DNA topoisomerase II in therapy-related acute promyelocytic leukemia

N Engl J Med. 2005 Apr 14;352(15):1529-38. doi: 10.1056/NEJMoa042715.

Abstract

Background: Chromosomal translocations leading to chimeric oncoproteins are important in leukemogenesis, but how they form is unclear. We studied acute promyelocytic leukemia (APL) with the t(15;17) translocation that developed after treatment of breast or laryngeal cancer with chemotherapeutic agents that poison topoisomerase II.

Methods: We used long-range polymerase chain reaction and sequence analysis to characterize t(15;17) genomic breakpoints in therapy-related APL. To determine whether topoisomerase II was directly involved in mediating breaks of double-stranded DNA at the observed translocation breakpoints, we used a functional in vitro assay to examine topoisomerase II-mediated cleavage in the normal homologues of the PML and RARA breakpoints.

Results: Translocation breakpoints in APL that developed after exposure to mitoxantrone, a topoisomerase II poison, were tightly clustered in an 8-bp region within PML intron 6. In functional assays, this "hot spot" and the corresponding RARA breakpoints were common sites of mitoxantrone-induced cleavage by topoisomerase II. Etoposide and doxorubicin also induced cleavage by topoisomerase II at the translocation breakpoints in APL arising after exposure to these agents. Short, homologous sequences in PML and RARA suggested the occurrence of DNA repair by means of the nonhomologous end-joining pathway.

Conclusions: Drug-induced cleavage of DNA by topoisomerase II mediates the formation of chromosomal translocation breakpoints in mitoxantrone-related APL and in APL that occurs after therapy with other topoisomerase II poisons.

Publication types

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

MeSH terms

  • Antineoplastic Agents / adverse effects
  • Antineoplastic Agents / pharmacology
  • DNA Damage
  • DNA Repair
  • DNA Topoisomerases, Type II / metabolism*
  • DNA, Neoplasm / drug effects
  • DNA, Neoplasm / metabolism*
  • Doxorubicin / adverse effects
  • Etoposide / adverse effects
  • Humans
  • In Vitro Techniques
  • Leukemia, Promyelocytic, Acute / chemically induced
  • Leukemia, Promyelocytic, Acute / enzymology
  • Leukemia, Promyelocytic, Acute / genetics*
  • Mitoxantrone / pharmacology
  • Neoplasms, Second Primary / chemically induced
  • Neoplasms, Second Primary / enzymology
  • Neoplasms, Second Primary / genetics*
  • Polymerase Chain Reaction
  • Sequence Analysis, DNA
  • Topoisomerase II Inhibitors
  • Translocation, Genetic*

Substances

  • Antineoplastic Agents
  • DNA, Neoplasm
  • Topoisomerase II Inhibitors
  • Etoposide
  • Doxorubicin
  • Mitoxantrone
  • DNA Topoisomerases, Type II