A novel variant of DNA polymerase ζ, Rev3ΔC, highlights differential regulation of Pol32 as a subunit of polymerase δ versus ζ in Saccharomyces cerevisiae

DNA Repair (Amst). 2014 Dec:24:138-149. doi: 10.1016/j.dnarep.2014.04.013. Epub 2014 May 10.

Abstract

Unrepaired DNA lesions often stall replicative DNA polymerases and are bypassed by translesion synthesis (TLS) to prevent replication fork collapse. Mechanisms of TLS are lesion- and species-specific, with a prominent role of specialized DNA polymerases with relaxed active sites. After nucleotide(s) are incorporated across from the altered base(s), the aberrant primer termini are typically extended by DNA polymerase ζ (pol ζ). As a result, pol ζ is responsible for most DNA damage-induced mutations. The mechanisms of sequential DNA polymerase switches in vivo remain unclear. The major replicative DNA polymerase δ (pol δ) shares two accessory subunits, called Pol31/Pol32 in yeast, with pol ζ. Inclusion of Pol31/Pol32 in the pol δ/pol ζ holoenzymes requires a [4Fe-4S] cluster in C-termini of the catalytic subunits. Disruption of this cluster in Pol ζ or deletion of POL32 attenuates induced mutagenesis. Here we describe a novel mutation affecting the catalytic subunit of pol ζ, rev3ΔC, which provides insight into the regulation of pol switches. Strains with Rev3ΔC, lacking the entire C-terminal domain and therefore the platform for Pol31/Pol32 binding, are partially proficient in Pol32-dependent UV-induced mutagenesis. This suggests an additional role of Pol32 in TLS, beyond being a pol ζ subunit, related to pol δ. In search for members of this regulatory pathway, we examined the effects of Maintenance of Genome Stability 1 (Mgs1) protein on mutagenesis in the absence of Rev3-Pol31/Pol32 interaction. Mgs1 may compete with Pol32 for binding to PCNA. Mgs1 overproduction suppresses induced mutagenesis, but had no effect on UV-mutagenesis in the rev3ΔC strain, suggesting that Mgs1 exerts its inhibitory effect by acting specifically on Pol32 bound to pol ζ. The evidence for differential regulation of Pol32 in pol δ and pol ζ emphasizes the complexity of polymerase switches.

Keywords: Mgs1; Pol32; Polymerase switch; Polymerase ζ; Translesion DNA synthesis; UV mutagenesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA Helicases / genetics
  • DNA Helicases / metabolism
  • DNA Polymerase III / genetics
  • DNA Polymerase III / metabolism*
  • DNA-Directed DNA Polymerase / genetics
  • DNA-Directed DNA Polymerase / metabolism*
  • Dose-Response Relationship, Radiation
  • Genomic Instability
  • Mutagenesis
  • Mutation
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / metabolism
  • Proliferating Cell Nuclear Antigen / metabolism
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / radiation effects
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Ubiquitination
  • Ultraviolet Rays

Substances

  • Pol32 protein, S cerevisiae
  • Proliferating Cell Nuclear Antigen
  • Saccharomyces cerevisiae Proteins
  • DNA polymerase zeta
  • Nucleotidyltransferases
  • REV1 protein, S cerevisiae
  • DNA Polymerase III
  • DNA-Directed DNA Polymerase
  • POL31 protein, S cerevisiae
  • REV3 protein, S cerevisiae
  • MGS1 protein, S cerevisiae
  • DNA Helicases