Control of topoisomerase II activity and chemotherapeutic inhibition by TCA cycle metabolites

Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through another and depends on the transient formation of double-stranded DNA breaks, a step exploited by frontline chemotherapeutics to kill cancer cells...

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Published inCell chemical biology Vol. 29; no. 3; pp. 476 - 489.e6
Main Authors Lee, Joyce H., Mosher, Eric P., Lee, Young-Sam, Bumpus, Namandjé N., Berger, James M.
Format Journal Article
LanguageEnglish
Published United States Elsevier Ltd 17.03.2022
Subjects
Antineoplastic Agents - pharmacology
cancer
chemotherapy
dexrazoxane
DNA - metabolism
DNA Topoisomerases, Type II - metabolism
DNA topology
etoposide
ICRF-187
metabolism
TCA cycle
topoisomerase
Topoisomerase II Inhibitors - pharmacology
dexrazoxane
DNA topology
ICRF-187
TCA cycle
topoisomerase
cancer
metabolism
etoposide
chemotherapy
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Abstract Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through another and depends on the transient formation of double-stranded DNA breaks, a step exploited by frontline chemotherapeutics to kill cancer cells. Although anti-topo II drugs are efficacious, they also elicit cytotoxic side effects in normal cells; insights into how topo II is regulated in different cellular contexts is essential to improve their targeted use. Using chemical fractionation and mass spectrometry, we have discovered that topo II is subject to metabolic control through the TCA cycle. We show that TCA metabolites stimulate topo II activity in vitro and that levels of TCA flux modulate cellular sensitivity to anti-topo II drugs in vivo. Our work reveals an unanticipated connection between the control of DNA topology and cellular metabolism, a finding with ramifications for the clinical use of anti-topo II therapies. [Display omitted] •TCA cycle intermediates stimulate the strand passage activity of S. cerevisiae topo II•Stimulation of enzyme activity by TCA metabolites is specific to eukaryotic topo IIs•Topo II activity and drug response is impacted by changes in TCA cycle flux in cells Lee et al. purify yeast metabolites that show activity against eukaryotic topoisomerase II (topo II). LC-MS/MS analysis identifies TCA cycle intermediates as stimulators of topo II activity. Modulating TCA cycle flux affects the cytotoxicity of topo II-targeting drugs, indicating that TCA cycle metabolism regulates topo II function in cells.
AbstractList Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through another and depends on the transient formation of double-strand DNA breaks, a step exploited by frontline chemotherapeutics to kill cancer cells. Although anti-topo II drugs are efficacious, they also elicit cytotoxic side effects in normal cells; insights into how topo II is regulated in different cellular contexts is essential to improve their targeted use. Using chemical fractionation and mass spectrometry, we have discovered that topo II is subject to metabolic control through the TCA cycle. We show that TCA metabolites stimulate topo II activity in vitro and that levels of TCA flux modulate cellular sensitivity to anti-topo II drugs in vivo . Our work reveals an unanticipated connection between the control of DNA topology and cellular metabolism, a finding with ramifications for the clinical use of anti-topo II therapies. Lee et al. purify yeast metabolites that show activity against eukaryotic topoisomerase II (topo II). LC-MS/MS analysis identifies TCA cycle intermediates as stimulators of topo II activity. Modulating TCA cycle flux affects the cytotoxicity of topo II-targeting drugs, indicating that TCA cycle metabolism regulates topo II function in cells.
Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through another and depends on the transient formation of double-stranded DNA breaks, a step exploited by frontline chemotherapeutics to kill cancer cells. Although anti-topo II drugs are efficacious, they also elicit cytotoxic side effects in normal cells; insights into how topo II is regulated in different cellular contexts is essential to improve their targeted use. Using chemical fractionation and mass spectrometry, we have discovered that topo II is subject to metabolic control through the TCA cycle. We show that TCA metabolites stimulate topo II activity in vitro and that levels of TCA flux modulate cellular sensitivity to anti-topo II drugs in vivo. Our work reveals an unanticipated connection between the control of DNA topology and cellular metabolism, a finding with ramifications for the clinical use of anti-topo II therapies.
Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through another and depends on the transient formation of double-stranded DNA breaks, a step exploited by frontline chemotherapeutics to kill cancer cells. Although anti-topo II drugs are efficacious, they also elicit cytotoxic side effects in normal cells; insights into how topo II is regulated in different cellular contexts is essential to improve their targeted use. Using chemical fractionation and mass spectrometry, we have discovered that topo II is subject to metabolic control through the TCA cycle. We show that TCA metabolites stimulate topo II activity in vitro and that levels of TCA flux modulate cellular sensitivity to anti-topo II drugs in vivo. Our work reveals an unanticipated connection between the control of DNA topology and cellular metabolism, a finding with ramifications for the clinical use of anti-topo II therapies. [Display omitted] •TCA cycle intermediates stimulate the strand passage activity of S. cerevisiae topo II•Stimulation of enzyme activity by TCA metabolites is specific to eukaryotic topo IIs•Topo II activity and drug response is impacted by changes in TCA cycle flux in cells Lee et al. purify yeast metabolites that show activity against eukaryotic topoisomerase II (topo II). LC-MS/MS analysis identifies TCA cycle intermediates as stimulators of topo II activity. Modulating TCA cycle flux affects the cytotoxicity of topo II-targeting drugs, indicating that TCA cycle metabolism regulates topo II function in cells.
Author Lee, Young-Sam
Lee, Joyce H.
Mosher, Eric P.
Berger, James M.
Bumpus, Namandjé N.
AuthorAffiliation 4 Lead Contact
2 Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
3 Department of Molecular and Cellular Biochemistry, College of Medicine, University of Kentucky, Lexington, KY 40536, USA
1 Department of Biophysics and Biophysical Chemistry, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
AuthorAffiliation_xml – name: 4 Lead Contact
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– name: 2 Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
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  givenname: Namandjé N.
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  email: jmberger@jhmi.edu
  organization: Department of Biophysics and Biophysical Chemistry, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
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Issue 3
Keywords dexrazoxane
DNA topology
ICRF-187
TCA cycle
topoisomerase
cancer
metabolism
etoposide
chemotherapy
Language English
License Copyright © 2021 Elsevier Ltd. All rights reserved.
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Notes JHL conducted in vitro assays, metabolite purification, and yeast growth assays. EPM conducted LC-MS/MS analysis. Data analysis was performed by JHL, EPM, and JMB. YSL contributed to the development of the yeast metabolite extraction method. JHL, EPM, NNB, and JMB contributed to conceptual planning, experimental design, and data interpretation. JHL, EPM, and JMB prepared the manuscript. All authors critically reviewed the manuscript and approved the final version.
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Snippet Topoisomerase II (topo II) is essential for disentangling newly replicated chromosomes. DNA unlinking involves the physical passage of one duplex through...
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SubjectTerms Antineoplastic Agents - pharmacology
cancer
chemotherapy
dexrazoxane
DNA - metabolism
DNA Topoisomerases, Type II - metabolism
DNA topology
etoposide
ICRF-187
metabolism
TCA cycle
topoisomerase
Topoisomerase II Inhibitors - pharmacology
Title Control of topoisomerase II activity and chemotherapeutic inhibition by TCA cycle metabolites
URI https://dx.doi.org/10.1016/j.chembiol.2021.08.014
https://www.ncbi.nlm.nih.gov/pubmed/34529934
https://pubmed.ncbi.nlm.nih.gov/PMC8913808
Volume 29
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