Dynamic SUMO remodeling drives a series of critical events during the meiotic divisions in Caenorhabditis elegans.
Dynamic SUMO remodeling drives a series of critical events during the meiotic divisions in Caenorhabditis elegans.
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DOI:
10.1371/journal.pgen.1007626
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发表时间:
2018-09
期刊:
影响因子:
4.5
通讯作者:
Wignall SM
中科院分区:
文献类型:
--
作者:
Davis-Roca AC;Divekar NS;Ng RK;Wignall SM
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. Most cells have two sets of chromosomes, one from each parent. Meiosis is a specialized form of cell division where chromosomes are duplicated once and segregated twice, in order to generate eggs (oocytes) or sperm with only one copy of every chromosome. This is necessary so that fertilization will produce an embryo that once again contains two complete copies of the genome. Using C. elegans as a model system, we have uncovered regulatory mechanisms important for the fidelity of these meiotic divisions. C. elegans oocytes use a kinetochore-independent chromosome segregation mechanism that relies on a large protein complex that localizes to the chromosomes. These protein complexes facilitate chromosome congression during metaphase and then are released from chromosomes in anaphase and progressively disassemble as the chromosomes segregate. We find that the stability and disassembly of these complexes is regulated by a protein modification called SUMO and by competition between enzymes that localize to the protein complex to either add or remove SUMO modifications. These findings provide insight into the mechanisms by which SUMO and SUMO enzymes regulate progression through cell division and illustrate a general strategy by which large protein complexes can be rapidly assembled and disassembled during dynamic cellular processes.
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DOI:
10.1083/jcb.200212052
发表时间:
2003-03-31
期刊:
The Journal of cell biology
影响因子:
--
作者:
Li SJ;Hochstrasser M
通讯作者:
Hochstrasser M
影响因子:
7.8
作者:
Azuma, Yoshiaki;Arnaoutov, Alexei;Dasso, Mary
通讯作者:
Dasso, Mary
DOI:
10.1083/jcb.153.6.1209
发表时间:
2001-06-11
期刊:
The Journal of cell biology
影响因子:
--
作者:
Oegema K;Desai A;Rybina S;Kirkham M;Hyman AA
通讯作者:
Hyman AA
影响因子:
4
作者:
Collette, Karishma S.;Petty, Emily L.;Csankovszki, Gyorgyi
通讯作者:
Csankovszki, Gyorgyi
影响因子:
3.3
作者:
Hayashi, Michiko;Mlynarczyk-Evans, Susanna;Villeneuve, Anne M.
通讯作者:
Villeneuve, Anne M.