Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II
Open accessAbstract
Many intercalative antitumor drugs have been shown to induce reversible protein-linked DNA breaks in cultured mammalian cells. Using purified mammalian DNA topoisomerase II, we have demonstrated that the antitumor drugs ellipticine and 2-methyl-9-hydroxyellipticine (2-Me-9-OH-E+) can produce reversible protein-linked DNA breaks in vitro. 2-Me-9-OH-E+ which is more cytotoxic toward L1210 cells and more active against experimental tumors than ellipticine is also more effective in stimulating DNA cleavage in vitro. Similar to the effect of 4'-(9-acridinylamino)-methanesulfon-m-anisidide (m-AMSA) on topoisomerase II in vitro, the mechanism of DNA breakage induced by ellipticines is most likely due to the drug stabilization of a cleavable complex formed between topoisomerase II and DNA. Protein denaturant treatment of the cleavable complex results in DNA breakage and covalent linking of one topoisomerase II subunit to each 5'-end of the cleaved DNA. Cleavage sites on pBR322 DNA produced by ellipticine or 2-Me-9-OH-E+ treatment mapped at the same positions. However, many of these cleavage sites are distinctly different from those produced by the antitumor drug m-AMSA which also targets at topoisomerase II. Our results thus suggest that although mammalian DNA topoisomerase II may be a common target of these antitumor drugs, drug-DNA-topoisomerase interactions for different antitumor drugs may be different.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Anthracyclines exert antitumor activity mainly by inhibiting topoisomerase II.
“Anthracyclines are among the most widely used antitumor antibiotics in the clinic and exert antitumor activity mainly by inhibiting topoisomerase II [215,216,217,218,219].”
From Marine Natural Products: A Source of Novel Anticancer Drugs (2019) · cites this paper as [215]
Cites
Gellert, M. F. (1981) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.50.070181.004311 · Cited by 990 · see citing works
DNA Gyrase and the Supercoiling of DNA
Cozzarelli, N. R. (1980) · Science · doi:10.1126/science.6243420 · Cited by 720 · see citing works
Waring, M. J. (1981) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.50.070181.001111 · Cited by 690 · see citing works
The Anticancer Agent Adriamycin Can Be Actively Cytotoxic Without Entering Cells
Triton, T. R., & Yee, G. K. (1982) · Science · doi:10.1126/science.7089561 · Cited by 573 · see citing works
Nelson, E. M., Tewey, K. M., & Liu, L. F. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.5.1361 · Cited by 561 · see citing works
Self-citationCleavage of DNA by mammalian DNA topoisomerase II.
Liu, L. F., Rowe, T. C., Yang, L., Tewey, K. M., & Chen, G. L. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43815-4 · Cited by 534 · see citing works
Self-citationLiu, L. F., Liu, C.-C., & Alberts, B. (1980) · Cell · doi:10.1016/s0092-8674(80)80046-8 · Cited by 486 · see citing works
Self-citationZwelling, L. A., Michaels, S., Erickson, L. C., Ungerleider, R. S., Nichols, M., & Kohn, K. W. (1981) · Biochemistry · doi:10.1021/bi00526a006 · Cited by 374 · see citing works
A homogeneous type II DNA topoisomerase from HeLa cell nuclei.
Miller, K. G., Liu, L. F., & Englund, P. T. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52552-2 · Cited by 359 · see citing works
Self-citationTerminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers
Sundin, O. H., & Varshavsky, A. J. (1980) · Cell · doi:10.1016/0092-8674(80)90118-x · Cited by 354 · see citing works
Eukaryotic DNA topoisomerases: two forms of type I DNA topoisomerases from HeLa cell nuclei.
