XB-ART-59528
Nature
2023 Jan 01;6137945:712-720. doi: 10.1038/s41586-022-05623-y.
Show Gene links
Show Anatomy links
A molecular network of conserved factors keeps ribosomes dormant in the egg.
Leesch F
,
Lorenzo-Orts L
,
Pribitzer C
,
Grishkovskaya I
,
Roehsner J
,
Chugunova A
,
Matzinger M
,
Roitinger E
,
Belačić K
,
Kandolf S
,
Lin TY
,
Mechtler K
,
Meinhart A
,
Haselbach D
,
Pauli A
.
???displayArticle.abstract???
Ribosomes are produced in large quantities during oogenesis and are stored in the egg. However, the egg and early embryo are translationally repressed1-4. Here, using mass spectrometry and cryo-electron microscopy analyses of ribosomes isolated from zebrafish (Danio rerio) and Xenopus laevis eggs and embryos, we provide molecular evidence that ribosomes transition from a dormant state to an active state during the first hours of embryogenesis. Dormant ribosomes are associated with four conserved factors that form two modules, consisting of Habp4-eEF2 and death associated protein 1b (Dap1b) or Dap in complex with eIF5a. Both modules occupy functionally important sites and act together to stabilize ribosomes and repress translation. Dap1b (also known as Dapl1 in mammals) is a newly discovered translational inhibitor that stably inserts into the polypeptide exit tunnel. Addition of recombinant zebrafish Dap1b protein is sufficient to block translation and reconstitute the dormant egg ribosome state in a mammalian translation extract in vitro. Thus, a developmentally programmed, conserved ribosome state has a key role in ribosome storage and translational repression in the egg.
???displayArticle.pubmedLink??? 36653451
???displayArticle.pmcLink??? PMC7614339
???displayArticle.link??? Nature
???displayArticle.grants??? [+]
Genes referenced: dap eif5a habp4
References [+] :
Amsterdam,
Many ribosomal protein genes are cancer genes in zebrafish.
2004, Pubmed
Amsterdam, Many ribosomal protein genes are cancer genes in zebrafish. 2004, Pubmed
Anger, Structures of the human and Drosophila 80S ribosome. 2013, Pubmed
Bachvarova, Stored and polysomal ribosomes of mouse ova. 1977, Pubmed
Balagopal, Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. 2011, Pubmed
Barandun, Evolutionary compaction and adaptation visualized by the structure of the dormant microsporidian ribosome. 2019, Pubmed
Beckert, Structure of a hibernating 100S ribosome reveals an inactive conformation of the ribosomal protein S1. 2018, Pubmed
Beckert, Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. 2017, Pubmed
Blobel, Studies on free and membrane-bound ribosomes in rat liver. I. Distribution as related to total cellular RNA. 1967, Pubmed
Brandis, Translation of oogenetic mRNA in sea urchin eggs and early embryos. Demonstration of a change in translational efficiency following fertilization. 1978, Pubmed
Brown, Structures of translationally inactive mammalian ribosomes. 2018, Pubmed
Burkholder, A storage form of ribosomes in mouse oocytes. 1971, Pubmed
Cabrera-Quio, Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition. 2021, Pubmed
Casteels, Apidaecins: antibacterial peptides from honeybees. 1989, Pubmed
Cenik, Maternal Ribosomes Are Sufficient for Tissue Diversification during Embryonic Development in C. elegans. 2019, Pubmed
Chandrasekaran, Mechanism of ribosome stalling during translation of a poly(A) tail. 2019, Pubmed
Chassé, Translational Control of Canonical and Non-Canonical Translation Initiation Factors at the Sea Urchin Egg to Embryo Transition. 2019, Pubmed
Chassé, Analysis of translation using polysome profiling. 2017, Pubmed
Chew, Ribosome profiling reveals resemblance between long non-coding RNAs and 5' leaders of coding RNAs. 2013, Pubmed
Danilchik, Sea urchin egg and embryo ribosomes: differences in translational activity in a cell-free system. 1981, Pubmed
Deiss, Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. 1995, Pubmed
Doblmann, apQuant: Accurate Label-Free Quantification by Quality Filtering. 2019, Pubmed
Dorfer, MS Amanda, a universal identification algorithm optimized for high accuracy tandem mass spectra. 2014, Pubmed
Emsley, Coot: model-building tools for molecular graphics. 2004, Pubmed
Feng, In vitro reconstitution of translational arrest pathways. 2018, Pubmed
Flis, tRNA Translocation by the Eukaryotic 80S Ribosome and the Impact of GTP Hydrolysis. 2018, Pubmed
Florin, An antimicrobial peptide that inhibits translation by trapping release factors on the ribosome. 2017, Pubmed
Fortier, Haploinsufficiency screen highlights two distinct groups of ribosomal protein genes essential for embryonic stem cell fate. 2015, Pubmed
Fujihara, The conserved fertility factor SPACA4/Bouncer has divergent modes of action in vertebrate fertilization. 2021, Pubmed
Gagnon, Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. 2014, Pubmed
Gagnon, Structures of proline-rich peptides bound to the ribosome reveal a common mechanism of protein synthesis inhibition. 2016, Pubmed
Gambino, Properties of the ribosomal salt wash from unfertilized and fertilized sea urchin eggs and its effect on natural mRNA translation. 1973, Pubmed
Gibson, Enzymatic assembly of DNA molecules up to several hundred kilobases. 2009, Pubmed
Goddard, UCSF ChimeraX: Meeting modern challenges in visualization and analysis. 2018, Pubmed
Greber, Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. 2012, Pubmed
Gutierrez, eIF5A promotes translation of polyproline motifs. 2013, Pubmed
