Mus81-mediated DNA cleavage resolves replication forks stalled by topoisomerase I-DNA complexes

J Cell Biol. 2011 Nov 28;195(5):739-49. doi: 10.1083/jcb.201104003.

Abstract

Deoxyribonucleic acid (DNA) topoisomerases are essential for removing the supercoiling that normally builds up ahead of replication forks. The camptothecin (CPT) Top1 (topoisomerase I) inhibitors exert their anticancer activity by reversibly trapping Top1-DNA cleavage complexes (Top1cc's) and inducing replication-associated DNA double-strand breaks (DSBs). In this paper, we propose a new mechanism by which cells avoid Top1-induced replication-dependent DNA damage. We show that the structure-specific endonuclease Mus81-Eme1 is responsible for generating DSBs in response to Top1 inhibition and for allowing cell survival. We provide evidence that Mus81 cleaves replication forks rather than excises Top1cc's. DNA combing demonstrated that Mus81 also allows efficient replication fork progression after CPT treatment. We propose that Mus81 cleaves stalled replication forks, which allows dissipation of the excessive supercoiling resulting from Top1 inhibition, spontaneous reversal of Top1cc, and replication fork progression.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Camptothecin / pharmacology
  • Cell Cycle / drug effects
  • Cell Cycle / genetics
  • DNA Breaks, Double-Stranded*
  • DNA Cleavage*
  • DNA Damage
  • DNA Replication / physiology*
  • DNA Topoisomerases, Type I / metabolism*
  • DNA Topoisomerases, Type I / physiology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Endonucleases / genetics
  • Endonucleases / metabolism
  • Endonucleases / physiology*
  • Humans
  • Topoisomerase I Inhibitors / pharmacology
  • Tumor Cells, Cultured

Substances

  • DNA-Binding Proteins
  • Topoisomerase I Inhibitors
  • Endonucleases
  • MUS81 protein, human
  • DNA Topoisomerases, Type I
  • TOP1 protein, human
  • Camptothecin