Abstract
Formation of mixed disulfides between glutathione and the cysteines of some proteins (glutathionylation) has been suggested as a mechanism through which protein functions can be regulated by the redox status. The aim of this study was to identify the proteins of T cell blasts that undergo glutathionylation under oxidative stress. To this purpose, we radiolabeled cellular glutathione with (35)S, exposed T cells to oxidants (diamide or hydrogen peroxide), and performed nonreducing, two-dimensional electrophoresis followed by detection of labeled proteins by phosphorimaging and their identification by mass spectrometry techniques. We detected several proteins previously not recognized to be glutathionylated, including cytoskeletal proteins (vimentin, myosin, tropomyosin, cofilin, profilin, and the already known actin), enzymes (enolase, aldolase, 6-phosphogluconolactonase, adenylate kinase, ubiquitin-conjugating enzyme, phosphoglycerate kinase, triosephosphate isomerase, and pyrophosphatase), redox enzymes (peroxiredoxin 1, protein disulfide isomerase, and cytochrome c oxidase), cyclophilin, stress proteins (HSP70 and HSP60), nucleophosmin, transgelin, galectin, and fatty acid binding protein. Based on the presence of several protein isoforms in control cells, we suggest that enolase and cyclophilin are heavily glutathionylated under basal conditions. We studied the effect of glutathionylation on some of the enzymes identified in the present study and found that some of them (enolase and 6-phosphogluconolactonase) are inhibited by glutathionylation, whereas the enzymatic activity of cyclophilin (peptidylprolyl isomerase) is not. These findings suggest that protein glutathionylation might be a common mechanism for the global regulation of protein functions.
MeSH Terms
Cells, Cultured
Diamide/pharmacology
Disulfides/metabolism
Electrophoresis, Gel, Two-Dimensional
Glutathione/metabolism
Humans
Hydrogen Peroxide/pharmacology
Mass Spectrometry
Molecular Weight
Oxidants/pharmacology
Oxidation-Reduction/drug effects
Oxidative Stress/drug effects
Proteome/chemistry,drug effects,metabolism
Rosaniline Dyes
Staining and Labeling
T-Lymphocytes/chemistry,drug effects,enzymology,metabolism
Chemicals
Disulfides
Oxidants
Proteome
Rosaniline Dyes
Diamide
Coomassie blue
Hydrogen Peroxide
Glutathione
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Fratelli Maddalena
Mario Negri Institute for Pharmacological Research, 20157 Milan, Italy.
Demol Hans
Puype Magda
Casagrande Simona
Eberini Ivano
Salmona Mario
Bonetto Valentina
Mengozzi Manuela
Duffieux Francis
Miclet Emeric
Bachi Angela
Vandekerckhove Joel
Gianazza Elisabetta
Ghezzi Pietro
References (33)
33 references, click to expand
-
Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans.
Biochem Biophys Res Commun. 1999 Oct 22;264(2):580-3
PMID: 10529405
-
Redox regulation of c-Jun DNA binding by reversible S-glutathiolation.
FASEB J. 1999 Sep;13(12):1481-90
PMID: 10463938
-
Protein identification methods in proteomics.
Electrophoresis. 2000 Apr;21(6):1145-54
PMID: 10786887
-
S-NO-actin: S-nitrosylation kinetics and the effect on isolated vascular smooth muscle.
J Muscle Res Cell Motil. 2000 Feb;21(2):171-81
PMID: 10961840
-
Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae.
J Biol Chem. 2000 Sep 1;275(35):27393-8
PMID: 10852912
-
Identification of oxidant-sensitive proteins: TNF-alpha induces protein glutathiolation.
Biochemistry. 2000 Sep 12;39(36):11121-8
PMID: 10998251
-
Protein S-nitrosylation: a physiological signal for neuronal nitric oxide.
Nat Cell Biol. 2001 Feb;3(2):193-7
PMID: 11175752
-
Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation.
J Biol Chem. 2001 Aug 3;276(31):29596-602
PMID: 11395496
-
NMR spectroscopic analysis of the first two steps of the pentose-phosphate pathway elucidates the role of 6-phosphogluconolactonase.
J Biol Chem. 2001 Sep 14;276(37):34840-6
PMID: 11457850
-
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
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Initial events in the degradation of soluble cellular enzymes: factors affecting the stability and proteolytic susceptibility of fructose-1,6-bisphosphate aldolase.
Acta Biol Med Ger. 1981;40(10-11):1365-74
PMID: 7044001
-
Role of glutathione in the regulation of inorganic pyrophosphatase activity in Streptococcus faecalis.
J Gen Microbiol. 1982 May;128(5):1023-6
PMID: 6125558
-
Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide.
Biochem Pharmacol. 1983 Sep 1;32(17):2529-34
PMID: 6615548
-
Redox control of enzyme activities by thiol/disulfide exchange.
Methods Enzymol. 1984;107:330-51
PMID: 6239077
-
Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins.
Nature. 1989 Feb 2;337(6206):476-8
PMID: 2492638
-
Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth.
Biochemistry. 1989 Feb 7;28(3):1033-9
PMID: 2713355
-
Exposure of thiol groups and bound nucleotide in G-actin: thiols as an indicator for the native state of actin.
Anticancer Res. 1990 Nov-Dec;10(6):1651-9
PMID: 2285239
-
Phagocytosis and stimulation of the respiratory burst by phorbol diester initiate S-thiolation of specific proteins in macrophages.
J Immunol. 1991 Jul 1;147(1):260-4
PMID: 1646844
-
Oxidized redox state of glutathione in the endoplasmic reticulum.
Science. 1992 Sep 11;257(5076):1496-502
PMID: 1523409
-
Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells.
Am J Physiol. 1994 Feb;266(2 Pt 1):G247-54
PMID: 8141298
-
Redox regulation of signal transduction: tyrosine phosphorylation and calcium influx.
Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3619-22
PMID: 7513425
-
Terminal marking of avian triosephosphate isomerases by deamidation and oxidation.
Arch Biochem Biophys. 1995 Feb 20;317(1):112-20
PMID: 7872772
-
S-nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation.
Am J Physiol. 1995 Sep;269(3 Pt 1):C739-49
PMID: 7573405
-
Regulation of HIV-1 protease activity through cysteine modification.
Biochemistry. 1996 Feb 20;35(7):2482-8
PMID: 8652592
-
Activity of ubiquitin-dependent pathway in response to oxidative stress. Ubiquitin-activating enzyme is transiently up-regulated.
J Biol Chem. 1997 Sep 12;272(37):23086-93
PMID: 9287309
-
Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress.
J Biol Chem. 1997 Nov 7;272(45):28218-26
PMID: 9353272
-
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
-
Peptides adsorbed on reverse-phase chromatographic beads as targets for femtomole sequencing by post-source decay matrix assisted laser desorption ionization-reflectron time of flight mass spectrometry (MALDI-RETOF-MS).
Electrophoresis. 1997 Dec;18(15):2950-60
PMID: 9504835
-
Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns.
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3071-6
PMID: 9501217
-
Glutathione homeostasis is disturbed in CD4-positive lymphocytes of HIV-seropositive individuals.
Eur J Clin Invest. 1998 Mar;28(3):187-93
PMID: 9568463
-
Bridge over troubled waters: sensing stress by disulfide bond formation.
Cell. 1999 Mar 19;96(6):751-3
PMID: 10102262
-
Probability-based protein identification by searching sequence databases using mass spectrometry data.
Electrophoresis. 1999 Dec;20(18):3551-67
PMID: 10612281