Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse

Paynton, Barbara V.; Rempel, Rachel E.; Bachvarova, Rosemary F.

doi:10.1016/0012-1606(88)90377-6

Cited by 284 publications

(241 citation statements)

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“…SLBP mRNA was present throughout preimplantation development, but the amount of RT-PCR product declined after the 2-cell stage (Fig. 3B) which is consistent with the widespread loss of maternal mRNA that occurs at this time (Paynton et al, 1988), and increased again by the blastocyst stage presumably as a result of the increased cell number. Thus, the quantity of SLBP protein remains high during the first two cell cycles, then declines to a much lower level once the embryo reaches the 4-cell stage and remains low during subsequent development.…”

Section: Slbp Accumulates During Meiotic Maturation and Remains Abundsupporting

confidence: 69%

“…In the case of other proteins that accumulate during oocyte maturation, including tissue-type plasminogen activator [tPA (Huarte et al, 1987)], HPRT (Paynton et al, 1988), mos (O'Keefe et al, 1989;Paules et al, 1989;Gebauer et al, 1994), FGF receptor (Culp and Musci, 1999) cyclin B (Polanski et al, 1998;Barkoff et al, 2000;Tay et al, 2000) and spindlin (Oh et al, 2000), this is due to increased translation of existing mRNAs. Translation of these mRNAs is regulated by U-rich sequences, termed adenylation control elements (ACE) or cytoplasmic polyadenylation elements (CPE), that are located in the 3′-untranslated region (utr) of the mRNA within about 100 nt of the polyadenylation signal (Richter, 1995;Gray and Wickens, 1998;Oh et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

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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: Slbp Accumulates During Meiotic Maturation and Remains Abundsupporting

confidence: 69%

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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“…Once a fully grown oocyte is hormonally stimulated, RNA synthesis ceases, the germinal vesicle breaks down, and the oocyte becomes arrested at meiotic metaphase 11. A process of deadenylation, adenylation, and degradation of maternal mRNA is initiated during meiotic maturation that results in a net loss of about 30% of the polyadenylated mRNA pool between the fully grown oocyte and ovulated oocyte stages (Bachvarova et al, 1985;Paynton et al, 1988). Active turnover of poly-(A) tails continues in the one-cell embryo (Clegg and Piko, 1983a,b) and by the mid-two-cell stage most of the poly-(Abcontaining mRNA is degraded (Piko and Clegg, 1982).…”

Section: Mouse Preimplantation Embryosmentioning

confidence: 99%

“…The decrease in maternal mRNA in early mouse embryos actually begins during meiotic maturation of the oocyte (Paynton et al, 1988). Between fertilization and the two-cell stage, there is a 40% decline in bulk maternal RNA (Bachvarova and DeLeon, 1980) and up to a 70% decrease in maternal poly-(A)' mRNA, which may reflect deadenylation as well as degradation (Levey et al, 1978;Piko and Clegg, 1982).…”

Section: Mousementioning

confidence: 99%

Transition from maternal to embryonic control in early mammalian development: A comparison of several species

Telford

Watson

Schultz

1990

Molecular Reproduction Devel

797

434

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“…qRT-PCR Oocyte growth and early development requires large amounts of maternally-derived transcripts which are subjected to massive destruction as oocytes mature. Of the estimated 85 pg of polyadenylated mRNAs present in a germinal vesicle (GV)-stage mouse oocyte, 50 pg of mRNAs are degraded during oocyte maturation [1]. Furthermore, transcript degradation is highly selective, primarily affecting genes involved in processes associated with meiotic arrest at the GV-stage and progression of oocyte maturation, such as oxidative phosphorylation, energy production, protein synthesis and metabolism [2].…”

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confidence: 99%

Differentially expressed micoRNAs in human oocytes

Wang

Ding

et al. 2011

J Assist Reprod Genet

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Purpose To identify differentially expressed microRNAs (miRNAs) and expression patterns of specific miRNAs during meiosis in human oocytes. Materials and methods To identify differentially expressed miRNAs, GV oocytes and MII oocytes matured at conventional FSH levels (5.5 ng/ml) were analyzed by miRNA microarray. Real-time RT-PCR was used to confirm the changed miRNAs. To validate the dynamic changes of miRNAs from GV to MII stages, oocytes were divided into four groups (#1-4), corresponding to GVoocytes, MI oocytes, MII oocytes matured in conventional FSH level and MII oocytes matured in high FSH level (2,000 ng/ml) respectively. Results Compared with GVoocytes, MII oocytes exhibited up-regulation of 4 miRNAs (hsa-miR-193a-5p, hsa-miR-297, hsa-miR-625 and hsa-miR-602), and down-regulation of 11 miRNAs (hsa-miR-888*, hsa-miR-212, hsa-miR-662, hsa-miR-299-5p, hsa-miR-339-5p, hsa-miR-20a, hsa-miR-486-5p, hsa-miR-141*, hsa-miR-768-5p, hsa-miR-376a and hsa-miR-15a). RT-PCR analysis of hsa-miR-15a and hsamiR-20a expression revealed concordant dynamic changes in oocytes from group 1 to group 4. Conclusion(s) Specific miRNAs in human oocytes had dynamic changes during meiosis. High-concentration FSH in IVM medium led to reverse effect on the expression of hsa-miR-15a and hsa-miR-20a.Keywords miRNA . Oocytes . In vitro maturation . qRT-PCR Oocyte growth and early development requires large amounts of maternally-derived transcripts which are subjected to massive destruction as oocytes mature. Of the estimated 85 pg of polyadenylated mRNAs present in a germinal vesicle (GV)-stage mouse oocyte, 50 pg of mRNAs are degraded during oocyte maturation [1]. Furthermore, transcript degradation is highly selective, primarily affecting genes involved in processes associated with meiotic arrest at the GV-stage and progression of oocyte maturation, such as oxidative phosphorylation, energy production, protein synthesis and metabolism [2]. On the other hand, up-regulation of a number of transcripts during oocyte maturation was also observed in mice, cattle, and humans in recent years [3][4][5].miRNAs are a family of small non-coding RNAs that play important regulatory roles in gene expression. Specifically, miRNA-mediated translational regulation involves cleavage of messenger RNAs or repression of mRNA translation [6]. It has been estimated that 30% or more of human mRNAs are regulated by miRNAs [7]. Likewise, miRNAs may also play an important role in modulating gene expression in oocytes [8].Dynamic changes in miRNA expression during oogenesis were first revealed by a real-time PCR-based miRNA expression profiling method in single mouse oocytes [8]. A Yan-Wen Xu and Bin Wang contributed equally to this study. Capsule Differentially expressed miRNAs in the human oocytes between GV and MII stages were identified by miRNA microarrays. Dynamic changes of miR-15a, hsa-miR-20a, and miR-602 during meiosis were validated by qRT-PCR.

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Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse

Cited by 284 publications

References 38 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

Transition from maternal to embryonic control in early mammalian development: A comparison of several species

Differentially expressed micoRNAs in human oocytes

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