Measurement and meaning of cellular thiol: Disufhide redox status

Free Radical Research

Volumn 50, Issue 2, 2016, Pages 246-271

  Comini, Marcelo A ^a  

^a INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

Glutaredoxin; glutathione; redox biosensor; redox signaling; thioredoxin

Indexed keywords

CYSTEINE; DISULFIDE; METAL; NITROGEN; SELENIUM; SULFENIC ACID DERIVATIVE; THIOL; FLUORESCENT DYE; GLUTATHIONE; PROTEIN; THIOL DERIVATIVE;

ARTICLE; BIOLOGY; BIOSENSOR; ENZYME ANALYSIS; FLUORESCENCE; HUMAN; MOLECULAR PROBE; NONHUMAN; NUCLEOPHILICITY; OXIDATION REDUCTION REACTION; PROTEIN ANALYSIS; PROTEOMICS; QUANTITATIVE ANALYSIS; SUBSTITUTION REACTION; WESTERN BLOTTING; ANIMAL; BACTERIUM; CHEMICAL ANALYSIS; EUKARYOTE; METABOLISM; OXIDATIVE STRESS; PROCEDURES;

ANIMALS; BACTERIA; CHEMISTRY TECHNIQUES, ANALYTICAL; DISULFIDES; EUKARYOTA; FLUORESCENT DYES; GLUTATHIONE; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEINS; PROTEOMICS; SULFHYDRYL COMPOUNDS;

EID: 84955475683     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1110241     Document Type: Article

References (169)

