DNA topoisomerases as molecular targets for anticancer drugs

References

• Forterre P, Gribaldo S, Gadelle D, Serre MC. Origin and evolution of DNA topoisomerases. Biochimie 2007;89:427–46.
   PubMed Web of Science ®Google Scholar
• Wang JC. Interaction between DNA and an Escherichia coli protein omega. J Mol Biol 1971;55:523–33.
   PubMed Web of Science ®Google Scholar
• Keller W. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc Natl Acad Sci USA 1975;72:4876–80.
   PubMed Web of Science ®Google Scholar
• Gellert M, Mizuuchi K, O'Dea MH, Nash HA. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci USA 1976;73:3872–6.
   PubMed Web of Science ®Google Scholar
• Baldi MI, Benedetti P, Mattoccia E, Tocchini-Valentini GP. In vitro catenation and decatenation of DNA and a novel eucaryotic ATP-dependent topoisomerase. Cell 1980;20:461–7.
   PubMed Web of Science ®Google Scholar
• Bansal S, Bajaj P, Pandey S, Tandon V. Topoisomerases: resistance versus sensitivity, how far we can go? Med Res Rev 2017;37:404–38.
   PubMed Web of Science ®Google Scholar
• Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 2001;70:369–413.
   PubMed Web of Science ®Google Scholar
• E. Mutschler G, Geisslinger HK, Kroemer S, Menzel PR, 22.3. Inhibitory topoizomerazy. In: Droździk M, Kocić I, Pawlak D, editors. Farmakologia i toksykologia. 4th ed. Wrocław: MedPharm Polska; 2016. p. 880.
   Google Scholar
• Baker NM, Rajan R, Mondragón A. Structural studies of type I topoisomerases. Nucleic Acids Res 2009;37:693–701.
   PubMed Web of Science ®Google Scholar
• Viard T, de la Tour CB. Type IA topoisomerases: a simple puzzle?. Biochimie 2007;89:456–67.
   PubMed Web of Science ®Google Scholar
• Nagaraja V, Godbole AA, Henderson SR, Maxwell A. DNA topoisomerase I and DNA gyrase as targets for TB therapy. Drug Discov Today 2017;22:510–8.
   PubMed Web of Science ®Google Scholar
• Capranico G, Marinello J, Chillemi G. Type I DNA topoisomerases. J Med Chem 2017;60:2169–92.
   PubMed Web of Science ®Google Scholar
• Bush NG, Evans-Roberts K, Maxwell A. DNA topoisomerases. EcoSal Plus 2015;6.
   PubMedGoogle Scholar
• Pommier Y, DNA topoisomerases and cancer. New York: Springer New York; 2012.
   Google Scholar
• Kirkegaard K, Wang JC. Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J. Mol. Biol 1985;185:625–37.
   PubMed Web of Science ®Google Scholar
• DiGate RJ, Marians KJ. Identification of a potent decatenating enzyme from Escherichia coli. J Biol Chem 1988;263:13366–73.
   PubMed Web of Science ®Google Scholar
• Jain C, Majumder H, Roychoudhury S. Natural compounds as anticancer agents targeting DNA topoisomerases. Curr Genomics 2017;18:75–92.
   PubMed Web of Science ®Google Scholar
• Viard T, Cossard R, Duguet M, Bouthier De La Tour C. Thermotoga maritima-Escherichia Coli chimeric topoisomerases. Answers about involvement of the carboxyl-terminal domain in DNA topoisomerase I-mediated catalysis. J Biol Chem 2004;279:30073–80.
   PubMed Web of Science ®Google Scholar
• Dekker NH, Rybenkov VV, Duguet M, et al. The mechanism of type IA topoisomerases. Proc Natl Acad Sci USA 2002;99:12126–31.
   PubMed Web of Science ®Google Scholar
• Delgado JL, Hsieh C-M, Chan N-L, Hiasa H. Topoisomerases as anticancer targets. Biochem J 2018;475:373–98.
   PubMed Web of Science ®Google Scholar
• Redinbo MR, Champoux JJ, Hol WG. Structural insights into the function of type IB topoisomerases. Curr Opin Struct Biol 1999;9:29–36.
   PubMed Web of Science ®Google Scholar
• Koster DA, Croquette V, Dekker C, et al. Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 2005;434:671–4.
   PubMed Web of Science ®Google Scholar
• Krogh BO, Shuman S. Catalytic mechanism of DNA topoisomerase IB. Mol Cell 2000;5:1035–41.
   PubMed Web of Science ®Google Scholar
• Cinelli MA. Topoisomerase 1B poisons: Over a half-century of drug leads, clinical candidates, and serendipitous discoveries. Med Res Rev 2019;39:1294–337.
   PubMed Web of Science ®Google Scholar
• Hevener KE, Verstak TA, Lutat KE, et al. Recent developments in topoisomerase-targeted cancer chemotherapy. Acta Pharm Sin B 2018;8:844–61.
   PubMed Web of Science ®Google Scholar
• Redinbo MR, Stewart L, Kuhn P, et al. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 1998;279:1504–13.
   PubMed Web of Science ®Google Scholar
• Slesarev AI, Stetter KO, Lake JA, et al. DNA topoisomerase V is a relative of eukaryotic topoisomerase I from a hyperthermophilic prokaryote. Nature 1993;364:735–7.
   PubMed Web of Science ®Google Scholar
• Taneja B, Schnurr B, Slesarev A, et al. Topoisomerase V relaxes supercoiled DNA by a constrained swiveling mechanism. Proc Natl Acad Sci USA 2007;104:14670–5.
