The Impact of Minor-Groove N2-Alkyl-2'-deoxyguanosine Lesions on DNA Replication in Human Cells

ACS Chem Biol. 2019 Aug 16;14(8):1708-1716. doi: 10.1021/acschembio.9b00129. Epub 2019 Aug 1.

Abstract

Endogenous metabolites and exogenous chemicals can induce covalent modifications on DNA, producing DNA lesions. The N2 of guanine was shown to be a common alkylation site in DNA; however, not much is known about the influence of the size of the alkyl group in N2-alkyldG lesions on cellular DNA replication or how translesion synthesis (TLS) polymerases modulate DNA replication past these lesions in human cells. To answer these questions, we employ a robust shuttle vector method to investigate the impact of four N2-alkyldG lesions (i.e., with the alkyl group being a methyl, ethyl, n-propyl, or n-butyl group) on DNA replication in human cells. We find that replication through the N2-alkyldG lesions was highly efficient and accurate in HEK293T cells or isogenic CRISPR-engineered cells with deficiency in polymerase (Pol) ζ or Pol η. Genetic ablation of Pol ι, Pol κ, or Rev1, however, results in decreased bypass efficiencies and elicits substantial frequencies of G → A transition and G → T transversion mutations for these lesions. Moreover, further depletion of Pol ζ in Pol κ- or Pol ι-deficient cells gives rise to elevated rates of G → A and G → T mutations and substantially decreased bypass efficiencies. Cumulatively, we demonstrate that the error-free replication past the N2-alkyldG lesions is facilitated by a specific subset of TLS polymerases, and we find that longer alkyl chains in these lesions induce diminished bypass efficiency and fidelity in DNA replication.

Publication types

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

MeSH terms

  • Alkylation
  • DNA / genetics
  • DNA / metabolism*
  • DNA Damage
  • DNA Repair
  • DNA Replication / drug effects*
  • DNA-Directed DNA Polymerase / physiology
  • Deoxyguanosine / analogs & derivatives*
  • Deoxyguanosine / metabolism*
  • Deoxyguanosine / toxicity
  • HEK293 Cells
  • Humans
  • Molecular Structure
  • Mutation
  • Nucleic Acid Conformation

Substances

  • DNA
  • DNA-Directed DNA Polymerase
  • Deoxyguanosine