1. Go YM, Chandler JD, Jones DP. The cysteine proteome. Free Radic Biol Med 2015;84:227-245.
2. Ferrer-Sueta G, Manta B, Botti H, Radi R, Trujillo M, Denicola A. Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol 2011;24:434-450.
3. Ghezzi P. Protein glutathionylation in health and disease. Biochim Biophys Acta 2013;1830:3165-3172.
4. Loi VV, Rossius M, Antelmann H. Redox regulation by reversible protein S-thiolation in bacteria. Front Microbiol 2015;6:187
5. Smith BC, Marletta MA. Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling. Curr Opin Chem Biol 2012;16:498-506.
6. Brigelius-Flohé R, Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 2011;15: 2335-2381.
7. Wouters MA, Iismaa S, Fan SW, Haworth NL. Thiol-based redox signalling: rust never sleeps. Int J Biochem Cell Biol 2011;43:1079-1085.
8. Miki H, Funato Y. Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species. J Biochem 2012;151:255-261.
9. Vázquez-Torres A. Redox active thiol sensors of oxidative and nitrosative stress. Antioxid Redox Signal 2012;17:1201-1214.
10. Rouhier N, Cerveau D, Couturier J, Reichheld JP, Rey P. Involvement of thiol-based mechanisms in plant development. Biochim Biophys Acta 2015;1850: 1479-1496.
11. Miseta A, Csutora P. Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Mol Biol Evol 2000;17:1232-1239.
12. Couturier J, Przybyla-Toscano J, Roret T, Didierjean C, Rouhier N. The roles of glutaredoxins ligating Fe-S clusters: sensing, transfer or repair functions? Biochim Biophys Acta 2015;1853:1513-1527.
13. Holmgren A, Johansson C, Berndt C, Lönn ME, Hudemann C, Lillig CH. Thiol redox control via thioredoxin and glutaredoxin systems. Biochem Soc Trans 2005;33:1375-1377.
14. Antelmann H, Helmann JD. Thiol-based redox switches and gene regulation. Antioxid Redox Signal 2011;14:1049-1063.
15. Hanschmann EM, Godoy JR, Berndt C, Hudemann C, Lillig CH. Thioredoxins, glutaredoxins, and peroxiredoxins - molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling. Antioxid Redox Signal 2013;19:1539-1605.
16. Sengupta R, Holmgren A. Thioredoxin and glutaredoxinmediated redox regulation of ribonucleotide reductase. World J Biol Chem 2014;5:68-74.
17. Lu J, Holmgren A. The thioredoxin antioxidant system. Free Radic Biol Med 2014;66:75-87.
18. Antelmann H. Oxidative stress responses and Redox signaling mechanisms in Bacillus subtilis and Staphylococcus aureus. In: Yi-Wei T, Dongyou L, Ian RP, Joseph DS, Max S, eds. Molecular medical microbiology. 2nd ed. New York: Academic Press; 2014:249-274 (Chapter 15).
19. Mohring F, Pretzel J, Jortzik E, Becker K. The redox systems of Plasmodium falciparum and Plasmodium vivax: comparison, in silico analyses and inhibitor studies. Curr Med Chem 2014;21:1728-1756.
20. Williams DL, Bonilla M, Gladyshev VN, Salinas G. Thioredoxin glutathione reductase-dependent redox networks in platyhelminth parasites. Antioxid Redox Signal 2013;19:735-745.
21. Müller S, Liebau E, Walter RD, Krauth-Siegel RL. Thiolbased redox metabolism of protozoan parasites. Trends Parasitol 2003;19:320-328.
22. Manta B, Comini M, Medeiros A, Hugo M, Trujillo M, Radi R. Trypanothione: a unique bis-glutathionyl derivative in trypanosomatids. Biochim Biophys Acta 2013;1830: 3199-3216.
23. Gaballa A, Newton GL, Antelmann H, Parsonage D, Upton H, Rawat M, et al. Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc Natl Acad Sci USA 2010;107:6482-6486.
24. Becker K, Kanzok SM, Iozef R, Fischer M, Schirmer RH, Rahlfs S. Plasmoredoxin, a novel redox-active protein unique for malarial parasites. Eur J Biochem 2003;270: 1057-1064.
25. Bonilla M, Denicola A, Marino SM, Gladyshev VN, Salinas G. Linked thioredoxin-glutathione systems in platyhelminth parasites: alternative pathways for glutathione reduction and deglutathionylation. J Biol Chem 2011;286:4959-4967.
26. Lillig CH, Berndt C. Glutaredoxins in thiol/disulfide exchange. Antioxid Redox Signal 2013;18:1654-1665.
27. Atkinson HJ, Babbitt PC. An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations. PLoS Comput Biol 2009;5:e1000541
28. Jensen KS, Hansen RE, Winther JR. Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation. Antioxid Redox Signal 2009;11:1047-1058.
29. Deponte M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 2013;1830:3217-3266.
30. Berndt C, Lillig CH, Flohé L. Redox regulation by glutathione needs enzymes. Front Pharmacol 2014;5:168
31. Østergaard H, Tachibana C, Winther JR. Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 2004;166:337-345.
32. Nkabyo YS, Ziegler TR, Gu LH, Watson WH, Jones DP. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am J Physiol Gastrointest Liver Physiol 2002;283:G1352-G1359.
33. Berndt C, Lillig CH, Holmgren A. Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 2008;1783:641-650.
34. Go YM, Jones DP. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 2008;1780:1273-1290.
35. Sen CK. Cellular thiols and redox-regulated signal transduction. Curr Top Cell Regul 2000;36:1-30.
