Widespread changes in the posttranscriptional landscape at the Drosophila oocyte-to-embryo transition

Cell Rep. 2014 Jun 12;7(5):1495-1508. doi: 10.1016/j.celrep.2014.05.002. Epub 2014 May 29.

Abstract

The oocyte-to-embryo transition marks the onset of development. The initial phase of this profound change from the differentiated oocyte to the totipotent embryo occurs in the absence of both transcription and mRNA degradation. Here we combine global polysome profiling, ribosome-footprint profiling, and quantitative mass spectrometry in a comprehensive approach to delineate the translational and proteomic changes that occur during this important transition in Drosophila. Our results show that PNG kinase is a critical regulator of the extensive changes in the translatome, acting uniquely at this developmental window. Analysis of the proteome in png mutants provided insights into the contributions of translation to changes in protein levels, revealing a compensatory dynamic between translation and protein turnover during proteome remodeling at the return to totipotency. The proteome changes additionally suggested regulators of meiosis and early embryogenesis, including the conserved H3K4 demethylase LID, which we demonstrated is required during this period despite transcriptional inactivity.

Publication types

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

MeSH terms

  • Animals
  • Drosophila / embryology
  • Drosophila / genetics
  • Drosophila / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental*
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Oocytes / metabolism
  • Polyribosomes / metabolism
  • Protein Stability
  • Protein-Serine-Threonine Kinases / genetics
  • Protein-Serine-Threonine Kinases / metabolism
  • Proteome / genetics
  • Proteome / metabolism*
  • RNA Processing, Post-Transcriptional*
  • RNA Stability
  • RNA, Messenger / metabolism

Substances

  • Drosophila Proteins
  • Proteome
  • RNA, Messenger
  • Histone Demethylases
  • Lid protein, Drosophila
  • png protein, Drosophila
  • Protein-Serine-Threonine Kinases

Associated data

  • GEO/GSE52799