   PubMed Web of Science ®Google Scholar
• Taneja B, Patel A, Slesarev A, Mondragón A. Structure of the N-terminal fragment of topoisomerase V reveals a new family of topoisomerases. Embo J 2006;25:398–408.
   PubMed Web of Science ®Google Scholar
• Belova GI, Prasad R, Kozyavkin SA, et al. A type IB topoisomerase with DNA repair activities. Proc Natl Acad Sci USA 2001;98:6015–20.
   PubMed Web of Science ®Google Scholar
• Belova GI, Prasad R, Nazimov IV, et al. The domain organization and properties of individual domains of DNA topoisomerase V, a type 1B topoisomerase with DNA repair activities. J Biol Chem 2002;277:4959–65.
   PubMed Web of Science ®Google Scholar
• Rajan R, Taneja B, Mondragón A. Structures of minimal catalytic fragments of topoisomerase V reveals conformational changes relevant for DNA binding. Structure 2010;18:829–38.
   PubMed Web of Science ®Google Scholar
• Schoeffler AJ, Berger JM. DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys 2008;41:41–101.
   PubMed Web of Science ®Google Scholar
• Corbett KD, Berger JM. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu Rev Biophys Biomol Struct 2004;33:95–118.
   PubMedGoogle Scholar
• Zechiedrich EL, Christiansen K, Andersen AH, et al. Double-stranded DNA cleavage/religation reaction of eukaryotic topoisomerase II: evidence for a nicked DNA intermediate. Biochemistry 1989;28:6229–36.
   PubMed Web of Science ®Google Scholar
• McClendon AK, Osheroff N. DNA topoisomerase II, genotoxicity, and cancer. Mutat Res 2007;623:83–97.
   PubMed Web of Science ®Google Scholar
• Deweese JE, Osheroff N. Coordinating the two protomer active sites of human topoisomerase IIalpha: nicks as topoisomerase II poisons. Biochemistry 2009;48:1439–41.
   PubMed Web of Science ®Google Scholar
• Deweese JE, Osheroff N. The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res 2009;37:738–48.
   PubMed Web of Science ®Google Scholar
• Chang CC, Wang YR, Chen SF, et al. New insights into DNA-binding by type IIA topoisomerases. Curr Opin Struct Biol 2013;23:125–33.
   PubMed Web of Science ®Google Scholar
• Gadelle D, Filée J, Buhler C, Forterre P. Phylogenomics of type II DNA topoisomerases. BioEssays 2003;25:232–42.
   PubMed Web of Science ®Google Scholar
• Roca J, Wang JC. DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell 1994;77:609–16.
   PubMed Web of Science ®Google Scholar
• Lima CD, Mondragón A. Mechanism of type II DNA topoisomerases: a tale of two gates. Structure 1994;2:559–60.
   PubMed Web of Science ®Google Scholar
• Berger JM, Gamblin SJ, Harrison SC, Wang JC. Structure and mechanism of DNA topoisomerase II. Nature 1996;379:225–32.
   PubMed Web of Science ®Google Scholar
• Schmidt BH, Burgin AB, Deweese JE, et al. A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 2010;465:641–4.
   PubMed Web of Science ®Google Scholar
• Laponogov I, Pan XS, Veselkov DA, et al. Structural basis of gate-DNA breakage and resealing by type II topoisomerases. PLoS One 2010;5: 1–8.
   Web of Science ®Google Scholar
• Osheroff N. Eukaryotic topoisomerase II. Characterization of enzyme turnover. J Biol Chem 1986;261:9944–50.
   PubMed Web of Science ®Google Scholar
• Pommier Y, Leo E, Zhang H, Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 2010;17:421–33.
   PubMed Web of Science ®Google Scholar
• Kellner U, Sehested M, Jensen PB, et al. Culprit and victim - DNA topoisomerase II. Lancet Oncol 2002;3:235–43.
   PubMed Web of Science ®Google Scholar
• Nitiss JL. DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 2009;9:327–37.
   PubMed Web of Science ®Google Scholar
• Kaur P, Kaur V, Kaur S, DNA Topoisomerase II: promising target for anticancer drugs. In: Gandhi V, Grover R, Pathak SAB, editor. Multi-targeted approach to treatment of cancer. Springer International Publishing; 2015:323–38.
   Google Scholar
• Lepiarczyk M, Bielawska A, Sosnowska K, Bielawski K. Ludzka topoizomeraza typu II jako molekularny punkt uchwytu leków przeciwnowotworowych. Gaz Farm 2011;20:24–6.
   Google Scholar
• Linka RM, Porter ACG, Volkov A, et al. C-Terminal regions of topoisomerase IIalpha and IIbeta determine isoform-specific functioning of the enzymes in vivo. Nucleic Acids Res 2007;35:3810–22.
   PubMed Web of Science ®Google Scholar
• Farr CJ, Antoniou-Kourounioti M, Mimmack ML, et al. The α isoform of topoisomerase II is required for hypercompaction of mitotic chromosomes in human cells. Nucleic Acids Res 2014;42:4414–26.
   PubMed Web of Science ®Google Scholar
• Tiwari VK, Burger L, Nikoletopoulou V, et al. Target genes of topoisomerase IIβ regulate neuronal survival and are defined by their chromatin state. Proc Natl Acad Sci USA 2012;109:934–43.
   Web of Science ®Google Scholar
• Bergerat A, Gadelle D, Forterre P. Purification of a DNA topoisomerase II from the hyperthermophilic archaeon Sulfolobus shibatae. A thermostable enzyme with both bacterial and eucaryal features. J Biol Chem 1994;269:27663–9.
   PubMed Web of Science ®Google Scholar
• Bergerat A, De Massy B, Gadelle D, et al. An atypical topoisomerase II from archaea with implications for meiotic recombination. Nature 1997;386:414–7.
