Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links

Oncogene. 2008 Aug 28;27(37):5045-56. doi: 10.1038/onc.2008.139. Epub 2008 May 12.

Abstract

The removal of DNA interstrand cross-links (ICLs) has proven to be notoriously complicated due to the involvement of multiple pathways of DNA repair, which include the Fanconi anemia/BRCA pathway, homologous recombination and components of the nucleotide excision and mismatch repair pathways. Members of the SNM1 gene family have also been shown to have a role in mediating cellular resistance to ICLs, although their precise function has remained elusive. Here, we show that knockdown of Snm1B/Apollo in human cells results in hypersensitivity to mitomycin C (MMC), but not to IR. We also show that Snm1B-deficient cells exhibit a defective S phase checkpoint in response to MMC, but not to IR, and this finding may account for the specific sensitivity to the cross-linking drug. Interestingly, although previous studies have largely implicated ATR as the major kinase activated in response to ICLs, we show that it is activation of the ATM-mediated checkpoint that is defective in Snm1B-deficient cells. The requirement for Snm1B in ATM checkpoint activation specifically after ICL damage is correlated with its role in promoting double-strand break formation, and thus replication fork collapse. Consistent with this result Snm1B was found to interact directly with Mus81-Eme1, an endonuclease previously implicated in fork collapse. In addition, we also show that Snm1B interacts with the Mre11-Rad50-Nbs1 (MRN) complex and with FancD2 further substantiating its role as a checkpoint/DNA repair protein.

Publication types

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

MeSH terms

  • Acid Anhydride Hydrolases
  • Cell Cycle Proteins / metabolism
  • Cells, Cultured
  • Cross-Linking Reagents / toxicity*
  • DNA Damage*
  • DNA Repair / genetics*
  • DNA Repair Enzymes / metabolism
  • DNA Repair Enzymes / physiology*
  • DNA Replication / genetics*
  • DNA-Binding Proteins / metabolism
  • Exodeoxyribonucleases
  • Fanconi Anemia Complementation Group D2 Protein / metabolism
  • Genes, cdc / physiology
  • Humans
  • MRE11 Homologue Protein
  • Models, Biological
  • Multiprotein Complexes / metabolism
  • Nuclear Proteins / metabolism
  • Nuclear Proteins / physiology*
  • Protein Binding
  • S Phase / genetics*

Substances

  • Cell Cycle Proteins
  • Cross-Linking Reagents
  • DNA-Binding Proteins
  • FANCD2 protein, human
  • Fanconi Anemia Complementation Group D2 Protein
  • MRE11 protein, human
  • Multiprotein Complexes
  • NBN protein, human
  • Nuclear Proteins
  • DCLRE1B protein, human
  • Exodeoxyribonucleases
  • MRE11 Homologue Protein
  • Acid Anhydride Hydrolases
  • RAD50 protein, human
  • DNA Repair Enzymes