DNA ligase III acts as a DNA strand break sensor in the cellular orchestration of DNA strand break repair

Nucleic Acids Res. 2015 Jan;43(2):875-92. doi: 10.1093/nar/gku1307. Epub 2014 Dec 24.

Abstract

In the current model of DNA SSBR, PARP1 is regarded as the sensor of single-strand breaks (SSBs). However, biochemical studies have implicated LIG3 as another possible SSB sensor. Using a laser micro-irradiation protocol that predominantly generates SSBs, we were able to demonstrate that PARP1 is dispensable for the accumulation of different single-strand break repair (SSBR) proteins at sites of DNA damage in live cells. Furthermore, we show in live cells for the first time that LIG3 plays a role in mediating the accumulation of the SSBR proteins XRCC1 and PNKP at sites of DNA damage. Importantly, the accumulation of LIG3 at sites of DNA damage did not require the BRCT domain-mediated interaction with XRCC1. We were able to show that the N-terminal ZnF domain of LIG3 plays a key role in the enzyme's SSB sensing function. Finally, we provide cellular evidence that LIG3 and not PARP1 acts as the sensor for DNA damage caused by the topoisomerase I inhibitor, irinotecan. Our results support the existence of a second damage-sensing mechanism in SSBR involving the detection of nicks in the genome by LIG3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • DNA Breaks*
  • DNA Breaks, Single-Stranded
  • DNA Ligase ATP
  • DNA Ligases / chemistry
  • DNA Ligases / metabolism
  • DNA Ligases / physiology*
  • DNA Repair Enzymes / metabolism
  • DNA Repair*
  • DNA-Binding Proteins / metabolism
  • HeLa Cells
  • Humans
  • Mice
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases / physiology
  • Poly-ADP-Ribose Binding Proteins
  • Protein Structure, Tertiary
  • X-ray Repair Cross Complementing Protein 1
  • Xenopus Proteins

Substances

  • DNA-Binding Proteins
  • Poly-ADP-Ribose Binding Proteins
  • X-ray Repair Cross Complementing Protein 1
  • XRCC1 protein, human
  • Xenopus Proteins
  • Xrcc1 protein, mouse
  • Parp1 protein, mouse
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases
  • PNKP protein, human
  • Phosphotransferases (Alcohol Group Acceptor)
  • DNA Ligases
  • DNA Repair Enzymes
  • DNA Ligase ATP
  • DNA ligase III alpha protein, Xenopus
  • LIG3 protein, human
  • Lig3 protein, mouse