Conserved Factors Create Molecular Network to Maintain Ribosome Dormancy in the Egg

Woodland, H. R. Changes in the polysome content of developing Xenopus laevis embryos. Dev. Biol. 40, 90–101 (1974).Article  CAS  Google Scholar  Brandis, J. W. & Raff, R. A. Translation of oogenetic mRNA in sea urchin eggs and early embryos. Demonstration of a change in translational efficiency following fertilization. Dev. Biol. 67, 99–113 (1978).Article  CAS  Google Scholar  Kronja, I. et al. Widespread changes in the posttranscriptional landscape at the Drosophila oocyte-to-embryo transition. Cell Rep. 7, 1495–1508 (2014).Article  CAS  Google Scholar  Bachvarova, R. & De Leon, V. Stored and polysomal ribosomes of mouse ova. Dev. Biol. 58, 248–254 (1977).Article  CAS  Google Scholar  Burkholder, G. D., Comings, D. E. & Okada, T. A. A storage form of ribosomes in mouse oocytes. Exp. Cell. Res. 69, 361–371 (1971).Article  CAS  Google Scholar  Alberts, B. et al. in Molecular Biology of the Cell 5th edn (eds Anderson, M. & Granum, S.) 1287–1291 (Garland Science, 2008).Locati, M. D. et al. Linking maternal and somatic 5S rRNA types with different sequence-specific non-LTR retrotransposons. RNA 23, 446–456 (2017).Article  CAS  Google Scholar  Locati, M. D. et al. Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development. RNA 23, 1188–1199 (2017).Article  CAS  Google Scholar  Cenik, E. S. et al. Maternal ribosomes are sufficient for tissue diversification during embryonic development in C. elegans. Dev. Cell 48, 811–826.e6 (2019).Article  CAS  Google Scholar  Danilchik, M. V. & Hille, M. B. Sea urchin egg and embryo ribosomes: differences in translational activity in a cell-free system. Dev. Biol. 84, 291–298 (1981).Article  CAS  Google Scholar  Chassé, H., Boulben, S., Cormier, P. & Morales, J. Translational control of canonical and non-canonical translation initiation factors at the sea urchin egg to embryo transition. Int. J. Mol. Sci. 20, 626 (2019).Article  Google Scholar  Subtelny, A. O., Eichhorn, S. W., Chen, G. R., Sive, H. & Bartel, D. P. Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508, 66–71 (2014).Article  ADS  CAS  Google Scholar  Stebbins-Boaz, B., Cao, Q., Moor, C. H., de, Mendez, R. & Richter, J. D. Maskin is a CPEB-associated factor that transiently interacts with eIF-4E. Mol. Cell 4, 1017–1027 (1999).Article  CAS  Google Scholar  Smith, P. R., Pandit, S. C., Loerch, S. & Campbell, Z. T. The space between notes: emerging roles for translationally silent ribosomes. Trends Biochem. Sci 47, 477–491 (2022).Article  CAS  Google Scholar  Beckert, B. et al. Structure of a hibernating 100S ribosome reveals an inactive conformation of the ribosomal protein S1. Nat. Microbiol. 3, 1115–1121 (2018).Article  CAS  Google Scholar  Beckert, B. et al. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J. 36, 2061–2072 (2017).Article  CAS  Google Scholar  Barandun, J., Hunziker, M., Vossbrinck, C. R. & Klinge, S. Evolutionary compaction and adaptation visualized by the structure of the dormant microsporidian ribosome. Nat. Microbiol. 4, 1798–1804 (2019).Article  CAS  Google Scholar  Brown, A., Baird, M. R., Yip, M. C., Murray, J. & Shao, S. Structures of translationally inactive mammalian ribosomes. eLife 7, e40486 (2018).Article  Google Scholar  Van Dyke, N., Baby, J. & Van Dyke, M. W. Stm1p, a ribosome-associated protein, is important for protein synthesis in Saccharomyces cerevisiae under nutritional stress conditions. J. Mol. Biol. 358, 1023–1031 (2006).Article  Google Scholar  Smith, P. R. et al. Functionally distinct roles for eEF2K in the control of ribosome availability and p-body abundance. Nat. Commun. 12, 6789 (2021).Article  ADS  CAS  Google Scholar  Shetty, S., Hofstetter, J., Battaglioni, S., Ritz, D. & Hall, M. N. TORC1 phosphorylates and inhibits the ribosome preservation factor Stm1 to activate dormant ribosomes. Preprint at https://doi.org/10.1101/2022.08.08.503151 (2022).Wells, J. N. et al. Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes. PLoS Biol. 18, e3000780 (2020).Article  CAS  Google Scholar  Seefeldt, A. C. et al. Structure of the mammalian antimicrobial peptide Bac7(1–16) bound within the exit tunnel of a bacterial ribosome. Nucleic Acids Res. 44, 2429–2438 (2016).Article  CAS  Google Scholar  Casteels, P., Ampe, C., Jacobs, F., Vaeck, M. & Tempst, P. Apidaecins: antibacterial peptides from honeybees. EMBO J. 8, 2387–2391 (1989).Article  CAS  Google Scholar  Krizsan, A., Prahl, C., Goldbach, T., Knappe, D. & Hoffmann, R. Short proline-rich antimicrobial peptides inhibit either the bacterial 70S ribosome or the assembly of its large 50S subunit. ChemBioChem 16, 2304–2308 (2015).Article  CAS  Google Scholar  Metafora, S., Felicetti, L. & Gambino, R. The mechanism of protein synthesis activation after fertilization of sea urchin eggs. Proc. Natl Acad. Sci. USA 68, 600–604 (1971).Article  ADS  CAS  Google Scholar  Gambino, R., Metafora, S., Felicetti, L. & Raisman, J. Properties of the ribosomal salt wash from unfertilized and fertilized sea urchin eggs and its effect on natural mRNA translation. Biochim. Biophys. Acta 312, 377–391 (1973).Article  CAS  Google Scholar  Hille, M. B. Inhibitor of protein synthesis isolated from ribosomes of unfertilised eggs and embryos of sea urchins. Nature 249, 556–558 (1974).Article  ADS  CAS  Google Scholar  Chassé, H., Boulben, S., Costache, V., Cormier, P. & Morales, J. Analysis of translation using polysome profiling. Nucleic Acids Res. 45, e15 (2017). Google Scholar  Chew, G.