Chapter 7 Oocyte Quality and Maternal Control of Development

Mtango, Namdori R.; Potireddy, Santhi; Latham, Keith E.

doi:10.1016/s1937-6448(08)00807-1

Cited by 76 publications

(51 citation statements)

References 500 publications

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“…Some recruited mRNAs contain recognizable cytoplasmic polyadenylation elements (CPEs), which participate in translational regulation, and other mRNAs contain binding motifs for DAZL (deleted in azoospermia-like), a CPEB-regulated protein that is critical for translational control of maternal mRNAs encoding spindle proteins . Many other mRNAs that are recruited stage specifically lack recognizable CPEs, indicating that multiple translational regulatory mechanisms may operate at different stages (Potireddy et al 2010).Given the complex and dynamic pattern of maternal mRNA recruitment during oocyte maturation and early embryogenesis (Potireddy et al 2006(Potireddy et al , 2010Mtango et al 2008;) and the prevalence of spindle-encoding mRNAs among these, we wished to test oocytes of a mammalian species for conservation of localized maternal mRNAs at the spindle. We tested whether the key translational regulator, EIF4EBP1, might likewise be enriched at the spindle as part of the overall regulatory mechanism.…”

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confidence: 99%

“…Given the complex and dynamic pattern of maternal mRNA recruitment during oocyte maturation and early embryogenesis (Potireddy et al 2006(Potireddy et al , 2010Mtango et al 2008;) and the prevalence of spindle-encoding mRNAs among these, we wished to test oocytes of a mammalian species for conservation of localized maternal mRNAs at the spindle. We tested whether the key translational regulator, EIF4EBP1, might likewise be enriched at the spindle as part of the overall regulatory mechanism.…”

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Association of Maternal mRNA and Phosphorylated EIF4EBP1 Variants With the Spindle in Mouse Oocytes: Localized Translational Control Supporting Female Meiosis in Mammals

et al. 2013

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In contrast to other species, localized maternal mRNAs are not believed to be prominent features of mammalian oocytes. We find by cDNA microarray analysis enrichment for maternal mRNAs encoding spindle and other proteins on the mouse oocyte metaphase II (MII) spindle. We also find that the key translational regulator, EIF4EBP1, undergoes a dynamic and complex spatially regulated pattern of phosphorylation at sites that regulate its association with EIF4E and its ability to repress translation. These phosphorylation variants appear at different positions along the spindle at different stages of meiosis. These results indicate that dynamic spatially restricted patterns of EIF4EBP1 phosphorylation may promote localized mRNA translation to support spindle formation, maintenance, function, and other nearby processes. Regulated EIF4EBP1 phosphorylation at the spindle may help coordinate spindle formation with progression through the cell cycle. The discovery that EIF4EBP1 may be part of an overall mechanism that integrates and couples cell cycle progression to mRNA translation and subsequent spindle formation and function may be relevant to understanding mechanisms leading to diminished oocyte quality, and potential means of avoiding such defects. The localization of maternal mRNAs at the spindle is evolutionarily conserved between mammals and other vertebrates and is also seen in mitotic cells, indicating that EIF4EBP1 control of localized mRNA translation is likely key to correct segregation of genetic material across cell types.T HE oocytes of many species, both invertebrate and vertebrate, contain a large collection of localized determinants in the form of proteins and translationally inactive maternal mRNAs. Similar localized determinants in mammalian oocytes have been proposed (Ciemerych et al. 2000), but this aspect of mammalian reproduction remains controversial (Hiiragi et al. 2006). Indeed, early mammalian embryogenesis is considered to be quite plastic and regulative in nature, so that localized determinants would not be expected to play essential functions. Embryo splitting can be used for twinning, and blastomere extirpation does not prevent elaboration of normal body plans and term development. Additionally, much of the volume of the mammalian oocyte eventually becomes allocated to cells that do not contribute to embryonic development, being destined instead to generate the placenta. Accordingly, prepatterning of the mammalian oocyte through localization of maternal mRNAs or proteins, if it occurs, appears to be dispensable for mammalian embryogenesis.One potential exception to this would relate to localization within the oocyte of maternal mRNAs that support a vital process that is evolutionarily conserved between mammals and other species, namely the formation and maintenance of the meiotic spindle. Recent studies in Xenopus revealed enriched localization to spindle microtubules of mRNAs encoding spindle proteins (Blower et al. 2007). The spindle is a complex structure; proteomic studies of is...