Liu, L. F., & Miller, K. G. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.6.3487 · Cited by 351 · see citing works
Self-citationStrand scission of DNA by bound adriamycin and daunorubicin in the presence of reducing agents
Lown, J. W., Sim, S.-K., Majumdar, K. C., & Chang, R.-Y. (1977) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(77)91557-1 · Cited by 260 · see citing works
The mechanism of the bleomycin-induced cleavage of DNA
Lown, J. W., & Sim, S.-K. (1977) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(77)80099-5 · Cited by 248 · see citing works
Qualitative and quantitative aspects of intercalator-induced DNA strand breaks
Ross, W. E., Glaubiger, D. L., & Kohn, K. W. (1979) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(79)90124-2 · Cited by 237 · see citing works
Protein-associated DNA breaks in cells treated with adriamycin or ellipticine
Ross, W. E., Glaubiger, D. L., & Kohn, K. W. (1978) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(78)90059-x · Cited by 236 · see citing works
Pecq, J. L., Nguyen‐Dat‐Xuong, Gosse, C., & Paoletti, C. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.12.5078 · Cited by 232 · see citing works
Novel topologically knotted DNA from bacteriophage P4 capsids: studies with DNA topoisomerases
Liu, L. F., Davis, J. L., & Calendar, R. L. (1981) · Nucleic Acids Research · doi:10.1093/nar/9.16.3979 · Cited by 223 · see citing works
Self-citationWozniak, A. J., & Ross, W. E. (1983) · PubMed · Cited by 216 · see citing works
Effect of VP-16-213 on the intracellular degradation of DNA in HeLa cells
Loike, J. D., & Horwitz, S. B. (1976) · Biochemistry · doi:10.1021/bi00670a004 · Cited by 193 · see citing works
Stähblin, H. (1973) · European Journal of Cancer (1965) · doi:10.1016/s0014-2964(73)80021-0 · Cited by 183 · see citing works
DNA double-strand breaks in mammalian cells after exposure to intercalating agents
Ross, W. E., & Bradley, M. O. (1981) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(81)90145-3 · Cited by 163 · see citing works
CAIN, B. F., & Atwell, G. J. (1974) · European Journal of Cancer (1965) · doi:10.1016/0014-2964(74)90079-6 · Cited by 160 · see citing works
Intra- and intermolecular strand transfer by HeLa DNA topoisomerase I.
Halligan, B. D., Davis, J. L., Edwards, K. A., & Liu, L. F. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)34881-6 · Cited by 124 · see citing works
Self-citationSingh, B., & Gupta, R. S. (1983) · PubMed · Cited by 119 · see citing works
Auclair, C., & Paoletti, C. (1981) · Journal of Medicinal Chemistry · doi:10.1021/jm00135a010 · Cited by 100 · see citing works
Zwelling, L. A., Kerrigan, D., & Michaels, S. (1982) · PubMed · Cited by 96 · see citing works
Zwelling, L. A., Michaels, S., Kerrigan, D., Pommier, Y. G., & Kohn, K. W. (1982) · Biochemical Pharmacology · doi:10.1016/0006-2952(82)90560-3 · Cited by 87 · see citing works
Identification of the breakage-reunion subunit of T4 DNA topoisomerase.
Rowe, T. C., Tewey, K. M., & Liu, L. F. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)47281-4 · Cited by 86 · see citing works
Self-citationGrieder, A., Maurer, R., & Stähelin, H. (1974) · PubMed · Cited by 78 · see citing works
The formation and resealing of intercalator-induced DNA strand breaks in isolated L1210 cell nuclei
Pommier, Y. G., Kerrigan, D., Schwartz, R. E., & Zwelling, L. A. (1982) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(82)91530-3 · Cited by 70 · see citing works
Effect of alkylating antitumor agents on the binding of DNA to protein.
Grunicke, H. H., Bock, K. W., Becher, H., Gäng, V., Schnierda, J., & Puschendorf, B. (1973) · PubMed · Cited by 62 · see citing works
Deaven, L. L., Oka, M. S., & Tobey, R. A. (1978) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/60.5.1155 · Cited by 55 · see citing works
Induction of limited DNA damage by the antitumor agent Cain's acridine.
