The cohesion establishment factor Esco1 acetylates α-tubulin to ensure proper spindle assembly in oocyte meiosis

Lu, Yajuan; Li, Sen; Cui, Zhaokang; Dai, Xinbin; Zhang, Mianqun; Miao, Yun; Zhou, Changyin; Ou, Xiang‐Hong; Xiong, Bo

doi:10.1093/nar/gky001

Cited by 32 publications

(31 citation statements)

References 41 publications

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“…Our previous studies reported that cohesin establishment factors, Esco1 and Esco2, regulate distinct functions during oocyte meiosis. Esco1 acetylates -tubulin to ensure microtubule stability to promote spindle assembly (42). Esco2 maintains H4K16 acetylation to participate in kinetochore functions for the SAC activity (43).…”

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confidence: 99%

The cohesin release factor Wapl interacts with Bub3 to govern SAC activity in female meiosis I

et al. 2020

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During mitotic prophase, cohesins are removed from chromosome arms by Wapl to ensure faithful sister chromatid separation. However, during female meiosis I, the resolution of chiasmata requires the proteolytic cleavage of cohesin subunit Rec8 along chromosome arms by Separase to separate homologs, and thus the role of Wapl remained unknown. Here, we report that Wapl functions as a regulator of spindle assembly checkpoint (SAC) to prevent aneuploidy in meiosis I. Depletion of Wapl accelerates meiotic progression, inactivates SAC, and causes meiotic defects such as aberrant spindle/chromosome structure and incorrect kinetochore-microtubule (K-MT) attachment, consequently leading to aneuploid eggs. Notably, we identify Bub3 as a binding partner of Wapl by immunoprecipitation and mass spectrometry analysis. We further determine that Wapl controls the SAC activity by maintaining Bub3 protein level and document that exogenous Bub3 restores the normal meiosis in Wapl-depleted oocytes. Together, our findings uncover unique, noncanonical roles for Wapl in mediating control of the SAC in female meiosis I.

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confidence: 99%

The cohesin release factor Wapl interacts with Bub3 to govern SAC activity in female meiosis I

et al. 2020

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“…For example, HDAC3 has been reported to affect the meiotic apparatus assembly by regulation of tubulin acetylation in mouse oocytes [ 15 ]. In addition, Esco1, which is involved in sister chromatid cohesion, acetylates α-tubulin to promote proper spindle assembly in meiosis [ 18 ]. In our study, we observed that a big proportion of spindle structure was destroyed after Kif18a KD, which correlated with a high tubulin acetylation level in comparison with the control oocytes.…”

Section: Discussionmentioning

confidence: 99%

Kif18a regulates Sirt2-mediated tubulin acetylation for spindle organization during mouse oocyte meiosis

et al. 2018

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BackgroundDuring oocyte meiosis, the cytoskeleton dynamics, especially spindle organization, are critical for chromosome congression and segregation. However, the roles of the kinesin superfamily in this process are still largely unknown.ResultsIn the present study, Kif18a, a member of the kinesin-8 family, regulated spindle organization through its effects on tubulin acetylation in mouse oocyte meiosis. Our results showed that Kif18a is expressed and mainly localized in the spindle region. Knock down of Kif18a caused the failure of first polar body extrusion, dramatically affecting spindle organization and resulting in severe chromosome misalignment. Further analysis showed that the disruption of Kif18a caused an increase in acetylated tubulin level, which might be the reason for the spindle organization defects after Kif18a knock down in oocyte meiosis, and the decreased expression of deacetylase Sirt2 was found after Kif18a knock down. Moreover, microinjections of tubulin K40R mRNA, which could induce tubulin deacetylation, protected the oocytes from the effects of Kif18a downregulation, resulting in normal spindle morphology in Kif18a-knock down oocytes.ConclusionsTaken together, our results showed that Kif18a affected Sirt2-mediated tubulin acetylation level for spindle organization during mouse oocyte meiosis. Our results not only revealed the critical effect of Kif18a on microtubule stability, but also extended our understanding of kinesin activity in meiosis.

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“…Moreover, tubulin acetylation exists primarily for spindle stability in oocytes and embryos (de Pennart et al, ). It was also shown that decline in α‐tubulin acetylation resulted in fewer long‐lived RPE cell microtubules (Xu et al, ) and caused defective spindle assemblies and misaligned chromosomes in mouse oocytes (Lu et al, ). Our recent study showed that the KIF4a knockdown affected tubulin acetylation levels in mouse oocytes (Tang et al, ).…”

Section: Discussionmentioning

confidence: 99%

Meiotic arrest and spindle defects are associated with altered KIF11 expression in porcine oocytes

Wan

Lan

Pan

et al. 2018

Environ and Mol Mutagen

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Kinesin superfamily proteins (KIFs) act as molecular motors and are involved in material transport along microtubules to maintain normal cellular functions. KIF11 (also named kinesin-5, Eg5, and KSP) is a plus-end-directed homotetrameric kinesin that regulates spindle formation for actuate chromosomal separation during mitosis. However, the roles of KIF11 in meiosis are still unclear. In this study, we investigated the regulatory functions of KIF11 during porcine oocyte maturation. The results indicated that KIF11 was expressed in different stages during porcine oocyte meiosis. Inhibition of KIF11 activity led to the failure of the first polar body extrusion, and we found that cell cycle progression was disturbed, which was confirmed by the decreased Cdc2 expression. Furthermore, inhibition of KIF11 resulted in decreased tubulin acetylation and caused sequential disruption of the spindle assembly and chromosome alignment. We also found that in postovulatory aging porcine oocytes, the KIF11 expression was altered, indicating that KIF11 was involved with aging-induced spindle disorganization. In summary, our results showed that KIF11 regulated the cell cycle and tubulin acetylation related spindle formation in porcine oocyte meiosis. Environ. Mol. Mutagen. 59:805-812, 2018. © 2018 Wiley Periodicals, Inc.

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The cohesion establishment factor Esco1 acetylates α-tubulin to ensure proper spindle assembly in oocyte meiosis

Cited by 32 publications

References 41 publications

The cohesin release factor Wapl interacts with Bub3 to govern SAC activity in female meiosis I

The cohesin release factor Wapl interacts with Bub3 to govern SAC activity in female meiosis I

Kif18a regulates Sirt2-mediated tubulin acetylation for spindle organization during mouse oocyte meiosis

Meiotic arrest and spindle defects are associated with altered KIF11 expression in porcine oocytes

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