A nuclear pore complex‐associated regulation of SUMOylation in meiosis

Abstract

The nuclear pore complex (NPC) provides a permeable barrier between the nucleoplasm and cytoplasm. In a subset of NPC constituents that regulate meiosis in the fission yeast Schizosaccharomyces pombe, we found that nucleoporin Nup132 (homolog of human Nup133) deficiency resulted in transient leakage of nuclear proteins during meiosis I, as observed in the nup132 genedeleted mutant. The nuclear protein leakage accompanied the liberation of the small ubiquitin-like modifier (SUMO)-specific ubiquitin-like protease 1 (Ulp1) from the NPC. Ulp1 retention at the nuclear pore prevented nuclear protein leakage and restored normal meiosis in a mutant lacking Nup132. Furthermore, using mass spectrometry analysis, we identified DNA topoisomerase 2 (Top2) and RCC1-related protein (Pim1) as the target proteins for SUMOylation. SUMOylation levels of Top2 and Pim1 were altered in meiotic cells lacking Nup132. HyperSUMOylated Top2 increased the binding affinity at the centromeres of nup132 gene-deleted meiotic cells. The Top2-12KR sumoylation mutant was less localized to the centromeric regions. Our results suggest that SUMOylation of chromatin-binding proteins is regulated by the NPCbound SUMO-specific protease and is important for the progression of meiosis.

The scaffold nucleoporins SAR1 and SAR3 are essential for proper meiotic progression in Arabidopsis thaliana

“…Interestingly, SUMOylation in plants, as well as in yeast, appears to be linked to the NPC, and SUMOylated proteins accumulate in mutants defective for NUA (structural component of the nuclear basket) and SAR1 ( Muthuswamy and Meier, 2011 ). In fission yeast, the Y-complex nucleoporin Nup132 is involved in the regulation of SUMOylation during meiosis, and mutants deficient for this nucleoporin exhibit upregulated SUMOylated proteins including Pim1, Top1, and Top2 ( Yang et al, 2023 ). Hyper-SUMOylation of Top2 alters meiotic chromosome architecture ( Li et al, 2013 ).…”

Editorial: Molecular architecture and dynamics of meiotic chromosomes

“…In yeast, basket nucleoporins appear to mediate interactions of meiotic chromosomes with the NE ( Komachi and Burgess, 2022 ), and these nucleoporins undergo a dynamic reorganization during meiotic divisions ( King et al, 2023 ). NPCs also contribute to control of meiotic progression by regulation of SUMOylation ( Yang et al, 2023 ). In addition, exportin-dependent nucleocytoplasmic trafficking via NPCs also plays important meiotic roles in yeast and mammals ( Onuma et al, 2018 ; Herruzo et al, 2023 ).…”