Furlong, N. B., Sato, J., Brown, T., Chavez, F., & Hurlbert, R. B. (1978) · PubMed · Cited by 46 · see citing works
Ellipticine and derivatives induce breakage of L1210 cells DNA in vitro
Paoletti, C., Lesca, C., CROS, S., Malvy, C., & Auclair, C. (1979) · Biochemical Pharmacology · doi:10.1016/0006-2952(79)90096-0 · Cited by 43 · see citing works
On the mechanism of action of 4′-[(9-acridinyl)-amino] methanesulphon-m-anisidide
Ralph, R. K. (1980) · European Journal of Cancer (1965) · doi:10.1016/0014-2964(80)90198-x · Cited by 26 · see citing works
Marshall, B., Ralph, R. K., & Hancock, R. E. W. (1983) · Nucleic Acids Research · doi:10.1093/nar/11.12.4251 · Cited by 19 · see citing works
Drewinko, B., Yang, L., & Barlogie, B. (1982) · PubMed · Cited by 14 · see citing works
SOME ACRIDINE-RESISTANT MUTATIONS OF BACTERIOPHAGE T4D
Rappaport, H., Russel, M., & Susman, M. (1974) · Genetics · doi:10.1093/genetics/78.2.579 · Cited by 9 · see citing works
Metabolic transformation of 2-methylellipticinium
Malvy, C., & Paoletti, C. (1980) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(80)91223-1 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gewirtz, D. (1999) · Biochemical Pharmacology · doi:10.1016/s0006-2952(98)00307-4 · Cited by 2,242 · see citing works
Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I.
Hsiang, Y. H., Hertzberg, R., Hecht, S., & Liu, L. F. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38654-4 · Cited by 2,362 · see citing works
Self-citationDNA Topoisomerases and Their Poisoning by Anticancer and Antibacterial Drugs
Pommier, Y. G., Leo, E., Zhang, H., & Marchand, C. (2010) · Chemistry & Biology · doi:10.1016/j.chembiol.2010.04.012 · Cited by 1,842 · see citing works
“Inhibition of Top2 catalytic activity without trapping cleavage complexes is also observed for DNA intercalators at drug concentrations that alter DNA structure, thereby preventing Top2 from binding DNA (step 1 in Figure 5A) or from forming Top2cc (step 3) (Pommier et al., 1984; Tewey et al., 1984).”
Targeting DNA topoisomerase II in cancer chemotherapy
Nitiss, J. L. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2607 · Cited by 1,803 · see citing works
Adriamycin-Induced DNA Damage Mediated by Mammalian DNA Topoisomerase II
Tewey, K. M., Rowe, T. C., Yang, L., Halligan, B. D., & Liu, L. F. (1984) · Science · doi:10.1126/science.6093249 · Cited by 1,542 · see citing works
Self-citationMultidrug resistance (MDR) in cancer
Krishna, R., & Mayer, L. D. (2000) · European Journal of Pharmaceutical Sciences · doi:10.1016/s0928-0987(00)00114-7 · Cited by 1,032 · see citing works
Kaufmann, S. H. (1989) · PubMed · Cited by 922 · see citing works
Cockerill, P. N., & Garrard, W. T. (1986) · Cell · doi:10.1016/0092-8674(86)90761-0 · Cited by 881 · see citing works
Nelson, W. G., & Kastan, M. B. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.3.1815 · Cited by 850 · see citing works
Drugging Topoisomerases: Lessons and Challenges
Pommier, Y. G. (2012) · ACS Chemical Biology · doi:10.1021/cb300648v · Cited by 844 · see citing works
Hsiang, Y. H., & Liu, L. F. (1988) · PubMed · Cited by 841 · see citing works
Self-citationNatural compounds for cancer treatment and prevention
Nobili, S., Lippi, D., Witort, E., Donnini, M., Bausi, L., Mini, E., & Capaccioli, S. (2009) · Pharmacological Research · doi:10.1016/j.phrs.2009.01.017 · Cited by 780 · see citing works
