Aurora B Kinase Maintains Chromatin Organization During the MI to MII Transition in Surf Clam Oocytes

George, Olivia; Johnston, Mantissa A; Shuster, Charles B.

doi:10.4161/cc.5.22.3444

Cited by 19 publications

(11 citation statements)

References 80 publications

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“…Histone H3 phosphorylation on serine 10 is an established marker for Aurora B kinase activity in a wide variety of organisms [Giet and Glover, 2001; Crosio et al, 2002; Goto et al, 2002; Ota et al, 2002; George et al, 2006], as is the organization of the central spindle through Aurora regulation of MKLP1 [Severson et al, 2000; Guse et al, 2005]. To verify that VX-680 treatment affected these processes in echinoderm zygotes, cells were treated with either DMSO carrier control or Aurora inhibitors and probed for chromatin and microtubule organization (Fig.…”

Section: Resultsmentioning

confidence: 99%

Centralspindlin and chromosomal passenger complex behavior during normal and Rappaport furrow specification in echinoderm embryos

et al. 2012

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The chromosomal passenger (CPC) and Centralspindlin complexes are essential for organizing the anaphase central spindle and providing cues that position the cytokinetic furrow between daughter nuclei. However, echinoderm zygotes are also capable of forming “Rappaport furrows” between asters positioned back-to-back without intervening chromosomes. To understand how these complexes contribute to normal and Rappaport furrow formation, we studied the localization patterns of Survivin and mitotic-kinesin-like-protein1 (MKLP1), members respectively of the CPC and the Centralspindlin complex, and the effect of CPC inhibition on cleavage in mono- and binucleate echinoderm zygotes. In zygotes, Survivin initially localized to metaphase chromosomes, upon anaphase onset relocalized to the central spindle and then, together with MKLP1 spread towards the equatorial cortex in an Aurora-dependent manner. Inhibition of Aurora kinase activity resulted in disruption of central spindle organization and furrow regression, although astral microtubule elongation and furrow initiation were normal. In binucleate cells containing two parallel spindles MKLP1 and Survivin localized to the plane of the former metaphase plate, but were not observed in the secondary cleavage plane formed between unrelated spindle poles, except when chromosomes were abnormally present there. However, the secondary furrow was sensitive to Aurora inhibition, indicating that Aurora kinase may still contribute to furrow ingression without chromosomes nearby. Our results provide insights that reconcile classic micromanipulation studies with current molecular understanding of furrow specification in animal cells.

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Section: Resultsmentioning

confidence: 99%

Centralspindlin and chromosomal passenger complex behavior during normal and Rappaport furrow specification in echinoderm embryos

et al. 2012

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“…For example, porcine oocyte incubation in ZM447439 results in prophase arrest (Jelinkova & Kubelka 2006). This may be species specific because, similar to mouse oocytes, in bovine oocytes or clam oocytes, VX680 and ZM447439 respectively block meiosis in MI or in interkinesis (George et al 2006, Uzbekova et al 2008. Gadea & Ruderman (2005) demonstrated in cycling Xenopus egg extracts that ZM447439 incubation disrupts spindle formation and chromosome condensation but does not arrest the cell cycle.…”

Section: Discussionmentioning

confidence: 99%

The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint

Lane

Chang²,

Jennings³

et al. 2010

Reproduction

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Previous studies have established that when maturing mouse oocytes are continuously incubated with the Aurora inhibitor ZM447439, meiotic maturation is blocked. In this study, we observe that by altering the time of addition of the inhibitor, oocyte maturation can actually be accelerated by 1 h as measured by the timing of polar body extrusion. ZM447439 also had the ability to overcome a spindle assembly checkpoint (SAC) arrest caused by nocodazole and so rescue polar body extrusion. Consistent with the ability of the SAC to inhibit cyclin B1 degradation by blocking activation of the anaphase-promoting complex, we could also observe a rescue in cyclin B1 degradation when ZM447439 was added to nocodazole-treated oocytes. The acceleration of the first meiotic division by ZM447439, which has not been achieved previously, and its effects on the SAC are all consistent with the proposed mitotic role of Aurora B in activating the SAC. We hypothesize that Aurora kinase activity controls the SAC in meiosis I, despite differences to the mitotic cell cycle division in spindle architecture brought about by the meiotic mono-orientation of sister kinetochores.

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“…ZM447439-treated oocytes are arrested just after GVBD in the late diakinesis stage [34]. Although AURKB is not required for chromosome condensation [34], it is required for maintenance of chromatin condensation in Xenopus [78] and surf clam oocytes [79], and thus AURKB activity might be critical for the correct MI/MII transition.…”

Section: Aurka Synthesis and Phosphorylation Were Independent From Mamentioning

confidence: 99%

Spatio-Temporal Expression Patterns of Aurora Kinases A, B, and C and Cytoplasmic Polyadenylation-Element-Binding Protein in Bovine Oocytes During Meiotic Maturation1

Uzbekova¹,

Arlot‐Bonnemains²,

Dupont³

et al. 2008

Biology of Reproduction

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Maturation of immature bovine oocytes requires cytoplasmic polyadenylation and synthesis of a number of proteins involved in meiotic progression and metaphase-II arrest. Aurora serine-threonine kinases--localized in centrosomes, chromosomes, and midbody--regulate chromosome segregation and cytokinesis in somatic cells. In frog and mouse oocytes, Aurora A regulates polyadenylation-dependent translation of several mRNAs such as MOS and CCNB1, presumably by phosphorylating CPEB, and Aurora B phosphorylates histone H3 during meiosis. We analyzed the expression of three Aurora kinase genes--AURKA, AURKB, and AURKC--in bovine oocytes during meiosis by reverse transcription followed by quantitative real-time PCR and immunodetection. Aurora A was the most abundant form in oocytes, both at mRNA and protein levels. AURKA protein progressively accumulated in the oocyte cytoplasm during antral follicle growth and in vitro maturation. AURKB associated with metaphase chromosomes. AURKB, AURKC, and Thr-phosphorylated AURKA were detected at a contractile ring/midbody during the first polar body extrusion. CPEB, localized in oocyte cytoplasm, was hyperphosphorylated during prophase/metaphase-I transition. Most CPEB degraded in metaphase-II oocytes and remnants remained localized in a contractile ring. Roscovitine, U0126, and metformin inhibited meiotic divisions; they all induced a decrease of CCNB1 and phospho-MAPK3/1 levels and prevented CPEB degradation. However, only metformin depleted AURKA. The Aurora kinase inhibitor VX680 at 100 nmol/L did not inhibit meiosis but led to multinuclear oocytes due to the failure of the polar body extrusion. Thus, in bovine oocyte meiosis, massive destruction of CPEB accompanies metaphase-I/II transition, and Aurora kinases participate in regulating segregation of the chromosomes, maintenance of metaphase-II, and formation of the first polar body.

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Aurora B Kinase Maintains Chromatin Organization During the MI to MII Transition in Surf Clam Oocytes

Cited by 19 publications

References 80 publications

Centralspindlin and chromosomal passenger complex behavior during normal and Rappaport furrow specification in echinoderm embryos

Centralspindlin and chromosomal passenger complex behavior during normal and Rappaport furrow specification in echinoderm embryos

The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint

Spatio-Temporal Expression Patterns of Aurora Kinases A, B, and C and Cytoplasmic Polyadenylation-Element-Binding Protein in Bovine Oocytes During Meiotic Maturation1

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