Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts

Iwabuchi, Masaki; Ohsumi, Keita; Yamamoto, Tomomi M.; Sawada, Wako; Kishimoto, Takeo

doi:10.1093/emboj/19.17.4513

Cited by 102 publications

(89 citation statements)

References 44 publications

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“…Xenopus laevis oocytes at stages I and VI (23) were obtained, and meiosis was resumed as described (24). To determine the meiotic stage of maturing oocytes after germinal vesicle breakdown (GVBD), oocytes were fixed and stained with 3.7% formaldehyde in MMR (100 mM NaCl͞2 mM KCl͞1 mM MgCl 2 ͞2 mM CaCl 2 ͞0.1 mM EDTA͞5 mM Hepes-KOH, pH 7.8) (25) containing 10 g͞ml Hoechst 33342, and their chromosomes at the animal pole region were observed through an epifluorescence microscope.…”

Section: Methodsmentioning

confidence: 99%

“…Interphase egg extracts were prepared by adding 0.4 mM CaCl 2 along with 50 g͞ml cycloheximide to CSF-arrested extracts and subsequently incubating for 30 min at 22°C. Mitotic cycling extracts were prepared according to Murray (27) with modifications as described (24). Demembranated sperm nuclei were added to all extracts to monitor the cell cycle phase (24).…”

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest

Ohsumi

Koyanagi

Yamamoto

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Oocytes of most vertebrates arrest at metaphase of the second meiosis (meta-II) to await fertilization, thus preventing parthenogenetic activation. This arrest is caused by a cytoplasmic activity called cytostatic factor (CSF), which was first identified in the frog Rana pipiens oocyte >30 years ago. CSF arrest is executed by maintaining the activity of cyclin B-Cdc2 at elevated levels largely through prevention of cyclin B destruction. Although CSF arrest is established by the Mos-mitogen-activated protein kinase pathway and is released by the Ca-calmodulin kinase II pathway, it remains unclear precisely how cyclin B destruction is regulated. Recently, an early mitotic inhibitor, Emi1, was reported to be a critical component of CSF. This report has been expected to provide a final resolution to the CSF problem because Emi1 inhibits the anaphasepromoting complex͞cyclosome, a ubiquitin ligase for cyclin B destruction, through sequestration of Cdc20, an activator for the anaphase-promoting complex͞cyclosome. In mitotic cycles, however, Emi1 is destroyed in every pro-metaphase, and accordingly, it is unclear why Emi1 should be required for CSF activity, which is seen only in meta-II. Here, we show that Emi1 is absent in unfertilized mature Xenopus eggs and that exogenous Emi1 is destroyed in meta-II and mitotic metaphase. The expression of Emi1 in oocytes hinders meiotic progression. Although both Emi1 and Mos can inhibit progression through M phase, the Emi1-mediated arrest does not require mitogen-activated protein kinase activity and is not released by Ca. Together, our results indicate that Emi1 is unlikely to be a component of CSF.M eiosis is comprised of two consecutive M phases, meiosis I and II, which result in the production of haploid gametes. In most metazoan oocytes, the cell cycle arrests twice during meiosis. The first arrest occurs at prophase of meiosis I and its resumption is generally controlled by a maturation-inducing hormone. The second arrest occurs after the hormone-initiated meiotic resumption but before fertilization. Because failure in the second arrest often leads to initiation of embryonic cell cycles in the absence of fertilization, the second arrest is implicated in the prevention of parthenogenesis (see ref. 1 for review). In most vertebrates, the second arrest is at metaphase of the second meiosis (meta-II), and the activity responsible for the meta-II arrest has been termed cytostatic factor (CSF) (see ref.2 for review), whose essential components are Mos (3) and the downstream effector, mitogen-activated protein kinase (MAPK) (4, 5). Although CSF was originally defined in the meta-II arrest of amphibian Rana pipiens oocytes (6), the same Mos-MAPK pathway causes the second arrest at G 1 phase after completion of meiosis II in starfish Asterina pectinifera eggs (7), and MAPK is responsible for preventing DNA replication in unfertilized sea urchin eggs arrested at the G 1 phase (8). Consequently, CSF can be considered as a cell cycle arrest factor that prevents parthenogenetic activat...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest

Ohsumi

Koyanagi

Yamamoto

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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“…It is generally accepted that Mos is required for the MI-MII transition (Kanki and Donoghue, 1991;Hashimoto et al, 1994;Dupre et al, 2002) because ablation of Mos translation clearly results in a failure of MII entry (and a consequent artificial interphase). Moreover, maintaining residual Cdc2 kinase activity at MI exit is necessary, as complete inhibition, either by chemical inhibitors or by overexpression of the inhibitory kinase Wee l promotes an artificial interphase (Iwabuchi et al, 2000). One unsettled question, however, concerns the role of the APC in the MI-MII transition.…”