DNA Topoisomerases: Essential Enzymes and Lethal Targets
Chen, A. Y., & Liu, L. F. (1994) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.34.040194.001203 · Cited by 737 · see citing works
Self-citationDNA-Damaging Agents in Cancer Chemotherapy: Serendipity and Chemical Biology
Cheung-Ong, K., Giaever, G. N., & Nislow, C. (2013) · Chemistry & Biology · doi:10.1016/j.chembiol.2013.04.007 · Cited by 585 · see citing works
Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor
Holloway, S. L., Glotzer, M., King, R. W., & Murray, A. W. (1993) · Cell · doi:10.1016/0092-8674(93)90364-v · Cited by 561 · see citing works
Marine Natural Products: A Source of Novel Anticancer Drugs
Khalifa, S. A. M., Elias, N., Farag, M. A., Chen, L., Saeed, A., Hegazy, M.-E. F., Moustafa, M. S., Abd El-Wahed, A., Al-Mousawi, S. M., Musharraf, S. G., et al. (2019) · Marine Drugs · doi:10.3390/md17090491 · Cited by 555 · see citing works
Hertzberg, R., Caranfa, M. J., & Hecht, S. M. (1989) · Biochemistry · doi:10.1021/bi00437a018 · Cited by 552 · see citing works
Nuclear reconstitution in vitro: Stages of assembly around protein-free DNA
Newport, J. W. (1987) · Cell · doi:10.1016/0092-8674(87)90424-7 · Cited by 536 · see citing works
Doxorubicin (adriamycin): A critical review of free radical-dependent mechanisms of cytotoxicity
Keizer, H. G., Pinedo, H. M., Schuurhuis, G. J., & Joenje, H. (1990) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(90)90088-j · Cited by 517 · see citing works
Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II
Varga‐Weisz, P., Wilm, M. S., Bonte, E. J., Dumas, K., Mann, M., & Becker, P. B. (1997) · Nature · doi:10.1038/41587 · Cited by 513 · see citing works
Tumor Cell Death Induced by Topoisomerase-Targeting Drugs
Li, T., & Liu, L. F. (2001) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.41.1.53 · Cited by 509 · see citing works
Self-citationMaser, R. S., Monsen, K. J., Nelms, B. E., & Petrini, J. H. J. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.10.6087 · Cited by 499 · see citing works
Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme
Burden, D. A., & Osheroff, N. (1998) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(98)00132-8 · Cited by 503 · see citing works
Localization of topoisomerase II in mitotic chromosomes.
Earnshaw, W. C., & Heck, M. M. S. (1985) · The Journal of Cell Biology · doi:10.1083/jcb.100.5.1716 · Cited by 495 · see citing works
Chen, G. L., Yang, L., Rowe, T. C., Halligan, B. D., Tewey, K. M., & Liu, L. F. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90729-5 · Cited by 492 · see citing works
Self-citationHuman topoisomerases and their roles in genome stability and organization
Pommier, Y., Nussenzweig, A., Takeda, S., & Austin, C. (2022) · Nature reviews. Molecular cell biology · doi:10.1038/s41580-022-00452-3 · Cited by 403 · see citing works
Jaxel, C., Kohn, K. W., Wani, M. C., Wall, M. E., & Pommier, Y. G. (1989) · PubMed · Cited by 449 · see citing works
Topoisomerase-targeting antitumor drugs
D’Arpa, P., & Liu, L. F. (1989) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/0304-419x(89)90041-3 · Cited by 434 · see citing works
Self-citationInvolvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons.
