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Cytoplasmic polyadenylation in mammalian oocyte maturation

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Oocyte developmental competence is the ability of the mature oocyte to be fertilized and subsequently drive early embryo development. Developmental competence is acquired by completion of oocyte maturation, a process that includes nuclear (meiotic) and cytoplasmic (molecular) changes. Given that maturing oocytes are transcriptionally quiescent (as are early embryos), they depend on post‐transcriptional regulation of stored transcripts for protein synthesis, which is largely mediated by translational repression and deadenylation of transcripts within the cytoplasm, followed by recruitment of specific transcripts in a spatiotemporal manner for translation during oocyte maturation and early development. Motifs within the 3′ untranslated region (UTR) of messenger RNA (mRNA) are thought to mediate repression and downstream activation by their association with binding partners that form dynamic protein complexes that elicit differing effects on translation depending on cell stage and interacting proteins. The cytoplasmic polyadenylation (CP) element, Pumilio binding element, and hexanucleotide polyadenylation signal are among the best understood motifs involved in CP, and translational regulation of stored transcripts as their binding partners have been relatively well‐characterized. Knowledge of CP in mammalian oocytes is discussed as well as novel approaches that can be used to enhance our understanding of the functional and contributing features to transcript CP and translational regulation during mammalian oocyte maturation. WIREs RNA 2016, 7:71–89. doi: 10.1002/wrna.1316 This article is categorized under: Translation > Translation Mechanisms RNA Turnover and Surveillance > Regulation of RNA Stability
Cytoplasmic polyadenylation element binding protein (CPEB) model of cytoplasmic polyadenylation (CP) and translational regulation in Xenopus. CPEB is the central protein (in yellow) that interacts with other key factors (in blue), such as Pumilio (PUM) and cleavage and polyadenylation specificity factor (CPSF), which together modulate formation of intricate protein complexes (in pink) responsible for repressing (red line) mRNA (brown line) translation in germinal vesicle and subsequently promoting CP and translational activation (green line) in metaphase II oocytes. A heterotrimer of two CPEB and one Maskin protein induce loop formation between the RNA termini as Maskin binds eukaryotic initiation factor 4E (eIF4E) preventing interaction between eIF4E and eukaryotic initiation factor 4G (eIF4G), precluding translation initiation. Symplekin (SYMPK) is believed to be a scaffolding protein enhancing CPSF and CPEB interaction prior to and during CP. In addition, CPEB interacts with a poly(A) polymerase, PAP associated domain containing 4 (PAPD4, aka GLD2), and poly(A)‐specific ribonuclease (PARN) which additionally interact with each other. Prior to translational activation PARN mediates deadenylation of transcripts, which is subsequently ejected from the complex upon CPEB phosphorylation (green circle) enabling CP. CPEB phosphorylation also results in its dissociation from embryonic poly(A) binding protein (ePAB, PABPC1L) which can then bind the newly synthesized poly(A) tail along with eIF4G displacing Maskin and enabling translational activation by mediating interaction of the eIF4 factors. Although PUM is not necessary for CPEB‐mediated translational regulation it has been found to enhance repression and translational activation under different contexts by interacting with CPEB, but has also been shown to induce repression independently of CPEB by recruitment of deadenylases (CCR4/NOT complex) and competing with eIF4E for 5′ end cap (black circle) binding which may extend to the CPEB model.
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3′ untranslated region (UTR) motif analysis of the CCNB1 and MOS genes for human, mouse, and cattle. Horizontal bars (gray) represent 3′UTR sequence only from the last exon measured in base pairs (bp), which for human includes two annotated mRNA splice variants (horizontal black lines). Cytoplasmic polyadenylation element (CPE) consensus (CPE‐C), CPE nonconsensus (CPE‐NC), CPE mammalian MOS (CPE‐MamMOS); hexanucleotide polyadenylation signal (Hex), Musashi binding element (MBE), Pumilio binding element (PBE), and translational control sequence (TCS).
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Expression of polyadenylation and translational regulator associated factors in mammalian metaphase II (MII) oocytes. Average gene expression values (RPKM) in human, mouse, and cattle MII oocytes. Genes failing to meet the expression cutoff (RPKM > 0.4 in at least two oocyte samples from their respective species) were assigned an RPKM ≤ 0.4 and are not considered to be expressed (red). Red and green represent the lowest and highest expression, respectively, across species and between genes belonging to respective gene families (CPEB, CPSF, DAZAP, MSI, PABP, PUM, and ZAR) or solely across species for respective genes not belonging to a gene family (DAZL, PAPD4, PARN, SYMPK, and TACC3).
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RNA Turnover and Surveillance > Regulation of RNA Stability
Translation > Translation Mechanisms

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