A molecular network of conserved factors keeps ribosomes dormant in the egg

معا للقضاء على التشيع

  • 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. & Sauvageau, G. Haploinsufficiency screen highlights two distinct groups of ribosomal protein genes essential for embryonic stem cell fate. Proc. Natl Acad. Sci. USA 112, 2127–2132 (2015).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Amsterdam, A. et al. Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol. 2, E139 (2004).

    Article 

    Google Scholar 

  • Vecchi, G. et al. Proteome-wide observation of the phenomenon of life on the edge of solubility. Proc. Natl Acad. Sci. USA 117, 1015–1020 (2020).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Liu, Y. et al. Autophagy-dependent ribosomal RNA degradation is essential for maintaining nucleotide homeostasis during C. elegans development. eLife 7, e36588 (2018).

    Article 

    Google Scholar 

  • Cohen, J. Statistical Power Analysis for the Behavioral Sciences https://doi.org/10.4324/9780203771587 (Routledge, 1988).

  • Juszkiewicz, S. et al. ZNF598 is a quality control sensor of collided ribosomes. Mol. Cell 72, 469–481.e7 (2018).

    Article 
    CAS 

    Google Scholar 

  • Li, W. et al. Structural basis for selective stalling of human ribosome nascent chain complexes by a drug-like molecule. Nat. Struct. Mol. Biol. 26, 501–509 (2019).

    Article 

    Google Scholar 

  • Chandrasekaran, V. et al. Mechanism of ribosome stalling during translation of a poly(A) tail. Nat. Struct. Mol. Biol. 26, 1132–1140 (2019).

    Article 
    CAS 

    Google Scholar 

  • Gagnon, J. A. et al. Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 9, e98186 (2014).

    Article 
    ADS 

    Google Scholar 

  • Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343–345 (2009).

    Article 
    CAS 

    Google Scholar 

  • Nair, S., Lindeman, R. E. & Pelegri, F. In vitro oocyte culture-based manipulation of zebrafish maternal genes. Dev. Dyn. 242, 44–52 (2013).

    Article 
    CAS 

    Google Scholar 

  • Sive, H. L., Grainger, R. M. & Harland, R. M. Early Development of Xenopus laevis (Cold Spring Harbor Laboratory Press, 2000).

  • Khatter, H. et al. Purification, characterization and crystallization of the human 80S ribosome. Nucleic Acids Res. 42, e49 (2014).

    Article 
    CAS 

    Google Scholar 

  • Dorfer, V. et al. MS Amanda, a universal identification algorithm optimized for high accuracy tandem mass spectra. J. Proteome Res. 13, 3679–3684 (2014).

    Article 
    CAS 

    Google Scholar 

  • Käll, L., Canterbury, J. D., Weston, J., Noble, W. S. & MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4, 923–925 (2007).

    Article 

    Google Scholar 

  • Taus, T. et al. Universal and confident phosphorylation site localization using phosphoRS. J. Proteome Res. 10, 5354–5362 (2011).

    Article 
    CAS 

    Google Scholar 

  • Doblmann, J. et al. apQuant: accurate label-free quantification by quality filtering. J. Proteome Res. 18, 535–541 (2019).

    CAS 

    Google Scholar 

  • Smyth, G. K. in Bioinformatics and Computational Biology Solutions Using R and Bioconductor (eds. Gentleman, R. et al.) 397–420 (Springer, 2005).

  • Pirklbauer, G. J. et al. MS Annika: a new cross-linking search engine. J. Proteome Res. 20, 2560–2569 (2021).

    Article 
    CAS 

    Google Scholar 

  • Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).

    Article 
    CAS 

    Google Scholar 

  • Sharma, A., Mariappan, M., Appathurai, S. & Hegde, R. S. In vitro dissection of protein translocation into the mammalian endoplasmic reticulum. Methods Mol. Biol. 619, 339–363 (2010).

    Article 
    CAS 

    Google Scholar 

  • Feng, Q. & Shao, S. In vitro reconstitution of translational arrest pathways. Methods 137, 20–36 (2018).

    Article 
    CAS 

    Google Scholar 

  • Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).

    Article 
    CAS 

    Google Scholar 

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article 
    CAS 

    Google Scholar 

  • Sanchez-Garcia, R. et al. DeepEMhancer: a deep learning solution for cryo-EM volume post-processing. Commun. Biol. 4, 874 (2021).

    Article 

    Google Scholar 

  • Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).

    Article 

    Google Scholar 

  • Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D 75, 861–877 (2019).

    Article 
    CAS 

    Google Scholar 

  • Yang, H. et al. Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank. Acta Crystallogr. D 60, 1833–1839 (2004).

    Article 

    Google Scholar 

  • Cabrera-Quio, L. E., Schleiffer, A., Mechtler, K. & Pauli, A. Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition. PLoS Genet. 17, e1009390 (2021).

    Article 
    CAS 

    Google Scholar 

  • Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).

    Article 
    CAS 

    Google Scholar 

  • Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Fujihara, Y. et al. The conserved fertility factor SPACA4/Bouncer has divergent modes of action in vertebrate fertilization. Proc. Natl Acad. Sci. USA 118, e2108777118 (2021).

    Article 
    CAS 

    Google Scholar 

  • Gagnon, M. G. et al. Structures of proline-rich peptides bound to the ribosome reveal a common mechanism of protein synthesis inhibition. Nucleic Acids Res. 44, 2439–2450 (2016).

    Article 
    CAS 

    Google Scholar 

  • Florin, T. et al. An antimicrobial peptide that inhibits translation by trapping release factors on the ribosome. Nat. Struct. Mol. Biol. 24, 752–757 (2017).

    Article 
    CAS 

    Google Scholar 

  • Kargas, V. et al. Mechanism of completion of peptidyltransferase centre assembly in eukaryotes. eLife 8, e44904 (2019).

    Article 
    CAS 

    Google Scholar 

  • Wu, S. et al. Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature 534, 133–137 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Polikanov, Y. S., Steitz, T. A. & Innis, C. A. A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol. 21, 787–793 (2014).

    Article 
    CAS 

    Google Scholar 

  • معا للقضاء على التشيع

    اترك تعليقاً

    لن يتم نشر عنوان بريدك الإلكتروني.

    زر الذهاب إلى الأعلى
    إغلاق