The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent

Class I glutaredoxins reversibly reduce glutathione- and nonglutathione disulfides with the help of reduced glutathione (GSH) using either a monothiol mechanism or a dithiol mechanism. The monothiol mechanism exclusively involves a single glutathionylated active-site cysteinyl residue, whereas the d...

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Main Authors: Lukas Lang, Philipp Reinert, Cedric Diaz, Marcel Deponte
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231724003884
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author Lukas Lang
Philipp Reinert
Cedric Diaz
Marcel Deponte
author_facet Lukas Lang
Philipp Reinert
Cedric Diaz
Marcel Deponte
author_sort Lukas Lang
collection DOAJ
description Class I glutaredoxins reversibly reduce glutathione- and nonglutathione disulfides with the help of reduced glutathione (GSH) using either a monothiol mechanism or a dithiol mechanism. The monothiol mechanism exclusively involves a single glutathionylated active-site cysteinyl residue, whereas the dithiol mechanism requires the additional formation of an intramolecular disulfide bond between the active-site cysteinyl residue and a resolving cysteinyl residue. While the oxidation of glutaredoxins by glutathione disulfide substrates has been extensively characterized, the enzyme-substrate interactions for the reduction of S-glutathionylated glutaredoxins or intramolecular glutaredoxin disulfides are still poorly characterized. Here we compared the thiol-specificity for the reduction of S-glutathionylated glutaredoxins and the intramolecular glutaredoxin disulfide. We show that S-glutathionylated glutaredoxins rapidly react with a plethora of thiols and that the 2nd glutathione-interaction site of class I glutaredoxins lacks specificity for GSH as a reducing agent. In contrast, the slower reduction of the partially strained intramolecular glutaredoxin disulfide involves specific interactions with both carboxylate groups of GSH at the 1st glutathione-interaction site. Thus, the dithiol mechanism of class I glutaredoxins promotes specificity for GSH as a reducing agent, which might explain the prevalence of dithiol glutaredoxins in pro- and eukaryotes.
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spelling doaj-art-df2f1c91a17943b78f6635b9d77bc4bb2024-12-08T06:09:57ZengElsevierRedox Biology2213-23172024-12-0178103410The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agentLukas Lang0Philipp Reinert1Cedric Diaz2Marcel Deponte3Faculty of Chemistry, Comparative Biochemistry, RPTU Kaiserslautern, D-67663, Kaiserslautern, GermanyFaculty of Chemistry, Comparative Biochemistry, RPTU Kaiserslautern, D-67663, Kaiserslautern, GermanyFaculty of Chemistry, Comparative Biochemistry, RPTU Kaiserslautern, D-67663, Kaiserslautern, GermanyCorresponding author.; Faculty of Chemistry, Comparative Biochemistry, RPTU Kaiserslautern, D-67663, Kaiserslautern, GermanyClass I glutaredoxins reversibly reduce glutathione- and nonglutathione disulfides with the help of reduced glutathione (GSH) using either a monothiol mechanism or a dithiol mechanism. The monothiol mechanism exclusively involves a single glutathionylated active-site cysteinyl residue, whereas the dithiol mechanism requires the additional formation of an intramolecular disulfide bond between the active-site cysteinyl residue and a resolving cysteinyl residue. While the oxidation of glutaredoxins by glutathione disulfide substrates has been extensively characterized, the enzyme-substrate interactions for the reduction of S-glutathionylated glutaredoxins or intramolecular glutaredoxin disulfides are still poorly characterized. Here we compared the thiol-specificity for the reduction of S-glutathionylated glutaredoxins and the intramolecular glutaredoxin disulfide. We show that S-glutathionylated glutaredoxins rapidly react with a plethora of thiols and that the 2nd glutathione-interaction site of class I glutaredoxins lacks specificity for GSH as a reducing agent. In contrast, the slower reduction of the partially strained intramolecular glutaredoxin disulfide involves specific interactions with both carboxylate groups of GSH at the 1st glutathione-interaction site. Thus, the dithiol mechanism of class I glutaredoxins promotes specificity for GSH as a reducing agent, which might explain the prevalence of dithiol glutaredoxins in pro- and eukaryotes.http://www.sciencedirect.com/science/article/pii/S2213231724003884Enzyme mechanismDisulfideDithiolGlutaredoxinGlutathioneRedox catalysis
spellingShingle Lukas Lang
Philipp Reinert
Cedric Diaz
Marcel Deponte
The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
Redox Biology
Enzyme mechanism
Disulfide
Dithiol
Glutaredoxin
Glutathione
Redox catalysis
title The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
title_full The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
title_fullStr The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
title_full_unstemmed The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
title_short The dithiol mechanism of class I glutaredoxins promotes specificity for glutathione as a reducing agent
title_sort dithiol mechanism of class i glutaredoxins promotes specificity for glutathione as a reducing agent
topic Enzyme mechanism
Disulfide
Dithiol
Glutaredoxin
Glutathione
Redox catalysis
url http://www.sciencedirect.com/science/article/pii/S2213231724003884
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