Acquisition of meiotic competence in growing mouse oocytes is controlled at both translational and posttranslational levels

Dev Biol. 1997 Jul 1;187(1):43-54. doi: 10.1006/dbio.1997.8599.

Abstract

Full-grown mouse oocytes spontaneously resume meiosis in vitro when released from their follicular environment. By contrast, growing oocytes are not competent to resume meiosis; the molecular basis of meiotic competence is not known. Entry into M phase of the eukaryotic cell cycle is controlled by MPF, a catalytically active complex comprising p34cdc2 kinase and cyclin B. Incompetent oocytes contain levels of cyclin B comparable to those in competent oocytes, while their level of p34cdc2 is markedly lower; p34cdc2 accumulates abruptly at the end of oocyte growth, at the time of meiotic competence acquisition. We show here that this change in p34cdc2 concentration is not secondary to a corresponding change in the concentration of the cognate mRNA, indicating that translational control may be involved. Microinjection of translatable p34cdc2 mRNA into incompetent oocytes yielded high levels of the protein, but it did not lead to resumption of meiosis. Similarly, microinjection of cyclin B1 mRNA resulted in accumulation of the protein, but not in the acquisition of meiotic competence. By contrast, the microinjection of both p34cdc2 and cyclin B1 mRNAs in incompetent oocytes induced histone H1 and MAP kinase activation, germinal vesicle breakdown, and entry into M-phase including the translational activation of a dormant mRNA. Thus, endogenous cyclin B1 in incompetent oocytes is not available for interaction with p34cdc2, suggesting that a posttranslational event must occur to achieve meiotic competence. Microinjection of either p34cdc2 or cyclin B1 mRNAs accelerated meiotic reinitiation of okadaic acid-treated incompetent oocytes. Taken together, these results suggest that acquisition of meiotic competence by mouse oocytes is regulated at both translational and posttranslational levels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CDC2 Protein Kinase / biosynthesis
  • CDC2 Protein Kinase / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Cell Cycle
  • Cells, Cultured
  • Cyclins / biosynthesis
  • Cyclins / metabolism*
  • Female
  • Histones / metabolism
  • Kinetics
  • Meiosis*
  • Mice
  • Oocytes / cytology*
  • Oocytes / physiology*
  • Plasmids
  • Protein Biosynthesis*
  • Protein Processing, Post-Translational*
  • RNA, Messenger / metabolism
  • Tissue Plasminogen Activator / metabolism

Substances

  • Cyclins
  • Histones
  • RNA, Messenger
  • Calcium-Calmodulin-Dependent Protein Kinases
  • CDC2 Protein Kinase
  • Tissue Plasminogen Activator