Home LiteratureArticle Details
PMID: 12119401 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems.

Casagrande S, Bonetto V, Fratelli M, Gianazza E, Eberini I, Massignan T, Salmona M, Chang G, Holmgren A, Ghezzi P

Abstract

To identify proteins undergoing glutathionylation (formation of protein-glutathione mixed disulfides) in human T cell blasts, we radiolabeled the glutathione pool with (35)S, exposed cells to the oxidant diamide, and analyzed cellular proteins by two-dimensional electrophoresis. One of the proteins undergoing glutathionylation was identified by molecular weight, isoelectric point, and immunoblotting as thioredoxin (Trx). Incubation of recombinant human Trx with glutathione disulfide or S-nitrosoglutathione led to the formation of glutathionylated Trx, identified by matrix-assisted laser desorption ionization-time-of-flight mass spectrometry. The glutathionylation site was identified as Cys-72. Glutathionylation of rhTrx abolished its enzymatic activity as insulin disulfide reductase in the presence of NADPH and Trx reductase. Activity was, however, regained with sigmoidal kinetics, indicating a process of autoactivation due to the ability of Trx to de-glutathionylate itself. These data suggest that the intracellular glutathione/glutathione disulfide ratio, an indicator of the redox state of the cell, can regulate Trx functions reversibly through thiol-disulfide exchange reactions.

MeSH Terms
Amino Acid Sequence Cells, Cultured Diamide/pharmacology Glutathione/metabolism Glutathione Disulfide/metabolism Humans Insulin/metabolism Kinetics Molecular Sequence Data Peptide Fragments/chemistry Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization T-Lymphocytes/metabolism Thioredoxins/chemistry,metabolism Trypsin
Chemicals
Insulin Peptide Fragments Diamide Thioredoxins Trypsin Glutathione Glutathione Disulfide
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Casagrande Simona
Mario Negri Institute for Pharmacological Research, Department of Biochemistry, 20157 Milan, Italy.
Bonetto Valentina
Fratelli Maddalena
Gianazza Elisabetta
Eberini Ivano
Massignan Tania
Salmona Mario
Chang Geng
Holmgren Arne
Ghezzi Pietro
References (33)
33 references, click to expand
  1. Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5854-9 PMID: 10801974
  2. Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH.
    Anal Biochem. 2000 Aug 1;283(2):214-21 PMID: 10906242
  3. Physiological functions of thioredoxin and thioredoxin reductase.
    Eur J Biochem. 2000 Oct;267(20):6102-9 PMID: 11012661
  4. Crystal structure of S-glutathiolated carbonic anhydrase III.
    FEBS Lett. 2000 Oct 6;482(3):237-41 PMID: 11024467
  5. Reaction of S-nitrosoglutathione with the heme group of deoxyhemoglobin.
    J Biol Chem. 2000 Nov 24;275(47):36562-7 PMID: 10945989
  6. Posttranslational modification of the glycosylation inhibiting factor (GIF) gene product generates bioactive GIF.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13251-6 PMID: 11069294
  7. Truncated thioredoxin is a mitogenic cytokine for resting human peripheral blood mononuclear cells and is present in human plasma.
    J Biol Chem. 2000 Dec 1;275(48):37474-80 PMID: 10982790
  8. Novel application of S-nitrosoglutathione-Sepharose to identify proteins that are potential targets for S-nitrosoglutathione-induced mixed-disulphide formation.
    Biochem J. 2000 Jul 15;349(Pt 2):567-78 PMID: 10880356
  9. S-nitrosylation: spectrum and specificity.
    Nat Cell Biol. 2001 Feb;3(2):E46-9 PMID: 11175760
  10. Glutathiolation of proteins by glutathione disulfide S-oxide derived from S-nitrosoglutathione. Modifications of rat brain neurogranin/RC3 and neuromodulin/GAP-43.
    J Biol Chem. 2001 Feb 2;276(5):3098-105 PMID: 11060308
  11. Proteolysis in mixed organic-aqueous solvent systems: applications for peptide mass mapping using mass spectrometry.
    Anal Chem. 2001 Jun 1;73(11):2682-5 PMID: 11403317
  12. Protein glutathionylation: coupling and uncoupling of glutathione to protein thiol groups in lymphocytes under oxidative stress and HIV infection.
    Mol Immunol. 2002 Feb;38(10):773-80 PMID: 11841837
  13. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  14. Isolation and characterization of calf liver thioredoxin.
    J Biol Chem. 1974 Jan 10;249(1):205-10 PMID: 4809626
  15. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli.
    J Biol Chem. 1980 Nov 10;255(21):10261-5 PMID: 7000775
  16. Rat liver thioredoxin and thioredoxin reductase: purification and characterization.
    Biochemistry. 1982 Dec 21;21(26):6628-33 PMID: 7159551
  17. Relative contributions of thioltransferase-and thioredoxin-dependent systems in reduction of low-molecular-mass and protein disulphides.
    Biochem J. 1983 Aug 1;213(2):519-23 PMID: 6351844
  18. Thioredoxin.
    Annu Rev Biochem. 1985;54:237-71 PMID: 3896121
  19. Thioredoxin and glutaredoxin systems.
    J Biol Chem. 1989 Aug 25;264(24):13963-6 PMID: 2668278
  20. Oxidized redox state of glutathione in the endoplasmic reticulum.
    Science. 1992 Sep 11;257(5076):1496-502 PMID: 1523409
  21. Mutagenesis of structural half-cystine residues in human thioredoxin and effects on the regulation of activity by selenodiglutathione.
    Biochemistry. 1993 Sep 21;32(37):9701-8 PMID: 8373774
  22. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1672-6 PMID: 8127864
  23. S-thiolation of glyceraldehyde-3-phosphate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes.
    J Biol Chem. 1994 Oct 7;269(40):25010-5 PMID: 7929187
  24. Redox regulation of cellular activation.
    Annu Rev Immunol. 1997;15:351-69 PMID: 9143692
  25. Recent trends in glutathione biochemistry--glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation?
    Biochem Biophys Res Commun. 1998 Jan 6;242(1):1-9 PMID: 9439600
  26. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1.
    EMBO J. 1998 May 1;17(9):2596-606 PMID: 9564042
  27. Measurements of plasma glutaredoxin and thioredoxin in healthy volunteers and during open-heart surgery.
    Free Radic Biol Med. 1998 May;24(7-8):1176-86 PMID: 9626572
  28. Nitric oxide inhibits c-Jun N-terminal kinase 2 (JNK2) via S-nitrosylation.
    Biochem Biophys Res Commun. 1998 Jun 29;247(3):809-13 PMID: 9647775
  29. Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells.
    J Exp Med. 1999 Jun 7;189(11):1783-9 PMID: 10359582
  30. Isoelectric focusing as a tool for the investigation of post-translational processing and chemical modifications of proteins.
    J Chromatogr A. 1995 Jun 23;705(1):67-87 PMID: 7620573
  31. Glutaredoxin.
    Methods Enzymol. 1995;252:283-92 PMID: 7476363
  32. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer.
    Structure. 1996 Jun 15;4(6):735-51 PMID: 8805557
  33. Oxidative inactivation of thioredoxin as a cellular growth factor and protection by a Cys73-->Ser mutation.
    Biochem Pharmacol. 1996 Dec 13;52(11):1741-7 PMID: 8986137
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-07-23
Epub
2002-00-15
Pages
9745-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC125000
Subset
IM
Grants
Telethon · TCP01010 · Italy
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com