The Control of Meiotic Maturation in Mammalian Oocytes

Holt, Janet E.; Lane, Simon I. R.; Jones, Kevin

doi:10.1016/b978-0-12-416024-8.00007-6

Cited by 84 publications

(68 citation statements)

References 97 publications

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“…Although this regulatory system is best understood in mice (Norris et al, 2009;Vaccari et al, 2009;Zhang et al, 2010;Kawamura et al, 2011;Tsuji et al, 2012;Geister et al, 2013), there is evidence that similar mechanisms operate in other mammals (Törnell et al, 1991;Peng et al, 2013;Hiradate et al, 2014;Zhang et al, 2014), including women (Kawamura et al, 2011;Liu et al, 2014). The LH-induced resumption of the meiotic cell cycle leads into a series of events by which the oocyte matures to become a fertilizable egg (Conti et al, 2012;Clift and Schuh, 2013;Holt et al, 2013;Mehlmann, 2013;Hunzicker-Dunn and Mayo, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…cAMP, which is produced in the oocyte (Mehlmann et al, 2002(Mehlmann et al, , 2004Horner et al, 2003;Hinckley et al, 2005;Ledent et al, 2005), maintains meiotic prophase arrest through activation of protein kinase A (PKA) (Bornslaeger et al, 1986;Kovo et al, 2006). PKA activity inhibits the CDC25B phosphatase and stimulates the WEE1B and MYT1 kinases, and this keeps the CDK1 kinase that controls the prophaseto-metaphase transition phosphorylated and inactive (Conti et al, 2012;Holt et al, 2013;Mehlmann, 2013). When LH signaling reduces oocyte levels of cGMP, and in turn cAMP, meiosis resumes.…”

Section: Introductionmentioning

confidence: 99%

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Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

et al. 2014

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In mammals, the meiotic cell cycle of oocytes starts during embryogenesis and then pauses. Much later, in preparation for fertilization, oocytes within preovulatory follicles resume meiosis in response to luteinizing hormone (LH). Before LH stimulation, the arrest is maintained by diffusion of cyclic (c)GMP into the oocyte from the surrounding granulosa cells, where it is produced by the guanylyl cyclase natriuretic peptide receptor 2 (NPR2). LH rapidly reduces the production of cGMP, but how this occurs is unknown. Here, using rat follicles, we show that within 10 min, LH signaling causes dephosphorylation and inactivation of NPR2 through a process that requires the activity of phosphoprotein phosphatase (PPP)-family members. The rapid dephosphorylation of NPR2 is accompanied by a rapid phosphorylation of the cGMP phosphodiesterase PDE5, an enzyme whose activity is increased upon phosphorylation. Later, levels of the NPR2 agonist C-type natriuretic peptide decrease in the follicle, and these sequential events contribute to the decrease in cGMP that causes meiosis to resume in the oocyte.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

et al. 2014

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“…Upon ovulation, MI resumes, with a concordant breakdown of the nuclear envelope and condensation of chromatin. Homologous chromosomes are then segregated during an asymmetric cytokinesis in which the first polar body, containing half the chromosomal complement, is extruded and the egg again arrests at metaphase II prior to fertilisation (Hirshfield 1991, McLaughlin & McIver 2009, Holt et al 2013.…”

Section: Introductionmentioning

confidence: 99%

Changing expression and subcellular distribution of karyopherins during murine oogenesis

et al. 2015

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Mammalian oocyte growth and development is driven by a strict program of gene expression that relies on the timely presence of transcriptional regulators via nuclear pores. By targeting specific cargos for nucleo-cytoplasmic transport, karyopherin (KPN) proteins are key to the relocation of essential transcription factors and chromatin-remodelling factors into and out of the nucleus. Using multiple complementary techniques, here we establish that KPNA genes and proteins are dynamically expressed and relocalised throughout mouse oogenesis and folliculogenesis. Of the KPNAs examined (Kpna1, Kpna2, Kpna3, Kpna4, Kpna6, Kpna7, Kpnb1, Ipo5 and Xpo1), all were expressed in the embryonic ovary with up-regulation of protein levels concomitant with meiotic entry for KPNA2, accompanied by the redistribution of the cellular localisation of KPNA2 and XPO1. In contrast, postnatal folliculogenesis revealed significant up-regulation of Kpna1, Kpna2, Kpna4, Kpna6 and Ipo5 and down-regulation of Kpnb1, Kpna7 and Xpo1 at the primordial to primary follicle transition. KPNAs exhibited different localisation patterns in both oocytes and granulosa cells during folliculogenesis, with three KPNAs -KPNA1, KPNA2 and IPO5 -displaying marked enrichment in the nucleus by antral follicle stage. Remarkably, varied subcellular expression profiles were also identified in isolated pre-ovulatory oocytes with KPNAs KPNA2, KPNB1 and IPO5 detected in the cytoplasm and at the nuclear rim and XPO1 in cytoplasmic aggregates. Intriguingly, meiotic spindle staining was also observed for KPNB1 and XPO1 in meiosis II eggs, implying roles for KPNAs outside of nucleo-cytoplasmic transport. Thus, we propose that KPNAs, by targeting specific cargoes, are likely to be key regulators of oocyte development. Reproduction (2015) 150 485-496

