Next-generation sequencing reveals the biological significance of the N(2),3-ethenoguanine lesion in vivo

Nucleic Acids Res. 2015 Jun 23;43(11):5489-500. doi: 10.1093/nar/gkv243. Epub 2015 Apr 2.

Abstract

Etheno DNA adducts are a prevalent type of DNA damage caused by vinyl chloride (VC) exposure and oxidative stress. Etheno adducts are mutagenic and may contribute to the initiation of several pathologies; thus, elucidating the pathways by which they induce cellular transformation is critical. Although N(2),3-ethenoguanine (N(2),3-εG) is the most abundant etheno adduct, its biological consequences have not been well characterized in cells due to its labile glycosidic bond. Here, a stabilized 2'-fluoro-2'-deoxyribose analog of N(2),3-εG was used to quantify directly its genotoxicity and mutagenicity. A multiplex method involving next-generation sequencing enabled a large-scale in vivo analysis, in which both N(2),3-εG and its isomer 1,N(2)-ethenoguanine (1,N(2)-εG) were evaluated in various repair and replication backgrounds. We found that N(2),3-εG potently induces G to A transitions, the same mutation previously observed in VC-associated tumors. By contrast, 1,N(2)-εG induces various substitutions and frameshifts. We also found that N(2),3-εG is the only etheno lesion that cannot be repaired by AlkB, which partially explains its persistence. Both εG lesions are strong replication blocks and DinB, a translesion polymerase, facilitates the mutagenic bypass of both lesions. Collectively, our results indicate that N(2),3-εG is a biologically important lesion and may have a functional role in VC-induced or inflammation-driven carcinogenesis.

Publication types

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

MeSH terms

  • DNA Adducts / chemistry
  • DNA Damage*
  • DNA Polymerase beta / metabolism
  • DNA Repair
  • DNA Repair Enzymes / metabolism
  • Dioxygenases / metabolism
  • Guanine / analogs & derivatives*
  • Guanine / chemistry
  • High-Throughput Nucleotide Sequencing
  • Mutagenesis
  • Mutation*
  • Sequence Analysis, DNA
  • Sequence Deletion

Substances

  • DNA Adducts
  • N(2),3-ethenoguanine
  • Guanine
  • Dioxygenases
  • DNA Polymerase beta
  • DNA Repair Enzymes