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

M. Almonacid , A. Al Jord , S. El-Hayek , A. Othmani , F. Coulpier , S. Lemoine , K. Miyamoto , R. Grosse , C. Klein , T. Piolot , P. Mailly , R. Voituriez , A. Genovesio , M.H. Verlhac

Bibtex , URL
Dev. Cell, 51, 2
Published 21 Oct. 2019
DOI: 10.1016/j.devcel.2019.09.010
ISSN: 1534-5807

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.