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A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis

Sulfuration of uridine 8, in bacterial and archaeal tRNAs, is catalyzed by enzymes formerly known as ThiI, but renamed here TtuI. Two different classes of TtuI proteins, which possess a PP-loop-containing pyrophosphatase domain that includes a conserved cysteine important for catalysis, have been id...

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Autores principales: He, Nisha, Zhou, Jingjing, Bimai, Ornella, Oltmanns, Jonathan, Ravanat, Jean-Luc, Velours, Christophe, Schünemann, Volker, Fontecave, Marc, Golinelli-Pimpaneau, Béatrice
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825150/
https://www.ncbi.nlm.nih.gov/pubmed/36533440
http://dx.doi.org/10.1093/nar/gkac1156
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author He, Nisha
Zhou, Jingjing
Bimai, Ornella
Oltmanns, Jonathan
Ravanat, Jean-Luc
Velours, Christophe
Schünemann, Volker
Fontecave, Marc
Golinelli-Pimpaneau, Béatrice
author_facet He, Nisha
Zhou, Jingjing
Bimai, Ornella
Oltmanns, Jonathan
Ravanat, Jean-Luc
Velours, Christophe
Schünemann, Volker
Fontecave, Marc
Golinelli-Pimpaneau, Béatrice
author_sort He, Nisha
collection PubMed
description Sulfuration of uridine 8, in bacterial and archaeal tRNAs, is catalyzed by enzymes formerly known as ThiI, but renamed here TtuI. Two different classes of TtuI proteins, which possess a PP-loop-containing pyrophosphatase domain that includes a conserved cysteine important for catalysis, have been identified. The first class, as exemplified by the prototypic Escherichia coli enzyme, possesses an additional C-terminal rhodanese domain harboring a second cysteine, which serves to form a catalytic persulfide. Among the second class of TtuI proteins that do not possess the rhodanese domain, some archaeal proteins display a conserved CXXC + C motif. We report here spectroscopic and enzymatic studies showing that TtuI from Methanococcus maripaludis and Pyrococcus furiosus can assemble a [4Fe–4S] cluster that is essential for tRNA sulfuration activity. Moreover, structural modeling studies, together with previously reported mutagenesis experiments of M. maripaludis TtuI, indicate that the [4Fe–4S] cluster is coordinated by the three cysteines of the CXXC + C motif. Altogether, our results raise a novel mechanism for U8-tRNA sulfuration, in which the cluster is proposed to catalyze the transfer of sulfur atoms to the activated tRNA substrate.
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spelling pubmed-98251502023-01-09 A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis He, Nisha Zhou, Jingjing Bimai, Ornella Oltmanns, Jonathan Ravanat, Jean-Luc Velours, Christophe Schünemann, Volker Fontecave, Marc Golinelli-Pimpaneau, Béatrice Nucleic Acids Res Nucleic Acid Enzymes Sulfuration of uridine 8, in bacterial and archaeal tRNAs, is catalyzed by enzymes formerly known as ThiI, but renamed here TtuI. Two different classes of TtuI proteins, which possess a PP-loop-containing pyrophosphatase domain that includes a conserved cysteine important for catalysis, have been identified. The first class, as exemplified by the prototypic Escherichia coli enzyme, possesses an additional C-terminal rhodanese domain harboring a second cysteine, which serves to form a catalytic persulfide. Among the second class of TtuI proteins that do not possess the rhodanese domain, some archaeal proteins display a conserved CXXC + C motif. We report here spectroscopic and enzymatic studies showing that TtuI from Methanococcus maripaludis and Pyrococcus furiosus can assemble a [4Fe–4S] cluster that is essential for tRNA sulfuration activity. Moreover, structural modeling studies, together with previously reported mutagenesis experiments of M. maripaludis TtuI, indicate that the [4Fe–4S] cluster is coordinated by the three cysteines of the CXXC + C motif. Altogether, our results raise a novel mechanism for U8-tRNA sulfuration, in which the cluster is proposed to catalyze the transfer of sulfur atoms to the activated tRNA substrate. Oxford University Press 2022-12-19 /pmc/articles/PMC9825150/ /pubmed/36533440 http://dx.doi.org/10.1093/nar/gkac1156 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://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 Nucleic Acid Enzymes
He, Nisha
Zhou, Jingjing
Bimai, Ornella
Oltmanns, Jonathan
Ravanat, Jean-Luc
Velours, Christophe
Schünemann, Volker
Fontecave, Marc
Golinelli-Pimpaneau, Béatrice
A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title_full A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title_fullStr A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title_full_unstemmed A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title_short A subclass of archaeal U8-tRNA sulfurases requires a [4Fe–4S] cluster for catalysis
title_sort subclass of archaeal u8-trna sulfurases requires a [4fe–4s] cluster for catalysis
topic Nucleic Acid Enzymes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825150/
https://www.ncbi.nlm.nih.gov/pubmed/36533440
http://dx.doi.org/10.1093/nar/gkac1156
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