D’Arpa, P., Beardmore, C., & Liu, L. F. (1990) · PubMed · Cited by 425 · see citing works
Self-citationPang, B., Qiao, X., Janssen, L., Velds, A., Groothuis, T. A., Kerkhoven, R. M., Nieuwland, M., Ovaa, H., Rottenberg, S., van Tellingen, O., et al. (2013) · Nature Communications · doi:10.1038/ncomms2921 · Cited by 417 · see citing works
New insights into the activities and toxicities of the old anticancer drug doxorubicin
van der Zanden, S. Y., Qiao, X., & Neefjes, J. (2020) · FEBS Journal · doi:10.1111/febs.15583 · Cited by 416 · see citing works
Chromosome assembly in vitro: Topoisomerase II is required for condensation
Adachi, Y., Luke, M. M., & Laemmli, U. K. (1991) · Cell · doi:10.1016/0092-8674(91)90215-k · Cited by 390 · see citing works
Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage
Anderson, L., Henderson, C., & Adachi, Y. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.5.1719-1729.2001 · Cited by 367 · see citing works
Topoisomerase II as a target for anticancer drugs: When enzymes stop being nice
Fortune, J. M., & Osheroff, N. (2000) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(00)64006-0 · Cited by 367 · see citing works
Holm, C., Covey, J. M., Kerrigan, D., & Pommier, Y. G. (1989) · PubMed · Cited by 366 · see citing works
Imbert, T. (1998) · Biochimie · doi:10.1016/s0300-9084(98)80004-7 · Cited by 351 · see citing works
Hollingshead, L. M., & Faulds, D. M. (1991) · Drugs · doi:10.2165/00003495-199142040-00010 · Cited by 346 · see citing works
Newport, J. W., & Spann, T. P. (1987) · Cell · doi:10.1016/0092-8674(87)90425-9 · Cited by 344 · see citing works
DNA Topoisomerases: Enzymes That Control DNA Conformation
Vosberg, H.-P. (1985) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-70227-3_2 · Cited by 321 · see citing works
Recent studies of DNA topoisomerases
Wang, J. C. (1987) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/0167-4781(87)90040-6 · Cited by 321 · see citing works
Miser, J. S., Kinsella, T. J., Triche, T. J., Tsokos, M., Jarosinski, P., Forquer, R., Wesley, R., & Magrath, I. (1987) · Journal of Clinical Oncology · doi:10.1200/jco.1987.5.8.1191 · Cited by 317 · see citing works
Super, H. J. G., McCabe, N., Thirman, M., Larson, R. A., Beau, M. M. L., Pedersen-Bjergaard, J., Philip, P., Diaz, M., & Rowley, J. (1993) · Blood · doi:10.1182/blood.v82.12.3705.3705 · Cited by 320 · see citing works
Preferential, cooperative binding of DNA topoisomerase II to scaffold‐associated regions.
Adachi, Y., Käs, E., & Laemmli, U. K. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb08582.x · Cited by 316 · see citing works
Roles of DNA topoisomerases in simian virus 40 DNA replication in vitro.
Yang, L., Wold, M. S., Li, J. J., Kelly, T. J., & Liu, L. F. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.4.950 · Cited by 289 · see citing works
Self-citationInvolvement of DNA topoisomerase I in transcription of human ribosomal RNA genes.
Zhang, H., Wang, J. C., & Liu, L. F. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.4.1060 · Cited by 284 · see citing works
Self-citationDrake, F. H., Zimmerman, J., McCabe, F. L., BARTUS, H. F., Per, S., Sullivan, D. M., Ross, W., Mr, M., Johnson, R., & Crooke, S. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)49317-9 · Cited by 278 · see citing works
Anthracyclines as Topoisomerase II Poisons: From Early Studies to New Perspectives
Marinello, J., Delcuratolo, M., & Capranico, G. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113480 · Cited by 234 · see citing works
“Initial findings clearly showed that anticancer Top2 poisons of different structural families induce DNA cleavage in a sequence-selective manner, which can be revealed experimentally as drug-specific cleavage intensity patterns in sequencing gels [47,48,57].”
BackgroundThe Clinical Pharmacology of Etoposide and Teniposide
CLARK, P. I., & Slevin, M. L. (1987) · Clinical Pharmacokinetics · doi:10.2165/00003088-198712040-00001 · Cited by 261 · see citing works
Deffie, A. M., Batra, J. K., & Goldenberg, G. J. (1989) · PubMed · Cited by 261 · see citing works
Interfacial inhibitors: targeting macromolecular complexes
Pommier, Y. G., & Marchand, C. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3404 · Cited by 260 · see citing works
Mechanistic Aspects of DNA Topoisomerases
Maxwell, A., & Gellert, M. F. (1986) · Advances in protein chemistry · doi:10.1016/s0065-3233(08)60526-4 · Cited by 259 · see citing works
Mitoxantrone, More than Just Another Topoisomerase II Poison
Evison, B. J., Sleebs, B. E., Watson, K. G., Phillips, D. R., & Cutts, S. M. (2015) · Medicinal Research Reviews · doi:10.1002/med.21364 · Cited by 257 · see citing works
Production and biological activity of rebeccamycin, a novel antitumor agent.