36. Cussiol JR, Alegria TG, Szweda LI, Netto LE. Ohr (organic hydroperoxide resistance protein) possesses a previously undescribed activity, lipoyl-dependent peroxidase. J Biol Chem 2010;285:21943-21950.
37. Ferguson AD, Labunskyy VM, Fomenko DE, Araç D, Chelliah Y, Amezcua CA, et al. NMR structures of the selenoproteins Sep15 and SelM reveal redox activity of a new thioredoxin-like family. J Biol Chem 2006;281: 3536-3543.
38. Labunskyy VM, Hatfield DL, Gladyshev VN. The Sep15 protein family: roles in disulfide bond formation and quality control in the endoplasmic reticulum. IUBMB Life 2007;59:1-5.
39. Lu J, Holmgren A. The thioredoxin superfamily in oxidative protein folding. Antioxid Redox Signal 2014;21:457-470.
40. Birk J, Meyer M, Aller I, Hansen HG, Odermatt A, Dick TP, et al. Endoplasmic reticulum: reduced and oxidized glutathione revisited. J Cell Sci 2013;126:1604-1617.
41. Lundstrom-Ljung J, Birnbach U, Rupp K, Soling HD, Holmgren A. Two resident ER-proteins, CaBP1 and CaBP2, with thioredoxin domains, are substrates for thioredoxin reductase: comparison with protein disulfide isomerase. FEBS Lett 1995;357:305-308.
42. Hino Y, Ishio S, Minakami S. Glucose-6-phosphate oxidation pathway in rat-liver microsomal vesicles. Stimulation under oxidative stress. Eur J Biochem 1987;165:195-199.
43. Piccirella S, Czegle I, Lizák B, Margittai E, Senesi S, Papp E, et al. Uncoupled redox systems in the lumen of the endoplasmic reticulum. Pyridine nucleotides stay reduced in an oxidative environment. J Biol Chem 2006;281:4671-4677.
44. Kojer K, Bien M, Gangel H, Morgan B, Dick TP, Riemer J. Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state. Embo J 2012;31:3169-3182.
45. Elbaz-Alon Y, Morgan B, Clancy A, Amoako TN, Zalckvar E, Dick TP, et al. The yeast oligo-peptide transporter Opt2 is localized to peroxisomes and affects glutathione redox homeostasis. FEMS Yeast Res 2014;14:1055-1067.
46. Morgan B, Ezerina D, Amoako TN, Riemer J, Seedorf M, Dick TP. Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat Chem Biol 2013;9:119-125.
47. Schwarzländer M, Dick TP, Meye AJ, Morgan B. Dissecting redox biology using fluorescent protein sensors. Antioxid Redox Signal 2015 Apr 13. [Epub ahead of print] PubMed PMID: 25867539.
48. Østergaard H, Henriksen A, Hansen FG, Winther JR. Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 2001;20:5853-5862.
49. Björnberg O, Østergaard H, Winther JR. Mechanistic insight provided by glutaredoxin within a fusion to redox sensitive yellow fluorescent protein. Biochem 2006;45:2362-2371.
50. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, et al. Real-time imaging of the intracellular glutathione redox potential. Nat Methods 2008;5:553-559.
51. Banerjee R. Redox outside the box: linking extracellular redox remodeling with intracellular redox metabolism. J Biol Chem 2012;287:4397-4402.
52. Hansen RE, Winther JR. An introduction to methods for analyzing thiols and disulfides: reactions, reagents, and practical considerations. Anal Biochem 2009;394: 147-158.
53. Chen X, Zhou Y, Peng X, Yoon J. Fluorescent and colorimetric probes for detection of thiols. Chem Soc Rev 2010;39:2120-2135.
54. LoConte M, Carroll KS. The chemistry of thiol oxidation and detection. In: Jakob U, ed. Oxidative stress and redox regulation. New York: Springer; 2012:1-42 (Chapter 1).
55. Peng H, Chen W, Cheng Y, Hakuna L, Strongin R, Wang B. Thiol reactive probes and chemosensors. Sensors 2012;12:15907-15946.
56. Winther JR, Thorpe C. Quantification of thiols and disulfides. Biochim Biophys Acta 2014;1840:838-846.
57. ELLMAN GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82:70-77.
58. Poole LB, Claiborne A. The non-flavin redox center of the streptococcal NADH peroxidase II. Evidence for a stabilized cysteine-sulfenic acid. J Biol Chem 1989;264:12330-12338.
59. Ellis HR, Poole LB. Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium. Biochemistry 1997;36:13349-13356.
60. Gupta V, Carroll KS. Sulfenic acid chemistry, detection and cellular lifetime. Biochim Biophys Acta 2014;1840:847-875.
61. Laragione T, Bonetto V, Casoni F, Massignan T, Bianchi G, Gianazza E, Ghezzi P. Redox regulation of surface protein thiols: identification of integrin alpha-4 as a molecular target by using redox proteomics. Proc Natl Acad Sci USA 2003;100:14737-14741.
62. Faulstich H, Tews P, Heintz D. Determination and derivatization of protein thiols by n-octyldithionitrobenzoic acid. Anal Biochem 1993;208:357-362.
63. Zhang H, Le M, Means GE. A kinetic approach to characterize the electrostatic environments of thiol groups in proteins. Bioorg Chem. 1998;26:356-364.
64. Zhu J, Dhimitruka I, Pei D. 5(2-Aminoethyl)dithio-2-nitrobenzoate as a more base-stable alternative to Ellman's reagent. Org Lett 2004;6:3809-3812.
65. Le M, Means GE. A procedure for the determination of monothiols in the presence of dithiothreitol-an improved assay for the reduction of disulfides. Anal Biochem 1995;229:264-271.
