Evolutionary origin and phylogenetic analysis of the novel oocyte-specific eukaryotic translation initiation factor 4E in Tetrapoda.

The Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609, USA.
Development Genes and Evolution (Impact Factor: 1.7). 01/2009; 219(2):111-8. DOI: 10.1007/s00427-008-0268-2
Source: PubMed

ABSTRACT The transcriptionally active, growing oocyte accumulates mRNAs essential for early stages of development, the oocyte-to-embryo transition, in a stable, dormant form. Translational repression of mRNAs in eggs of various species is conferred by interactions, either direct or via intermediate proteins, of repressive factors bound to the 3'-untranslated regions with the proteins of the eukaryotic translation initiation factor 4E (eIF4E) family bound to the 5'-cap of the transcripts. Recently, a novel oocyte-specific eIF4E encoded by the Eif41b gene in mammals has been identified by our group. To further investigate this gene, the available cDNA libraries, as well as genome assemblies of nonmammalian vertebrates, were surveyed. This analysis revealed that the Eif4e1b gene arose in Tetrapoda as a result of the ancestral Eif4e locus duplication. Unlike other known proteins of three subfamilies comprising eIF4E family (eIF4E1, eIF4E2, and eIF4E3), cDNA library evidence suggests that Eif41b locus has an oocyte-restricted expression across all classes of Tetrapoda. To further understand the role of eIF4E1B during oocyte maturation, injections of antisense morpholino nucleotides in the X. tropicalis fully-grown stage VI oocytes were performed. The resulted ablation of eIF4E1B protein led to significant acceleration of oocyte maturation after progesterone induction; morpholino-injected oocytes formed the metaphase plate 30 min faster than the control groups. These results suggest that eIF4E1B protein acts as a repressor in translational regulation of maternal mRNAs activated during, and required for, oocyte maturation.

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    ABSTRACT: Caenorhabditis elegans expresses five family members of the translation initiation factor eIF4E whose individual physiological roles are only partially understood. We report a specific role for IFE-2 in a conserved temperature-sensitive meiotic process. ife-2 deletion mutants have severe temperature-sensitive chromosome-segregation defects. Mutant germ cells contain the normal six bivalents at diakinesis at 20 degrees C but 12 univalents at 25 degrees C, indicating a defect in crossover formation. Analysis of chromosome pairing in ife-2 mutants at the permissive and restrictive temperatures reveals no defects. The presence of RAD-51-marked early recombination intermediates and 12 well condensed univalents indicate that IFE-2 is not essential for formation of meiotic double-strand breaks or their repair through homologous recombination but is required for crossover formation. However, RAD-51 foci in ife-2 mutants persist into inappropriately late stages of meiotic prophase at 25 degrees C, similar to mutants defective in MSH-4/HIM-14 and MSH-5, which stabilize a critical intermediate in crossover formation. In wild-type worms, mRNAs for msh-4/him-14 and msh-5 shift from free messenger ribonucleoproteins to polysomes at 25 degrees C but not in ife-2 mutants, suggesting that IFE-2 translationally upregulates synthesis of MSH-4/HIM-14 and MSH-5 at elevated temperatures to stabilize Holliday junctions. This is confirmed by an IFE-2-dependent increase in MSH-5 protein levels.
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