Stability of RNA synthesized by the mouse oocyte during its major growth phase

Jahn, Carolyn L.; Baran, Madelyn M.; Bachvarova, Rosemary F.

doi:10.1002/jez.1401970202

Cited by 73 publications

(31 citation statements)

References 22 publications

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“…4B). Based on earlier estimations (17,27), the peak values of ZP2 and ZP3 represent 1% and 0.4%, respectively, of the total poly(A)+ content of growing oocytes. The ZP2 and ZP3 transcripts accumulated in parallel, and ZP2 was present in approximately twofold molar excess throughout oocyte growth.…”

Section: Resultsmentioning

confidence: 86%

Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.

Liang¹,

Chamow²,

Dean³

1990

Mol. Cell. Biol.

139

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The zona pellucida surrounds all mammalian oocytes and plays a vital role at fertilization and in early development. The genes that code for two of the mouse zona proteins (ZP2 and ZP3) represent a developmentally regulated set of genes whose expression serves as markers of mouse oocyte growth and differentiation. We previously characterized the single-copy Zp-3 gene and showed that its expression is oocyte specific and restricted to a narrow window of oocyte development. We now define the Zp-2 gene transcript and show that it is coordinately expressed with Zp-3 only during the 2-week growth phase of oogenesis that occurs prior to ovulation. Like Zp-3, the expression of Zp-2 is restricted to oocytes, and, although not detectable in resting oocytes, both ZP2 and ZP3 transcripts accumulate to become very abundant messengers in 50-,um-diameter oocytes. Ovulated eggs contain ZP2 and ZP3 transcripts which are 200 nucleotides shorter than those found in growing oocytes and have an abundance of less than 5% of the peak levels. In an attempt to understand the molecular details associated with the developmentally regulated, tissue-specific gene expression of the zona genes, the Zp-2 genetic locus has been characterized and its 5' flanking sequences have been compared with those of Zp-3. Both genes contain three short (8-to 12-base-pair) DNA sequences of 80 to 88% identity located within 250 base pairs of their transcription start sites.At birth the mouse ovary contains 10,000 to 15,000 primordial oocytes (29), the vast majority of which are in the prophase of the first meiotic division. During the reproductive life of the female, cohorts of these resting oocytes (10 to 15 p.m in diameter) enter into a 2-week growth phase which culminates in meiotic maturation and subsequent ovulation (3, 11). Virtually nothing is known about the signals that induce this growth and differentiation, but one potential marker of these phenomena is the expression of the zona pellucida genes.The zona pellucida surrounds all mammalian oocytes; in the mouse it is composed of three sulfated glycoproteins, ZP1, ZP2, and ZP3 (7,45). The mouse zona proteins are coordinately synthesized in the growing oocyte (8,45) and are secreted to form a filamentous zona matrix (39) in which ZP2 and ZP3 complex into copolymers cross-linked by ZP1 (24). At fertilization, sperm initially bind to ZP3 via 0-linked oligosaccharide side chains (9, 10, 21). Following the induction of the sperm acrosome reaction on the surface of the zona, ZP2 acts as a secondary sperm receptor that is necessary for the maintenance of sperm binding to the egg (6). ZP2 is proteolytically cleaved after fertilization (5, 36), and this modification, along with presumed changes in ZP3, are postulated to play an important role in the postfertilization block to polyspermy.The genes that code for the mouse zona pellucida represent a remarkable set of developmentally regulated, oocytespecific genes which specifiy products vital to fertilization and early mammalian development. We have previously ...

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Section: Resultsmentioning

confidence: 86%

Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.

Liang¹,

Chamow²,

Dean³

1990

Mol. Cell. Biol.

139

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“…Whether the time of accumulation of a specific "maternal" mRNA reflects only the period during which the relevant gene is transcribed into a stable mRNA species, or whether there are discrete times at which individual mRNAs are selectively stabilized, is not yet known. The t-PA mRNA level remained constant in fully grown primary oocytes cultured under conditions that prevent resumption of meiosis, even when transcription was blocked by actinomycin D. Therefore, transcription of the t-PA gene is probably very low, and t-PA mRNA is stable in these cells, as has also been found for the bulk of endogenous oocyte RNA (Jahn et al 1976;Bachvarova 1985) and for injected mRNAs (Ebert et al 1984). Cell fractionation revealed that most of t-PA mRNA is in the oocyte's cytoplasm; it follows that its dormancy and stability do not result from nuclear sequestration.…”

Section: Translation Of T-pa In Mouse Oocytesmentioning

confidence: 84%

Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA.

