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Cytoplasmic forces functionally reorganize nuclear condensates in oocytes

Author

Listed:
  • Adel Al Jord

    (Université PSL)

  • Gaëlle Letort

    (Université PSL)

  • Soline Chanet

    (Université PSL)

  • Feng-Ching Tsai

    (Université PSL)

  • Christophe Antoniewski

    (Sorbonne Université, Institut Français de Bioinformatique)

  • Adrien Eichmuller

    (Université PSL)

  • Christelle Da Silva

    (Université PSL)

  • Jean-René Huynh

    (Université PSL)

  • Nir S. Gov

    (Weizmann Institute of Science)

  • Raphaël Voituriez

    (Sorbonne Université)

  • Marie-Émilie Terret

    (Université PSL)

  • Marie-Hélène Verlhac

    (Université PSL)

Abstract

Cells remodel their cytoplasm with force-generating cytoskeletal motors. Their activity generates random forces that stir the cytoplasm, agitating and displacing membrane-bound organelles like the nucleus in somatic and germ cells. These forces are transmitted inside the nucleus, yet their consequences on liquid-like biomolecular condensates residing in the nucleus remain unexplored. Here, we probe experimentally and computationally diverse nuclear condensates, that include nuclear speckles, Cajal bodies, and nucleoli, during cytoplasmic remodeling of female germ cells named oocytes. We discover that growing mammalian oocytes deploy cytoplasmic forces to timely impose multiscale reorganization of nuclear condensates for the success of meiotic divisions. These cytoplasmic forces accelerate nuclear condensate collision-coalescence and molecular kinetics within condensates. Disrupting the forces decelerates nuclear condensate reorganization on both scales, which correlates with compromised condensate-associated mRNA processing and hindered oocyte divisions that drive female fertility. We establish that cytoplasmic forces can reorganize nuclear condensates in an evolutionary conserved fashion in insects. Our work implies that cells evolved a mechanism, based on cytoplasmic force tuning, to functionally regulate a broad range of nuclear condensates across scales. This finding opens new perspectives when studying condensate-associated pathologies like cancer, neurodegeneration and viral infections.

Suggested Citation

  • Adel Al Jord & Gaëlle Letort & Soline Chanet & Feng-Ching Tsai & Christophe Antoniewski & Adrien Eichmuller & Christelle Da Silva & Jean-René Huynh & Nir S. Gov & Raphaël Voituriez & Marie-Émilie Terr, 2022. "Cytoplasmic forces functionally reorganize nuclear condensates in oocytes," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32675-5
    DOI: 10.1038/s41467-022-32675-5
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    References listed on IDEAS

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