MD, Fernandez Puentes JL Polyaromatic alkaloids from marine invertebrates as cytotoxic compounds and inhibitors of multidrug resistance caused by P-glycoprotein Br J Cancer 1996;74:677-82
100. Facompre M, Tardy C, Bal-Mahieu C, et al Lamellarin D: a novel potent inhibitor of topoisomerase I Cancer Res 2003;63:7392-9
101. Tardy C, Facompre M, Laine W, et al Topoisomerase I-mediated DNA cleavage as a guide to the development of antitumor agents derived from the marine alkaloid lamellarin D: triester derivatives incorporating amino acid residues Bioorg Med Chem 2004;12:1697-712
102. PharmaMar, S.A.U Antitumoral analogs of lamellarins WO014917; 2004
103. Bailly C DNA relaxation and cleavage assays to study topoisomerase I inhibitors Methods Enzymol 2001;340:610-23
104. Dexheimer TS, Pommier Y DNA cleavage assay for the identification of topoisomerase I inhibitors Nat Protoc 2008;3:1736-50 Description of assays for topo I inhibition
105. Huang KC, Gao H, Yamasaki EF, et al Topoisomerase II poisoning by ICRF-193 J Biol Chem 2001;276:44488-94
106. Kerrigan JE, Pilch DS, Ruchelman AL, et al 5H-8,9-dimethoxy-5-(2-N, Ndimethylaminoethyl) dibenzo[c,h][1,6] naphthyridin-6-ones and related compounds as TOP1-targeting agents: influence of structure on the ternary cleavable complex formation Bioorg Med Chem Lett 2003;13:3395-9
107. Wu CC, Li TK, Farh L, et al Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide Science 2011;333:459-62
108. Chillemi G, Fiorani P, Benedetti P, Desideri A Protein concerted motions in the DNA-human topoisomerase I complex Nucleic Acids Res 2003;31:1525-35
109. Mancini G, D'Annessa I, Coletta A, et al Structural and dynamical effects induced by the anticancer drug topotecan on the human topoisomerase I-DNA complex PLoS One 2010;5:e10934
110. Mancini G, D'Annessa I, Coletta A, et al Binding of an Indenoisoquinoline to the topoisomerase-DNA complex induces reduction of linker mobility and strengthening of protein-DNA interaction PLoS One 2012;7:e51354
111. Seiter K Toxicity of the topoisomerase II inhibitors Expert Opin Drug Saf 2005;4:219-34
112. Pilati P, Nitti D, Mocellin S Cancer resistance to type II topoisomerase inhibitors Curr Med Chem 2012;19:3900-6
113. Nelson EM, Tewey KM, Liu LF Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4'-(9-acridinylamino)- methanesulfon-manisidide Proc Natl Acad Sci USA 1984;81:1361-5
114. Tewey KM, Chen GL, Nelson EM, Liu LF Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II J Biol Chem 1984;259:9182-7
115. Chen GL, Yang L, Rowe TC, et al Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II J Biol Chem 1984;259:13560-6
116. Tewey KM, Rowe TC, Yang L, et al Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II Science 1984;226:466-8
117. Hsiang YH, Hertzberg R, Hecht S, Liu LF Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I J Biol Chem 1985;260:14873-8
118. Crespi MD, Ivanier SE, Genovese J, Baldi A Mitoxantrone affects topoisomerase activities in human breast cancer cells Biochem Biophys Res Commun 1986;136:521-8
119. Trask DK, Muller MT Stabilization of type I topoisomerase-DNA covalent complexes by actinomycin D Proc Natl Acad Sci USA 1988;85:1417-21
120. Hsiang YH, Jiang JB, Liu LF Topoisomerase II-mediated DNA cleavage by amonafide and its structural analogs Mol Pharmacol 1989;36:371-6
121. Yamashita Y, Fujii N, Murakata C, et al Induction of mammalian DNA topoisomerase I mediated DNA cleavage by antitumor indolocarbazole derivatives Biochemistry 1992;31:12069-75
122. Chen AY, Yu C, Bodley A, et al A new mammalian DNA topoisomerase I poison Hoechst 33342: cytotoxicity and drug resistance in human cell cultures Cancer Res 1993;53:1332-7