The Conserved ATM Kinase RAG2-S365 Phosphorylation Site Limits Cleavage Events in Individual Cells Independent of Any Repair Defect

Cell Rep. 2017 Oct 24;21(4):979-993. doi: 10.1016/j.celrep.2017.09.084.

Abstract

Many DNA lesions associated with lymphoid malignancies are linked to off-target cleavage by the RAG1/2 recombinase. However, off-target cleavage has mostly been analyzed in the context of DNA repair defects, confounding any mechanistic understanding of cleavage deregulation. We identified a conserved SQ phosphorylation site on RAG2 365 to 366 that is involved in feedback control of RAG cleavage. Mutation of serine 365 to a non-phosphorylatable alanine permits bi-allelic and bi-locus RAG-mediated breaks in the same cell, leading to reciprocal translocations. This phenomenon is analogous to the phenotype we described for ATM kinase inactivation. Here, we establish deregulated cleavage itself as a driver of chromosomal instability without the associated repair defect. Intriguingly, a RAG2-S365E phosphomimetic rescues the deregulated cleavage of ATM inactivation, reducing the incidence of reciprocal translocations. These data support a model in which feedback control of cleavage and maintenance of genome stability involves ATM-mediated phosphorylation of RAG2.

Keywords: ATM; RAG cleavage regulation; RAG2S365; V(D)J recombination; developing lymphocytes; genome stability; reciprocal translocations.

MeSH terms

  • Amino Acid Motifs
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Chromosomal Instability*
  • Conserved Sequence
  • DNA Repair
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Humans
  • Lymphocytes / metabolism
  • Mutation
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphorylation
  • Protein Processing, Post-Translational*

Substances

  • DNA-Binding Proteins
  • Nuclear Proteins
  • RAG2 protein, human
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins