Meneau F , Dupré A , Jessus C , Daldello EM .

18-CE13-0013-01 Agence Nationale de la Recherche

             M phase
             translation
             cell cycle
             meiosis I
             meiosis II
             nuclear envelope disassembly

	Figure 1. Four phases of Xenopus oocyte meiosis. (1) The growth period: Oocytes enter prophase of the first meiotic division and arrest at the diplotene stage (Prophase I). Growing oocytes have been classified into six stages by Dumont [31]. (2) The fully-grown oocyte: when oocyte growth is complete, transcription and vitellogenesis stop, and oocytes become competent to undergo meiotic maturation. (3) Meiosis resumption: Progesterone releases the prophase arrest and oocytes resume meiosis. (4) Meiosis progression: Following nuclear envelope breakdown (NEBD), oocytes assemble the metaphase I (Met I) spindle. After anaphase I, the first polar body is extruded, and a metaphase II (Met II) spindle assembles.
	Figure 2. Changes in the total mRNA level during the growth period. (A) Changes in mRNA levels between stages I–II (starting of the growth period) and stages V–VI (end of the growth period) have been plotted. (B) Selection of the gene ontology terms enriched among the 1557 transcripts whose levels increase during the growth period.
	Figure 3. Genome-wide analysis of the fully-grown prophase-arrested oocytes. (A) The expression level of each mRNA quantified using two independent published datasets [37,72]. Each transcript is ranked in the two databases according to its level of expression. The average rank is used to highlight the 1000 transcripts with either the lowest (yellow) or the highest level of expression (black). (B) Gene ontology terms enriched among 1000 highest (black) or 1000 lowest (yellow) expressed transcripts from panel A. (C) The translation efficiency (TE) is defined as the fraction of mRNAs recovered in the polysomes divided by the concentration of total mRNAs of each transcript. TE has been correlated with its total level [37,72]. The extent of the poly(A) tail length has been color-coded: black (30 to 60 nt), green (≤30 nt), orange (≥60 nt), grey (poly(A) length not available). (D) Gene ontology terms enriched among the transcripts with poly(A) tail ≥ 60 nucleotides (dark orange) and TE ≥ 0.45 (light orange) or among poly(A) tail ≤ 30 nucleotides (dark green) and TE ≤ 30 (light green) from panel C. (E) The expression level of each protein is compared to the level of its mRNA [37,70,72]. The same color code as panel C is applied for the poly(A) length. (F) Gene ontology terms enriched among 1000 highest expressed proteins from panel E.
	Figure 4. Genome-wide analysis of oocytes during meiotic maturation. (A) Changes in total mRNA levels [37,72]. Left panel: Changes between prophase I and metaphase I oocytes. Blue: mRNAs, whose level decreases more than 2-fold. Middle panel: Changes between prophase I (Pro I) and metaphase II (Met II) oocytes. The average rank is used to highlight the 1000 transcripts whose levels decrease the most during this period of meiotic maturation (blue). Right panel: Selection of the gene ontology terms enriched among the 1000 mRNAs from the middle panel. (B) Changes in the poly(A) tail length of each mRNA during meiotic maturation [72]. A color-code depicts 4 groups of transcripts. Light red: constitutively activated transcripts with poly(A) tail ≥ 60 nt at all periods; dark red: activated mRNAs whose poly(A) tail increases, at least, by 10 nt and is longer than 60 nt in Met I/Met II; light blue: constitutively repressed mRNAs with poly(A) tail ≤ 30 nt at all periods; dark blue: repressed mRNAs whose poly(A) tail decreases more than 10 nt and is shorter than 30 nt in Met I/Met II. Left panel: Changes between prophase I and metaphase I (Met I) oocytes. Middle panel: Changes between prophase I and metaphase II (Met II) oocytes. Right panel: Selection of the gene ontology terms enriched among the 4 groups of transcripts. (C) Left panel: Changes in the protein levels between prophase I and metaphase II oocytes [70]. The proteins whose copy number increases or decreases more than 2-fold are colored in red or blue, respectively. Right panel: Selection of the gene ontology terms enriched among the proteins whose level decreases more than 2-fold, from the right panel.
	Figure 5. The relationship between poly(A) tail length, translation, and mRNA degradation. (A) Changes in translation efficiency (TE) and in the poly(A) tail length between fully-grown prophase (Pro I) and metaphase II (Met II) oocytes [72]. Transcripts are divided into three groups: transcripts whose poly(A) tail decreases, at least, by 10 nt and TE decreases, at least, by 0.1 (blue—repression of translation and de-adenylation), transcripts whose poly(A) tail increases less than 10 nt and TE increases more than 0.1 (red—activation of translation without polyadenylation), and mRNAs whose poly(A) tail increases more than 20 nt and TE increases, at least, by 0.1 (orange—activation of translation and polyadenylation). (B) Median values of translation efficiency and poly(A) tail length of the three groups described in panel A. (C) 3′-UTRs of the mRNAs whose poly(A) tail increases, at least, by 10 nt and is longer than 60 nt in metaphase I (Met I) oocytes are retrieved from the UCSC database. Sequences of cytoplasmic polyadenylation elements (CPEs) and CPE overlapping the PAS from Pique et al. [92] are searched within the 3′-UTRs. The pie chart represents the percentage of transcripts containing at least one CPE or one CPE overlapping the PAS or none. (D) Changes in total mRNA levels between fully-grown prophase (Pro I) and metaphase II (Met II) oocytes are compared to the length of the poly(A) tail in Met II oocytes [72]. A color-code depicts two groups. Light blue: mRNAs with a poly(A) tail length ≤ 20 in both Pro I and Met II oocytes; dark blue: mRNAs whose poly(A) tail length decreases, at least, by 20 nt between both stages. (E) Changes in the total mRNA levels between fully-grown prophase I (Pro I) and metaphase II (Met II) in Xenopus oocytes [72] are compared with mRNAs that are stabilized in btg4 (left panel) or cnot6l (right panel) knockout mouse Met II oocytes [114]. Blue: transcripts degraded in Xenopus Met II oocytes and stabilized in btg4 (left panel) or cnot6l (right panel) knock-out mouse Met II oocytes.
	Figure 6. The bidirectional regulation between protein translation and meiosis progression. The fully-grown prophase-arrested oocyte actively translates proteins related to cell metabolism and ribosome biogenesis. mRNAs encoding proteins involved in M-phase progression, DNA replication, and mRNA splicing exhibit short poly(A) tails and are stored for future translation. The prophase arrest is maintained by the high activity of protein kinase A (PKA) and the phosphorylation of its substrates, which indirectly inhibit the activation of the M-phase promoting factor (MPF). In the vertebrates, the prophase arrest is released by a decrease of PKA activity and the dephosphorylation of PKA substrates. De novo protein synthesis occurs before NEBD (“Early” translation), and a sub-group of the de novo synthesized proteins is required to activate Cdk1 (Class I). Two RNA-binding proteins (RBPs) have been involved in the activation of the early translation wave—CPEB and Musashi. Once activated, Cdk1 activates the “late translation” (purple box). This second translation wave involves the phosphorylation and degradation of inhibitory RBPs, including CPEB1 and Zar2. The translated proteins are involved in meiosis progression (Class II), support embryonic cell divisions, such as components of the DNA replication machinery (Class III), and further contribute to regulating RNA translation and degradation by de-adenylation in metaphase II. Among the transcripts that are de-adenylated are ribosome compounds and translation initiation factors.

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