Cited by 889Cancer therapeutics and mechanismsBioactive Compounds and Antitumor AgentsMetal complexes synthesis and properties

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Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II

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Tewey, K M, Chen, G L, Nelson, E M, Liu, L F·1984·Journal of Biological Chemistry

DOI 10.1016/s0021-9258(17)47282-6

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Abstract

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.

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DNA Topoisomerases
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Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4'-(9-acridinylamino)-methanesulfon-m-anisidide.
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
Self-citation
Cleavage of DNA by mammalian DNA topoisomerase II.
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Self-citation
Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break.
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Background
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Effects of the antitumor drug VP16 (etoposide) on the archaebacterialHalobacteriumGRB 1.7kb plasmidin vivo
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Establishment and characterization of human gastric and colonic xenograft lines resistant to CPT‐11 (A new derivative of camptothecin)
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Comparison of the effects of treatment with the polyamine analogue N1,N8bis(ethyl)spermidine (BESpd) or difluoromethylornithine (DFMO) on the topoisomerase II mediated formation of 4′-(9-acridinylamino) methanesulfon-m-anisidide (m-AMSA) induced cleavable complex in the human lung carcinoma line NCI H157
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Vibrational spectroscopic analysis, molecular dynamics simulations and molecular docking study of 5-nitro-2-phenoxymethyl benzimidazole
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An Integrated Drosophila Model System Reveals Unique Properties for F14512, a Novel Polyamine-Containing Anticancer Drug That Targets Topoisomerase II
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Mitoxantrone-related acute leukemia in MS
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Digital Holographic Imaging as a Method for Quantitative, Live Cell Imaging of Drug Response to Novel Targeted Cancer Therapies
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Emerging Targets in the Bioactivity of Ellipticines and Derivatives
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DNA interactions of 2-pyrrolinodoxorubicin, a distinctively more potent daunosamine-modified analogue of doxorubicin
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“thereby preventing topoII from binding DNA [25, 29, 30].”
Purification and properties of DNA topoisomerase I from broccoli
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Physicochemical properties, cytotoxic activity and topoisomerase ii inhibition of 2,3-diaza-anthracenediones
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DNA Damage Signaling in Hematopoietic Cells: A Role for Mre11 Complex Repair of Topoisomerase Lesions
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Disassembly of chromatin into ≅50 kb units by detergent
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Effect of the DNA topoisomerase II inhibitor VP-16 on illegitimate recombination in yeast chromosomes
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Germ-cell mutagenicity of etoposide: induction of meiotic micronuclei in cultured rat seminiferous tubules
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Possible role of DNA topoisomerase II on transcription of the homeobox geneHox-2.1in F9 embryonal carcinoma cells
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The role of p53 in the chemotherapeutic responses to cisplatin, doxorubicin and 5-fluorouracil treatment
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“The p53 tumour suppressor has been shown to modulate the effects of many cytotoxic agents including 5-fluorouracil (37), and doxorubicin (38) whereas the effect of p53 on cisplatin activity is ambiguous and remains to be fully elucidated.”
Background
Synthesis of hetero annulated carbazoles: exploration of in vitro cytotoxicity and molecular docking studies
Indumathi, T., Muthusankar, A., Shanmughavel, P., & Prasad, K. J. R. (2013) · MedChemComm · doi:10.1039/c2md20335a · Cited by 16
Computational analysis of Amsacrine resistance in human topoisomerase II alpha mutants (R487K and E571K) using homology modeling, docking and all-atom molecular dynamics simulation in explicit solvent
Sader, S., & Wu, C. F. (2017) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2016.11.019 · Cited by 17
The Indenoisoquinoline LMP517: A Novel Antitumor Agent Targeting both TOP1 and TOP2
Marzi, L., Sun, Y., Huang, S.-Y. N., James, A. E., Difilippantonio, S., & Pommier, Y. G. (2020) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-19-1064 · Cited by 16

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)
DOI: 10.1016/s0021-9258(17)47282-6
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: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 13270 d)
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

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Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II

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