Section: Introductionmentioning

confidence: 99%

Cdc2 and Mos Regulate Emi2 Stability to Promote the Meiosis I–Meiosis II Transition

Tang

Guo

et al. 2008

MBoC

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The transition of oocytes from meiosis I (MI) to meiosis II (MII) requires partial cyclin B degradation to allow MI exit without S phase entry. Rapid reaccumulation of cyclin B allows direct progression into MII, producing a cytostatic factor (CSF)-arrested egg. It has been reported that dampened translation of the anaphase-promoting complex (APC) inhibitor Emi2 at MI allows partial APC activation and MI exit. We have detected active Emi2 translation at MI and show that Emi2 levels in MI are mainly controlled by regulated degradation. Emi2 degradation in MI depends not on Ca2+/calmodulin-dependent protein kinase II (CaMKII), but on Cdc2-mediated phosphorylation of multiple sites within Emi2. As in MII, this phosphorylation is antagonized by Mos-mediated recruitment of PP2A to Emi2. Higher Cdc2 kinase activity in MI than MII allows sufficient Emi2 phosphorylation to destabilize Emi2 in MI. At MI anaphase, APC-mediated degradation of cyclin B decreases Cdc2 activity, enabling Cdc2-mediated Emi2 phosphorylation to be successfully antagonized by Mos-mediated PP2A recruitment. These data suggest a model of APC autoinhibition mediated by stabilization of Emi2; Emi2 proteins accumulate at MI exit and inhibit APC activity sufficiently to prevent complete degradation of cyclin B, allowing MI exit while preventing interphase before MII entry.

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“…In meiosis I these cohesins are digested in the chromosome arms, but not at the centromeres, which therefore remain unsplit . Likewise cyclin B remains partially undigested between meiosis I and II (Iwabuchi et al, 2000). Thus this interval is not a true interphase and is incompetent to initiate replication; as assumed (Cavalier-Smith, 1981) the cell remains in M phase until anaphase II when the centromeres split, cyclin B is digested and it reverts to G1.…”

Section: Origin Of Meiosismentioning

confidence: 89%

“…Mitotic chromosome and centromere splitting are caused by a protease that digests cohesins. The cell cycle switch from mitosis to the growth state (G1 phase) where replication is allowed is also by proteolytic digestion -of cyclin B attached to the cyclin-dependent kinase which phosphorylates the proteins whose activity has to change (Iwabuchi et al, 2000). A direct causal connection between centromere splitting and cyclin digestion has not yet been demonstrated, but if there is one, then meiosis could have originated by a single key change (Cavalier-Smith, 1981): blocking centromeric cohesin digestion in meiosis I.…”

Section: Origin Of Meiosismentioning

confidence: 99%

Origins of the machinery of recombination and sex

2002

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Mutation plays the primary role in evolution that Weismann mistakenly attributed to sex. Homologous recombination, as in sex, is important for population genetics -shuffling of minor variants, but relatively insignificant for large-scale evolution. Major evolutionary innovations depend much more on illegitimate recombination, which makes novel genes by gene duplication and by gene chimaerisationessentially mutational forces. The machinery of recombination and sex evolved in two distinct bouts of quantum evolution separated by nearly 3 Gy of stasis; I discuss their nature and causes. The dominant selective force in the evolution of recombination and sex has been selection for replicational fidelity and viability; without the recombination machinery, accurate reproduction, stasis, resistance to radical deleterious evolutionary change and preservation of evolutionary innovations would be impossible. Recombination proteins betray in their phylogeny and domain structure a key role for gene duplication and chimaerisation in their own origin. They arose about 3.8 Gy ago to enable faithful replication and segregation of the first circular DNA genomes in precellular ancestors of Gram-negative eubacteria. Then they were recruited and modified by selfish genetic parasites (viruses; transposons) to help them spread from host to host. Bacteria differ fundamentally from eukaryotes in that gene transfer between cells, whether incidental to their absorptive feeding on DNA and virus infection or directly by plasmids, involves only genomic fragments. This was radically changed by the neomuran revolution about 850 million years ago when a posibacterium evolved

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Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts

Cited by 102 publications

References 44 publications

Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest

Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest

Cdc2 and Mos Regulate Emi2 Stability to Promote the Meiosis I–Meiosis II Transition

Origins of the machinery of recombination and sex

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