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Association of Maternal mRNA and Phosphorylated EIF4EBP1 Variants With the Spindle in Mouse Oocytes: Localized Translational Control Supporting Female Meiosis in Mammals

et al. 2013

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“…33 Our data showed that the cytoplasm of mature mouse oocytes is abundant with both H3.3A and H3.3B mRNAs. These maternal mRNAs are gradually degraded upon oocyte activation and become largely depleted by the first embryonic cleavage (20 …”

Section: H33 Is Required For Embryonic Development Of Parthenogenetimentioning

confidence: 52%

H3.3 replacement facilitates epigenetic reprogramming of donor nuclei in somatic cell nuclear transfer embryos

Wen

Banaszynski

Rosenwaks

et al. 2014

Nucleus

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T ransfer of a somatic nucleus into an enucleated oocyte is the most efficient approach for somatic cell reprogramming. While this process is known to involve extensive chromatin remodeling of the donor nucleus, the maternal factors responsible and the underlying chromatin-based mechanisms remain largely unknown. Here we discuss our recent findings demonstrating that the histone variant H3.3 plays an essential role in reprogramming and is required for reactivation of key pluripotency genes in somatic cell nuclear transfer (SCNT) embryos. Maternal-derived H3.3 replaces H3 in the donor nucleus shortly after oocyte activation, with the amount of replacement directly related to the differentiation status of the donor nucleus in SCNT embryos. We provide additional evidence to suggest that de novo synthesized H3.3 replaces histone H3 carrying repressive modifications in the donor nuclei of SCNT embryos, and hypothesize that replacement may occur at specific loci that must be reprogrammed for gene reactivation.

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“…Oocytes and early embryos are notable for their large cell size compared with somatic cells, and many other features such as altered cell cycles, altered metabolic properties, and altered homeostatic mechanisms (37). Each blastomere represents a substantial fraction of the future embryo and must be kept intact.…”

Section: Discussionmentioning

confidence: 99%

Early transcription from the maternal genome controlling blastomere integrity in mouse two-cell-stage embryos

Han

Mtango²,

Zhong³

et al. 2010

American Journal of Physiology-Cell Physiology

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Han Z, Mtango NR, Zhong Z, Vassena R, Latham KE. Early transcription from the maternal genome controlling blastomere integrity in mouse two-cell-stage embryos. Am J Physiol Cell Physiol 298: C1235-C1244, 2010. First published January 27, 2010 doi:10.1152/ajpcell.00393.2009Blastomere cytofragmentation in mammalian embryos poses a significant problem in applied and clinical embryology. Mouse two-cell-stage embryos display strain-dependent differences in the rate of cytofragmentation, with a high rate observed in C3H/HeJ embryos and a lower rate observed in C57BL/6 embryos. The maternally inherited genome exerts the strongest effect on the process, with lesser effects mediated by the paternally inherited genome and the ooplasm. The effect of the maternal genome is transcription dependent and independent of the mitochondrial strain of origin. To identify molecular mechanisms that underlie cytofragmentation, we evaluated transcriptional activities of embryos possessing maternal pronuclei (mPN) of different origins. The mPN from C57BL/6 and C3H/HeJ strains directed specific transcription at the two-cell stage of mRNAs corresponding to 935 and 864 Affymetrix probe set IDs, respectively. Comparing transcriptomes of two-cell-stage embryos with different mPN revealed 64 transcribed genes with differential expression (1.4-fold or greater). Some of these genes occupy molecular pathways that may regulate cytofragmentation via a combination of effects related to apoptosis and effects on the cytoskeleton. These results implicate specific molecular mechanisms that may regulate cytofragmentation in early mammalian embryos. The most striking effect of mPN strain of origin on gene expression was on adenylate cyclase 2 (Adcy2). Treatment with dibutyryl cAMP (dbcAMP) elicits a high rate and severe form of cytofragmentation, and the effective dbcAMP concentration varies with maternal genotype. An activator of exchange proteins directly activated by cAMP (EPACs, or RAPGEF 3 and 4) 8-pCPT-2=-O-methyl-cAMP, elicits a high level of fragmentation while the PKA-specific activator N6-benzoyl-cAMP does not. Inhibition of A kinase anchor protein activities with st-Ht31 induces fragmentation. Inhibition of phosphatidylinositol 3-kinase signaling also induces fragmentation. These results reveal novel mechanisms by which maternal genotype affects cytofragmentation, including a system of opposing signaling pathways that most likely operate by controlling cytoskeletal function.

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Chapter 7 Oocyte Quality and Maternal Control of Development

Cited by 76 publications

References 500 publications

Association of Maternal mRNA and Phosphorylated EIF4EBP1 Variants With the Spindle in Mouse Oocytes: Localized Translational Control Supporting Female Meiosis in Mammals

Association of Maternal mRNA and Phosphorylated EIF4EBP1 Variants With the Spindle in Mouse Oocytes: Localized Translational Control Supporting Female Meiosis in Mammals

H3.3 replacement facilitates epigenetic reprogramming of donor nuclei in somatic cell nuclear transfer embryos

Early transcription from the maternal genome controlling blastomere integrity in mouse two-cell-stage embryos

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