Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes

Stutz, André; Conne, Béatrice; Huarte, Joachim; Gubler, Pascale; Völkel, Valérie; Flandin, Pierre; Vassalli, Jean‐Dominique

doi:10.1101/gad.12.16.2535

Cited by 106 publications

(86 citation statements)

References 74 publications

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“…All control embryos had cleaved by the end of the treatment period, whereas none of the drug-treated embryos had done so; 25 eggs per lane. mRNAs in immature oocytes (Stutz et al, 1997;Stutz et al, 1998). The increase in SLBP synthesis in M-phase oocytes may depend on interaction of oocyte factors with analogous elements in the 3′-utr of SLBP mRNA.…”

Section: Discussionmentioning

confidence: 99%

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Allard

Champigny

Skoggard

et al. 2002

Journal of Cell Science

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The stem-loop binding protein (SLBP) binds to the 3′ end of histone mRNA and participates in 3′-processing of the newly synthesized transcripts, which protects them from degradation, and probably also promotes their translation. In proliferating cells, translation of SLBP mRNA begins at G1/S and the protein is degraded following DNA replication. These post-transcriptional mechanisms closely couple SLBP expression to S-phase of the cell cycle, and play a key role in restricting synthesis of replication-dependent histones to S-phase. In contrast to somatic cells,replication-dependent histone mRNAs accumulate and are translated independently of DNA replication in oocytes and early embryos. We report here that SLBP expression and activity also differ in mouse oocytes and early embryos compared with somatic cells. SLBP is present in oocytes that are arrested at prophase of G2/M, where it is concentrated in the nucleus. Upon entry into M-phase of meiotic maturation, SLBP begins to accumulate rapidly,reaching a very high level in mature oocytes arrested at metaphase II. Following fertilization, SLBP remains abundant in the nucleus and the cytoplasm throughout the first cell cycle, including both G1 and G2 phases. It declines during the second and third cell cycles, reaching a relatively low level by the late 4-cell stage. SLBP can bind the histone mRNA-stem-loop at all stages of the cell cycle in oocytes and early embryos, and it is the only stem-loop binding activity detectable in these cells. We also report that SLBP becomes phosphorylated rapidly following entry into M-phase of meiotic maturation through a mechanism that is sensitive to roscovitine, an inhibitor of cyclin-dependent kinases. SLBP is rapidly dephosphorylated following fertilization or parthenogenetic activation, and becomes newly phosphorylated at M-phase of mitosis. Phosphorylation does not affect its stem-loop binding activity. These results establish that, in contrast to Xenopus, mouse oocytes and embryos contain a single SLBP. Expression of SLBP is uncoupled from S-phase in oocytes and early embryos, which indicates that the mechanisms that impose cell-cycle-regulated expression of SLBP in somatic cells do not operate in oocytes or during the first embryonic cell cycle. This distinctive pattern of SLBP expression may be required for accumulation of histone proteins required for sperm chromatin remodelling and assembly of newly synthesized embryonic DNA into chromatin.

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Section: Discussionmentioning

confidence: 99%

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Allard

Champigny

Skoggard

et al. 2002

Journal of Cell Science

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“…In growing mouse oocytes, tPA mRNA is partially deadenylated (from 250 down to 40 A's) upon binding of ACEB to the 45-nucleotide (nt) ACE. Deadenylation translationally silences this mRNA in the resting oocyte, and ACEB is required to maintain dormancy (Stutz et al, 1998). Resumption of meiosis results in either modification or displacement of ACEB and subsequent translational activation and polyadenylation.…”

