Meiosis I in<i>Xenopus</i>oocytes is not error-prone despite lacking spindle assembly checkpoint

Liu, Dandan; Shao, Hua; Wang, Hongmei; Liu, X Johné

doi:10.4161/cc.28562

Cited by 6 publications

(6 citation statements)

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“…Given that MAD2 is not essential for viability in S. cerevisiae , this indicates a much greater requirement for the SAC in the accurate segregation of homologs during meiosis I than in mitosis. In contrast, Xenopus laevis oocytes have been reported to divide without being able to mount a detectable checkpoint delay, and despite this the error rate of chromosome segregation is not worse than in mammalian oocytes, which can induce a SAC delay (Shao et al, 2013 ; Liu et al, 2014 ). In Drosophila oocytes, the SAC components Mps1 and BubR1 are required for correct chromosome segregation in meiosis I (Gilliland et al, 2005 ; Malmanche et al, 2007 ), but according to one study, without detectable influence on APC/C activity (Batiha and Swan, 2012 ), and therefore potentially independently of the SAC.…”

Section: General Introduction Into Meiosismentioning

confidence: 99%

Multiple Duties for Spindle Assembly Checkpoint Kinases in Meiosis

Marston

Wassmann

2017

Front. Cell Dev. Biol.

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Cell division in mitosis and meiosis is governed by evolutionary highly conserved protein kinases and phosphatases, controlling the timely execution of key events such as nuclear envelope breakdown, spindle assembly, chromosome attachment to the spindle and chromosome segregation, and cell cycle exit. In mitosis, the spindle assembly checkpoint (SAC) controls the proper attachment to and alignment of chromosomes on the spindle. The SAC detects errors and induces a cell cycle arrest in metaphase, preventing chromatid separation. Once all chromosomes are properly attached, the SAC-dependent arrest is relieved and chromatids separate evenly into daughter cells. The signaling cascade leading to checkpoint arrest depends on several protein kinases that are conserved from yeast to man. In meiosis, haploid cells containing new genetic combinations are generated from a diploid cell through two specialized cell divisions. Though apparently less robust, SAC control also exists in meiosis. Recently, it has emerged that SAC kinases have additional roles in executing accurate chromosome segregation during the meiotic divisions. Here, we summarize the main differences between mitotic and meiotic cell divisions, and explain why meiotic divisions pose special challenges for correct chromosome segregation. The less-known meiotic roles of the SAC kinases are described, with a focus on two model systems: yeast and mouse oocytes. The meiotic roles of the canonical checkpoint kinases Bub1, Mps1, the pseudokinase BubR1 (Mad3), and Aurora B and C (Ipl1) will be discussed. Insights into the molecular signaling pathways that bring about the special chromosome segregation pattern during meiosis will help us understand why human oocytes are so frequently aneuploid.

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Section: General Introduction Into Meiosismentioning

confidence: 99%

Multiple Duties for Spindle Assembly Checkpoint Kinases in Meiosis

Marston

Wassmann

2017

Front. Cell Dev. Biol.

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“…It is possible that in such large cells the SAC cannot fully inhibit APC activity. Indeed, in Xenopus laevis eggs, which are ∼1 mm in diameter, there does not appear to be any influence of the SAC on meiotic divisions (Shao et al, 2013;Liu et al, 2014). However, SAC activity can be restored by raising the nuclear :cytoplasmic ratio by adding sperm nuclei to cytoplasmic Xenopus egg homogenates (Minshull et al, 1994).…”

Section: Introductionmentioning

confidence: 99%

Chromosome biorientation and APC activity remain uncoupled in oocytes with reduced volume

Lane

Jones

2017

Journal of Cell Biology

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“…As mentioned above, missegregation rates in mammalian oocytes are high, and therefore, the existence of the checkpoint in female meiosis has been put into question in the past. Indeed, in Xenopus laevis oocytes, the SAC does not exist, and the rate of chromosome missegregations is by far not as high as in mammalian oocytes devoid of checkpoint control (Liu et al 2014). The type of aneuploidy occurring is usually the loss of one chromosome at the first meiotic division.…”

Section: Mouse Oocytes Have a Spindle Checkpoint Too!mentioning

confidence: 97%

How oocytes try to get it right: spindle checkpoint control in meiosis

Touati

Wassmann

2015

Chromosoma

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The generation of a viable, diploid organism depends on the formation of haploid gametes, oocytes, and spermatocytes, with the correct number of chromosomes. Halving the genome requires the execution of two consecutive specialized cell divisions named meiosis I and II. Unfortunately, and in contrast to male meiosis, chromosome segregation in oocytes is error prone, with human oocytes being extraordinarily "meiotically challenged". Aneuploid oocytes, that are with the wrong number of chromosomes, give rise to aneuploid embryos when fertilized. In humans, most aneuploidies are lethal and result in spontaneous abortions. However, some trisomies survive to birth or even adulthood, such as the well-known trisomy 21, which gives rise to Down syndrome (Nagaoka et al. in Nat Rev Genet 13:493-504, 2012). A staggering 20-25 % of oocytes ready to be fertilized are aneuploid in humans. If this were not bad enough, there is an additional increase in meiotic missegregations as women get closer to menopause. A woman above 40 has a risk of more than 30 % of getting pregnant with a trisomic child. Worse still, in industrialized western societies, child birth is delayed, with women getting their first child later in life than ever. This trend has led to an increase of trisomic pregnancies by 70 % in the last 30 years (Nagaoka et al. in Nat Rev Genet 13:493-504, 2012; Schmidt et al. in Hum Reprod Update 18:29-43, 2012). To understand why errors occur so frequently during the meiotic divisions in oocytes, we review here the molecular mechanisms at works to control chromosome segregation during meiosis. An important mitotic control mechanism, namely the spindle assembly checkpoint or SAC, has been adapted to the special requirements of the meiotic divisions, and this review will focus on our current knowledge of SAC control in mammalian oocytes. Knowledge on how chromosome segregation is controlled in mammalian oocytes may help to identify risk factors important for questions related to human reproductive health.

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Meiosis I inXenopusoocytes is not error-prone despite lacking spindle assembly checkpoint

Cited by 6 publications

References 50 publications

Multiple Duties for Spindle Assembly Checkpoint Kinases in Meiosis

Multiple Duties for Spindle Assembly Checkpoint Kinases in Meiosis

Chromosome biorientation and APC activity remain uncoupled in oocytes with reduced volume

How oocytes try to get it right: spindle checkpoint control in meiosis

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