Cargando…

Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria

Mitochondrial mRNAs encode key subunits of the oxidative phosphorylation complexes that produce energy for the cell. In Saccharomyces cerevisiae, mitochondrial translation is under the control of translational activators, specific to each mRNA. In Schizosaccharomyces pombe, which more closely resemb...

Descripción completa

Detalles Bibliográficos
Autores principales: Herbert, Christopher J, Labarre-Mariotte, Sylvie, Cornu, David, Sophie, Cyrielle, Panozzo, Cristina, Michel, Thomas, Dujardin, Geneviève, Bonnefoy, Nathalie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8565316/
https://www.ncbi.nlm.nih.gov/pubmed/34634819
http://dx.doi.org/10.1093/nar/gkab789
_version_ 1784593800163753984
author Herbert, Christopher J
Labarre-Mariotte, Sylvie
Cornu, David
Sophie, Cyrielle
Panozzo, Cristina
Michel, Thomas
Dujardin, Geneviève
Bonnefoy, Nathalie
author_facet Herbert, Christopher J
Labarre-Mariotte, Sylvie
Cornu, David
Sophie, Cyrielle
Panozzo, Cristina
Michel, Thomas
Dujardin, Geneviève
Bonnefoy, Nathalie
author_sort Herbert, Christopher J
collection PubMed
description Mitochondrial mRNAs encode key subunits of the oxidative phosphorylation complexes that produce energy for the cell. In Saccharomyces cerevisiae, mitochondrial translation is under the control of translational activators, specific to each mRNA. In Schizosaccharomyces pombe, which more closely resembles the human system by its mitochondrial DNA structure and physiology, most translational activators appear to be either lacking, or recruited for post-translational functions. By combining bioinformatics, genetic and biochemical approaches we identified two interacting factors, Cbp7 and Cbp8, controlling Cytb production in S. pombe. We show that their absence affects cytb mRNA stability and impairs the detection of the Cytb protein. We further identified two classes of Cbp7/Cbp8 partners and showed that they modulated Cytb or Cox1 synthesis. First, two isoforms of bS1m, a protein of the small mitoribosomal subunit, that appear mutually exclusive and confer translational specificity. Second, a complex of four proteins dedicated to Cox1 synthesis, which includes an RNA helicase that interacts with the mitochondrial ribosome. Our results suggest that S. pombe contains, in addition to complexes of translational activators, a heterogeneous population of mitochondrial ribosomes that could specifically modulate translation depending on the mRNA translated, in order to optimally balance the production of different respiratory complex subunits.
format Online
Article
Text
id pubmed-8565316
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-85653162021-11-04 Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria Herbert, Christopher J Labarre-Mariotte, Sylvie Cornu, David Sophie, Cyrielle Panozzo, Cristina Michel, Thomas Dujardin, Geneviève Bonnefoy, Nathalie Nucleic Acids Res Molecular Biology Mitochondrial mRNAs encode key subunits of the oxidative phosphorylation complexes that produce energy for the cell. In Saccharomyces cerevisiae, mitochondrial translation is under the control of translational activators, specific to each mRNA. In Schizosaccharomyces pombe, which more closely resembles the human system by its mitochondrial DNA structure and physiology, most translational activators appear to be either lacking, or recruited for post-translational functions. By combining bioinformatics, genetic and biochemical approaches we identified two interacting factors, Cbp7 and Cbp8, controlling Cytb production in S. pombe. We show that their absence affects cytb mRNA stability and impairs the detection of the Cytb protein. We further identified two classes of Cbp7/Cbp8 partners and showed that they modulated Cytb or Cox1 synthesis. First, two isoforms of bS1m, a protein of the small mitoribosomal subunit, that appear mutually exclusive and confer translational specificity. Second, a complex of four proteins dedicated to Cox1 synthesis, which includes an RNA helicase that interacts with the mitochondrial ribosome. Our results suggest that S. pombe contains, in addition to complexes of translational activators, a heterogeneous population of mitochondrial ribosomes that could specifically modulate translation depending on the mRNA translated, in order to optimally balance the production of different respiratory complex subunits. Oxford University Press 2021-10-11 /pmc/articles/PMC8565316/ /pubmed/34634819 http://dx.doi.org/10.1093/nar/gkab789 Text en © The Author(s) 2021. 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 Molecular Biology
Herbert, Christopher J
Labarre-Mariotte, Sylvie
Cornu, David
Sophie, Cyrielle
Panozzo, Cristina
Michel, Thomas
Dujardin, Geneviève
Bonnefoy, Nathalie
Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title_full Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title_fullStr Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title_full_unstemmed Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title_short Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria
title_sort translational activators and mitoribosomal isoforms cooperate to mediate mrna-specific translation in schizosaccharomyces pombe mitochondria
topic Molecular Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8565316/
https://www.ncbi.nlm.nih.gov/pubmed/34634819
http://dx.doi.org/10.1093/nar/gkab789
work_keys_str_mv AT herbertchristopherj translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT labarremariottesylvie translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT cornudavid translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT sophiecyrielle translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT panozzocristina translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT michelthomas translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT dujardingenevieve translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria
AT bonnefoynathalie translationalactivatorsandmitoribosomalisoformscooperatetomediatemrnaspecifictranslationinschizosaccharomycespombemitochondria