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The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli

When Escherichia coli encounters stress, the endoribonuclease MazF initiates a post-transcriptional response that results in the reprogramming of protein synthesis. By removing the 3΄-terminus of the 16S rRNA, MazF generates specialized ribosomes that selectively translate mRNAs likewise processed b...

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Autores principales: Temmel, Hannes, Müller, Christian, Sauert, Martina, Vesper, Oliver, Reiss, Ariela, Popow, Johannes, Martinez, Javier, Moll, Isabella
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
RNA
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5416887/
https://www.ncbi.nlm.nih.gov/pubmed/27789694
http://dx.doi.org/10.1093/nar/gkw1018
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author Temmel, Hannes
Müller, Christian
Sauert, Martina
Vesper, Oliver
Reiss, Ariela
Popow, Johannes
Martinez, Javier
Moll, Isabella
author_facet Temmel, Hannes
Müller, Christian
Sauert, Martina
Vesper, Oliver
Reiss, Ariela
Popow, Johannes
Martinez, Javier
Moll, Isabella
author_sort Temmel, Hannes
collection PubMed
description When Escherichia coli encounters stress, the endoribonuclease MazF initiates a post-transcriptional response that results in the reprogramming of protein synthesis. By removing the 3΄-terminus of the 16S rRNA, MazF generates specialized ribosomes that selectively translate mRNAs likewise processed by MazF. Given the energy required for de novo ribosome biosynthesis, we considered the existence of a repair mechanism operating upon stress relief to recycle the modified ribosomes. Here, we show that the stress-ribosomes and the 3΄-terminal 16S rRNA fragment are stable during adverse conditions. Moreover, employing in vitro and in vivo approaches we demonstrate that the RNA ligase RtcB catalyzes the re-ligation of the truncated 16S rRNA present in specialized ribosomes Thereby their ability to translate canonical mRNAs is fully restored. Together, our findings not only provide a physiological function for the RNA ligase RtcB in bacteria but highlight the reversibility of ribosome heterogeneity, a crucial but hitherto undescribed concept for translational regulation.
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spelling pubmed-54168872017-05-05 The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli Temmel, Hannes Müller, Christian Sauert, Martina Vesper, Oliver Reiss, Ariela Popow, Johannes Martinez, Javier Moll, Isabella Nucleic Acids Res RNA When Escherichia coli encounters stress, the endoribonuclease MazF initiates a post-transcriptional response that results in the reprogramming of protein synthesis. By removing the 3΄-terminus of the 16S rRNA, MazF generates specialized ribosomes that selectively translate mRNAs likewise processed by MazF. Given the energy required for de novo ribosome biosynthesis, we considered the existence of a repair mechanism operating upon stress relief to recycle the modified ribosomes. Here, we show that the stress-ribosomes and the 3΄-terminal 16S rRNA fragment are stable during adverse conditions. Moreover, employing in vitro and in vivo approaches we demonstrate that the RNA ligase RtcB catalyzes the re-ligation of the truncated 16S rRNA present in specialized ribosomes Thereby their ability to translate canonical mRNAs is fully restored. Together, our findings not only provide a physiological function for the RNA ligase RtcB in bacteria but highlight the reversibility of ribosome heterogeneity, a crucial but hitherto undescribed concept for translational regulation. Oxford University Press 2017-05-05 2016-10-25 /pmc/articles/PMC5416887/ /pubmed/27789694 http://dx.doi.org/10.1093/nar/gkw1018 Text en © The Author(s) 2016. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://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 RNA
Temmel, Hannes
Müller, Christian
Sauert, Martina
Vesper, Oliver
Reiss, Ariela
Popow, Johannes
Martinez, Javier
Moll, Isabella
The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title_full The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title_fullStr The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title_full_unstemmed The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title_short The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli
title_sort rna ligase rtcb reverses mazf-induced ribosome heterogeneity in escherichia coli
topic RNA
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5416887/
https://www.ncbi.nlm.nih.gov/pubmed/27789694
http://dx.doi.org/10.1093/nar/gkw1018
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