RNA synthesis and cytoplasmic polyadenylation in the one-cell mouse embryo

Clegg, Kerry B.; Pikó, Lajos

doi:10.1038/295342a0

Cited by 144 publications

(56 citation statements)

References 22 publications

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“…In Xenopus, after 12 rapid synchronous cleavages, when the developing embryo is composed of ∼4000 cells, the mid-blastula transition occurs and is characterized by lengthening of the cell cycle, inclusion of G1 and G2, and activation of zygotic transcription (Newport and Kirschner 1982a,b). In mouse and human, induction of transcription in the embryo occurs at the two-cell, and four-to eight-cell stages, respectively (Clegg and Piko 1982;Flach et al 1982;Braude et al 1988). Despite the earlier occurrence of zygotic transcription, activation of maternally inherited mRNAs in mammals seems to use translation mechanisms similar to those in other vertebrates (Richter 1999;Oh et al 2000).…”

mentioning

confidence: 99%

Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades

Vasudevan¹,

Seli²,

Steitz³

2006

Genes Dev.

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confidence: 99%

Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades

Vasudevan¹,

Seli²,

Steitz³

2006

Genes Dev.

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“…In Xenopus, after 12 rapid synchronous cleavages generating Ͼ4,000 cells, the mid-blastula transition occurs and is characterized by the activation of zygotic transcription, also called zygotic gene activation (ZGA) (17,18). In mouse and human, ZGA occurs at the two-cell and four-to eight-cell stages, respectively (19)(20)(21). Despite the earlier occurrence of ZGA in mammals compared with Xenopus, translational activation of maternally inherited mRNAs appears to use similar mechanisms (13,16,22).…”

mentioning

confidence: 99%

An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos

Seli

Lalioti

Flaherty

et al. 2005

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

119

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Gene expression during oocyte maturation, fertilization, and early embryo development until zygotic gene activation is regulated mainly by translational activation of maternally derived mRNAs. This process requires the presence of a poly(A)-binding protein. However, the cytoplasmic somatic cell poly(A)-binding protein (PABP1) is not expressed until later in embryogenesis. We recently identified an embryonic poly(A)-binding protein (ePAB) in Xenopus. ePAB is the predominant cytoplasmic PABP in Xenopus oocytes and early embryos and prevents deadenylation of mRNAs, suggesting its importance in the regulation of gene expression during early Xenopus development. Here we report the identification of the mouse ortholog of Xenopus ePAB. The mouse ePAB gene on chromosome 2 contains 14 exons that specify an alternatively spliced mRNA encoding a protein of 608 or 561 aa with Ϸ65% identity to Xenopus ePAB. Mouse ePAB mRNA is expressed in ovaries and testis but not in somatic tissues. In situ hybridization localizes ePAB RNA to oocytes and confirms its absence from surrounding somatic cells in the mouse ovary. During early development, mouse ePAB is expressed in prophase I and metaphase II oocytes and one-cell and two-cell embryos and then becomes undetectable in four-or-more-cell embryos. In contrast, PABP1 mRNA expression is minimal in oocytes and early embryos until the eight-cell stage when it increases, becoming predominant at the blastocyst stage. The expression of mouse ePAB before zygotic gene activation argues for its importance in translational activation of maternally derived mRNAs during mammalian oocyte and early preimplantation embryo development.translational activation ͉ embryogenesis ͉ oogenesis M echanisms for establishing the germline and carrying out oogenesis in evolutionarily distant animals exhibit common themes. Gametes develop from primordial germ cells that are set aside during early embryogenesis (1). In most metazoans, primordial germ cells have an extragonadal origin and migrate to reach the somatic gonad, where they proliferate by mitosis to form oocytes (1). Oocytes, in turn, enter meiosis only to be arrested at the prophase of the first meiotic division (2, 3). This first meiotic arrest may last up to a few years in Xenopus and several decades in humans and is characterized by synthesis and storage of large quantities of dormant mRNA (4, 5). The resumption of meiosis is stimulated by progesterone in Xenopus (6, 7) or by gonadotropins in mouse and human (8, 9) and marks the onset of oocyte maturation.Oocyte maturation is accompanied by a complex network of translational activation and repression of dormant maternal mRNAs (10-13), whereas transcription is limited at best. These maternal mRNAs drive the oocyte's reentry into meiosis and control the rate of mitosis during the early cleavage divisions of the embryo (13-16). The transcriptional silencing that begins with oocyte maturation persists during the initial mitotic divisions of the embryonic cells. In Xenopus, after 12 rapid synchronous cle...

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“…Since transcription from zygotic genes is first detected at the two-cell stage of mouse development (Clegg and Piko 1982), it appeared inappropriate for PyV and SV40 early gene promoters to express the PyV T antigen required for PyV DNA replication in one-cell embryos that remained morphologically as one-cell embryos. Furthermore, PyV DNA injected into one-cell embryos was injected only into the male pronucleus.…”

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confidence: 99%

The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus.

Martínez‐Salas

Linney²,

Hassell³

et al. 1989

Genes Dev.

111

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Microinjection of the firefly luciferase gene coupled to a thymidine kinase (tk) promoter provided a quantitative assay to evaluate the requirements for gene expression in individual mouse oocytes and embryos. Polyoma virus (PyV) enhancers had no effect on the level of gene expression or competition for transcription factors as long as the DNA remained either in the oocyte germinal vesicle or the pronuclei of one-cell embryos. Expression of injected genes could be observed in pronuclei because the signal that normally triggers zygotic gene expression in two-cell embryos still occurred in one-cell embryos arrested in S phase. However, when the tk promoter was injected into zygotic nuclei of two-cell embryos, enhancers increased the number of embryos that expressed luciferase as well as the level of luciferase activity per embryo. PyV enhancer mutation FlOl, selected for growth in mouse embryonal carcinoma F9 cells, stimulated expression in developing two-cell embryos about seven times better than the wild-type PyV enhancer and competed effectively for factors required for transcription. These results were consistent with the fact that enhancers are required to activate the PyV origin of DNA replication in developing two-cell embryos but not in one-cell embryos. The maximum levels of gene expression in oocytes, one-cell embryos, and developing two-cell embryos (1 : 67 : 21) were inversely related to the extent of chromatin assembly, but the need for enhancers was independent of chromatin assembly. Therefore, it appears that the need for enhancers to activate promoters or origins of replication results from some negative regulatory factor that first appears as a component of zygotic nuclear structure.

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RNA synthesis and cytoplasmic polyadenylation in the one-cell mouse embryo

Cited by 144 publications

References 22 publications

Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades

Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades

An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos

The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus.

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