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

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

Author information

1
CIRB, Collège de France/CNRS-UMR7241/INSERM-U1050, PSL Research University, Equipe Labellisée FRM, Paris 75005, France.
2
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS/CNRS-UMR8197/INSERM-U1024, PSL Research University, Paris 75005, France.
3
Laboratory of Molecular Developmental Biology, Faculty of Biology-Oriented Science and Technology, Kindai University, Wakayama 649-6493, Japan.
4
Institute of Pharmacology, University of Freiburg, 79104 Freiburg, Germany; CIBSS - Centre for Integrative Biological Signaling Studies, University of Freiburg, 79104 Freiburg, Germany.
5
Centre de Recherche des Cordeliers, CNRS, UMRS 1138/ INSERM/ UPMC, Paris 75006, France.
6
CNRS-UMR 7600 and 8237/UPMC, Paris 75005, France.
7
Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS/CNRS-UMR8197/INSERM-U1024, PSL Research University, Paris 75005, France. Electronic address: auguste.genovesio@ens.fr.
8
CIRB, Collège de France/CNRS-UMR7241/INSERM-U1050, PSL Research University, Equipe Labellisée FRM, Paris 75005, France. Electronic address: marie-helene.verlhac@college-de-france.fr.

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

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