A SUMO-Dependent Protein Network Regulates Chromosome Congression during Oocyte Meiosis

Summary

During Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localized between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC, and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO interaction motifs (SIMs), allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus, dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.

Graphical Abstract

Highlights

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  SUMO conjugates accumulate in the ring complex within the midbivalent during meiosis

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  Ring complex assembly requires active sumoylation

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  The SUMO E3 ligase GEI-17/PIAS sumoylates the chromokinesin KLP-19 in vivo and in vitro

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  Meiotic chromosome congression depends on sumoylation and non-covalent SUMO binding

Abstract

Pelisch et al. provide evidence that highly dynamic, coordinated, and spatially constrained sumoylation regulates chromosome congression during meiosis in C. elegans oocytes.