53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination

J Exp Med. 2010 Apr 12;207(4):855-65. doi: 10.1084/jem.20100244. Epub 2010 Apr 5.

Abstract

Class switch recombination (CSR) diversifies antibodies by joining highly repetitive DNA elements, which are separated by 60-200 kbp. CSR is initiated by activation-induced cytidine deaminase, an enzyme that produces multiple DNA double-strand breaks (DSBs) in switch regions. Switch regions are joined by a mechanism that requires an intact DNA damage response and classical or alternative nonhomologous end joining (A-NHEJ). Among the DNA damage response factors, 53BP1 has the most profound effect on CSR. We explore the role of 53BP1 in intrachromosomal DNA repair using I-SceI to introduce paired DSBs in the IgH locus. We find that the absence of 53BP1 results in an ataxia telangiectasia mutated-dependent increase in DNA end resection and that resected DNA is preferentially repaired by microhomology-mediated A-NHEJ. We propose that 53BP1 favors long-range CSR in part by protecting DNA ends against resection, which prevents A-NHEJ-dependent short-range rejoining of intra-switch region DSBs.

Publication types

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

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / metabolism
  • Cell Cycle Proteins / antagonists & inhibitors
  • Cell Cycle Proteins / metabolism
  • Chromosomal Proteins, Non-Histone
  • Chromosome Pairing / genetics
  • Cytidine Deaminase / genetics
  • DNA Breaks, Double-Stranded
  • DNA Repair / physiology*
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / metabolism
  • Deoxyribonucleases, Type II Site-Specific / genetics
  • Immunoglobulin Class Switching / physiology*
  • Immunoglobulin Heavy Chains / genetics
  • Integrases / genetics
  • Interleukin-4 / pharmacology
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Lipopolysaccharides / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / metabolism
  • Recombination, Genetic / physiology*
  • Tumor Suppressor Proteins / antagonists & inhibitors
  • Tumor Suppressor Proteins / metabolism
  • Tumor Suppressor p53-Binding Protein 1

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Immunoglobulin Heavy Chains
  • Intracellular Signaling Peptides and Proteins
  • Lipopolysaccharides
  • Trp53bp1 protein, mouse
  • Tumor Suppressor Proteins
  • Tumor Suppressor p53-Binding Protein 1
  • Interleukin-4
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Protein Serine-Threonine Kinases
  • Cre recombinase
  • Integrases
  • Deoxyribonucleases, Type II Site-Specific
  • AICDA (activation-induced cytidine deaminase)
  • Cytidine Deaminase