   PubMed Web of Science ®Google Scholar
• Buhler C, Lebbink JHG, Bocs C, et al. DNA Topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs. J Biol Chem 2001;276:37215–22.
   PubMed Web of Science ®Google Scholar
• Corbett KD, Berger JM. Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. Embo J 2003;22:151–63.
   PubMed Web of Science ®Google Scholar
• Hartung F, Puchta H. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res 2000;28:1548–54.
   PubMed Web of Science ®Google Scholar
• Malik S-B, Ramesh MA, Hulstrand AM, Logsdon JM. Protist homologs of the meiotic Spo11 gene and topoisomerase VI reveal an evolutionary history of gene duplication and lineage-specific loss. Mol Biol Evol 2007;24:2827–41.
   PubMed Web of Science ®Google Scholar
• Sugimoto-Shirasu K, Stacey NJ, Corsar J, et al. DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 2002;12:1782–6.
   PubMed Web of Science ®Google Scholar
• Gadelle D, Krupovic M, Raymann K, et al. DNA topoisomerase VIII: a novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in archaea and bacteria. Nucleic Acids Res 2014;42:8578–91.
   PubMed Web of Science ®Google Scholar
• Drwal MN, Marinello J, Manzo SG, et al. Novel DNA topoisomerase IIα inhibitors from combined ligand- and structure- based virtual screening. PLoS One 2014;9:1–16.
   Web of Science ®Google Scholar
• Pourquier P, Pommier Y, Topoisomerase I-mediated DNA damage. In: Pourquier P, Pommier Y, editors. Advances in cancer research. Vol. 80. Elsevier; 2001. p. 189–216.
   Google Scholar
• Capranico G, Binaschi M, Borgnetto ME, et al. A protein-mediated mechanism for the DNA sequence-specific action of topoisomerase II poisons. Trends Pharmacol. Sci 1997;18:323–9.
   PubMed Web of Science ®Google Scholar
• Chen SH, Chan N-L, Hsieh T. New mechanistic and functional insights into DNA topoisomerases. Annu Rev Biochem 2013;82:139–70.
   PubMed Web of Science ®Google Scholar
• Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chem Biol 2013;8:82–95.
   PubMed Web of Science ®Google Scholar
• Pommier Y, Kiselev E, Marchand C. Interfacial inhibitors. Bioorg Med Chem Lett 2015;25:3961–5.
   PubMed Web of Science ®Google Scholar
• Zhang C, Li S, Ji L, et al. Design, synthesis and antitumor activity of non-camptothecin topoisomerase i inhibitors. Bioorg Med Chem Lett 2015;25:4693–6.
   PubMed Web of Science ®Google Scholar
• Kümler I, Brünner N, Stenvang J, et al. A systematic review on topoisomerase 1 inhibition in the treatment of metastatic breast cancer. Breast Cancer Res Treat 2013;138:347–58.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hsiang YH, Liu LF. Identification of mammalian DNA topoisomerase i as an intracellular target of the anticancer drug camptothecin. Cancer Res 1988;48:1722–6.
   PubMed Web of Science ®Google Scholar
• Wall ME, Wani MC, Cook CE, et al. Plant antitumor agents. I. The isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminata. J Am Chem Soc 1966;88:3888–90.
   Web of Science ®Google Scholar
• Kacprzak KM, Chemistry and biology of camptothecin and its derivatives. In: Natural products: phytochemistry, botany and metabolism of alkaloids, phenolics and terpenes. Berlin Heidelberg: Springer; 2013. p. 643–682.
   Google Scholar
• Muqeet W, Bano Q. Camptothecin and its analogs antitumour activity by poisoning topoisomerase I, their structure activity relationship and clinical development perspective of analogs. J App Pharm 2014;6:386–95.
   Google Scholar
• Pizzolato JF, Saltz LB. The camptothecins. Lancet 2003;361:2235–42.
   PubMed Web of Science ®Google Scholar
• Strumberg D, Pilon AA, Smith M, et al. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5'-phosphorylated DNA double-strand breaks by replication runoff. Mol Cell Biol 2000;20:3977–87.
   PubMed Web of Science ®Google Scholar
• Sané AT, Bertrand R. Caspase inhibition in camptothecin-treated U-937 cells is coupled with a shift from apoptosis to transient G1 arrest followed by necrotic cell death. Cancer Res 1999;59:3565–9.
   PubMed Web of Science ®Google Scholar
• Li LH, Fraser TJ, Olin EJ, Bhuyan BK. Action of camptothecin on mammalian cells in culture. Cancer Res 1972;32:2643–50.
   PubMed Web of Science ®Google Scholar
• Pommier Y. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem Rev 2009;109:2894–902.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hertzberg RP, Caranfa MJ, Hecht SM. On the mechanism of topoisomerase I inhibition by camptothecin: evidence for binding to an enzyme-DNA complex. Biochemistry 1989;28:4629–38.
   PubMed Web of Science ®Google Scholar
• Garst J. Topotecan: An evolving option in the treatment of relapsed small cell lung cancer. Ther Clin Risk Manag 2007;3:1087–95.
   PubMedGoogle Scholar
• Armstrong DK, Spriggs D, Levin Y, et al. Hematologic safety and tolerability of topotecan in recurrent ovarian cancer and small cell lung cancer: an integrated analysis. Oncologist 2005;10:686–94.
   PubMed Web of Science ®Google Scholar
• Brave M, Dagher R, Farrell A, et al. Topotecan in combination with cisplatin for the treatment of stage IVB, recurrent, or persistent cervical cancer. Oncology (Williston Park, N.Y.) 2006;20:1401–10.