Hayashi, Tight interaction of eEF2 in the presence of Stm1 on ribosome. 2018, Pubmed
Hille, Inhibitor of protein synthesis isolated from ribosomes of unfertilised eggs and embryos of sea urchins. 1974, Pubmed
Juszkiewicz, ZNF598 Is a Quality Control Sensor of Collided Ribosomes. 2018, Pubmed
Kao, Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. 2011, Pubmed
Kargas, Mechanism of completion of peptidyltransferase centre assembly in eukaryotes. 2019, Pubmed
Khatter, Purification, characterization and crystallization of the human 80S ribosome. 2014, Pubmed
Klingauf-Nerurkar, The GTPase Nog1 co-ordinates the assembly, maturation and quality control of distant ribosomal functional centers. 2020, Pubmed
Koren, DAP1, a novel substrate of mTOR, negatively regulates autophagy. 2010, Pubmed
Krizsan, Short Proline-Rich Antimicrobial Peptides Inhibit Either the Bacterial 70S Ribosome or the Assembly of its Large 50S Subunit. 2015, Pubmed
Kronja, Widespread changes in the posttranscriptional landscape at the Drosophila oocyte-to-embryo transition. 2014, Pubmed
Käll, Semi-supervised learning for peptide identification from shotgun proteomics datasets. 2007, Pubmed
Li, Structural basis for selective stalling of human ribosome nascent chain complexes by a drug-like molecule. 2019, Pubmed
Liebschner, Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. 2019, Pubmed
Liu, Autophagy-dependent ribosomal RNA degradation is essential for maintaining nucleotide homeostasis during C. elegans development. 2018, Pubmed
Locati, Linking maternal and somatic 5S rRNA types with different sequence-specific non-LTR retrotransposons. 2017, Pubmed
Locati, Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development. 2017, Pubmed , Xenbase
Ma, Regulation of cell proliferation in the retinal pigment epithelium: Differential regulation of the death-associated protein like-1 DAPL1 by alternative MITF splice forms. 2018, Pubmed
Ma, DAPL1, a susceptibility locus for age-related macular degeneration, acts as a novel suppressor of cell proliferation in the retinal pigment epithelium. 2017, Pubmed
Marygold, The ribosomal protein genes and Minute loci of Drosophila melanogaster. 2007, Pubmed
Metafora, The mechanism of protein synthesis activation after fertilization of sea urchin eggs. 1971, Pubmed
Nair, In vitro oocyte culture-based manipulation of zebrafish maternal genes. 2013, Pubmed
Park, Functional significance of eIF5A and its hypusine modification in eukaryotes. 2010, Pubmed
Pauli, Toddler: an embryonic signal that promotes cell movement via Apelin receptors. 2014, Pubmed
Perez-Riverol, The PRIDE database and related tools and resources in 2019: improving support for quantification data. 2019, Pubmed
Pettersen, UCSF Chimera--a visualization system for exploratory research and analysis. 2004, Pubmed
Pirklbauer, MS Annika: A New Cross-Linking Search Engine. 2021, Pubmed
Polikanov, A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. 2014, Pubmed
Punjani, cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. 2017, Pubmed
Rodnina, Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. 1997, Pubmed
Rossi, Evidence for a Negative Cooperativity between eIF5A and eEF2 on Binding to the Ribosome. 2016, Pubmed
Saini, Hypusine-containing protein eIF5A promotes translation elongation. 2009, Pubmed
Sanchez-Garcia, DeepEMhancer: a deep learning solution for cryo-EM volume post-processing. 2021, Pubmed
Schmidt, Structure of the hypusinylated eukaryotic translation factor eIF-5A bound to the ribosome. 2016, Pubmed
Schuller, eIF5A Functions Globally in Translation Elongation and Termination. 2017, Pubmed
Seefeldt, Structure of the mammalian antimicrobial peptide Bac7(1-16) bound within the exit tunnel of a bacterial ribosome. 2016, Pubmed
Session, Genome evolution in the allotetraploid frog Xenopus laevis. 2016, Pubmed , Xenbase
Sharma, In vitro dissection of protein translocation into the mammalian endoplasmic reticulum. 2010, Pubmed
Shetty, TORC1 phosphorylates and inhibits the ribosome preservation factor Stm1 to activate dormant ribosomes. 2023, Pubmed
Smith, The space between notes: emerging roles for translationally silent ribosomes. 2022, Pubmed
Smith, Functionally distinct roles for eEF2K in the control of ribosome availability and p-body abundance. 2021, Pubmed
Stebbins-Boaz, Maskin is a CPEB-associated factor that transiently interacts with elF-4E. 1999, Pubmed , Xenbase
Subtelny, Poly(A)-tail profiling reveals an embryonic switch in translational control. 2014, Pubmed , Xenbase
Sun, EEDA: a protein associated with an early stage of stratified epithelial differentiation. 2006, Pubmed
Taus, Universal and confident phosphorylation site localization using phosphoRS. 2011, Pubmed
Van Dyke, Stm1p, a ribosome-associated protein, is important for protein synthesis in Saccharomyces cerevisiae under nutritional stress conditions. 2006, Pubmed
Vecchi, Proteome-wide observation of the phenomenon of life on the edge of solubility. 2020, Pubmed
Wells, Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes. 2020, Pubmed
Woodland, Changes in the polysome content of developing Xenopus laevis embryos. 1974, Pubmed , Xenbase
Wu, Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. 2016, Pubmed
Yang, Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank. 2004, Pubmed
Zhong, CryoDRGN: reconstruction of heterogeneous cryo-EM structures using neural networks. 2021, Pubmed