-L. et al. Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140, 2828–2834 (2013).Article  CAS  Google Scholar  Pauli, A. et al. Toddler: an embryonic signal that promotes cell movement via apelin receptors. Science 343, 1248636 (2014).Article  Google Scholar  Gutierrez, E. et al. eIF5A promotes translation of polyproline motifs. Mol. Cell 51, 35–45 (2013).Article  CAS  Google Scholar  Schuller, A. P., Wu, C. C.-C., Dever, T. E., Buskirk, A. R. & Green, R. eIF5A functions globally in translation elongation and termination. Mol. Cell 66, 194–205.e5 (2017).Article  CAS  Google Scholar  Schmidt, C. et al. Structure of the hypusinylated eukaryotic translation factor eIF-5A bound to the ribosome. Nucleic Acids Res. 44, 1944–1951 (2016).Article  Google Scholar  Rodnina, M. V., Savelsbergh, A., Katunin, V. I. & Wintermeyer, W. Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37–41 (1997).Article  ADS  CAS  Google Scholar  Flis, J. et al. tRNA translocation by the eukaryotic 80S ribosome and the Impact of GTP hydrolysis. Cell Rep. 25, 2676–2688.e7 (2018).Article  CAS  Google Scholar  Hayashi, H. et al. Tight interaction of eEF2 in the presence of Stm1 on ribosome. J. Biochem. 163, 177–185 (2018).Article  CAS  Google Scholar  Anger, A. M. et al. Structures of the human and Drosophila 80S ribosome. Nature 497, 80–85 (2013).Article  ADS  CAS  Google Scholar  Sun, L., Ryan, D. G., Zhou, M., Sun, T.-T. & Lavker, R. M. EEDA: a protein associated with an early stage of stratified epithelial differentiation. J. Cell. Physiol. 206, 103–111 (2006).Article  CAS  Google Scholar  Ma, X. et al. Regulation of cell proliferation in the retinal pigment epithelium: differential regulation of the death-associated protein like-1 DAPL1 by alternative MITF splice forms. Pigment Cell Melanoma Res. 31, 411–422 (2018).Article  CAS  Google Scholar  Ma, X. et al. DAPL1, a susceptibility locus for age-related macular degeneration, acts as a novel suppressor of cell proliferation in the retinal pigment epithelium. Hum. Mol. Genet. 26, 1612–1621 (2017).Article  CAS  Google Scholar  Deiss, L. P., Feinstein, E., Berissi, H., Cohen, O. & Kimchi, A. Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the γ interferon-induced cell death. Genes Dev. 9, 15–30 (1995).Article  CAS  Google Scholar  Koren, I., Reem, E. & Kimchi, A. DAP1, a novel substrate of mTOR, negatively regulates autophagy. Curr. Biol. 20, 1093–1098 (2010).Article  CAS  Google Scholar  Saini, P., Eyler, D. E., Green, R. & Dever, T. E. Hypusine-containing protein eIF5A promotes translation elongation. Nature 459, 118–121 (2009).Article  ADS  CAS  Google Scholar  Park, M. H., Nishimura, K., Zanelli, C. F. & Valentini, S. R. Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38, 491–500 (2010).Article  CAS  Google Scholar  Greber, B. J., Boehringer, D., Montellese, C. & Ban, N. Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat. Struct. Mol. Biol. 19, 1228–1233 (2012).Article  CAS  Google Scholar  Klingauf-Nerurkar, P. et al. The GTPase Nog1 co-ordinates the assembly, maturation and quality control of distant ribosomal functional centers. eLife 9, e52474 (2020).Article  CAS  Google Scholar  Zhong, E. D., Bepler, T., Berger, B. & Davis, J. H. CryoDRGN: reconstruction of heterogeneous cryo-EM structures using neural networks. Nat. Methods 18, 176–185 (2021).Article  CAS  Google Scholar  Rossi, D. et al. Evidence for a negative cooperativity between eIF5A and eEF2 on binding to the ribosome. PLoS ONE 11, e0154205 (2016).Article  Google Scholar  Kao, A. et al. Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. Mol. Cell. Proteomics 10, M110.002212 (2011).Article  Google Scholar  Balagopal, V. & Parker, R. Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. RNA 17, 835–842 (2011).Article  CAS  Google Scholar  Blobel, G. & Potter, V. R. Studies on free and membrane-bound ribosomes in rat liver: I. Distribution as related to total cellular RNA. J. Mol. Biol. 26, 279–292 (1967).Article  CAS  Google Scholar  Marygold, S. J. et al. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol, 8, R216 (2007).Article  Google Scholar  Fortier, S., MacRae, T., Bilodeau, M., Sargeant, T. &…

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