   PubMed Web of Science ®Google Scholar
• Fuchs C, Mitchell EP, Hoff PM. Irinotecan in the treatment of colorectal cancer. Cancer Treat. Rev 2006;32:491–503.
   PubMed Web of Science ®Google Scholar
• Ohtsuka K, Inoue S, Kameyama M, et al. Intracellular conversion of irinotecan to its active form, SN-38, by native carboxylesterase in human non-small cell lung cancer. Lung Cancer 2003;41:187–98.
   PubMed Web of Science ®Google Scholar
• Mullangi R, Ahlawat P, Srinivas NR. Irinotecan and its active metabolite, SN-38: review of bioanalytical methods and recent update from clinical pharmacology perspectives. Biomed Chromatogr 2010;24:104–23.
   PubMed Web of Science ®Google Scholar
• Haaz MC, Rivory L, Jantet S, et al. Glucuronidation of SN-38, the active metabolite of irinotecan, by human hepatic microsomes. Pharmacol Toxicol 1997;80:91–6.
   PubMedGoogle Scholar
• Tadokoro JI, Kakihata K, Shimazaki M, et al. Post-marketing surveillance (PMS) of all patients treated with irinotecan in Japan: clinical experience and ADR profile of 13,935 patients. Jpn J Clin Oncol 2011;41:1101–11.
   PubMed Web of Science ®Google Scholar
• Martino E, Della Volpe S, Terribile E, et al. The long story of camptothecin: from traditional medicine to drugs. Bioorg Med Chem Lett 2017;27:701–7.
   PubMed Web of Science ®Google Scholar
• Crul M. CKD-602 Chong Kun Dang. Curr Opin Investig Drugs 2003;4:1455–9.
   PubMedGoogle Scholar
• Park YH, Chung CU, Park BM, et al. Lesser toxicities of belotecan in patients with small cell lung cancer: a retrospective single-center study of camptothecin analogs. Can Respir J 2016;2016:1–8.
   Web of Science ®Google Scholar
• Lee S, Ho JY, Liu JJ, et al. CKD-602, a topoisomerase I inhibitor, induces apoptosis and cell-cycle arrest and inhibits invasion in cervical cancer. Mol. Med 2019;25:23.
   PubMed Web of Science ®Google Scholar
• Joerger M, Hess D, Delmonte A, et al. Phase-I dose finding and pharmacokinetic study of the novel hydrophilic camptothecin ST-1968 (namitecan) in patients with solid tumors. Invest New Drugs 2015;33:472–9.
   PubMed Web of Science ®Google Scholar
• Joerger M, Hess D, Delmonte A, et al. Integrative population pharmacokinetic and pharmacodynamic dose finding approach of the new camptothecin compound namitecan (ST1968). Br J Clin Pharmacol 2015;80:128–38.
   PubMed Web of Science ®Google Scholar
• Cao Z, Kozielski A, Liu X, et al. Crystalline camptothecin-20(S)-O-propionate hydrate: a novel anticancer agent with strong activity against 19 human tumor xenografts. Cancer Res 2009;69:4742–9.
   PubMed Web of Science ®Google Scholar
• Bom D, Curran DP, Kruszewski S, et al. The novel silatecan 7-tert-butyldimethylsilyl-10-hydroxycamptothecin displays high lipophilicity, improved human blood stability, and potent anticancer activity. J Med Chem 2000;43:3970–80.
   PubMed Web of Science ®Google Scholar
• Pratesi G, Beretta GL, Zunino F. Gimatecan, a novel camptothecin with a promising preclinical profile. Anticancer Drugs 2004;15:545–52.
   PubMed Web of Science ®Google Scholar
• De Cesare M, Pratesi G, Perego P, et al. Potent antitumor activity and improved pharmacological profile of ST1481, a novel 7-substituted camptothecin. Cancer Res 2001;61:7189–95.
   PubMed Web of Science ®Google Scholar
• De Cesare M. High efficacy of intravenous gimatecan on human tumor xenografts. Anticancer Res 2018;38:5783–90.
   PubMed Web of Science ®Google Scholar
• Sheng C, Miao Z, Zhang W. New strategies in the discovery of novel non-camptothecin topoisomerase I inhibitors. Curr Med Chem 2011;18:4389–409.
   PubMed Web of Science ®Google Scholar
• Teicher BA. Next generation topoisomerase I inhibitors: rationale and biomarker strategies. Biochem Pharmacol 2008;75:1262–71.
   PubMed Web of Science ®Google Scholar
• Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006;6:789–802.
   PubMed Web of Science ®Google Scholar
• Kummar S, Chen A, Gutierrez M, et al. Clinical and pharmacologic evaluation of two dosing schedules of indotecan (LMP400), a novel indenoisoquinoline, in patients with advanced solid tumors. Cancer Chemother Pharmacol 2016;78:73–81.
   PubMed Web of Science ®Google Scholar
• Saif MW, Diasio RB. Edotecarin: a novel topoisomerase I inhibitor. Clin Colorectal Cancer 2005;5:27–36.
   PubMedGoogle Scholar
• Li TK, Houghton PJ, Desai SD, et al. Characterization of ARC-111 as a novel topoisomerase I-targeting anticancer drug. Cancer Res 2003;63:8400–7.
   PubMed Web of Science ®Google Scholar
• Yoshinari T, Ohkubo M, Fukasawa K, et al. Mode of action of a new indolocarbazole anticancer agent, J-107088, targeting topoisomerase I. Cancer Res 1999;59:4271–5.