Section: Introductionmentioning

confidence: 99%

“…Among these mRNAs are those encoding tPA, c-mos, cyclin B1, and cyclin A1 (Sheets et al, 1994(Sheets et al, , 1995Stutz et al, 1998). Elongation of the poly(A) tail depends on the nuclear polyadenylation sequence AAUAAA (NPS) and UArich sequences termed either adenylation control elements (ACEs) for mice or cytoplasmic polyadenylation elements (CPEs) for frogs (Huarte et al, 1992;Hake and Richter, 1994;Stebbins-Boaz et al, 1996;Stutz et al, 1998;Mendez and Richter, 2001). In frog oocytes, polyadenylation is initiated when the CPE binding protein (CPEB) is phosphorylated and recruits the cleavage and polyadenylation specificity factor (CPSF) to the NPS (Mendez et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Zygotic control of maternal cyclin A1 translation and mRNA stability

Audic

Garbrecht

Fritz

et al. 2002

Developmental Dynamics

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Cyclin mRNAs are unstable in the adult cell cycle yet are stable during the first 12 cell divisions in Xenopus laevis. We recently reported that cyclin A1 and B2 maternal mRNAs are deadenylated upon completion of the 12th division (Audic et al. [2001] Mol. Cell Biol. 21: 1662-1671). Deadenylation is mediated by the 3 untranslated region (UTR) of the mRNA and precedes the terminal disappearance of the cyclin proteins, with both processes requiring zygotic transcription. The purpose of the current study was (1) to ask whether deadenylation leads to translational repression and/or destabilization of endogenous cyclin A1 and B2 mRNAs, and (2) to further characterize the regulatory sequences required. We show that zygote-driven deadenylation leads to translational repression and mRNA destabilization. A 99-nucleotide region of the 3UTR of the cyclin A1 mRNA mediates both deadenylation and destabilization. Surprisingly, two AU-rich consensus elements within this region are dispensable for this activity. These results suggest that zygote-dependent deadenylation, translational repression, and mRNA destabilization by means of novel 3UTR elements contribute to the disappearance of maternal cyclins. They also suggest that translational control of cyclins may play a role in the transition to the adult cell cycle. These data concur with previous studies in Drosophila showing that zygote-mediated degradation of maternal cdc25 mRNA may be a general mechanism whereby transition to the adult cell cycle proceeds.

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“…Both aspects of CPE function require the CPE-binding protein (CPEB) (9,(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).…”

mentioning

confidence: 99%

Cytoplasmic Polyadenylation Element (CPE)- and CPE-binding Protein (CPEB)-independent Mechanisms Regulate Early Class Maternal mRNA Translational Activation in Xenopus Oocytes

Charlesworth

Cox

MacNicol

2004

Journal of Biological Chemistry

147

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Meiotic cell cycle progression during vertebrate oocyte maturation requires the correct temporal translation of maternal mRNAs encoding key regulatory proteins. The mechanism by which specific mRNAs are temporally activated is unknown, although both cytoplasmic polyadenylation elements (CPE) within the 3 -untranslated region (3 -UTR) of mRNAs and the CPEbinding protein (CPEB) have been implicated. We report that in progesterone-stimulated Xenopus oocytes, the early cytoplasmic polyadenylation and translational activation of multiple maternal mRNAs occur in a CPEand CPEB-independent manner. We demonstrate that polyadenylation response elements, originally identified in the 3 -UTR of the mRNA encoding the Mos protooncogene, direct CPE-and CPEB-independent polyadenylation of an early class of Xenopus maternal mRNAs. Our findings refute the hypothesis that CPE sequences alone account for the range of temporal inductions of maternal mRNAs observed during Xenopus oocyte maturation. Rather, our data indicate that the sequential action of distinct 3 -UTR-directed translational control mechanisms coordinates the complex temporal patterns and extent of protein synthesis during vertebrate meiotic cell cycle progression.

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Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes

Cited by 106 publications

References 74 publications

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Zygotic control of maternal cyclin A1 translation and mRNA stability

Cytoplasmic Polyadenylation Element (CPE)- and CPE-binding Protein (CPEB)-independent Mechanisms Regulate Early Class Maternal mRNA Translational Activation in Xenopus Oocytes

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