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Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases

Glycyl tRNA synthetase (GlyRS) provides a unique case among class II aminoacyl tRNA synthetases, with two clearly widespread types of enzymes: a dimeric (α(2)) species present in some bacteria, archaea, and eukaryotes; and a heterotetrameric form (α(2)β(2)) present in most bacteria. Although the dif...

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Autores principales: Valencia-Sánchez, Marco Igor, Rodríguez-Hernández, Annia, Ferreira, Ruben, Santamaría-Suárez, Hugo Aníbal, Arciniega, Marcelino, Dock-Bregeon, Anne-Catherine, Moras, Dino, Beinsteiner, Brice, Mertens, Haydyn, Svergun, Dmitri, Brieba, Luis G., Grøtli, Morten, Torres-Larios, Alfredo
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/PMC4938167/
https://www.ncbi.nlm.nih.gov/pubmed/27226617
http://dx.doi.org/10.1074/jbc.M116.730382
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author Valencia-Sánchez, Marco Igor
Rodríguez-Hernández, Annia
Ferreira, Ruben
Santamaría-Suárez, Hugo Aníbal
Arciniega, Marcelino
Dock-Bregeon, Anne-Catherine
Moras, Dino
Beinsteiner, Brice
Mertens, Haydyn
Svergun, Dmitri
Brieba, Luis G.
Grøtli, Morten
Torres-Larios, Alfredo
author_facet Valencia-Sánchez, Marco Igor
Rodríguez-Hernández, Annia
Ferreira, Ruben
Santamaría-Suárez, Hugo Aníbal
Arciniega, Marcelino
Dock-Bregeon, Anne-Catherine
Moras, Dino
Beinsteiner, Brice
Mertens, Haydyn
Svergun, Dmitri
Brieba, Luis G.
Grøtli, Morten
Torres-Larios, Alfredo
author_sort Valencia-Sánchez, Marco Igor
collection PubMed
description Glycyl tRNA synthetase (GlyRS) provides a unique case among class II aminoacyl tRNA synthetases, with two clearly widespread types of enzymes: a dimeric (α(2)) species present in some bacteria, archaea, and eukaryotes; and a heterotetrameric form (α(2)β(2)) present in most bacteria. Although the differences between both types of GlyRS at the anticodon binding domain level are evident, the extent and implications of the variations in the catalytic domain have not been described, and it is unclear whether the mechanism of amino acid recognition is also dissimilar. Here, we show that the α-subunit of the α(2)β(2) GlyRS from the bacterium Aquifex aeolicus is able to perform the first step of the aminoacylation reaction, which involves the activation of the amino acid with ATP. The crystal structure of the α-subunit in the complex with an analog of glycyl adenylate at 2.8 Å resolution presents a conformational arrangement that properly positions the cognate amino acid. This work shows that glycine is recognized by a subset of different residues in the two types of GlyRS. A structural and sequence analysis of class II catalytic domains shows that bacterial GlyRS is closely related to alanyl tRNA synthetase, which led us to define a new subclassification of these ancient enzymes and to propose an evolutionary path of α(2)β(2) GlyRS, convergent with α(2) GlyRS and divergent from AlaRS, thus providing a possible explanation for the puzzling existence of two proteins sharing the same fold and function but not a common ancestor.
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spelling pubmed-49381672016-07-19 Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases Valencia-Sánchez, Marco Igor Rodríguez-Hernández, Annia Ferreira, Ruben Santamaría-Suárez, Hugo Aníbal Arciniega, Marcelino Dock-Bregeon, Anne-Catherine Moras, Dino Beinsteiner, Brice Mertens, Haydyn Svergun, Dmitri Brieba, Luis G. Grøtli, Morten Torres-Larios, Alfredo J Biol Chem Protein Structure and Folding Glycyl tRNA synthetase (GlyRS) provides a unique case among class II aminoacyl tRNA synthetases, with two clearly widespread types of enzymes: a dimeric (α(2)) species present in some bacteria, archaea, and eukaryotes; and a heterotetrameric form (α(2)β(2)) present in most bacteria. Although the differences between both types of GlyRS at the anticodon binding domain level are evident, the extent and implications of the variations in the catalytic domain have not been described, and it is unclear whether the mechanism of amino acid recognition is also dissimilar. Here, we show that the α-subunit of the α(2)β(2) GlyRS from the bacterium Aquifex aeolicus is able to perform the first step of the aminoacylation reaction, which involves the activation of the amino acid with ATP. The crystal structure of the α-subunit in the complex with an analog of glycyl adenylate at 2.8 Å resolution presents a conformational arrangement that properly positions the cognate amino acid. This work shows that glycine is recognized by a subset of different residues in the two types of GlyRS. A structural and sequence analysis of class II catalytic domains shows that bacterial GlyRS is closely related to alanyl tRNA synthetase, which led us to define a new subclassification of these ancient enzymes and to propose an evolutionary path of α(2)β(2) GlyRS, convergent with α(2) GlyRS and divergent from AlaRS, thus providing a possible explanation for the puzzling existence of two proteins sharing the same fold and function but not a common ancestor. American Society for Biochemistry and Molecular Biology 2016-07-08 2016-05-23 /pmc/articles/PMC4938167/ /pubmed/27226617 http://dx.doi.org/10.1074/jbc.M116.730382 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 Structure and Folding
Valencia-Sánchez, Marco Igor
Rodríguez-Hernández, Annia
Ferreira, Ruben
Santamaría-Suárez, Hugo Aníbal
Arciniega, Marcelino
Dock-Bregeon, Anne-Catherine
Moras, Dino
Beinsteiner, Brice
Mertens, Haydyn
Svergun, Dmitri
Brieba, Luis G.
Grøtli, Morten
Torres-Larios, Alfredo
Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title_full Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title_fullStr Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title_full_unstemmed Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title_short Structural Insights into the Polyphyletic Origins of Glycyl tRNA Synthetases
title_sort structural insights into the polyphyletic origins of glycyl trna synthetases
topic Protein Structure and Folding
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4938167/
https://www.ncbi.nlm.nih.gov/pubmed/27226617
http://dx.doi.org/10.1074/jbc.M116.730382
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