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Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes

Cells adjust to nutrient deprivation by reversible translational shutdown. This is accompanied by maintaining inactive ribosomes in a hibernation state, in which they are bound by proteins with inhibitory and protective functions. In eukaryotes, such a function was attributed to suppressor of target...

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Autores principales: Wells, Jennifer N., Buschauer, Robert, Mackens-Kiani, Timur, Best, Katharina, Kratzat, Hanna, Berninghausen, Otto, Becker, Thomas, Gilbert, Wendy, Cheng, Jingdong, Beckmann, Roland
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7392345/
https://www.ncbi.nlm.nih.gov/pubmed/32687489
http://dx.doi.org/10.1371/journal.pbio.3000780
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author Wells, Jennifer N.
Buschauer, Robert
Mackens-Kiani, Timur
Best, Katharina
Kratzat, Hanna
Berninghausen, Otto
Becker, Thomas
Gilbert, Wendy
Cheng, Jingdong
Beckmann, Roland
author_facet Wells, Jennifer N.
Buschauer, Robert
Mackens-Kiani, Timur
Best, Katharina
Kratzat, Hanna
Berninghausen, Otto
Becker, Thomas
Gilbert, Wendy
Cheng, Jingdong
Beckmann, Roland
author_sort Wells, Jennifer N.
collection PubMed
description Cells adjust to nutrient deprivation by reversible translational shutdown. This is accompanied by maintaining inactive ribosomes in a hibernation state, in which they are bound by proteins with inhibitory and protective functions. In eukaryotes, such a function was attributed to suppressor of target of Myb protein 1 (Stm1; SERPINE1 mRNA-binding protein 1 [SERBP1] in mammals), and recently, late-annotated short open reading frame 2 (Lso2; coiled-coil domain containing short open reading frame 124 [CCDC124] in mammals) was found to be involved in translational recovery after starvation from stationary phase. Here, we present cryo-electron microscopy (cryo-EM) structures of translationally inactive yeast and human ribosomes. We found Lso2/CCDC124 accumulating on idle ribosomes in the nonrotated state, in contrast to Stm1/SERBP1-bound ribosomes, which display a rotated state. Lso2/CCDC124 bridges the decoding sites of the small with the GTPase activating center (GAC) of the large subunit. This position allows accommodation of the duplication of multilocus region 34 protein (Dom34)-dependent ribosome recycling system, which splits Lso2-containing, but not Stm1-containing, ribosomes. We propose a model in which Lso2 facilitates rapid translation reactivation by stabilizing the recycling-competent state of inactive ribosomes.
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spelling pubmed-73923452020-08-12 Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes Wells, Jennifer N. Buschauer, Robert Mackens-Kiani, Timur Best, Katharina Kratzat, Hanna Berninghausen, Otto Becker, Thomas Gilbert, Wendy Cheng, Jingdong Beckmann, Roland PLoS Biol Research Article Cells adjust to nutrient deprivation by reversible translational shutdown. This is accompanied by maintaining inactive ribosomes in a hibernation state, in which they are bound by proteins with inhibitory and protective functions. In eukaryotes, such a function was attributed to suppressor of target of Myb protein 1 (Stm1; SERPINE1 mRNA-binding protein 1 [SERBP1] in mammals), and recently, late-annotated short open reading frame 2 (Lso2; coiled-coil domain containing short open reading frame 124 [CCDC124] in mammals) was found to be involved in translational recovery after starvation from stationary phase. Here, we present cryo-electron microscopy (cryo-EM) structures of translationally inactive yeast and human ribosomes. We found Lso2/CCDC124 accumulating on idle ribosomes in the nonrotated state, in contrast to Stm1/SERBP1-bound ribosomes, which display a rotated state. Lso2/CCDC124 bridges the decoding sites of the small with the GTPase activating center (GAC) of the large subunit. This position allows accommodation of the duplication of multilocus region 34 protein (Dom34)-dependent ribosome recycling system, which splits Lso2-containing, but not Stm1-containing, ribosomes. We propose a model in which Lso2 facilitates rapid translation reactivation by stabilizing the recycling-competent state of inactive ribosomes. Public Library of Science 2020-07-20 /pmc/articles/PMC7392345/ /pubmed/32687489 http://dx.doi.org/10.1371/journal.pbio.3000780 Text en © 2020 Wells et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wells, Jennifer N.
Buschauer, Robert
Mackens-Kiani, Timur
Best, Katharina
Kratzat, Hanna
Berninghausen, Otto
Becker, Thomas
Gilbert, Wendy
Cheng, Jingdong
Beckmann, Roland
Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title_full Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title_fullStr Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title_full_unstemmed Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title_short Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes
title_sort structure and function of yeast lso2 and human ccdc124 bound to hibernating ribosomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7392345/
https://www.ncbi.nlm.nih.gov/pubmed/32687489
http://dx.doi.org/10.1371/journal.pbio.3000780
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