Dynamic SUMO remodeling drives a series of critical events during the meiotic divisions in Caenorhabditis elegans.

Amanda C Davis-Roca,Rachel K Ng,Sarah M Wignall,Nikita S Divekar,Scott Keeney

doi:10.1371/journal.pgen.1007626

Abstract

Chromosome congression and segregation in C. elegans oocytes depend on a complex of conserved proteins that forms a ring around the center of each bivalent during prometaphase; these complexes are then removed from chromosomes at anaphase onset and disassemble as anaphase proceeds. Here, we uncover mechanisms underlying the dynamic regulation of these ring complexes (RCs), revealing a strategy by which protein complexes can be progressively remodeled during cellular processes. We find that the assembly, maintenance, and stability of RCs is regulated by a balance between SUMO conjugating and deconjugating activity. During prometaphase, the SUMO protease ULP-1 is targeted to the RCs but is counteracted by SUMO E2/E3 enzymes; then in early anaphase the E2/E3 enzymes are removed, enabling ULP-1 to trigger RC disassembly and completion of the meiotic divisions. Moreover, we found that SUMO regulation is essential to properly connect the RCs to the chromosomes and then also to fully release them in anaphase. Altogether, our work demonstrates that dynamic remodeling of SUMO modifications facilitates key meiotic events and highlights how competition between conjugation and deconjugation activity can modulate SUMO homeostasis, protein complex stability, and ultimately, progressive processes such as cell division.

Highlights

Meiosis is a specialized form of cell division where chromosomes are duplicated once and segregated twice, in order to reduce the chromosome number by half to generate haploid gametes
C. elegans oocytes use a kinetochore-independent chromosome segregation mechanism that relies on a large protein complex that localizes to the chromosomes
We found that SUMO is present on the ring complexes (RCs) after nuclear envelope breakdown (NEBD) and by late anaphase had relocalized to spindle microtubules

Summary

Introduction

Meiosis is a specialized form of cell division where chromosomes are duplicated once and segregated twice, in order to reduce the chromosome number by half to generate haploid gametes. The exact mechanism driving chromosome segregation remains controversial, it is clear that both congression and segregation depend upon a large protein complex that forms a ring around the center of each bivalent in Meiosis I (MI) and around the sister chromatid interface in Meiosis II (MII). These ring complexes (RCs) are comprised of a number of conserved cell division proteins, including the Chromosome Passenger Complex/ CPC (containing AIR-2/Aurora B kinase, ICP-1, CSC-1, and BIR-1), the kinesin-4 family motor KLP-19 [1], and the kinase BUB-1 [2]. Understanding how the RC assembles and is regulated will provide valuable insights into how chromosomes are accurately partitioned in oocytes

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