Cargando…
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...
Autores principales: | , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1782441819927216128 |
---|---|
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. |
format | Online Article Text |
id | pubmed-4938167 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | American Society for Biochemistry and Molecular Biology |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT valenciasanchezmarcoigor structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT rodriguezhernandezannia structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT ferreiraruben structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT santamariasuarezhugoanibal structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT arciniegamarcelino structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT dockbregeonannecatherine structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT morasdino structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT beinsteinerbrice structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT mertenshaydyn structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT svergundmitri structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT briebaluisg structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT grøtlimorten structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases AT torreslariosalfredo structuralinsightsintothepolyphyleticoriginsofglycyltrnasynthetases |