BUSH, J. A., Long, B. H., Catino, J. J., & Bradner, W. T. (1987) · The Journal of Antibiotics · doi:10.7164/antibiotics.40.668 · Cited by 252 · see citing works
Biochemical basis for the interactions of type I and type II topoisomerases with DNA
Osheroff, N. (1989) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(89)90108-3 · Cited by 252 · see citing works
A consensus sequence for cleavage by vertebrate DNA topoisomerase II
Spitzner, J. R., & Muller, M. T. (1988) · Nucleic Acids Research · doi:10.1093/nar/16.12.5533 · Cited by 249 · see citing works
Peña-Morán, O. A., Villarreal, M., Álvarez, L., Meneses‐Acosta, A., & Rodríguez-López, V. (2016) · Molecules · doi:10.3390/molecules21081013 · Cited by 248 · see citing works
Shamu, C., & Murray, A. W. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.117.5.921 · Cited by 237 · see citing works
Sander, M., & Hsieh, T. (1985) · Nucleic Acids Research · doi:10.1093/nar/13.4.1057 · Cited by 234 · see citing works
Hirano, T., & Mitchison, T. J. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.3.601 · Cited by 233 · see citing works
Breslow, N. E., Takashima, J. R., Whitton, J. A., Moksness, J., D’Angio, G. J., & Green, D. M. (1995) · Journal of Clinical Oncology · doi:10.1200/jco.1995.13.8.1851 · Cited by 226 · see citing works
Osheroff, N. (1989) · Biochemistry · doi:10.1021/bi00441a005 · Cited by 226 · see citing works
Sequence-Selective DNA Recognition: Natural Products and Nature’s Lessons
Tse, W. C., & Boger, D. L. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2003.08.012 · Cited by 225 · see citing works
DNA topoisomerase II-mediated interaction of doxorubicin and daunorubicin congeners with DNA.
Bodley, A. L., Liu, L. F., Israel, M., Seshadri, R., Koseki, Y., Giuliani, F. C., Kirschenbaum, S., Silber, R., & Potmĕsil, M. (1989) · PubMed · Cited by 225 · see citing works
Self-citationDanks, M. K., Yalowich, J. C., & Beck, W. T. (1987) · PubMed · Cited by 225 · see citing works
Sugimoto, Y., Tsukahara, S., Oh‐hara, T., Isoe, T., & TSURUO, T. (1990) · PubMed · Cited by 223 · see citing works
Selective cleavage of kinetoplast DNA minicircles promoted by antitrypanosomal drugs.
Shapiro, T. A., & Englund, P. T. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.3.950 · Cited by 222 · see citing works
Li, C. J., Averboukh, L., & Pardee, A. B. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)41552-9 · Cited by 219 · see citing works
Effects of CPT‐11 in combination with other anti‐cancer agents in culture
Kano, Y., Suzuki, K., Akutsu, M., Suda, K., Indue, Y., Yosnida, M., Sakamoto, S., & Miura, Y. (1992) · International Journal of Cancer · doi:10.1002/ijc.2910500420 · Cited by 218 · see citing works
Mapping the active site tyrosine of Escherichia coli DNA gyrase.
Horowitz, D. S., & Wang, J. C. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61193-7 · Cited by 217 · see citing works
Bonjean, K., Pauw-Gillet, M. C. D., Defresne, M. P., Colson, P., Houssier, C., Dassonneville, L., Bailly, C., Greimers, R., Wright, C. W., Quetin‐Leclercq, J., et al. (1998) · Biochemistry · doi:10.1021/bi972927q · Cited by 216 · see citing works
Mechanism of quinolone inhibition of DNA gyrase
Shen, L. L., Kohlbrenner, W. E., Weigl, D., & Baranowski, J. L. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)81708-8 · Cited by 215 · see citing works
Yoshinori, Y., Kawada, S., & Nakano, H. (1990) · Biochemical Pharmacology · doi:10.1016/0006-2952(90)90153-c · Cited by 215 · see citing works
Swift, L. H., & Golsteyn, R. M. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms15033403 · Cited by 214 · see citing works
Purification and characterization of a type II DNA topoisomerase from bovine calf thymus.