   PubMed Web of Science ®Google Scholar
• Pommier Y, Cushman M. The indenoisoquinoline noncamptothecin topoisomerase I inhibitors: update and perspectives. Mol. Cancer Ther 2009;8:1008–14.
   PubMed Web of Science ®Google Scholar
• Cuya SM, Bjornsti M-A, van Waardenburg RCAM. DNA topoisomerase-targeting chemotherapeutics: what's new? Cancer Chemother Pharmacol 2017;80:1–14.
   PubMed Web of Science ®Google Scholar
• A phase I study of indenoisoquinolines LMP400 and LMP776 in adults with relapsed solid tumors and lymphomas - full text view - ClinicalTrials.gov. [accessed 2020 Jun 1]. https://clinicaltrials.gov/ct2/show/NCT01051635
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zhu S, Ruchelman AL, Zhou N, et al. Esters and amides of 2,3-dimethoxy-8,9-methylenedioxy-benzo[i]phenanthridine-12-carboxylic acid: potent cytotoxic and topoisomerase I-targeting agents. Bioorg Med Chem 2005;13:6782–94.
   PubMed Web of Science ®Google Scholar
• Satyanarayana M, Feng W, Cheng L, et al. Syntheses and biological evaluation of topoisomerase I-targeting agents related to 11-[2-(N,N-dimethylamino)ethyl]-2,3-dimethoxy-8,9-methylenedioxy-11H-isoquino[4,3-c]cinnolin-12-one (ARC-31). Bioorg Med Chem 2008;16:7824–31.
   PubMed Web of Science ®Google Scholar
• Feng W, Satyanarayana M, Tsai YC, et al. 12-Substituted 2,3-dimethoxy-8,9-methylenedioxybenzo[i]phenanthridines as novel topoisomerase I-targeting antitumor agents. Bioorg Med Chem 2009;17:2877–85.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Sooryakumar D, Dexheimer TS, Teicher BA, Pommier Y. Molecular and cellular pharmacology of the novel noncamptothecin topoisomerase I inhibitor Genz-644282. Mol Cancer Ther 2011;10:1490–9.
   PubMed Web of Science ®Google Scholar
• Pogorelčnik B, Brvar M, Žegura B, et al. Discovery of mono- and disubstituted 1H-pyrazolo[3,4]pyrimidines and 9H-purines as catalytic inhibitors of human DNA topoisomerase IIα. ChemMedChem 2015;10:345–59.
   PubMed Web of Science ®Google Scholar
• Vos SM, Tretter EM, Schmidt BH, Berger JM. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat Rev Mol Cell Biol 2011;12:827–41.
   PubMed Web of Science ®Google Scholar
• de Almeida SMV, Ribeiro AG, de Lima Silva GC, et al. Alves de Lima M do C. DNA binding and topoisomerase inhibition: how can these mechanisms be explored to design more specific anticancer agents? Biomed. Pharmacother 2017;96:1538–56.
   PubMed Web of Science ®Google Scholar
• Nitiss JL. Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 2009;9:338–50.
   PubMed Web of Science ®Google Scholar
• Bailly C. Contemporary challenges in the design of topoisomerase II inhibitors for cancer chemotherapy. Chem Rev 2012;112:3611–40.
   PubMed Web of Science ®Google Scholar
• Clark PI, Slevin ML. The clinical pharmacology of etoposide and teniposide. Clin Pharmacokinet 1987;12:223–52.
   PubMed Web of Science ®Google Scholar
• King LS, Sullivan M. The similarity of the effect of podophyllin and colchicine and their use in the treatment of condylomata acuminata. Science 1946;104:244–5.
   Web of Science ®Google Scholar
• Greenspan EM, Leiter J, Shear MJ. Effect of alpha-peltatin, beta-peltatin, and podophyllotoxin on lymphomas and other transplanted tumors. J Natl Cancer Inst 1950;10:1295–333.
   PubMedGoogle Scholar
• Hande KR. Etoposide: four decades of development of a topoisomerase II inhibitor. Eur J Cancer 1998;34:1514–21.
   PubMed Web of Science ®Google Scholar
• Kingma PS, Burden DA, Osheroff N. Binding of etoposide to topoisomerase II in the absence of DNA: Decreased affinity as a mechanism of drug resistance. Biochemistry 1999;38:3457–61.
   PubMed Web of Science ®Google Scholar
• Burden DA, Kingma PS, Froelich-Ammon SJ, et al. Topoisomerase II.etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J Biol Chem 1996;271:29238–44.
   PubMed Web of Science ®Google Scholar
• Wilstermann AM, Bender RP, Godfrey M, et al. Topoisomerase II - drug interaction domains: identification of substituents on etoposide that interact with the enzyme. Biochemistry 2007;46:8217–25.
   PubMed Web of Science ®Google Scholar
• Baldwin EL, Osheroff N. Etoposide, topoisomerase II and cancer. Curr Med Chem Anticancer Agents 2005;5:363–72.
   PubMedGoogle Scholar
• Stähelin HF, von Wartburg A. The chemical and biological route from podophyllotoxin glucoside to etoposide: ninth cain memorial award lecture. Cancer Res 1991;51:5–15.
   PubMed Web of Science ®Google Scholar
• Montecucco A, Zanetta F, Biamonti G. Molecular mechanisms of etoposide. Excli J 2015;14:95–108.
   PubMed Web of Science ®Google Scholar
• Kuruppu AI, Paranagama P, Goonasekara CL. Medicinal plants commonly used against cancer in traditional medicine formulae in Sri Lanka. Saudi Pharm J 2019;27:565–73.
