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Bacterial tail anchors can target to the mitochondrial outer membrane

BACKGROUND: During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Mitochondria harbor proteomes derived from coding information...

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Autores principales: Lutfullahoğlu-Bal, Güleycan, Keskin, Abdurrahman, Seferoğlu, Ayşe Bengisu, Dunn, Cory D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5525287/
https://www.ncbi.nlm.nih.gov/pubmed/28738827
http://dx.doi.org/10.1186/s13062-017-0187-0
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author Lutfullahoğlu-Bal, Güleycan
Keskin, Abdurrahman
Seferoğlu, Ayşe Bengisu
Dunn, Cory D.
author_facet Lutfullahoğlu-Bal, Güleycan
Keskin, Abdurrahman
Seferoğlu, Ayşe Bengisu
Dunn, Cory D.
author_sort Lutfullahoğlu-Bal, Güleycan
collection PubMed
description BACKGROUND: During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Mitochondria harbor proteomes derived from coding information located both inside and outside the organelle, and the rate-limiting step toward the formation of eukaryotic cells may have been development of an import apparatus allowing protein entry to mitochondria. Currently, a widely conserved translocon allows proteins to pass from the cytosol into mitochondria, but how proteins encoded outside of mitochondria were first directed to these organelles at the dawn of eukaryogenesis is not clear. Because several proteins targeted by a carboxyl-terminal tail anchor (TA) appear to have the ability to insert spontaneously into the mitochondrial outer membrane (OM), it is possible that self-inserting, tail-anchored polypeptides obtained from bacteria might have formed the first gate allowing proteins to access mitochondria from the cytosol. RESULTS: Here, we tested whether bacterial TAs are capable of targeting to mitochondria. In a survey of proteins encoded by the proteobacterium Escherichia coli, predicted TA sequences were directed to specific subcellular locations within the yeast Saccharomyces cerevisiae. Importantly, TAs obtained from DUF883 family members ElaB and YqjD were abundantly localized to and inserted at the mitochondrial OM. CONCLUSIONS: Our results support the notion that eukaryotic cells are able to utilize membrane-targeting signals present in bacterial proteins obtained by lateral gene transfer, and our findings make plausible a model in which mitochondrial protein translocation was first driven by tail-anchored proteins. REVIEWERS: This article was reviewed by Michael Ryan and Thomas Simmen. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13062-017-0187-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-55252872017-07-26 Bacterial tail anchors can target to the mitochondrial outer membrane Lutfullahoğlu-Bal, Güleycan Keskin, Abdurrahman Seferoğlu, Ayşe Bengisu Dunn, Cory D. Biol Direct Research BACKGROUND: During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Mitochondria harbor proteomes derived from coding information located both inside and outside the organelle, and the rate-limiting step toward the formation of eukaryotic cells may have been development of an import apparatus allowing protein entry to mitochondria. Currently, a widely conserved translocon allows proteins to pass from the cytosol into mitochondria, but how proteins encoded outside of mitochondria were first directed to these organelles at the dawn of eukaryogenesis is not clear. Because several proteins targeted by a carboxyl-terminal tail anchor (TA) appear to have the ability to insert spontaneously into the mitochondrial outer membrane (OM), it is possible that self-inserting, tail-anchored polypeptides obtained from bacteria might have formed the first gate allowing proteins to access mitochondria from the cytosol. RESULTS: Here, we tested whether bacterial TAs are capable of targeting to mitochondria. In a survey of proteins encoded by the proteobacterium Escherichia coli, predicted TA sequences were directed to specific subcellular locations within the yeast Saccharomyces cerevisiae. Importantly, TAs obtained from DUF883 family members ElaB and YqjD were abundantly localized to and inserted at the mitochondrial OM. CONCLUSIONS: Our results support the notion that eukaryotic cells are able to utilize membrane-targeting signals present in bacterial proteins obtained by lateral gene transfer, and our findings make plausible a model in which mitochondrial protein translocation was first driven by tail-anchored proteins. REVIEWERS: This article was reviewed by Michael Ryan and Thomas Simmen. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13062-017-0187-0) contains supplementary material, which is available to authorized users. BioMed Central 2017-07-24 /pmc/articles/PMC5525287/ /pubmed/28738827 http://dx.doi.org/10.1186/s13062-017-0187-0 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Lutfullahoğlu-Bal, Güleycan
Keskin, Abdurrahman
Seferoğlu, Ayşe Bengisu
Dunn, Cory D.
Bacterial tail anchors can target to the mitochondrial outer membrane
title Bacterial tail anchors can target to the mitochondrial outer membrane
title_full Bacterial tail anchors can target to the mitochondrial outer membrane
title_fullStr Bacterial tail anchors can target to the mitochondrial outer membrane
title_full_unstemmed Bacterial tail anchors can target to the mitochondrial outer membrane
title_short Bacterial tail anchors can target to the mitochondrial outer membrane
title_sort bacterial tail anchors can target to the mitochondrial outer membrane
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5525287/
https://www.ncbi.nlm.nih.gov/pubmed/28738827
http://dx.doi.org/10.1186/s13062-017-0187-0
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