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Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast

During eukaryotic ribosome biogenesis, pre-ribosomes travel from the nucleolus, where assembly is initiated, to the nucleoplasm and then are exported to the cytoplasm, where assembly concludes. Although nuclear export of pre-ribosomes has been extensively investigated, the release of pre-ribosomes f...

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Autores principales: LaPeruta, Amber J, Micic, Jelena, Woolford Jr., John L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639060/
https://www.ncbi.nlm.nih.gov/pubmed/35736211
http://dx.doi.org/10.1093/nar/gkac430
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author LaPeruta, Amber J
Micic, Jelena
Woolford Jr., John L
author_facet LaPeruta, Amber J
Micic, Jelena
Woolford Jr., John L
author_sort LaPeruta, Amber J
collection PubMed
description During eukaryotic ribosome biogenesis, pre-ribosomes travel from the nucleolus, where assembly is initiated, to the nucleoplasm and then are exported to the cytoplasm, where assembly concludes. Although nuclear export of pre-ribosomes has been extensively investigated, the release of pre-ribosomes from the nucleolus is an understudied phenomenon. Initial data indicate that unfolded rRNA interacts in trans with nucleolar components and that, when rRNA folds due to ribosomal protein (RP) binding, the number of trans interactions drops below the threshold necessary for nucleolar retention. To validate and expand on this idea, we performed a bioinformatic analysis of the protein components of the Saccharomyces cerevisiae ribosome assembly pathway. We found that ribosome biogenesis factors (RiBi factors) contain significantly more predicted trans interacting regions than RPs. We also analyzed cryo-EM structures of ribosome assembly intermediates to determine how nucleolar pre-ribosomes differ from post-nucleolar pre-ribosomes, specifically the capacity of RPs, RiBi factors, and rRNA components to interact in trans. We observed a significant decrease in the theoretical trans-interacting capability of pre-ribosomes between nucleolar and post-nucleolar stages of assembly due to the release of RiBi factors from particles and the folding of rRNA. Here, we provide a mechanism for the release of pre-ribosomes from the nucleolus.
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spelling pubmed-106390602023-11-15 Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast LaPeruta, Amber J Micic, Jelena Woolford Jr., John L Nucleic Acids Res Computational Biology During eukaryotic ribosome biogenesis, pre-ribosomes travel from the nucleolus, where assembly is initiated, to the nucleoplasm and then are exported to the cytoplasm, where assembly concludes. Although nuclear export of pre-ribosomes has been extensively investigated, the release of pre-ribosomes from the nucleolus is an understudied phenomenon. Initial data indicate that unfolded rRNA interacts in trans with nucleolar components and that, when rRNA folds due to ribosomal protein (RP) binding, the number of trans interactions drops below the threshold necessary for nucleolar retention. To validate and expand on this idea, we performed a bioinformatic analysis of the protein components of the Saccharomyces cerevisiae ribosome assembly pathway. We found that ribosome biogenesis factors (RiBi factors) contain significantly more predicted trans interacting regions than RPs. We also analyzed cryo-EM structures of ribosome assembly intermediates to determine how nucleolar pre-ribosomes differ from post-nucleolar pre-ribosomes, specifically the capacity of RPs, RiBi factors, and rRNA components to interact in trans. We observed a significant decrease in the theoretical trans-interacting capability of pre-ribosomes between nucleolar and post-nucleolar stages of assembly due to the release of RiBi factors from particles and the folding of rRNA. Here, we provide a mechanism for the release of pre-ribosomes from the nucleolus. Oxford University Press 2022-06-23 /pmc/articles/PMC10639060/ /pubmed/35736211 http://dx.doi.org/10.1093/nar/gkac430 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Computational Biology
LaPeruta, Amber J
Micic, Jelena
Woolford Jr., John L
Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title_full Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title_fullStr Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title_full_unstemmed Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title_short Additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
title_sort additional principles that govern the release of pre-ribosomes from the nucleolus into the nucleoplasm in yeast
topic Computational Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639060/
https://www.ncbi.nlm.nih.gov/pubmed/35736211
http://dx.doi.org/10.1093/nar/gkac430
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