A novel mechanism of cell killing by anti-topoisomerase II bisdioxopiperazines

J Biol Chem. 2000 Jan 21;275(3):2137-46. doi: 10.1074/jbc.275.3.2137.

Abstract

Bisdioxopiperazines are a unique class of topoisomerase II inhibitors that lock topoisomerase II at a point in the enzyme reaction cycle where the enzyme forms a closed clamp around DNA. We examined cell killing by ICRF-187 and ICRF-193 in yeast cells expressing human topoisomerase II alpha (htop-IIalpha). Expression of htop-IIalpha in yeast cells sensitizes them to both ICRF-187 and ICRF-193, compared with cells expressing yeast topoisomerase II. ICRF-193 is still able to exert growth inhibition in the presence of genes encoding both ICRF-193-resistant and ICRF-193-sensitive htop-IIalpha enzymes, indicating that sensitivity to bisdioxopiperazines is dominant. Killing by ICRF-193 occurs more rapidly, than the killing in yeast cells due to a temperature-sensitive yeast topoisomerase II incubated at the non-permissive temperature. These results are reminiscent of a top-II poison such as etoposide. However, the killing caused by ICRF-193 and ICRF-187 is not enhanced by mutations in the RAD52 pathway. The levels of drug-induced DNA cleavage observed with htop-IIalpha in vitro is insufficient to explain the sensitivity induced by this enzyme in yeast cells. Finally, arrest of cells in G(1) does not protect cells from ICRF-193 lethality, a result inconsistent with killing mechanisms due to catalytic inhibition of top-II or stabilization of a cleavable complex. We suggest that the observed pattern of cell killing is most consistent with a poisoning of htop-II by ICRF-193 by a novel mechanism. The accumulation of closed clamp conformations of htop-II induced by ICRF-193 that are trapped on DNA might interfere with transcription, or other DNA metabolic processes, resulting in cell death.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alleles
  • Antineoplastic Agents / pharmacology*
  • Cell Cycle / drug effects
  • DNA Topoisomerases, Type II / genetics
  • DNA Topoisomerases, Type II / metabolism
  • Diketopiperazines
  • Dose-Response Relationship, Drug
  • Drug Resistance, Microbial
  • Enzyme Inhibitors / pharmacology*
  • Genes, Dominant
  • Humans
  • Microbial Sensitivity Tests
  • Mutagenesis
  • Piperazines / pharmacology*
  • Protein Conformation
  • Razoxane / pharmacology*
  • Saccharomyces cerevisiae / drug effects
  • Time Factors
  • Topoisomerase II Inhibitors*
  • Ultracentrifugation

Substances

  • Antineoplastic Agents
  • Diketopiperazines
  • Enzyme Inhibitors
  • Piperazines
  • Topoisomerase II Inhibitors
  • 4,4'-(1,2-dimethyl-1,2-ethanediyl)bis-2,6-piperazinedione
  • Razoxane
  • DNA Topoisomerases, Type II