Cytoplasmic forces functionally reorganize nuclear condensates in oocytes

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 Terret and Marie-Hélène Verlhac
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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

Nature Communications, 2022, vol. 13, issue 1, 1-19

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-32675-5

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