SPARTAN promotes genetic diversification of the immunoglobulin-variable gene locus in avian DT40 cells

DNA Repair (Amst). 2018 Aug:68:50-57. doi: 10.1016/j.dnarep.2018.06.003. Epub 2018 Jun 18.

Abstract

Prolonged replication arrest on damaged templates is a cause of fork collapse, potentially resulting in genome instability. Arrested replication is rescued by translesion DNA synthesis (TLS) and homologous recombination (HR)-mediated template switching. SPARTAN, a ubiquitin-PCNA-interacting regulator, regulates TLS via mechanisms incompletely understood. Here we show that SPARTAN promotes diversification of the chicken DT40 immunoglobulin-variable λ gene by facilitating TLS-mediated hypermutation and template switch-mediated gene-conversion, both induced by replication blocks at abasic sites. SPARTAN-/- and SPARTAN-/-/Polη-/-/Polζ-/- cells showed defective and similar decrease in hypermutation rates, as well as alterations in the mutation spectra, with decreased dG-to-dC transversions and increased dG-to-dA transitions. Strikingly, SPARTAN-/- cells also showed reduced template switch-mediated gene-conversion at the immunoglobulin locus, while being proficient in HR-mediated double strand break repair, and sister chromatid recombination. Notably, SPARTAN's ubiquitin-binding zinc-finger 4 domain, but not the PCNA interacting peptide domain or its DNA-binding domain, was specifically required for the promotion of immunoglobulin gene-conversion, while all these three domains were shown to contribute similarly to TLS. In all, our results suggest that SPARTAN mediates TLS in concert with the Polη-Polζ pathway and that it facilitates HR-mediated template switching at a subset of stalled replication forks, potentially by interacting with unknown ubiquitinated proteins.

Keywords: DNA damage tolerance pathways; Gene-conversion; Homologous recombination; SPARTAN; Translesion DNA synthesis (TLS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibody Diversity
  • Avian Proteins / metabolism
  • Cell Line, Tumor
  • Chickens / genetics
  • Chickens / immunology
  • Chickens / metabolism*
  • DNA / metabolism
  • DNA Repair*
  • DNA Replication*
  • DNA-Binding Proteins / metabolism*
  • DNA-Directed DNA Polymerase / metabolism
  • Homologous Recombination
  • Immunoglobulin Variable Region / genetics*
  • Somatic Hypermutation, Immunoglobulin*
  • Ubiquitin / metabolism

Substances

  • Avian Proteins
  • DNA-Binding Proteins
  • Immunoglobulin Variable Region
  • Ubiquitin
  • DNA
  • DNA polymerase zeta
  • DNA-Directed DNA Polymerase
  • Rad30 protein