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Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing

Isoleucyl-tRNA synthetase (IleRS) is unusual among aminoacyl-tRNA synthetases in having a tRNA-dependent pre-transfer editing activity. Alongside the typical bacterial IleRS (such as Escherichia coli IleRS), some bacteria also have the enzymes (eukaryote-like) that cluster with eukaryotic IleRSs and...

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Autores principales: Cvetesic, Nevena, Dulic, Morana, Bilus, Mirna, Sostaric, Nikolina, Lenhard, Boris, Gruic-Sovulj, Ita
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4861432/
https://www.ncbi.nlm.nih.gov/pubmed/26921320
http://dx.doi.org/10.1074/jbc.M115.698225
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author Cvetesic, Nevena
Dulic, Morana
Bilus, Mirna
Sostaric, Nikolina
Lenhard, Boris
Gruic-Sovulj, Ita
author_facet Cvetesic, Nevena
Dulic, Morana
Bilus, Mirna
Sostaric, Nikolina
Lenhard, Boris
Gruic-Sovulj, Ita
author_sort Cvetesic, Nevena
collection PubMed
description Isoleucyl-tRNA synthetase (IleRS) is unusual among aminoacyl-tRNA synthetases in having a tRNA-dependent pre-transfer editing activity. Alongside the typical bacterial IleRS (such as Escherichia coli IleRS), some bacteria also have the enzymes (eukaryote-like) that cluster with eukaryotic IleRSs and exhibit low sensitivity to the antibiotic mupirocin. Our phylogenetic analysis suggests that the ileS1 and ileS2 genes of contemporary bacteria are the descendants of genes that might have arisen by an ancient duplication event before the separation of bacteria and archaea. We present the analysis of evolutionary constraints of the synthetic and editing reactions in eukaryotic/eukaryote-like IleRSs, which share a common origin but diverged through adaptation to different cell environments. The enzyme from the yeast cytosol exhibits tRNA-dependent pre-transfer editing analogous to E. coli IleRS. This argues for the presence of this proofreading in the common ancestor of both IleRS types and an ancient origin of the synthetic site-based quality control step. Yet surprisingly, the eukaryote-like enzyme from Streptomyces griseus IleRS lacks this capacity; at the same time, its synthetic site displays the 10(3)-fold drop in sensitivity to antibiotic mupirocin relative to the yeast enzyme. The discovery that pre-transfer editing is optional in IleRSs lends support to the notion that the conserved post-transfer editing domain is the main checkpoint in these enzymes. We substantiated this by showing that under error-prone conditions S. griseus IleRS is able to rescue the growth of an E. coli lacking functional IleRS, providing the first evidence that tRNA-dependent pre-transfer editing in IleRS is not essential for cell viability.
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spelling pubmed-48614322016-05-10 Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing Cvetesic, Nevena Dulic, Morana Bilus, Mirna Sostaric, Nikolina Lenhard, Boris Gruic-Sovulj, Ita J Biol Chem Protein Synthesis and Degradation Isoleucyl-tRNA synthetase (IleRS) is unusual among aminoacyl-tRNA synthetases in having a tRNA-dependent pre-transfer editing activity. Alongside the typical bacterial IleRS (such as Escherichia coli IleRS), some bacteria also have the enzymes (eukaryote-like) that cluster with eukaryotic IleRSs and exhibit low sensitivity to the antibiotic mupirocin. Our phylogenetic analysis suggests that the ileS1 and ileS2 genes of contemporary bacteria are the descendants of genes that might have arisen by an ancient duplication event before the separation of bacteria and archaea. We present the analysis of evolutionary constraints of the synthetic and editing reactions in eukaryotic/eukaryote-like IleRSs, which share a common origin but diverged through adaptation to different cell environments. The enzyme from the yeast cytosol exhibits tRNA-dependent pre-transfer editing analogous to E. coli IleRS. This argues for the presence of this proofreading in the common ancestor of both IleRS types and an ancient origin of the synthetic site-based quality control step. Yet surprisingly, the eukaryote-like enzyme from Streptomyces griseus IleRS lacks this capacity; at the same time, its synthetic site displays the 10(3)-fold drop in sensitivity to antibiotic mupirocin relative to the yeast enzyme. The discovery that pre-transfer editing is optional in IleRSs lends support to the notion that the conserved post-transfer editing domain is the main checkpoint in these enzymes. We substantiated this by showing that under error-prone conditions S. griseus IleRS is able to rescue the growth of an E. coli lacking functional IleRS, providing the first evidence that tRNA-dependent pre-transfer editing in IleRS is not essential for cell viability. American Society for Biochemistry and Molecular Biology 2016-04-15 2016-02-26 /pmc/articles/PMC4861432/ /pubmed/26921320 http://dx.doi.org/10.1074/jbc.M115.698225 Text en © 2016 by The American Society for Biochemistry and Molecular Biology, Inc. Author's Choice—Final version free via Creative Commons CC-BY license (http://creativecommons.org/licenses/by/4.0) .
spellingShingle Protein Synthesis and Degradation
Cvetesic, Nevena
Dulic, Morana
Bilus, Mirna
Sostaric, Nikolina
Lenhard, Boris
Gruic-Sovulj, Ita
Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title_full Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title_fullStr Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title_full_unstemmed Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title_short Naturally Occurring Isoleucyl-tRNA Synthetase without tRNA-dependent Pre-transfer Editing
title_sort naturally occurring isoleucyl-trna synthetase without trna-dependent pre-transfer editing
topic Protein Synthesis and Degradation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4861432/
https://www.ncbi.nlm.nih.gov/pubmed/26921320
http://dx.doi.org/10.1074/jbc.M115.698225
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