Triplex structures induce DNA double strand breaks via replication fork collapse in NER deficient cells

Nucleic Acids Res. 2016 Sep 19;44(16):7742-54. doi: 10.1093/nar/gkw515. Epub 2016 Jun 13.

Abstract

Structural alterations in DNA can serve as natural impediments to replication fork stability and progression, resulting in DNA damage and genomic instability. Naturally occurring polypurine mirror repeat sequences in the human genome can create endogenous triplex structures evoking a robust DNA damage response. Failures to recognize or adequately process these genomic lesions can result in loss of genomic integrity. Nucleotide excision repair (NER) proteins have been found to play a prominent role in the recognition and repair of triplex structures. We demonstrate using triplex-forming oligonucleotides that chromosomal triplexes perturb DNA replication fork progression, eventually resulting in fork collapse and the induction of double strand breaks (DSBs). We find that cells deficient in the NER damage recognition proteins, XPA and XPC, accumulate more DSBs in response to chromosomal triplex formation than NER-proficient cells. Furthermore, we demonstrate that XPC-deficient cells are particularly prone to replication-associated DSBs in the presence of triplexes. In the absence of XPA or XPC, deleterious consequences of triplex-induced genomic instability may be averted by activating apoptosis via dual phosphorylation of the H2AX protein. Our results reveal that damage recognition by XPC and XPA is critical to maintaining replication fork integrity and preventing replication fork collapse in the presence of triplex structures.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Cell Line
  • DNA Breaks, Double-Stranded*
  • DNA Repair*
  • DNA Replication*
  • DNA-Binding Proteins / metabolism
  • Fibroblasts / metabolism*
  • Genomic Instability
  • Mice, Transgenic
  • Nucleic Acid Conformation*
  • Oligonucleotides / chemistry
  • Phosphorylation
  • Rad51 Recombinase / metabolism
  • Replication Protein A / metabolism
  • Xeroderma Pigmentosum Group A Protein / metabolism

Substances

  • DNA-Binding Proteins
  • Oligonucleotides
  • Replication Protein A
  • Xeroderma Pigmentosum Group A Protein
  • Xpa protein, mouse
  • Xpc protein, mouse
  • Rad51 Recombinase
  • Rad51 protein, mouse