Abstract
The study of oocytes has made enormous contributions to the understanding of the G2/M transition. The complementarity of investigations carried out on various model organisms has led to the identification of the M-phase promoting factor (MPF) and to unravel the basis of cell cycle regulation. Thanks to the power of biochemical approaches offered by frog oocytes, this model has allowed to identify the core signaling components involved in the regulation of M-phase. A central emerging layer of regulation of cell division regards protein translation. Oocytes are a unique model to tackle this question as they accumulate large quantities of dormant mRNAs to be used during meiosis resumption and progression, as well as the cell divisions during early embryogenesis. Since these events occur in the absence of transcription, they require cascades of successive unmasking, translation, and discarding of these mRNAs, implying a fine regulation of the timing of specific translation. In the last years, the Xenopus genome has been sequenced and annotated, enabling the development of omics techniques in this model and starting its transition into the genomic era. This review has critically described how the different phases of meiosis are orchestrated by changes in gene expression. The physiological states of the oocyte have been described together with the molecular mechanisms that control the critical transitions during meiosis progression, highlighting the connection between translation control and meiosis dynamics.
Highlights
Meiosis is a specialized cell division that is essential for sexual reproduction in eukaryotes as it allows germ cells to reduce by half their ploidy
The ability of progesterone or the protein kinase A (PKA)-inhibitor (PKI) to induce meiosis resumption is abolished if the translation is inhibited by protein synthesis inhibitors, such as cycloheximide [45,46], suggesting that, during the prophase arrest, PKA prevents the synthesis of crucial proteins required for meiosis resumption
Three of these putative PKA substrates have a known function related to the control of protein synthesis—Rps6, Spats2, and Akt1s1—which are, respectively, a component of the ribosome, an RNA-binding protein involved in male meiosis, and a regulatory subunit of the master regulator of protein synthesis, mTORC1 [71]
Summary
Meiosis is a specialized cell division that is essential for sexual reproduction in eukaryotes as it allows germ cells to reduce by half their ploidy. Changes in gene expression occur and regulate meiosis resumption and progression by targeting mRNAs that have accumulated during early oogenesis. They shape the proteome of the oocyte by modulating mRNA stability (transcriptome), the degree of mRNA translation (translatome), and protein stability. The regulation of gene expression allows the achievement of four major sequential steps that orchestrate oogenesis: the oocyte growth phase, the arrest of the fully-grown oocyte, meiosis resumption, from the hormonal stimulation to NEBD, and meiosis progression from NEBD to the metaphase II arrest. Plk protein accumulates between stages V and VI, when oocytes become competent to resume meiosis These results suggest that translation during early oogenesis is temporally regulated, and the machinery required for meiosis progression is acquired progressively during oogenesis. This will help to explore the molecular mechanisms behind the oocyte genome silencing, the spatial polarization of oocytes, and the acquisition of the competence to resume meiosis
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