Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification

J Exp Med. 2002 Aug 19;196(4):469-80. doi: 10.1084/jem.20020851.

Abstract

Nonreciprocal translocations and gene amplifications are commonly found in human tumors. Although little is known about the mechanisms leading to such aberrations, tissue culture models predict that they can arise from DNA breakage, followed by cycles of chromatid fusion, asymmetric mitotic breakage, and replication. Mice deficient in both a nonhomologous end joining (NHEJ) DNA repair protein and the p53 tumor suppressor develop lymphomas at an early age harboring amplification of an IgH/c-myc fusion. Here we report that these chromosomal rearrangements are initiated by a recombination activating gene (RAG)-induced DNA cleavage. Subsequent DNA repair events juxtaposing IgH and c-myc are mediated by a break-induced replication pathway. Cycles of breakage-fusion-bridge result in amplification of IgH/c-myc while chromosome stabilization occurs through telomere capture. Thus, mice deficient in NHEJ provide excellent models to study the etiology of unbalanced translocations and amplification events during tumorigenesis.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigens, Nuclear*
  • Base Sequence
  • DNA Damage*
  • DNA Helicases*
  • DNA Repair*
  • DNA Replication*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Gene Amplification
  • Gene Rearrangement
  • Immunoglobulin Heavy Chains / genetics*
  • Ku Autoantigen
  • Lymphoma, B-Cell / genetics*
  • Mice
  • Mice, Knockout
  • Mice, SCID
  • Molecular Sequence Data
  • Nuclear Proteins / genetics
  • Nuclear Proteins / physiology
  • Oncogenes
  • Proto-Oncogene Proteins c-myc / genetics*
  • Telomere
  • Thymus Neoplasms / genetics*
  • Translocation, Genetic*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / physiology

Substances

  • Antigens, Nuclear
  • DNA-Binding Proteins
  • Immunoglobulin Heavy Chains
  • Nuclear Proteins
  • Proto-Oncogene Proteins c-myc
  • Rag2 protein, mouse
  • Tumor Suppressor Protein p53
  • V(D)J recombination activating protein 2
  • DNA Helicases
  • XRCC5 protein, human
  • Xrcc6 protein, human
  • Xrcc6 protein, mouse
  • Ku Autoantigen