   PubMed Web of Science ®Google Scholar
• Bender RP, Osheroff N, DNA topoisomerases as targets for the chemotherapeutic treatment of cancer. In: Dai W, editor. Checkpoint responses in cancer therapy. Totowa: Humana Press; 2008. p. 57–91.
   Google Scholar
• Barret JM, Kruczynski A, Vispé S, et al. F14512, a potent antitumor agent targeting topoisomerase II vectored into cancer cells via the polyamine transport system. Cancer Res 2008;68:9845–53.
   PubMed Web of Science ®Google Scholar
• Thakur D. Topoisomerase II Inhibitors in cancer treatment. Int J Pharm Sci Nanotechnol 2011;3:1173–81.
   Google Scholar
• Najar IA, Johri RK. Pharmaceutical and pharmacological approaches for bioavailability enhancement of etoposide. J Biosci 2014;39:139–44.
   PubMed Web of Science ®Google Scholar
• Li J, Chen W, Zhang P, Li N. Topoisomerase II trapping agent teniposide induces apoptosis and G2/M or S phase arrest of oral squamous cell carcinoma. World J Surg Oncol 2006;4:41.
   PubMedGoogle Scholar
• Sun J, Wei Q, Zhou Y, et al. A systematic analysis of FDA-approved anticancer drugs. BMC Syst Biol 2017;11:87.
   PubMed Web of Science ®Google Scholar
• Guerram M, Jiang ZZ, Zhang LY. Podophyllotoxin, a medicinal agent of plant origin: past, present and future. Chin J Nat Med 2012;10:161–9.
   Web of Science ®Google Scholar
• Hartmann JT, Lipp HP. Camptothecin and podophyllotoxin derivatives: inhibitors of topoisomerase I and II - mechanisms of action, pharmacokinetics and toxicity profile. Drug Saf 2006;29:209–30.
   PubMed Web of Science ®Google Scholar
• Gentry AC, Pitts SL, Jablonsky MJ, et al. Interactions between the etoposide derivative F14512 and human type II topoisomerases: implications for the C4 spermine moiety in promoting enzyme-mediated DNA cleavage. Biochemistry 2011;50:3240–9.
   PubMed Web of Science ®Google Scholar
• Casero RA, Marton LJ. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 2007;6:373–90.
   PubMed Web of Science ®Google Scholar
• Bombarde O, Larminat F, Gomez D, et al. The DNA-binding polyamine moiety in the vectorized DNA topoisomerase II inhibitor F14512 alters reparability of the consequent enzyme-linked DNA double-strand breaks. Mol Cancer Ther 2017;16:2166–77.
   PubMed Web of Science ®Google Scholar
• Kruczynski A, Vandenberghe I, Pillon A, et al. Preclinical activity of F14512, designed to target tumors expressing an active polyamine transport system. Invest New Drugs 2011;29:9–21.
   PubMed Web of Science ®Google Scholar
• Jasra S, Anampa J. Anthracycline use for early stage breast cancer in the modern era: a review. Curr Treat Options Oncol 2018;19:30.
   PubMed Web of Science ®Google Scholar
• Nebigil CG, Désaubry L. Updates in anthracycline-mediated cardiotoxicity. Front Pharmacol 2018;9:1262.
   PubMed Web of Science ®Google Scholar
• Aleman BMP, Moser EC, Nuver J, et al. Cardiovascular disease after cancer therapy. EJC Suppl 2014;12:18–28.
   PubMedGoogle Scholar
• Zunino F, Capranico G. DNA topoisomerase II as the primary target of anti-tumor anthracyclines. Anticancer Drug Des 1990;5:307–17.
   PubMedGoogle Scholar
• Binaschi M, Bigioni M, Cipollone A, et al. Anthracyclines: selected new developments. Curr Med Chem Anticancer Agents 2001;1:113–30.
   PubMedGoogle Scholar
• Thorn CF, Oshiro C, Marsh S, et al. Doxorubicin pathways: pharmacodynamics and adverse effects. Pharmacogenet Genomics 2011;21:440–6.
   PubMed Web of Science ®Google Scholar
• Menna P, Minotti G, Salvatorelli E. In vitro modeling of the structure-activity determinants of anthracycline cardiotoxicity. Cell Biol Toxicol 2007;23:49–62.
   PubMed Web of Science ®Google Scholar
• Pogorelcnik B, Perdih A, Solmajer T. Recent developments of DNA poisons-human DNA topoisomerase IIα inhibitors-as anticancer agents. Curr Pharm Des 2013;19:2474–88.
   PubMed Web of Science ®Google Scholar
• Moro S, Beretta GL, Dal Ben D, et al. Interaction model for anthracycline activity against DNA topoisomerase II. Biochemistry 2004;43:7503–13.
   PubMed Web of Science ®Google Scholar
• Lyu YL, Liu LF, 13- Doxorubicin cardiotoxicity revisited: ROS versus Top2. In: Liu X-Y, Pestka S, Shi Y-F, editors. Recent advances in cancer research and therapy. Elsevier Inc.; 2012. p. 351–369.
   Google Scholar
• Carvalho C, Santos R, Cardoso S, et al. Doxorubicin: the good, the bad and the ugly effect. Curr Med Chem 2009;16:3267–85.
   PubMed Web of Science ®Google Scholar
• Zhang S, Liu X, Bawa-Khalfe T, et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med 2012;18:1639–42.
   PubMed Web of Science ®Google Scholar
• Pugazhendhi A, Edison TNJI, Velmurugan BK, et al. Toxicity of doxorubicin (Dox) to different experimental organ systems. Life Sci 2018;200:26–30.
   PubMed Web of Science ®Google Scholar
• Zhao L, Zhang B. Doxorubicin induces cardiotoxicity through upregulation of death receptors mediated apoptosis in cardiomyocytes. Sci Rep 2017;7:44735.
