Cited by 404Redox biology and oxidative stressSulfur Compounds in BiologyGlutathione Transferases and Polymorphisms

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Glutaredoxin 2 Catalyzes the Reversible Oxidation and Glutathionylation of Mitochondrial Membrane Thiol Proteins

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Beer, Samantha M., Taylor, Ellen R., Brown, Stephanie E., Dahm, Christina C., Costa, Nikola J., Runswick, Michael J., Murphy, Michael P.·2004·Journal of Biological Chemistry

DOI 10.1074/jbc.m408011200

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Abstract

The redox poise of the mitochondrial glutathione pool is central in the response of mitochondria to oxidative damage and redox signaling, but the mechanisms are uncertain. One possibility is that the oxidation of glutathione (GSH) to glutathione disulfide (GSSG) and the consequent change in the GSH/GSSG ratio causes protein thiols to change their redox state, enabling protein function to respond reversibly to redox signals and oxidative damage. However, little is known about the interplay between the mitochondrial glutathione pool and protein thiols. Therefore we investigated how physiological GSH/GSSG ratios affected the redox state of mitochondrial membrane protein thiols. Exposure to oxidized GSH/GSSG ratios led to the reversible oxidation of reactive protein thiols by thiol-disulfide exchange, the extent of which was dependent on the GSH/GSSG ratio. There was an initial rapid phase of protein thiol oxidation, followed by gradual oxidation over 30 min. A large number of mitochondrial proteins contain reactive thiols and most of these formed intraprotein disulfides upon oxidation by GSSG; however, a small number formed persistent mixed disulfides with glutathione. Both protein disulfide formation and glutathionylation were catalyzed by the mitochondrial thiol transferase glutaredoxin 2 (Grx2), as were protein deglutathionylation and the reduction of protein disulfides by GSH. Complex I was the most prominent protein that was persistently glutathionylated by GSSG in the presence of Grx2. Maintenance of complex I with an oxidized GSH/GSSG ratio led to a dramatic loss of activity, suggesting that oxidation of the mitochondrial glutathione pool may contribute to the selective complex I inactivation seen in Parkinson's disease. Most significantly, Grx2 catalyzed reversible protein glutathionylation/deglutathionylation over a wide range of GSH/GSSG ratios, from the reduced levels accessible under redox signaling to oxidized ratios only found under severe oxidative stress. Our findings indicate that Grx2 plays a central role in the response of mitochondria to both redox signals and oxidative stress by facilitating the interplay between the mitochondrial glutathione pool and protein thiols. The redox poise of the mitochondrial glutathione pool is central in the response of mitochondria to oxidative damage and redox signaling, but the mechanisms are uncertain. One possibility is that the oxidation of glutathione (GSH) to glutathione disulfide (GSSG) and the consequent change in the GSH/GSSG ratio causes protein thiols to change their redox state, enabling protein function to respond reversibly to redox signals and oxidative damage. However, little is known about the interplay between the mitochondrial glutathione pool and protein thiols. Therefore we investigated how physiological GSH/GSSG ratios affected the redox state of mitochondrial membrane protein thiols. Exposure to oxidized GSH/GSSG ratios led to the reversible oxidation of reactive protein thiols by thiol-disulfide exchange, the extent of which was dependent on the GSH/GSSG ratio. There was an initial rapid phase of protein thiol oxidation, followed by gradual oxidation over 30 min. A large number of mitochondrial proteins contain reactive thiols and most of these formed intraprotein disulfides upon oxidation by GSSG; however, a small number formed persistent mixed disulfides with glutathione. Both protein disulfide formation and glutathionylation were catalyzed by the mitochondrial thiol transferase glutaredoxin 2 (Grx2), as were protein deglutathionylation and the reduction of protein disulfides by GSH. Complex I was the most prominent protein that was persistently glutathionylated by GSSG in the presence of Grx2. Maintenance of complex I with an oxidized GSH/GSSG ratio led to a dramatic loss of activity, suggesting that oxidation of the mitochondrial glutathione pool may contribute to the selective complex I inactivation seen in Parkinson's disease. Most significantly, Grx2 catalyzed reversible protein glutathionylation/deglutathionylation over a wide range of GSH/GSSG ratios, from the reduced levels accessible under redox signaling to oxidized ratios only found under severe oxidative stress. Our findings indicate that Grx2 plays a central role in the response of mitochondria to both redox signals and oxidative stress by facilitating the interplay between the mitochondrial glutathione pool and protein thiols. Oxidative damage and redox signaling can regulate protein thiol redox state (1Gilbert H.F. Methods Enzymol. 1984; 107: 330-351Crossref PubMed Scopus (236) Google Scholar, 2Schafer F.Q. Buettner G.R. Free Rad. Biol. Med. 2002; 30: 1191-1212Crossref Scopus (3655) Google Scholar, 3Gilbert H.F. Methods Enzymol. 1995; 251: 8-28Crossref PubMed Scopus Google Scholar, H.F. Enzymol. Google A in which is the response of protein thiols to in the glutathione (GSH) to glutathione disulfide (GSSG) ratio F.Q. Buettner G.R. Free Rad. Biol. Med. 2002; 30: 1191-12

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Authors: Beer, S. M., Taylor, E. R., Brown, S. E., Dahm, C. C., Costa, N. J., Runswick, M. J., & Murphy, M. P.
Affiliations: MRC Mitochondrial Biology Unit (GB)
Corresponding author: Murphy, Michael P.
ORCID: Brown, Stephanie E.
Dahm, Christina C.
Murphy, Michael P.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2004-11
Volume: 279
Issue: 46
Pages: 47939-47951
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m408011200
OpenAlex: W2133966054
Cited by: 404
References: 52
Citations by year: 2026: 8 · 2025: 12 · 2024: 6 · 2023: 12 · 2022: 19 · 2021: 11 · 2020: 18 · 2019: 11 · 2018: 15 · 2017: 19 · 2016: 10 · 2015: 20 · 2014: 26 · 2013: 17 · 2012: 32
FWCI: 8.29
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 5799 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Sulfur Compounds in Biology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glutathione Transferases and Polymorphisms
Keywords: glutaredoxin 2, glutathionylation, deglutathionylation, GSH/GSSG ratio, thiol-disulfide exchange, mitochondrial complex I, oxidative stress, redox signaling, Parkinson's disease, mitochondrial membrane proteins, mixed disulfides, protein oxidation
MeSH terms: Amino Acid Sequence, Animals, Antioxidants, Cattle, Disulfides, Glutathione, Membrane Proteins, Molecular Sequence Data, Oxidation-Reduction, Oxidoreductases, Sulfhydryl Compounds, Oxidative Stress, Glutathione Disulfide, Mitochondrial Proteins, Electron Transport Complex I, Mice, Glutaredoxins

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Glutaredoxin 2 Catalyzes the Reversible Oxidation and Glutathionylation of Mitochondrial Membrane Thiol Proteins

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