Halligan, B. D., Edwards, K. A., & Liu, L. F. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)89578-3 · Cited by 212 · see citing works
Self-citationAvemann, K., Knippers, R., Koller, T., & Sogo, J. M. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3026 · Cited by 211 · see citing works
Cellular Determinants of Sensitivity and Resistance to DNA Topoisomerase Inhibitors
Pommier, Y. G., Pharm, D., Fesen, M. R., Fujimori, A., Bertrand, R., Solary, É., Kohlhagen, G., & Kohn, K. W. (1994) · Cancer Investigation · doi:10.3109/07357909409021413 · Cited by 208 · see citing works
DNA End Resection: Nucleases Team Up with the Right Partners to Initiate Homologous Recombination
Ćejka, P. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.675942 · Cited by 200 · see citing works
DNA Topoisomerases as Anticancer Drug Targets
Schneider, E., Hsiang, Y. H., & Liu, L. F. (1990) · Advances in pharmacology · doi:10.1016/s1054-3589(08)60342-7 · Cited by 193 · see citing works
Self-citationDNA topoisomerases as targets for cancer therapy
Ross, W. E. (1985) · Biochemical Pharmacology · doi:10.1016/0006-2952(85)90273-4 · Cited by 190 · see citing works
Mechanisms of Anthracycline Cardiotoxicity and Strategies to Decrease Cardiac Damage
Geisberg, C. A., & Sawyer, D. B. (2010) · Current Hypertension Reports · doi:10.1007/s11906-010-0146-y · Cited by 189 · see citing works
Long, B. H., Musial, S. T., & Brattain, M. G. (1985) · PubMed · Cited by 188 · see citing works
Luteolin, an emerging anti-cancer flavonoid, poisons eukaryotic DNA topoisomerase I
CHOWDHURY, A. R., Sharma, S., Mandal, S., Goswami, A., Mukhopadhyay, S., & Majumder, H. K. (2002) · Biochemical Journal · doi:10.1042/bj20020098 · Cited by 186 · see citing works
Genotoxicity of benzene and its metabolites
Whysner, J. A., Reddy, M. V., Ross, P. M., Mohan, M., & Lax, E. A. (2003) · Mutation Research/Reviews in Mutation Research · doi:10.1016/s1383-5742(03)00053-x · Cited by 178 · see citing works
Käs, E., & Laemmli, U. K. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05103.x · Cited by 176 · see citing works
Pommier, Y. G., Zwelling, L. A., Kao-Shan, C. S., Whang‐Peng, J., & Bradley, M. O. (1985) · PubMed · Cited by 174 · see citing works
Tepper, A. D., de Vries, E., BLITTERSWIJK, W. J. V., & Borst, J. G. (1999) · Journal of Clinical Investigation · doi:10.1172/jci5457 · Cited by 173 · see citing works
Smith, M. A., Rubinstein, L., & Ungerleider, R. S. (1994) · Medical and Pediatric Oncology · doi:10.1002/mpo.2950230205 · Cited by 171 · see citing works
The Secondary Leukemias: Challenges and Research Directions
Smith, M. A., McCaffrey, R. P., & Karp, J. E. (1996) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/88.7.407 · Cited by 166 · see citing works
Proliferation dependence of topoisomerase II-mediated drug action
Sullivan, D. M., Glisson, B. S., Hodges, P. K., Smallwood-Kentro, S., & Ross, W. E. (1986) · Biochemistry · doi:10.1021/bi00356a060 · Cited by 166 · see citing works
Uncoupling DNA damage from chromatin damage to detoxify doxorubicin
Qiao, X., van der Zanden, S. Y., Wander, D. P. A., Borràs, D., Song, J., Li, X., van Duikeren, S., van Gils, N., Rutten, A. P., van Herwaarden, T., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1922072117 · Cited by 164 · see citing works
Relationship between topoisomerase II level and chemosensitivity in human tumor cell lines.
