Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules

J Cell Biol. 2013 Sep 30;202(7):1041-55. doi: 10.1083/jcb.201302139. Epub 2013 Sep 23.

Abstract

Temporal control of messenger RNA (mRNA) translation is an important mechanism for regulating cellular, neuronal, and developmental processes. However, mechanisms that coordinate timing of translational activation remain largely unresolved. Full-grown oocytes arrest meiosis at prophase I and deposit dormant mRNAs. Of these, translational control of cyclin B1 mRNA in response to maturation-inducing hormone is important for normal progression of oocyte maturation, through which oocytes acquire fertility. In this study, we found that dormant cyclin B1 mRNA forms granules in the cytoplasm of zebrafish and mouse oocytes. Real-time imaging of translation revealed that the granules disassemble at the time of translational activation during maturation. Formation of cyclin B1 RNA granules requires binding of the mRNA to Pumilio1 protein and depends on actin filaments. Disruption of cyclin B1 RNA granules accelerated the timing of their translational activation after induction of maturation, whereas stabilization hindered translational activation. Thus, our results suggest that RNA granule formation is critical for the regulation of timing of translational activation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Blotting, Western
  • Cyclin B1 / genetics*
  • Cyclin B1 / metabolism
  • Cytoplasmic Granules / genetics*
  • Female
  • Gene Expression Regulation, Developmental
  • In Situ Hybridization
  • Meiosis / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Oocytes / cytology
  • Oocytes / metabolism
  • Protein Biosynthesis / physiology*
  • RNA Processing, Post-Transcriptional / physiology*
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Time Factors
  • Zebrafish

Substances

  • Cyclin B1
  • RNA, Messenger
  • RNA-Binding Proteins
  • pumilio 1 protein, mouse