   PubMed Web of Science ®Google Scholar
• Langer SW. Dexrazoxane for the treatment of chemotherapy-related side effects. Cancer Manag Res 2014;6:357–63.
   PubMed Web of Science ®Google Scholar
• Drugs@FDA: FDA-Approved Drugs–Doxorubicin. [accessed 2020 Jun 19]. https://www.accessdata.fda.gov/scripts/cder/daf/index.cfm?event=overview.process&ApplNo=050467
   Google Scholar
• Robert J. Epirubicin: clinical pharmacology and dose-effect relationship. Drugs 1993;45:20–30.
   PubMedGoogle Scholar
• Coukell AJ, Faulds D. Epirubicin. An updated review of its pharmacodynamic and pharmacokinetic properties and therapeutic efficacy in the management of breast cancer. Drugs 1997;53:453–82.
   PubMed Web of Science ®Google Scholar
• Singh Z, Kaur H. Toxicological aspects of antineoplastic drugs doxorubicin and epirubicin. J Clin Mol Med 2019;2: 1–5.
   Google Scholar
• Israel M, Potti PG, Seshadri R. Adriamycin analogues. Rationale, synthesis, and preliminary antitumor evaluation of highly active DNA-nonbinding N-(trifluoroacetyl)adriamycin 14-O-hemiester derivatives1, 2. J Med Chem 1985;28:1223–8.
   PubMed Web of Science ®Google Scholar
• Onrust SV, Lamb HM. Valrubicin. Drugs Aging 1999;15:69–75.
   PubMed Web of Science ®Google Scholar
• Drug Approval Package: Valstar (Valrubicin) NDA# 20-892. [accessed 2020 Jun 9]. https://www.accessdata.fda.gov/drugsatfda_docs/nda/98/20892.cfm
   Google Scholar
• Hanada M, Mizuno S, Fukushima A, et al. A new antitumor agent amrubicin induces cell growth inhibition by stabilizing topoisomerase II-DNA complex. Jpn J Cancer Res 1998;89:1229–38.
   PubMedGoogle Scholar
• Sakurai R, Kaira K, Miura Y, et al. Clinical significance of topoisomerase-II expression in patients with advanced non-small cell lung cancer treated with amrubicin. Thorac Cancer 2020;11:426–35.
   PubMed Web of Science ®Google Scholar
• Yamaoka T, Hanada M, Ichii S, et al. Cytotoxicity of amrubicin, a novel 9-aminoanthracycline, and its active metabolite amrubicinol on human tumor cells. Jpn J Cancer Res 1998;89:1067–73.
   PubMedGoogle Scholar
• Kurata T, Okamoto I, Tamura K, Fukuoka M. Amrubicin for non-small-cell lung cancer and small-cell lung cancer. Invest New Drugs 2007;25:499–504.
   PubMed Web of Science ®Google Scholar
• Marrero L, Wyczechowska D, Musto AE, et al. Therapeutic efficacy of aldoxorubicin in an intracranial xenograft mouse model of human glioblastoma. Neoplasia 2014;16:874–82.
   PubMed Web of Science ®Google Scholar
• Kratz F, Warnecke A, Scheuermann K, et al. Probing the cysteine-34 position of endogenous serum albumin with thiol-binding doxorubicin derivatives. Improved efficacy of an acid-sensitive doxorubicin derivative with specific albumin-binding properties compared to that of the parent compound. J Med Chem 2002;45:5523–33.
   PubMed Web of Science ®Google Scholar
• Graeser R, Esser N, Unger H, et al. INNO-206, the (6-maleimidocaproyl hydrazone derivative of doxorubicin), shows superior antitumor efficacy compared to doxorubicin in different tumor xenograft models and in an orthotopic pancreas carcinoma model. Invest New Drugs 2010;28:14–9.
   PubMed Web of Science ®Google Scholar
• Kratz F, Fichtner I, Graeser R. Combination therapy with the albumin-binding prodrug of doxorubicin (INNO-206) and doxorubicin achieves complete remissions and improves tolerability in an ovarian A2780 xenograft model. Invest New Drugs 2012;30:1743–9.
   PubMed Web of Science ®Google Scholar
• Sanchez E, Li M, Wang C, et al. Anti-myeloma effects of the novel anthracycline derivative INNO-206. Clin Cancer Res 2012;18:3856–67.
   PubMed Web of Science ®Google Scholar
• White RJ, Durr FE. Development of mitoxantrone. Invest New Drugs 1985;3:85–93.
   PubMed Web of Science ®Google Scholar
• Murdock KC, Child RG, Fabio PF, et al. Antitumor agents. 1. 1,4-bis[(aminoalkyl)amino]-9,10-anthracenediones. J Med Chem 1979;22:1024–30.
   PubMed Web of Science ®Google Scholar
• Johnson RK, Zee-Cheng RK, Lee WW, et al. Experimental antitumor activity of aminoanthraquinones. Cancer Treat Rep 1979;63:425–39.
   PubMedGoogle Scholar
• Zee-Cheng RKY, Cheng CC. Antineoplastic agents. Structure-activity relationship study of bis(substituted aminoalkylamino)anthraquinones. J Med Chem 1978;21:291–4.
   PubMed Web of Science ®Google Scholar
• Halterman P, Vogelzang NJ, Farabishahadel A, Goodman OB, Mitoxantrone. In: Drug management of prostate cancer. New York: Springer; 2010. p. 125–131.
   Google Scholar
• Capranico G, De Isabella P, Tinelli S, et al. Similar sequence specificity of mitoxantrone and VM-26 stimulation of in vitro DNA cleavage by mammalian DNA topoisomerase II. Biochemistry 1993;32:3038–46.