Fry, A. M., Chresta, C. M., Davies, S. M., Walker, M. C., Harris, A. L., Hartley, J. A., Masters, J. R., & Hickson, I. D. (1991) · PubMed · Cited by 163 · see citing works
Davies, S. M., Robson, C. N., Davies, S. L., & Hickson, I. D. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)77896-x · Cited by 163 · see citing works
Bugg, B. Y., Danks, M. K., Beck, W. T., & Suttle, D. P. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7654 · Cited by 159 · see citing works
Jong, D. S., Zijlstra, J. G., de Vries, E. G. E., & Mulder, N. H. (1990) · PubMed · Cited by 159 · see citing works
Molecular and cellular mechanisms of anthracycline cardiotoxicity
Chen, B., Peng, X., Pentassuglia, L., Lim, C. C., & Sawyer, D. B. (2007) · Cardiovascular Toxicology · doi:10.1007/s12012-007-0005-5 · Cited by 157 · see citing works
“In the late 1970s and early 1980s, it was discovered that anthracyclines would induce strand breaks in DNA of L1210 leukemic cells through association with proteins later identified to be topoisomerase II [27].”
BackgroundOshi, M., Takahashi, H., Tokumaru, Y., Yan, L., Rashid, O. M., Matsuyama, R., Endo, I., & Takabe, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082921 · Cited by 157 · see citing works
Ratain, M. J., & Rowley, J. D. (1992) · Annals of Oncology · doi:10.1093/oxfordjournals.annonc.a058121 · Cited by 156 · see citing works
“Inhibitors of topoisomerase II include both the intercalators [45] and non-intercalating epipodophyllotoxins [46].”
BackgroundPrinciples and practice of DNA filter elution
Kohn, K. W. (1991) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(91)90022-e · Cited by 155 · see citing works
Chronic daily administration of oral etoposide--a phase I trial.
Hainsworth, J. D., Johnson, D. H., Redlin-Frazier, S., & Greco, F. A. (1989) · Journal of Clinical Oncology · doi:10.1200/jco.1989.7.3.396 · Cited by 150 · see citing works
Small Molecule Mitochondrial Uncouplers and Their Therapeutic Potential
Childress, E. S., Alexopoulos, S. J., Hoehn, K. L., & Santos, W. L. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b01182 · Cited by 144 · see citing works
- Authors
- Tewey, K. M., Chen, G. L., Nelson, E. M., & Liu, L. F.
- Affiliations
- Johns Hopkins University (US)
- ORCID
- Liu, L F
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1984-07
- Volume
- 259
- Issue
- 14
- Pages
- 9182-9187
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1514525963
- Cited by
- 887
- References
- 39
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 4 · 2023: 4 · 2022: 6 · 2021: 9 · 2020: 10 · 2019: 16 · 2018: 9 · 2017: 15 · 2016: 19 · 2015: 14 · 2014: 14 · 2013: 16 · 2012: 14
- FWCI
- 15.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer therapeutics and mechanisms
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Bioactive Compounds and Antitumor Agents
- Health Sciences › Medicine › Oncology › Metal complexes synthesis and properties
- Keywords
- topoisomerase II, epipodophyllotoxins, etoposide, doxorubicin, cleavable complex, drug-enzyme interaction, nalidixic acid, DNA gyrase, cytotoxicity mechanism
- MeSH terms
- Alkaloids, Animals, Antineoplastic Agents, Cattle, DNA, DNA Topoisomerases, Type II, DNA Topoisomerases, Type I, DNA, Viral, Ellipticines, HeLa Cells, Humans, Intercalating Agents, Kinetics, Osmolar Concentration, Plasmids, Protein Binding, Thymus Gland
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
