Etoposide quinone is a covalent poison of human topoisomerase IIβ

Nicholas A Smith1, Jo Ann W Byl, Susan L Mercer

  • 1Departments of †Biochemistry, ‡Medicine (Hematology/Oncology), and §Pharmacology, Vanderbilt University School of Medicine , Nashville, Tennessee 37232-0146, United States.

Biochemistry
|April 29, 2014
PubMed

Insights

Etoposide metabolite, etoposide quinone, is a potent covalent poison of topoisomerase IIβ, potentially explaining its role in treatment-related acute myeloid leukemias (t-AMLs). This finding advances understanding of etoposide-induced leukemogenesis.

Area of Science:

  • Biochemistry
  • Molecular Biology
  • Oncology

Background:

  • Etoposide is a widely used chemotherapy drug for various cancers.
  • A subset of patients develop acute myeloid leukemias (t-AMLs) after etoposide treatment, often with MLL gene rearrangements.
  • Etoposide metabolites, like etoposide quinone, and topoisomerase IIβ are suspected contributors to t-AML development.

Purpose of the Study:

  • To investigate the effects of etoposide quinone on human topoisomerase IIβ activity.
  • To compare the activity of etoposide quinone against topoisomerase IIβ and topoisomerase IIα.
  • To elucidate the mechanism by which etoposide quinone interacts with topoisomerase IIβ.

Main Methods:

  • In vitro assays to measure enzyme-mediated DNA cleavage.
  • Comparative analysis of etoposide quinone's potency against topoisomerase IIα and IIβ.
  • Assessment of etoposide quinone's reaction kinetics and ATP dependence.
  • Evaluation of the effect of reducing agents and pre-incubation on enzyme activity.

Main Results:

  • Etoposide quinone induced approximately 4 times more DNA cleavage than etoposide.
  • Etoposide quinone was about 2 times more potent against topoisomerase IIβ than IIα and reacted faster with the β isoform.
  • Etoposide quinone acted as a covalent poison, with activity abolished by reducing agents and capable of inactivating the enzyme prior to DNA addition.
  • The metabolite showed a higher ratio of double- to single-stranded DNA breaks and less ATP dependence compared to etoposide.

Conclusions:

  • Etoposide quinone is a potent covalent poison of human topoisomerase IIβ.
  • The interaction of etoposide quinone with topoisomerase IIβ provides a molecular mechanism for etoposide-related leukemogenesis.
  • These findings highlight the critical role of etoposide metabolites in chemotherapy-induced secondary malignancies.

Related Concept Videos

DNA Topoisomerases02:02

DNA Topoisomerases

Topoisomerases are enzymes that relax overwound DNA molecules during various cell processes, including DNA replication and transcription. These enzymes regulate positive and negative DNA supercoiling without changing the nucleotide sequence. DNA overwinding in a clockwise direction results in positively supercoiled DNA, whereas underwinding in a counterclockwise direction produces negatively supercoiled DNA.
Types and Mechanism of action
Topoisomerases are divided into two main types. ...
32.3K
Inhibitors of Bacterial DNA Synthesis01:28

Inhibitors of Bacterial DNA Synthesis

Bacterial pathogens depend on precise and efficient DNA replication to sustain infection. Two type II topoisomerases—DNA gyrase and topoisomerase IV—are critical to this process, as they resolve DNA supercoiling and unlink chromosomes during replication. Fluoroquinolones, synthetic derivatives of quinolones, exploit this mechanism by stabilizing the transient DNA–enzyme cleavage complex, preventing strand religation, and causing lethal double-strand breaks. These...
130
Oxidation of Phenols to Quinones01:17

Oxidation of Phenols to Quinones

In the presence of oxidizing agents, phenols are oxidized to quinones. Quinones can be easily reduced back to phenols using mild reducing agents. The electron-donating hydroxyl group enhances the reactivity of the aromatic ring, enabling oxidation of the ring even in the absence of an α hydrogen.
o-hydroxy phenols are oxidized to o-quinones and p-hydroxy phenols to p-quinones. Such redox reactions involve the transfer of two electrons and two protons. The reversible redox...
4.6K
The Electron Transport Chain01:30

The Electron Transport Chain

The electron transport chain or oxidative phosphorylation is an exothermic process in which free energy released during electron transfer reactions is coupled to ATP synthesis. This process is a significant source of energy in aerobic cells, and therefore inhibitors of the electron transport chain can be detrimental to the cell's metabolic processes.
Inhibitors of the electron transport chain
Rotenone, a widely used pesticide, prevents electron transfer from Fe-S cluster to ubiquinone or Q...
13.8K
Electron Transport Chain: Complex I and II01:46

Electron Transport Chain: Complex I and II

The mitochondrial electron transport chain (ETC) is the main energy generation system in the eukaryotic cells. However, mitochondria also produce cytotoxic reactive oxygen species (ROS) due to the large electron flow during oxidative phosphorylation. While Complex I is one of the primary sources of superoxide radicals, ROS production by Complex II is uncommon and may only be observed in cancer cells with mutated complexes.
ROS generation is regulated and maintained at moderate levels necessary...
11.9K
Electron Transport Chain: Complex III and IV01:43

Electron Transport Chain: Complex III and IV

During the electron transport chain, electrons from NADH and FADH2 are first transferred to complexes I and II, respectively. These two complexes then transfer the electrons to ubiquinol, which carries them further to complex III. Complex III passes the electrons across the intermembrane space to Cyt c, which carries them further to complex IV. Complex IV donates electrons to oxygen and reduces it to water. As electrons pass through complexes I, III, and IV, the energy released aids the pumping...
6.7K