The DNA Damage Checkpoint Eliminates Mouse Oocytes with Chromosome Synapsis Failure

Mol Cell. 2017 Sep 21;67(6):1026-1036.e2. doi: 10.1016/j.molcel.2017.07.027. Epub 2017 Aug 24.

Abstract

Pairing and synapsis of homologous chromosomes during meiosis is crucial for producing genetically normal gametes and is dependent upon repair of SPO11-induced double-strand breaks (DSBs) by homologous recombination. To prevent transmission of genetic defects, diverse organisms have evolved mechanisms to eliminate meiocytes containing unrepaired DSBs or unsynapsed chromosomes. Here we show that the CHK2 (CHEK2)-dependent DNA damage checkpoint culls not only recombination-defective mouse oocytes but also SPO11-deficient oocytes that are severely defective in homolog synapsis. The checkpoint is triggered in oocytes that accumulate a threshold level of spontaneous DSBs (∼10) in late prophase I, the repair of which is inhibited by the presence of HORMAD1/2 on unsynapsed chromosome axes. Furthermore, Hormad2 deletion rescued the fertility of oocytes containing a synapsis-proficient, DSB repair-defective mutation in a gene (Trip13) required for removal of HORMADs from synapsed chromosomes, suggesting that many meiotic DSBs are normally repaired by intersister recombination in mice.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities
  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • Animals
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cell Death
  • Checkpoint Kinase 2 / genetics
  • Checkpoint Kinase 2 / metabolism*
  • Chromosome Pairing*
  • DNA Damage*
  • Endodeoxyribonucleases / deficiency
  • Endodeoxyribonucleases / genetics
  • Female
  • Fertility
  • Genotype
  • Infertility, Female / enzymology
  • Infertility, Female / genetics
  • Infertility, Female / pathology
  • Meiosis*
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Oocytes / enzymology*
  • Oocytes / pathology
  • Pachytene Stage
  • Phenotype
  • Recombinational DNA Repair
  • Time Factors
  • Tissue Culture Techniques

Substances

  • Cell Cycle Proteins
  • HORMAD2 protein, mouse
  • Nohma protein, mouse
  • Checkpoint Kinase 2
  • Chek2 protein, mouse
  • Endodeoxyribonucleases
  • meiotic recombination protein SPO11
  • Adenosine Triphosphatases
  • ATPases Associated with Diverse Cellular Activities
  • Trip13 protein, mouse