Long Neural Genes Harbor Recurrent DNA Break Clusters in Neural Stem/Progenitor Cells

Cell. 2016 Feb 11;164(4):644-55. doi: 10.1016/j.cell.2015.12.039.

Abstract

Repair of DNA double-strand breaks (DSBs) by non-homologous end joining is critical for neural development, and brain cells frequently contain somatic genomic variations that might involve DSB intermediates. We now use an unbiased, high-throughput approach to identify genomic regions harboring recurrent DSBs in primary neural stem/progenitor cells (NSPCs). We identify 27 recurrent DSB clusters (RDCs), and remarkably, all occur within gene bodies. Most of these NSPC RDCs were detected only upon mild, aphidicolin-induced replication stress, providing a nucleotide-resolution view of replication-associated genomic fragile sites. The vast majority of RDCs occur in long, transcribed, and late-replicating genes. Moreover, almost 90% of identified RDC-containing genes are involved in synapse function and/or neural cell adhesion, with a substantial fraction also implicated in tumor suppression and/or mental disorders. Our characterization of NSPC RDCs reveals a basis of gene fragility and suggests potential impacts of DNA breaks on neurodevelopment and neural functions.

Publication types

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

MeSH terms

  • Animals
  • Aphidicolin / pharmacology
  • Basic Helix-Loop-Helix Transcription Factors
  • Brain / cytology
  • Cell Adhesion
  • Cell Adhesion Molecules, Neuronal / metabolism
  • DNA Breaks* / drug effects
  • DNA End-Joining Repair
  • DNA Repair
  • GPI-Linked Proteins / metabolism
  • Genome
  • Humans
  • Mice
  • Nerve Tissue Proteins / metabolism
  • Neural Stem Cells / metabolism*
  • Synapses
  • Transcription Factors / metabolism
  • Translocation, Genetic

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Cell Adhesion Molecules, Neuronal
  • GPI-Linked Proteins
  • NPAS3 protein, human
  • Nerve Tissue Proteins
  • Transcription Factors
  • limbic system-associated membrane protein
  • Aphidicolin