The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition

Development. 2014 Apr;141(8):1694-704. doi: 10.1242/dev.105940.

Abstract

The oocyte (maternal) nucleolus is essential for early embryonic development and embryos originating from enucleolated oocytes arrest at the 2-cell stage. The reason for this is unclear. Surprisingly, RNA polymerase I activity in nucleolus-less mouse embryos, as manifested by pre-rRNA synthesis, and pre-rRNA processing are not affected, indicating an unusual role of the nucleolus. We report here that the maternal nucleolus is indispensable for the regulation of major and minor satellite repeats soon after fertilisation. During the first embryonic cell cycle, absence of the nucleolus causes a significant reduction in major and minor satellite DNA by 12% and 18%, respectively. The expression of satellite transcripts is also affected, being reduced by more than half. Moreover, extensive chromosome bridging of the major and minor satellite sequences was observed during the first mitosis. Finally, we show that the absence of the maternal nucleolus alters S-phase dynamics and causes abnormal deposition of the H3.3 histone chaperone DAXX in pronuclei of nucleolus-less zygotes.

Keywords: Centromere; Chromosome bridging; Mice; Nucleolus precursor body; Replication stress; Satellite DNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blastocyst / cytology
  • Blastocyst / metabolism
  • Cell Nucleolus / metabolism*
  • Centromere / metabolism*
  • Chromatin Assembly and Disassembly / genetics
  • Chromosomes, Mammalian / metabolism
  • DNA Replication / genetics
  • Embryo, Mammalian / cytology*
  • Embryo, Mammalian / metabolism
  • Female
  • Genome / genetics
  • Heterochromatin / genetics
  • Male
  • Mice
  • Microsatellite Repeats / genetics*
  • Minisatellite Repeats / genetics*
  • Oocytes / cytology*
  • Oocytes / metabolism
  • RNA Precursors / genetics
  • RNA Processing, Post-Transcriptional / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Ribosomal / biosynthesis
  • RNA, Ribosomal / genetics
  • Recombination, Genetic / genetics
  • S Phase / genetics
  • Transcription, Genetic

Substances

  • Heterochromatin
  • RNA Precursors
  • RNA, Messenger
  • RNA, Ribosomal