Checkpoint kinase 1 is essential for meiotic cell cycle regulation in mouse oocytes

Chen, Lei; Chao, Shi Bin; Wang, Zhen Bo; Qi, Shu-Tao; Zhu, Xiu Lan; Yang, Shang Wu; Yang, Cai‐Rong; Zhang, Qing; Ouyang, Ying‐Chun; Hou, Yi; Schatten, Heide; Sun, Qing‐Yuan

doi:10.4161/cc.20279

Cited by 33 publications

(27 citation statements)

References 48 publications

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“…It has been reported that in C. cinerea, treatment of primordial caps at premeiotic S phase with hydroxyurea arrests further fruiting body development, while treatment after karyogamy at later meiotic stages also affects sporulation but still allows fruiting body maturation (Raudaskoski and Lu 1980). In animal germ cells, the ATR/CHK1 checkpoint pathway is activated during entry into meiosis (Miles et al 2010;Chen et al 2012), further supporting the idea that in C. cinerea this signaling cascade might be required in the replicative premeiotic S phase. In addition, recent work indicated the presence of checkpoint arrest in several meiotic mutants in C. cinerea (Anderson et al 2012).…”

Section: Discussionsupporting

confidence: 51%

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

et al. 2013

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The fungal fruiting body or mushroom is a multicellular structure essential for sexual reproduction. It is composed of dikaryotic cells that contain one haploid nucleus from each mating partner sharing the same cytoplasm without undergoing nuclear fusion. In the mushroom, the pileus bears the hymenium, a layer of cells that includes the specialized basidia in which nuclear fusion, meiosis, and sporulation occur. Coprinopsis cinerea is a well-known model fungus used to study developmental processes associated with the formation of the fruiting body. Here we describe that knocking down the expression of Atr1 and Chk1, two kinases shown to be involved in the response to DNA damage in a number of eukaryotic organisms, dramatically impairs the ability to develop fruiting bodies in C. cinerea, as well as other developmental decisions such as sclerotia formation. These developmental defects correlated with the impairment in silenced strains to sustain an appropriated dikaryotic cell cycle. Dikaryotic cells in which chk1 or atr1 genes were silenced displayed a higher level of asynchronous mitosis and as a consequence aberrant cells carrying an unbalanced dose of nuclei. Since fruiting body initiation is dependent on the balanced mating-type regulator doses present in the dikaryon, we believe that the observed developmental defects were a consequence of the impaired cell cycle in the dikaryon. Our results suggest a connection between the DNA damage response cascade, cell cycle regulation, and developmental processes in this fungus. IN fungal cells, mating-the process equivalent to fertilizationbrings together two haploid nuclei in the same cytoplasm. It is generally thought that this process is essentially followed by nuclear fusion, resulting in a diploid nucleus that either enters meiosis immediately (as occurs in the fission yeast Schizosaccharomyces pombe) or is maintained and proliferates in the diploid state (as happens in the budding yeast Saccharomyces cerevisiae). However, in a large number of fungi, mating does not result in diploid nuclei. Instead, they form dikaryons, cells that contain one haploid nucleus from each mating partner sharing the same cytoplasm for a period of time without undergoing nuclear fusion or meiosis. These dikaryons continue to propagate, and eventually nuclear fusion will take place, which will be followed by meiosis, closing the sexual cycle (Brown and Casselton 2001).Dikaryon cell division, also called conjugate division, represents a big challenge to the cell since it has to ensure that each daughter dikaryon inherits a balance of each parental genome. For that, a complex cell cycle is required that involves distinct mechanisms to maintain heterokaryosis after cell division. For example, for a large number of Basidiomycota (e.g., the mushroom Coprinopsis cinerea), conjugate division includes the formation of a structure known as the clamp connection or clamp cell, as well as the sorting of one of the nuclei to this structure (Casselton 1978;Brown and Casselton 2001). In the...

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Section: Discussionsupporting

confidence: 51%

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

et al. 2013

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“…17 The Chek1 kinase is mainly responding to single-strand breaks (SSBs), and overexpression of Chek1 in GV oocytes could arrest oocytes at the GV stage. 22 Goodarzi et al proposed that the DSB repair pathway was controlled by the chromatin structure. 23 However, we still do not understand SSBs in oocytes and the mechanisms by which ATM may activate Chek1.…”

Section: Discussionmentioning

confidence: 99%

The effects of DNA double-strand breaks on mouse oocyte meiotic maturation

Ouyang

Wang

et al. 2013

Cell Cycle

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“…During mitosis, γ-tubulin is a component of pericentriole material and is exclusively located at the centrosome throughout the cell cycle (Xiong et al, 2008). Spindle assembly is directed to a large extent by centrosomes, which are the main sites of microtubule polymerization during mitosis (Brunet and Maro, 2005; Chen et al, 2012). In this study, we found that when Chk2 activity was blocked, γ-tubulin localization was disrupted in spindle poles in mouse oocytes, which confirmed the role of Chk2 in spindle formation.…”

Section: Discussionmentioning

confidence: 99%

Chk2 Regulates Cell Cycle Progression during Mouse Oocyte Maturation and Early Embryo Development

Dai

Duan

Liu

et al. 2014

Molecules and Cells

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As a tumor suppressor homologue during mitosis, Chk2 is involved in replication checkpoints, DNA repair, and cell cycle arrest, although its functions during mouse oocyte meiosis and early embryo development remain uncertain. We investigated the functions of Chk2 during mouse oocyte maturation and early embryo development. Chk2 exhibited a dynamic localization pattern; Chk2 expression was restricted to germinal vesicles at the germinal vesicle (GV) stage, was associated with centromeres at pro-metaphase I (Pro-MI), and localized to spindle poles at metaphase I (MI). Disrupting Chk2 activity resulted in cell cycle progression defects. First, inhibitor-treated oocytes were arrested at the GV stage and failed to undergo germinal vesicle breakdown (GVBD); this could be rescued after Chk2 inhibition release. Second, Chk2 inhibition after oocyte GVBD caused MI arrest. Third, the first cleavage of early embryo development was disrupted by Chk2 inhibition. Additionally, in inhibitor-treated oocytes, checkpoint protein Bub3 expression was consistently localized at centromeres at the MI stage, which indicated that the spindle assembly checkpoint (SAC) was activated. Moreover, disrupting Chk2 activity in oocytes caused severe chromosome misalignments and spindle disruption. In inhibitor-treated oocytes, centrosome protein γ-tubulin and Polo-like kinase 1 (Plk1) were dissociated from spindle poles. These results indicated that Chk2 regulated cell cycle progression and spindle assembly during mouse oocyte maturation and early embryo development.

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Checkpoint kinase 1 is essential for meiotic cell cycle regulation in mouse oocytes

Cited by 33 publications

References 48 publications

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

The effects of DNA double-strand breaks on mouse oocyte meiotic maturation

Chk2 Regulates Cell Cycle Progression during Mouse Oocyte Maturation and Early Embryo Development

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