Enforcing temporal control of maternal mRNA translation during oocyte cell-cycle progression

EMBO J. 2010 Jan 20;29(2):387-97. doi: 10.1038/emboj.2009.337. Epub 2009 Dec 3.

Abstract

Meiotic cell-cycle progression in progesterone-stimulated Xenopus oocytes requires that the translation of pre-existing maternal mRNAs occur in a strict temporal order. Timing of translation is regulated through elements within the mRNA 3' untranslated region (3' UTR), which respond to cell cycle-dependant signalling. One element that has been previously implicated in the temporal control of mRNA translation is the cytoplasmic polyadenylation element (CPE). In this study, we show that the CPE does not direct early mRNA translation. Rather, early translation is directed through specific early factors, including the Musashi-binding element (MBE) and the MBE-binding protein, Musashi. Our findings indicate that although the cyclin B5 3' UTR contains both CPEs and an MBE, the MBE is the critical regulator of early translation. The cyclin B2 3' UTR contains CPEs, but lacks an MBE and is translationally activated late in maturation. Finally, utilizing antisense oligonucleotides to attenuate endogenous Musashi synthesis, we show that Musashi is critical for the initiation of early class mRNA translation and for the subsequent activation of CPE-dependant mRNA translation.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Cell Cycle*
  • Cyclin B2 / metabolism
  • Cyclins / metabolism
  • Gene Expression Regulation, Developmental*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Oocytes / cytology*
  • Oogenesis
  • Polyadenylation
  • Protein Biosynthesis*
  • RNA, Messenger, Stored / genetics*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Ribonucleoproteins
  • Xenopus / metabolism*
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism

Substances

  • 3' Untranslated Regions
  • Cyclin B2
  • Cyclins
  • Nerve Tissue Proteins
  • RNA, Messenger, Stored
  • RNA-Binding Proteins
  • Ribonucleoproteins
  • Xenopus Proteins
  • ccnb2 protein, Xenopus
  • cyclin B5 protein, Xenopus
  • Msi1 protein, Xenopus