Direct Binding to Replication Protein A (RPA)-coated Single-stranded DNA Allows Recruitment of the ATR Activator TopBP1 to Sites of DNA Damage

J Biol Chem. 2016 Jun 17;291(25):13124-31. doi: 10.1074/jbc.M116.729194. Epub 2016 Apr 26.

Abstract

A critical event for the ability of cells to tolerate DNA damage and replication stress is activation of the ATR kinase. ATR activation is dependent on the BRCT (BRCA1 C terminus) repeat-containing protein TopBP1. Previous work has shown that recruitment of TopBP1 to sites of DNA damage and stalled replication forks is necessary for downstream events in ATR activation; however, the mechanism for this recruitment was not known. Here, we use protein binding assays and functional studies in Xenopus egg extracts to show that TopBP1 makes a direct interaction, via its BRCT2 domain, with RPA-coated single-stranded DNA. We identify a point mutant that abrogates this interaction and show that this mutant fails to accumulate at sites of DNA damage and that the mutant cannot activate ATR. These data thus supply a mechanism for how the critical ATR activator, TopBP1, senses DNA damage and stalled replication forks to initiate assembly of checkpoint signaling complexes.

Keywords: ATR kinase; BRCT domain; DNA damage response; DNA repair; DNA replication; RPA; TopBP1; cell cycle; checkpoint control; ssDNA.

Publication types

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

MeSH terms

  • Animals
  • Carrier Proteins / chemistry*
  • DNA Damage
  • DNA, Single-Stranded / chemistry*
  • DNA-Binding Proteins
  • Protein Binding
  • Protein Structure, Tertiary
  • Replication Protein A / chemistry*
  • Xenopus laevis

Substances

  • Carrier Proteins
  • DNA, Single-Stranded
  • DNA-Binding Proteins
  • Replication Protein A
  • TopBP1 protein, Xenopus