Huarte

Belin²,

Vassalli³

et al. 1987

Genes Dev.

209

139

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The serine protease tissue-type plasminogen activator (t-PA) is synthesized by murine oocytes undergoing meiotic maturation, but not by arrested primary oocytes. Dormant, stable t-PA mRNA accumulates during oocyte growth, so that fully grown, arrested primary oocytes contain in their cytoplasm approximately 10,000 copies of this molecule. Translation of t-PA mRNA is triggered upon resumption of meiosis and is accompanied by a progressive and concerted increase in its size. This structural change can be accounted for by increased polyadenylation at the 3' end of the molecule. Following its translation, t-PA mRNA is degraded; it is no longer detectable in fertilized eggs. The identification of a dormant mRNA in murine oocytes and the demonstration that its translational activation is accompanied by elongation of its poly(A) tail may provide insights into the control of gene expression during meiotic maturation and early mammalian development.

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“…For example, these oocytes are contained within growing antral follicles and are, in large part, transcriptionally inactive while cumulus cells are transcriptionally active. Furthermore, oocytes contain maternal pools of RNA, protein, and energy stores that accumulated during the growth phase [18][19][20], a period during which features of oocyte total RNA are more like somatic cells [18,[21][22][23][24][25][26]. Thereafter, maternal stores are critical for providing sustenance not only while the "quiescent" oocyte is resident within antral follicle (GV-stage), but during maturation, after ovulation, fertilization, and up through embryonic genome activation.…”

Section: Discussionmentioning

confidence: 99%

General Features of Certain RNA Populations from Gametes and Cumulus Cells

Payton

Rispoli

Edwards

2010

Journal of Reproduction and Development

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Abstract.Results described herein provide insight regarding certain features of gamete RNA and how they compare to cumulus cell RNA. In particular, 28S/18S rRNA ratio and size distribution of RNA molecules differed in total RNA from oocytes versus surrounding cumulus cells. Specifically, oocyte total RNA had a lower rRNA ratio and an increased abundance of smaller RNA sizes compared to RNA from surrounding cumulus. Extensive efforts demonstrated that observed differences were repeatable whether oocyte maturation occurred in vitro or in vivo, and were similar between the nuclear stages examined. Features of oocyte RNA were conserved across six mammalian species, yet differed from surrounding cumulus. Profiles of sperm RNA were also examined but had no discernible ribosomal RNA peaks and were conserved across four mammalian species. Because the oocyte and spermatozoon are highly specialized cells representing unique molecular entities required for proper embryo development, dissimilarities described herein likely represent real gamete versus cumulus RNA differences. Key words: Bioanalyzer, Cumulus, Oocyte, RNA, Sperm (J. Reprod. Dev. 56: [583][584][585][586][587][588][589][590][591][592] 2010) pon resumption of meiosis and germinal vesicle breakdown, oocytes become transcriptionally quiescent and must rely upon pools of RNA accumulated during the growth phase for protein synthesis [1]. Transcriptional inactivity and reliance upon maternal RNA stores persist until after fertilization and, in some species, until the third cleavage division [2]. In our laboratory, stress-induced perturbations in the total amount of polyadenylated RNA in oocytes during maturation were coincident with reductions in developmental competence [3]. Before performing microarray analyses to identify the impact on individual transcripts, assessment of RNA integrity was an important first step. To this end, initial efforts using microcapillary electrophoresis suggested differences between oocyte and cumulus RNA [4]. The first notable difference was that the rRNA ratio of total RNA from oocytes was significantly less than that observed in total RNA from their surrounding cumulus cells. A second notable feature was that oocyte RNA appeared to have an increased abundance of smaller RNA sizes.This serendipitous finding led us to conduct a series of investigations to address the extent to which certain features of oocyte RNA differ from surrounding cumulus, which are more somatic cell-like. In this regard, extensive effort was taken to determine whether RNA features were oocyte-specific or an artifact related to procedures or origin (i.e., from oocytes of antral follicles not otherwise destined to ovulate). Specifically, bovine oocyte RNA from different stages of in vitro maturation was evaluated in retrospect using data originating from different studies. When available, cumulus RNA characteristics were also included for comparison to RNA from oocytes. Additional effort was then put forth to examine 1) conservation of certain oocyte RNA feature...

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Stability of RNA synthesized by the mouse oocyte during its major growth phase

Cited by 73 publications

References 22 publications

Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.

Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.

Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA.

General Features of Certain RNA Populations from Gametes and Cumulus Cells

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