C. elegans eIF4E-family member upregulates translation at elevated temperatures of mRNAs encoding MSH-5 and other meiotic crossover proteins

• Published in: Journal of cell science Vol. 123; no. 13; pp. 2228 - 2237
• Main Authors: Song, Anren, Labella, Sara, Korneeva, Nadejda L, Keiper, Brett D, Aamodt, Eric J, Zetka, Monique, Rhoads, Robert E
• Format: Journal Article
• Language: English
• Published: England The Company of Biologists Limited 01.07.2010; Company of Biologists
• Subjects: Animals; Caenorhabditis elegans - genetics; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Crossing Over, Genetic; DNA - genetics; DNA - metabolism; DNA - radiation effects; DNA Breaks, Double-Stranded; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Eukaryotic Initiation Factor-4E - genetics; Eukaryotic Initiation Factor-4E - metabolism; Female; Hot Temperature; Male; Meiosis - physiology; Mutation; Oogenesis - physiology; Phenotype; Protein Biosynthesis; Recombinant Fusion Proteins - genetics; Recombinant Fusion Proteins - metabolism; RNA, Messenger - genetics; RNA, Messenger - metabolism; Spermatogenesis - physiology
• ISSN: 0021-9533; 1477-9137
• DOI: 10.1242/jcs.063107

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°C but 12 univalents at 25°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°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°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.