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“…Timely APC/C activation depends on satisfaction of the SAC [28,42], so we asked whether inappropriate SAC activity was the reason for arrest in Ccnb3 -/-oocytes. Kinetochore recruitment of SAC components, such as MAD2, is a readout for SAC activation [43].…”

Section: Cell Cycle Arrest In Ccnb3mentioning

confidence: 99%

“…Under these conditions, germinal vesicle breakdown (GVBD, corresponding to nuclear envelope breakdown in mitosis) occurred with normal timing (within 90 min) and efficiency in Ccnb3 -/-oocytes ( Figure 1D), indicating that cyclin B3 is dispensable for entry into meiosis I. At ~7-10 hours in culture after entry into meiosis I, depending on the mouse strain, oocytes extrude a polar body (PB), indicating execution of the first division and exit from meiosis I [6,28]. Unlike for other aspects of female reproduction described above, Ccnb3 -/-mice displayed a highly penetrant defect at this stage of meiosis: oocytes failed to extrude a PB in most cyclin B3-deficient mice (50 out of 58 mice) ( Figure 1D).…”

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confidence: 99%

Cyclin B3 promotes APC/C activation and anaphase I onset in oocyte meiosis

Bouftas

Keeney

et al. 2018

Preprint

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As obligate kinase partners, cyclins control the switch-like cell cycle transitions that orchestrate orderly duplication and segregation of genomes. Meiosis, the cell division that generates gametes for sexual reproduction, poses unique challenges because two rounds of chromosome segregation must be executed without intervening DNA replication. Mammalian cells express numerous, temporally regulated cyclins, but how these proteins collaborate to control meiosis remains poorly understood. Here, we delineate an essential function for mouse cyclin B3 in the first meiotic division of oocytes. Females genetically ablated for cyclin B3 are viable, indicating the protein is dispensable for mitotic divisions, but are sterile. Mutant oocytes appear normal until metaphase I but then display a highly penetrant failure to transition to anaphase I. They arrest with hallmarks of defective APC/C activation, including no separase activity and high MPF, cyclin B1, and securin levels. Partial APC/C activation occurs, however, as exogenously expressed APC/C substrates can be degraded and arrest can be suppressed by inhibiting MPF kinase. Cyclin B3 is itself targeted for degradation by the APC/C. Cyclin B3 forms active kinase complexes with CDK1, and meiotic progression requires cyclin B3-associated kinase activity. Collectively, our findings indicate that cyclin B3 is essential for oocyte meiosis because it fine-tunes APC/C activity as a kinase-activating CDK partner. Cyclin B3 homologs from frog, zebrafish, and fruitfly rescue meiotic progression in cyclin B3-deficient mouse oocytes, indicating conservation of the biochemical properties and possibly cellular functions of this germline-critical cyclin. IntroductionEukaryotic cell division depends on oscillations of cyclindependent kinases (CDKs) associated with specific cyclins [1][2][3][4]. In vertebrate somatic cells, progression from G1 into S phase, G2, and mitosis depends on the cyclin D family, followed by the cyclin E, A, and B families [4]. Ordered CDK activity likewise governs progression through meiosis: chromosome condensation, congression, and alignment require a rise in cyclin B-CDK1 activity, then anaphase onset and chromosome segregation are driven by sudden inactivation of cyclin B-CDK1 by the anaphase promoting complex/ cyclosome (APC/C), an E3 ubiquitin ligase that targets substrates for degradation by the 26S proteasome [5]. Cyclin B-CDK1 activity re-accumulates following its depletion, but meiotic cells have the challenge of not inducing DNA replication during the period of low cyclin B-CDK1 activity between meiosis I and II [6,7]. The roles of specific cyclins in shaping CDK oscillations and thus in determining the orderly progression of meiosis remain poorly understood, particularly in mammalian oocytes.In this context, cyclin B3 is particularly enigmatic. Cyclin B3 belongs to a separate family with characteristics of both A-and B-type cyclins [8,9] and is evolutionarily conserved from early metazoans to human [10]. Ciona intestinalis cyclin B3 counteracts zyg...

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The Control of Meiotic Maturation in Mammalian Oocytes

Cited by 84 publications

References 97 publications

Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

Changing expression and subcellular distribution of karyopherins during murine oogenesis

Cyclin B3 promotes APC/C activation and anaphase I onset in oocyte meiosis

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