Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations

Cell. 2002 Jun 28;109(7):811-21. doi: 10.1016/s0092-8674(02)00770-5.

Abstract

Amplification of large genomic regions associated with complex translocations (complicons) is a basis for tumor progression and drug resistance. We show that pro-B lymphomas in mice deficient for both p53 and nonhomologous end-joining (NHEJ) contain complicons that coamplify c-myc (chromosome 15) and IgH (chromosome 12) sequences. While all carry a translocated (12;15) chromosome, coamplified sequences are located within a separate complicon that often involves a third chromosome. Complicon formation is initiated by recombination of RAG1/2-catalyzed IgH locus double-strand breaks with sequences downstream of c-myc, generating a dicentric (15;12) chromosome as an amplification intermediate. This recombination event employs a microhomology-based end-joining repair pathway, as opposed to classic NHEJ or homologous recombination. These findings suggest a general model for oncogenic complicon formation.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Chromosomes / genetics
  • DNA Damage / genetics*
  • DNA Repair*
  • Gene Amplification / genetics*
  • Gene Expression Regulation, Neoplastic
  • Genes, RAG-1
  • Genes, myc / genetics*
  • In Situ Hybridization, Fluorescence
  • Lymphoma, B-Cell / genetics
  • Mice
  • Molecular Sequence Data
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Recombination, Genetic / genetics
  • Translocation, Genetic / genetics*
  • Tumor Suppressor Protein p53 / deficiency*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • RNA, Messenger
  • Tumor Suppressor Protein p53