SUMO‐1 plays crucial roles for spindle organization, chromosome congression, and chromosome segregation during mouse oocyte meiotic maturation

Yuan, Yifeng; Zhai, Rui; Liu, Xiaoming; Khan, Hina; Zhen, Yan-Hong; Huo, Li‐Jun

doi:10.1002/mrd.22339

Cited by 34 publications

(35 citation statements)

References 57 publications

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“…However, SUMO is not essential for SC assembly in early pachytene in nematodes (Bhalla et al., 2008) and localizes mainly at the midbivalent, where key regulators of chromosome congression (like KLP-19) reside. As in nematodes, it has been shown in rat spermatocytes that SUMO does not co-localize with the synaptonemal complex during pachytene (Rogers et al., 2004), while depletion of SUMO or UBC9 caused abnormal spindle organization, and led to chromosome misalignment, segregation defects, and aneuploidy in rat oocytes (Yuan et al., 2014). Additionally, SUMO-1 concentrates in spindle poles and between segregating chromosomes in anaphase I, while SUMO-2/3 co-localized with condensed chromatin in mouse oocytes (Wang et al., 2010).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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SummaryDuring 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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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“…SENP1 is a protease that appears to be localized in several compartments and deconjugates a large number of SUMOylated proteins [18–20]. Recently, protein post-translational modification SUMOylation has been reported to play an important role in germ cell function, especially in mammalian meiosis [21–23]. Several studies have characterized expression of SUMO-1 and SUMO-2/3 in oocytes.…”

Section: Introductionmentioning

confidence: 99%

“…While SUMO-2/3 proteins are localized in nucleoplasm, SUMO-1 is concentrated at spindle organization and chromosome in transcriptionally active oocytes with little location on nuclear membrane in quiescent oocytes. Moreover, this specific localization of SUMO-1 plays a critical role during oocytes maturation [21–23]. It has also been reported that differential localization of SENP1 regulate SUMOylation in a temporal and spatial fashion along the oocyte meiosis procession [24, 25].…”

Section: Introductionmentioning

confidence: 99%

Stromal Senp1 promotes mouse early folliculogenesis by regulating BMP4 expression

et al. 2017

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BackgroundMammalian folliculogenesis, maturation of the ovarian follicles, require both growth factors derived from oocyte and surrounding cells, including stromal cells. However, the mechanism by which stromal cells and derived factors regulate oocyte development remains unclear.ResultsWe observed that SENP1, a small ubiquitin-related modifier (SUMO)-specific isopeptidase, was expressed in sm22α-positive stromal cells of mouse ovary. The sm22α-positive stromal cells tightly associated with follicle maturation. By using the sm22α-specific Cre system, we show that mice with a stromal cell-specific deletion of SENP1 exhibit attenuated stroma-follicle association, delayed oocyte growth and follicle maturation with reduced follicle number and size at early oocyte development, leading to premature ovarian failure at late stages of ovulating life. Mechanistic studies suggest that stromal SENP1 deficiency induces down-regulation of BMP4 in stromal cells concomitant with decreased expression of BMP4 receptor BMPR1b and BMPR2 on oocytes.ConclusionsOur data support that protein SUMOylation-regulating enzyme SENP1 plays a critical role in early ovarian follicle development by regulating gene expression of BMP4 in stroma and stroma-oocyte communication.Electronic supplementary materialThe online version of this article (doi:10.1186/s13578-017-0163-5) contains supplementary material, which is available to authorized users.

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“…The results are consistent with a missegregation of MIC chromosomes during mitosis. The requirement for SUMOylation in chromosome segregation is well established for other species (48)(49)(50)(51). In budding yeast, deletion of UBC9 results in gross defects in chromosome structure and integrity as well as aberrant segregation and polyploidy (15).…”

Section: Discussionmentioning

confidence: 99%

Depletion of UBC9 Causes Nuclear Defects during the Vegetative and Sexual Life Cycles in Tetrahymena thermophila

et al. 2015

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Ubc9p is the sole E2-conjugating enzyme for SUMOylation, and its proper function is required for regulating key nuclear events such as transcription, DNA repair, and mitosis. In Tetrahymena thermophila, the genome is separated into a diploid germ line micronucleus (MIC) that divides by mitosis and a polyploid somatic macronucleus (MAC) that divides amitotically. This unusual nuclear organization provides novel opportunities for the study of SUMOylation and Ubc9p function. We identified the UBC9 gene and demonstrated that its complete deletion from both MIC and MAC genomes is lethal. Rescue of the lethal phenotype with a GFP-UBC9 fusion gene driven by a metallothionein promoter generated a cell line with CdCl 2 -dependent expression of green fluorescent protein (GFP)-Ubc9p. Depletion of Ubc9p in vegetative cells resulted in the loss of MICs, but MACs continued to divide. In contrast, expression of catalytically inactive Ubc9p resulted in the accumulation of multiple MICs. Critical roles for Ubc9p were also identified during the sexual life cycle of Tetrahymena. Cell lines that were depleted for Ubc9p did not form mating pairs and therefore could not complete any of the subsequent stages of conjugation, including meiosis and macronuclear development. Mating between cells expressing catalytically inactive Ubc9p resulted in arrest during macronuclear development, consistent with our observation that Ubc9p accumulates in the developing macronucleus. P osttranslational modification by small ubiquitin-related modifier (SUMO) is a major regulator of protein function (reviewed in references 1-5). Unlike ubiquitin, which primarily targets proteins for proteasome-mediated degradation, SUMOylation alters the intracellular localization, protein-protein interactions, or posttranslational modifications of the target (6, 7). The importance of SUMOylation is evident from its roles in the regulation of transcription, mitosis, meiosis, and DNA damage repair (2, 8-10). The SUMO protein is expressed in known eukaryotes, and many proteins required for SUMOylation, including Ubc9p, are highly conserved from protozoa to multicellular species (8). Like ubiquitin, mature SUMO proteins are activated by a heterodimeric E1-activating enzyme (9) in an ATP-dependent reaction. Subsequently, SUMO is transferred from the E1 enzyme active-site Cys to a Cys residue-linked thioester bond in the E2 enzyme known as Ubc9p (10). In the last step, SUMO is attached to the target protein through a Lys-linked isopeptide bond. In vitro, conjugation of SUMO onto substrates can be done directly by Ubc9p; in vivo, E3 ligases increase the specificity and efficiency of the reaction (11, 12).Ubc9p is the only known SUMO E2 enzyme and therefore is a key modulator of SUMOylation. Ubc9p was first described as an essential protein for mitosis in fission yeast (13). Studies of several eukaryotes highlight its importance in multiple aspects of mitosis, including the maintenance of chromosome integrity, proper chromosome segregation, cell cycle progression, kinetochore ...

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SUMO‐1 plays crucial roles for spindle organization, chromosome congression, and chromosome segregation during mouse oocyte meiotic maturation

Cited by 34 publications

References 57 publications

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

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

Stromal Senp1 promotes mouse early folliculogenesis by regulating BMP4 expression

Depletion of UBC9 Causes Nuclear Defects during the Vegetative and Sexual Life Cycles in Tetrahymena thermophila

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