Active Fluctuations of the Nuclear Envelope Shape the Transcriptional Dynamics in Oocytes

Dev Cell. 2019 Oct 21;51(2):145-157.e10. doi: 10.1016/j.devcel.2019.09.010. Epub 2019 Oct 10.

Abstract

Nucleus position in cells can act as a developmental cue. Mammalian oocytes position their nucleus centrally using an F-actin-mediated pressure gradient. The biological significance of nucleus centering in mammalian oocytes being unknown, we sought to assess the F-actin pressure gradient effect on the nucleus. We addressed this using a dedicated computational 3D imaging approach, biophysical analyses, and a nucleus repositioning assay in mouse oocytes mutant for cytoplasmic F-actin. We found that the cytoplasmic activity, in charge of nucleus centering, shaped the nucleus while promoting nuclear envelope fluctuations and chromatin motion. Off-centered nuclei in F-actin mutant oocytes were misshaped with immobile chromatin and modulated gene expression. Restoration of F-actin in mutant oocytes rescued nucleus architecture fully and gene expression partially. Thus, the F-actin-mediated pressure gradient also modulates nucleus dynamics in oocytes. Moreover, this study supports a mechano-transduction model whereby cytoplasmic microfilaments could modulate oocyte transcriptome, essential for subsequent embryo development.

Keywords: F-actin; bio-physics; mechano-transduction; mouse oocyte; nuclear dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actins / metabolism
  • Animals
  • Cell Nucleus / metabolism
  • Chromatin / metabolism
  • Cytoplasm / metabolism*
  • Female
  • Male
  • Meiosis / physiology
  • Mice, Transgenic
  • Nuclear Envelope / metabolism*
  • Oocytes / metabolism*

Substances

  • Actins
  • Chromatin