5-Formylcytosine mediated DNA-protein cross-links block DNA replication and induce mutations in human cells

Nucleic Acids Res. 2018 Jul 27;46(13):6455-6469. doi: 10.1093/nar/gky444.

Abstract

5-Formylcytosine (5fC) is an epigenetic DNA modification introduced via TET protein-mediated oxidation of 5-methyl-dC. We recently reported that 5fC form reversible DNA-protein conjugates (DPCs) with histone proteins in living cells (Ji et al. (2017) Angew. Chem. Int. Ed., 56:14130-14134). We now examined the effects of 5fC mediated DPCs on DNA replication. Synthetic DNA duplexes containing site-specific DPCs between 5fC and lysine-containing proteins and peptides were subjected to primer extension experiments in the presence of human translesion synthesis DNA polymerases η and κ. We found that DPCs containing histones H2A or H4 completely inhibited DNA replication, but the replication block was removed when the proteins were subjected to proteolytic digestion. Cross-links to 11-mer or 31-mer peptides were bypassed by both polymerases in an error-prone manner, inducing targeted C→T transitions and -1 deletions. Similar types of mutations were observed when plasmids containing 5fC-peptide cross-links were replicated in human embryonic kidney (HEK) 293T cells. Molecular simulations of the 11-mer peptide-dC cross-links bound to human polymerases η and κ revealed that the peptide fits well on the DNA major groove side, and the modified dC forms a stable mismatch with incoming dATP via wobble base pairing in the polymerase active site.

Publication types

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

MeSH terms

  • Cytosine / analogs & derivatives*
  • Cytosine / chemistry
  • DNA / chemistry*
  • DNA Replication*
  • DNA-Directed DNA Polymerase / metabolism
  • HEK293 Cells
  • Histones
  • Humans
  • Molecular Dynamics Simulation
  • Mutation*
  • Peptides

Substances

  • 5-formylcytosine
  • Histones
  • Peptides
  • Cytosine
  • DNA
  • DNA-Directed DNA Polymerase