   PubMed Web of Science ®Google Scholar
• Wu CC, Li YC, Wang YR, et al. On the structural basis and design guidelines for type II topoisomerase-targeting anticancer drugs. Nucleic Acids Res 2013;41:10630–40.
   PubMed Web of Science ®Google Scholar
• Damiani RM, Moura DJ, Viau CM, et al. Pathways of cardiac toxicity: comparison between chemotherapeutic drugs doxorubicin and mitoxantrone. Arch Toxicol 2016;90:2063–76.
   PubMed Web of Science ®Google Scholar
• Rossato LG, Costa VM, De Pinho PG, et al. The metabolic profile of mitoxantrone and its relation with mitoxantrone-induced cardiotoxicity. Arch Toxicol 2013;87:1809–20.
   PubMed Web of Science ®Google Scholar
• Drugs@FDA: FDA-Approved Drugs–Mitoxantrone. [accessed 2020 Jun 19]. https://www.accessdata.fda.gov/scripts/cder/daf/index.cfm?event=overview.process&ApplNo=019297
   Google Scholar
• Enache M, Toader AM, Enache MI. Mitoxantrone-surfactant interactions: a physicochemical overview. Molecules 2016;21:1356.
   Web of Science ®Google Scholar
• Patel KJ, Trédan O, Tannock IF. Distribution of the anticancer drugs doxorubicin, mitoxantrone and topotecan in tumors and normal tissues. Cancer Chemother. Pharmacol 2013;72:127–38.
   PubMed Web of Science ®Google Scholar
• Ketron AC, Denny WA, Graves DE, Osheroff N. Amsacrine as a topoisomerase II poison: importance of drug-DNA interactions. Biochemistry 2012;51:1730–9.
   PubMed Web of Science ®Google Scholar
• Murphy MB, Mercer SL, Deweese JE, Inhibitors and poisons of mammalian type II topoisomerases. In: Advances in molecular toxicology. Vol. 11. Elsevier B.V.; 2017. p. 203–240.
   Google Scholar
• Tomita K, Tsuzuki Y, Shibamori K. i, et al. Synthesis and structure-activity relationships of novel 7-substituted 1,4-dihydro-4-oxo-1-(2-thiazolyl)-1,8-naphthyridine-3-carboxylic acids as antitumor agents. Part 1. J. Med. Chem 2002;45:5564–75.
   PubMed Web of Science ®Google Scholar
• Abbas JA, Stuart RK. Vosaroxin : a novel antineoplastic quinolone. Expert Opin Investig Drugs 2012;21:1223–33.
   PubMed Web of Science ®Google Scholar
• Paubelle E, Zylbersztejn F, Thomas X. The preclinical discovery of vosaroxin for the treatment of acute myeloid leukemia. Expert Opin Drug Discov 2017;12:747–53.
   PubMed Web of Science ®Google Scholar
• Li PH, Zeng P, Chen SB, et al. Synthesis and mechanism studies of 1,3-benzoazolyl substituted pyrrolo[2,3-b]pyrazine derivatives as nonintercalative topoisomerase II catalytic inhibitors. J Med Chem 2016;59:238–52.
   PubMed Web of Science ®Google Scholar
• Deng S, Yan T, Nikolova T, et al. The catalytic topoisomerase II inhibitor dexrazoxane induces DNA breaks, ATF3 and the DNA damage response in cancer cells. Br J Pharmacol 2015;172:2246–57.
   PubMed Web of Science ®Google Scholar
• Vann KR, Ergün Y, Zencir S, et al. Inhibition of human DNA topoisomerase IIα by two novel ellipticine derivatives. Bioorg Med Chem Lett 2016;26:1809–12.
   PubMed Web of Science ®Google Scholar
• Jones RL. Utility of dexrazoxane for the reduction of anthracycline-induced cardiotoxicity. Expert Rev Cardiovasc Ther 2008;6:1311–7.
   PubMedGoogle Scholar
• Cvetković RS, Scott LJ. Dexrazoxane: a review of its use for cardioprotection during anthracycline chemotherapy. Drugs 2005;65:1005–24.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jensen LH, Nitiss KC, Rose A, et al. A novel mechanism of cell killing by anti-topoisomerase II bisdioxopiperazines. J Biol Chem 2000;275:2137–46.
   PubMed Web of Science ®Google Scholar
• Classen S, Olland S, Berger JM. Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc Natl Acad Sci USA 2003;100:10629–34.
   PubMed Web of Science ®Google Scholar
• Hasinoff BB, Patel D, Wu X. A QSAR study that compares the ability of bisdioxopiperazine analogs of the doxorubicin cardioprotective agent dexrazoxane (ICRF-187) to protect myocytes with DNA topoisomerase II inhibition. Toxicol Appl Pharmacol 2020;399:115038.
   PubMed Web of Science ®Google Scholar
• Fortune JM, Osheroff N. Merbarone inhibits the catalytic activity of human topoisomerase IIalpha by blocking DNA cleavage. J Biol Chem 1998;273:17643–50.
   PubMed Web of Science ®Google Scholar
• Pastor N, Domínguez I, Orta ML, et al. The DNA topoisomerase II catalytic inhibitor merbarone is genotoxic and induces endoreduplication. Mutat Res 2012;738-739: 45–51.
   PubMed Web of Science ®Google Scholar
• Tripathi N, Guchhait SK, Bharatam PV. Pharmacoinformatics analysis of merbarone binding site in human topoisomerase IIα. J Mol Graph Model 2019;86:1–18.
   PubMed Web of Science ®Google Scholar