BAF-1–VRK-1 mediated release of meiotic chromosomes from the nuclear periphery is important for genome integrity

Dimitra Paouneskou, Antoine Baudrimont, Réka Kelemen, Marwan Elkrewi, Angela Graf, Shehab Moukbel Ali Aldawla, Claudia Kölbl, Irene Tiemann-Boege, Beatriz Vicoso and Verena Jantsch ()
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Dimitra Paouneskou: Vienna BioCenter, Max Perutz Labs, Department of Chromosome Biology, University of Vienna
Antoine Baudrimont: Vienna BioCenter, Max Perutz Labs, Department of Chromosome Biology, University of Vienna
Réka Kelemen: Institute of Science and Technology Austria
Marwan Elkrewi: Institute of Science and Technology Austria
Angela Graf: Vienna BioCenter, Max Perutz Labs, Department of Chromosome Biology, University of Vienna
Shehab Moukbel Ali Aldawla: Johannes Kepler University, Institute for Biophysics
Claudia Kölbl: Vienna BioCenter, Max Perutz Labs, Department of Chromosome Biology, University of Vienna
Irene Tiemann-Boege: Johannes Kepler University, Institute for Biophysics
Beatriz Vicoso: Institute of Science and Technology Austria
Verena Jantsch: Vienna BioCenter, Max Perutz Labs, Department of Chromosome Biology, University of Vienna

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: Abstract Rapid prophase chromosome movements ensure faithful alignment of the parental homologous chromosomes and successful synapsis formation during meiosis. These movements are driven by cytoplasmic forces transmitted to the nuclear periphery, where chromosome ends are attached through transmembrane proteins. During many developmental stages a specific genome architecture with chromatin nuclear periphery contacts mediates specific gene expression. Whether chromatin is removed from the nuclear periphery as a consequence of chromosome motions or by a specific mechanism is not fully understood. Here, we identify a mechanism to remove chromatin from the nuclear periphery through vaccinia related kinase (VRK-1)–dependent phosphorylation of Barrier to Autointegration Factor 1 (BAF-1) in Caenorhabditis elegans early prophase of meiosis. Interfering with chromatin removal delays chromosome pairing, impairs synapsis, produces oocytes with abnormal chromosomes and elevated apoptosis. Long read sequencing reveals deletions and duplications in offspring lacking VRK-1 underscoring the importance of the BAF-1–VRK-1 module in preserving genome stability in gametes during rapid chromosome movements.

Date: 2025
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DOI: 10.1038/s41467-025-65420-9

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