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

Huarte, Joachim; Belin, Dominique; Vassalli, Anne; Strickland, Sidney; Vassalli, Jean‐Dominique

doi:10.1101/gad.1.10.1201

Cited by 209 publications

(144 citation statements)

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“…The c-mos transcripts in these oocytes lack detectable poly(A) tails but become polyadenylylated after resumption of meiosis (9). Such posttranscriptional polyadenylylation is indicative of recruitment of maternal mRNAs for translation in both the mouse and lower organisms (10)(11)(12)(13). Consistent with the fate of other maternal mRNAs in the mouse (14), c-mos RNA is degraded by the two-cell stage (2,15,16).…”

mentioning

confidence: 55%

Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg.

O’Keefe

Wolfes

Kiessling

et al. 1989

Proc. Natl. Acad. Sci. U.S.A.

167

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Injection of antisense oligonucleotides was used to investigate the function of c-mos in murine oocytes. Oocytes injected with antisense c-mos oligonucleotides completed the first meiotic division but failed to initiate meiosis H. Instead, loss of c-mos function led to chromosome decondensation, reformation of a nucleus after meiosis I, and cleavage to two cells. Therefore, c-mos is required for meiosis II during murine oocyte maturation.The ability of activated oncogenes to induce neoplastic transformation suggests that their normal cellular progenitors, the protooncogenes, may also play important roles in regulating cell growth and differentiation. While some protooncogenes are expressed in many cell types, others display more restricted patterns of expression, suggesting that they play a role in particular developmental schemes. c-mos is unique among the protooncogenes in that its major sites of expression appear limited to male and female germ cells of the mouse and of several other species (1-8), suggesting a specific function for c-mos in meiotic cell types.The murine oocyte, which is arrested at the diplotene stage of meiotic prophase, accumulates large amounts of c-mos RNA during its growth (2, 3). The c-mos transcripts in these oocytes lack detectable poly(A) tails but become polyadenylylated after resumption of meiosis (9). Such posttranscriptional polyadenylylation is indicative of recruitment of maternal mRNAs for translation in both the mouse and lower organisms (10-13). Consistent with the fate of other maternal mRNAs in the mouse (14), c-mos RNA is degraded by the two-cell stage (2, 15, 16). These results imply that c-mos is a maternal mRNA that is translated and may function during meiosis.In the present study, we have used injection of antisense oligonucleotides to investigate the function of c-mos in the murine oocyte. Meiosis in the murine oocyte is easily followed in vitro. After the reinitiation of meiosis, germinal vesicle (nuclear) breakdown (GVBD) occurs within 4 hr. The first polar body is extruded 6-8 hr later, indicating the completion of meiosis I. Upon reaching metaphase II, the now mature oocyte (egg) will once again arrest awaiting fertilization. After sperm penetration, the egg completes meiosis II, extrudes the second polar body, and cleaves to two cells within 24 Typically, 20-35 cumulus-enclosed oocytes were washed twice through 2.5 ml of DPBS containing 5% fetal calf serum to remove IBMX and initiate maturation. Oocytes were transferred to 350 1LI of DPBS containing 5% fetal calf serum under silicone oil, visualized by using Hoffman diffractioninterference contrast optics, and injected in the cytoplasm with 10 pl of oligonucleotide (1 ptgld) in 0.6x DPBS containing 0.15 mM EDTA; a beveled injection pipette with an outer diameter of 2.5 pm= was used. Injection volume was controlled with a Picoinjector 100 (Medical Systems, Greenvale, NY 7038The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked ...

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mentioning

confidence: 55%

Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg.

O’Keefe

Wolfes

Kiessling

et al. 1989

Proc. Natl. Acad. Sci. U.S.A.

167

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“…Tissue plasminogen activator (tPA) mRNA is translationally activated by cytoplasmic polyadenylylation during meiotic maturation of mouse oocytes (12,21). As shown previously, an RNA representing the terminal 455 nt of this mRNA's 3' UTR (diagrammed in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The plasmid encoding Ll+CPEmUt (named pLl+CPEmUt/4Z) was generated by cleaving pLl+CPE/3Z with EcoRI to release the insert, which was subcloned into pGEM3Zf+. Site (20)(21)(22)(23). Approximately 10 pl of a filtered, 0.1 M KCI solution containing 2.5 pg of RNA were microinjected into the cytoplasm of each oocyte.…”

Section: Methodsmentioning

confidence: 99%

Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation.

Verrotti

Thompson²,

Wreden³

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

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Cytoplasmic polyadenylylation is an evolutionarily conserved mechanism involved in the translational activation of a set of maternal messenger RNAs (mRNAs) during early development. In this report, we show by interspecies injections that Xenopus and mouse use the same regulatory sequences to control cytoplasmic poly(A) addition during meiotic maturation. Similarly, Xenopus and Drosophila embryos exploit functionally conserved signals to regulate polyadenylylation during early post-fertilization development.These experiments demonstrate that the sequence elements that govern cytoplasmic polyadenylylation, and hence one form of translational activation, function across species. We infer that the requisite regulatory sequence elements, and likely the trans-acting components with which they interact, have been conserved since the divergence of vertebrates and arthropods.

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“…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%

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.

show abstract

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

Cited by 209 publications

References 36 publications

Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg.

Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg.

Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation.

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

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