Cyclin B3 controls anaphase onset independent of spindle assembly checkpoint in meiotic oocytes

Zhang, Teng; Qi, Shu-Tao; Huang, Lin; Ma, Xue‐Shan; Ouyang, Ying‐Chun; Hou, Yi; Shen, Wei; Schatten, Heide; Sun, Qing‐Yuan

doi:10.1080/15384101.2015.1064567

Cited by 35 publications

(49 citation statements)

References 36 publications

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“…14 Our results show that inhibition of anaphase initiation accompanies the downregulation of homologous genes encoding APC Cdc20 -Esp1 and SAC protein in cyc17D cells. This finding supports previous reports that cohesion resolution is regulated by a SAC-independent pathway during meiosis, 17,37,41 and suggests that Esp1 downregulation may be responsible for the cyc17D phenotype ( Fig. 4C and 4D).…”

Section: Cyc17 Is Essential For Chromosome Segregationsupporting

confidence: 93%

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Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation inTetrahymena thermophila

et al. 2016

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Although the role of cyclins in controlling nuclear division is well established, their function in ciliate meiosis remains unknown. In ciliates, the cyclin family has undergone massive expansion which suggests that diverse cell cycle systems exist, and this warrants further investigation. A screen for cyclins in the model ciliate Tetrahymena thermophila showed that there are 34 cyclins in this organism. Only 1 cyclin, Cyc17, contains the complete cyclin core and is specifically expressed during meiosis. Deletion of CYC17 led to meiotic arrest at the diakinesis-like metaphase I stage. Expression of genes involved in DNA metabolism and chromosome organization (chromatin remodeling and basic chromosomal structure) was repressed in cyc17 knockout matings. Further investigation suggested that Cyc17 is involved in regulating spindle pole attachment, and is thus essential for chromosome segregation at meiosis. These findings suggest a simple model in which chromosome segregation is influenced by Cyc17.

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Section: Cyc17 Is Essential For Chromosome Segregationsupporting

confidence: 93%

“…36 A recent study in mice showed that Cyclin B3 controls anaphase onset in meiotic oocytes. 37 These reports suggest that Cyc17 might also be involved in meiosis in T. thermophila.…”

Section: Resultsmentioning

confidence: 97%

Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation inTetrahymena thermophila

et al. 2016

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“…CycA and CycB are required together to achieve a proper metaphase. CycB3 appears to be the major driver of anaphase, and may function in this respect by promoting APC/C activity (McCleland et al 2009; Yuan and O’Farrell 2015), a function that appears to be conserved (Deyter et al 2011; Zhang et al 2015). Therefore, the cyclins are collectively essential for mitosis but they show considerable overlap in their individual contributions.…”

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confidence: 99%

Distinct and Overlapping Requirements for Cyclins A, B, and B3 inDrosophilaFemale Meiosis

Bourouh

Dhaliwal

Rana

et al. 2016

G3 Genes|Genomes|Genetics

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Meiosis, like mitosis, depends on the activity of the cyclin dependent kinase Cdk1 and its cyclin partners. Here, we examine the specific requirements for the three mitotic cyclins, A, B, and B3 in meiosis of Drosophila melanogaster. We find that all three cyclins contribute redundantly to nuclear envelope breakdown, though cyclin A appears to make the most important individual contribution. Cyclin A is also required for biorientation of homologs in meiosis I. Cyclin B3, as previously reported, is required for anaphase progression in meiosis I and in meiosis II. We find that it also plays a redundant role, with cyclin A, in preventing DNA replication during meiosis. Cyclin B is required for maintenance of the metaphase I arrest in mature oocytes, for spindle organization, and for timely progression through the second meiotic division. It is also essential for polar body formation at the completion of meiosis. With the exception of its redundant role in meiotic maturation, cyclin B appears to function independently of cyclins A and B3 through most of meiosis. We conclude that the three mitotic cyclin-Cdk complexes have distinct and overlapping functions in Drosophila female meiosis.

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“…2009), while expression studies in mammals point to a meiosisspecific function (Nguyen et al, 2002). Interestingly, loss-offunction analysis has consistently revealed an anaphase function for cyclin B3, as both mitotic and meiotic cell cycles show a metaphase arrest (van der Voet et al, 2009;Deyter et al, 2010;Zhang et al, 2015); however, in some cases the metaphase arrest is dependent on the spindle assembly checkpoint (SAC) (Deyter et al, 2010) whereas in others it is not (Zhang et al, 2015). Even within C. elegans the exact role of CYB-3 during mitosis has been difficult to pin down.…”

Section: Discussionmentioning

confidence: 99%

“…Depletion of CYB-3 causes a more severe delay in NEB, and cells then arrest at metaphase (Cowan and Hyman, 2006;van der Voet et al, 2009;Deyter et al, 2010). Thus, as is the case for cyclin B3 proteins in other organisms (Yuan and O'Farrell, 2015;Zhang et al, 2015), CYB-3 is required to promote anaphase. Interestingly, work in C. elegans has revealed additional functions for CYB-3 prior to mitotic entry (Deyter et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Cyclin CYB-3 controls both S-phase and mitosis and is asymmetrically distributed in the early C. elegans embryo

Michael

2016

Development

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In early C. elegans embryos the timing of cell division is both invariant and developmentally regulated, yet how the cell cycle is controlled in the embryo and how cell cycle timing impacts early development remain important, unanswered questions. Here, I focus on the cyclin B3 ortholog CYB-3, and show that this cyclin has the unusual property of controlling both the timely progression through S-phase and mitotic entry, suggesting that CYB-3 is both an S-phase-promoting and mitosis-promoting factor. Furthermore, I find that CYB-3 is asymmetrically distributed in the two-cell embryo, such that the somatic precursor AB cell contains ∼2.5-fold more CYB-3 than its sister cell, the germline progenitor P 1 . CYB-3 is not only physically limited in P 1 but also functionally limited, and this asymmetry is controlled by the par polarity network. These findings highlight the importance of the CYB-3 B3-type cyclin in cell cycle regulation in the early embryo and suggest that CYB-3 asymmetry helps establish the well-documented cell cycle asynchrony that occurs during cell division within the P-lineage.

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Cyclin B3 controls anaphase onset independent of spindle assembly checkpoint in meiotic oocytes

Cited by 35 publications

References 36 publications

Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation inTetrahymena thermophila

Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation inTetrahymena thermophila

Distinct and Overlapping Requirements for Cyclins A, B, and B3 inDrosophilaFemale Meiosis

Cyclin CYB-3 controls both S-phase and mitosis and is asymmetrically distributed in the early C. elegans embryo

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