4.8 Article

Cytoplasmic forces functionally reorganize nuclear condensates in oocytes

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NATURE COMMUNICATIONS
卷 13, 期 1, 页码 -

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NATURE PORTFOLIO
DOI: 10.1038/s41467-022-32675-5

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资金

  1. CNRS
  2. INSERM
  3. College de France
  4. Bettencourt Schueller Foundation
  5. program much less than Investissements d'Avenir much greater than
  6. ANR [ANR-10-LABX54 MEMO LIFE, ANR-11-IDEX-0001-02 PSL, ANR-11LABX0038, ANR-10-IDEX-0001-02, ANR-18CE13, ANR-16-CE13, ANR-15-CE13-0001-01]
  7. Fondation pour la Recherche Medicale [DEQ201903007796, DEQ20160334884]
  8. Institut Curie
  9. ARC fellowship
  10. ARC [PDF2017050561]
  11. Labex Memolife 2.0
  12. Labex Memolife 2.0, Fonds Saint-Michel
  13. Fondation du College de France
  14. Agence Nationale de la Recherche (ANR) [ANR-15-CE13-0001] Funding Source: Agence Nationale de la Recherche (ANR)

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Cells can regulate the function of nuclear condensates through the use of cytoplasmic forces generated by cytoskeletal motors. This finding has implications for understanding and studying diseases associated with nuclear condensates.
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. Cytoskeletal activity generates mechanical forces known to agitate and displace membrane-bound organelles in the cytoplasm. In oocytes, Al Jord et al. discover that these cytoplasmic forces functionally remodel nuclear RNA-processing condensates across scales for developmental success.

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