66. Grassetti DR, Murray JF. Determination of sulfhydryl groups with 2,2′- or 4,4′-dithiodipyridine. Arch Biochem Biophys 1967;119:41-49.
67. Riener CK, Kada G, Gruber HJ. Quick measurement of protein sulfhydryls with Ellman's reagent and with 4,4′-dithiodipyridine. Anal Bioanal Chem 2002;373:266-276.
68. Hansen RE, Østergaard H, Nørgaard P, Winther JR. Quantification of protein thiols and dithiols in the picomolar range using sodium borohydride and 4,4′-dithiodipyridine. Anal Biochem 2007;363:77-82.
69. Hansen RE, Roth D, Winther JR. Quantifying the global cellular thiol-disulfide status. Proc Natl Acad Sci USA 2009;106:422-427.
70. Hansen RE, Otsu M, Braakman I, Winther JR. quantifying changes in the cellular thiol-disulfide status during differentiation of B cells into antibody-secreting plasma cells. Int J Cell Biol 2013; 2013:898563
71. Pullela PK, Chiku T, Carvan MJ, Sem DS. Fluorescencebased detection of thiols in vitro and in vivo using dithiol probes. Anal Biochem 2006;352:265-273.
72. Rodakis GC, Kafatos FC. Origin of evolutionary novelty in proteins: how a high-cysteine chorion protein has evolved. Proc Natl Acad Sci USA 1982;79:3552-3555.
73. Piggott AM, Karuso P. Fluorometric assay for the determination of glutathione reductase activity. Anal Chem 2007;79:8769-8773.
74. Cao X, Lin W, Yu Q. A ratiometric fluorescent probe for thiols based on a tetrakis(4-hydroxyphenyl)porphyrin-coumarin scaffold. J Org Chem 2011;76:7423-7430.
75. Pires MM, Chmielewski J. Fluorescence imaging of cellular glutathione using a latent rhodamine. Org Lett 2008;10:837-840.
76. Zhang M, Yu M, Li F, Zhu M, Li M, Gao Y, et al. A highly selective fluorescence turn-on sensor for cysteine/homocysteine and its application in bioimaging. J Am Chem Soc 2007;129:10322-10323.
77. Lim CS, Masanta G, Kim HJ, Han JH, Kim HM, Cho BR. Ratiometric detection of mitochondrial thiols with a twophoton fluorescent probe. J Am Chem Soc 2011;133:11132-11135.
78. Lee JH, Lim CS, Tian YS, Han JH, Cho BR. A two-photon fluorescent probe for thiols in live cells and tissues. J Am Chem Soc 2010;132:1216-1217.
79. Zhang L, Duan D, Liu Y, Ge C, Cui X, Sun J, Fang J. Highly selective off-on fluorescent probe for imaging thioredoxin reductase in living cells. J Am Chem Soc 2014;136:226-233.
80. Tang B, Xing Y, Li P, Zhang N, Yu F, Yang G. A rhodaminebased fluorescent probe containing a Se-N bond for detecting thiols and its application in living cells. J Am Chem Soc 2007;129:11666-11667.
81. Tang B, Yin L, Wang X, Chen Z, Tong L, Xu K. A fastresponse, highly sensitive and specific organoselenium fluorescent probe for thiols and its application in bioimaging. Chem Commun (Camb) 2009;35: 5293-5295.
82. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 2004;279:22284-22293.
83. Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, Novak J, et al. Confocal imaging of glutathione redox potential in living plant cells. J Microsc 2008;231:299-316.
84. Maeda H, Matsuno H, Ushida M, Katayama K, Saeki K, Itoh N. 24-Dinitrobenzenesulfonyl fluoresceins as fluorescent alternatives to Ellman's reagent in thiol-quantification enzyme assays. Angew Chem Int Ed Engl 2005;44:2922-2925.
85. Bouffard J, Kim Y, Swager TM, Weissleder R, Hilderbrand SA. A highly selective fluorescent probe for thiol bioimaging. Org Lett 2008;10:37-40.
86. Maeda H, Katayama K, Matsuno H, Uno T. 3′-(2,4-Dinitrobenzenesulfonyl)-2′,7′-dimethylfluorescein as a fluorescent probe for selenols. Angew Chem Int Ed Engl 2006;45:1810-1813.
87. Shao J, Guo H, Ji S, Zhao J. Styryl-BODIPY based redemitting fluorescent OFF-ON molecular probe for specific detection of cysteine. Biosens Bioelectron 2011;26:3012-3017.
88. Becerra A, Echeverría C, Varela D, Sarmiento D, Armisén R, Nuñez-Villena F, et al. Transient receptor potential melastatin 4 inhibition prevents lipopolysaccharide induced endothelial cell death. Cardiovasc Res 2011;91:677-684.
89. Crankshaw MW, Grant GA. Modification of cysteine. Curr Protoc Protein Sci 2001; Chapter 15: Unit15.1.
90. Ercal N, Yang P, Aykin N. Determination of biological thiols by high-performance liquid chromatography following derivatization by ThioGlo maleimide reagents. J Chromatogr B Biomed Sci Appl 2001;753:287-292.
91. Matsumoto T, Urano Y, Shoda T, Kojima H, Nagano T. A thiol-reactive fluorescence probe based on donor-excited photoinduced electron transfer: key role of ortho substitution. Org Lett 2007;9:3375-3377.
92. Liu Y, Zhang S, Lv X, Sun YQ, Liu J, Guo W. Constructing a fluorescent probe for specific detection of cysteine over homocysteine and glutathione based on a novel cysteine-binding group but-3-yn-2-one. Analyst 2014;139:4081-4087.
93. Yi L, Li H, Sun L, Liu L, Zhang C, Xi Z. A highly sensitive fluorescence probe for fast thiol-quantification assay of glutathione reductase. Angew Chem Int Ed Engl 2009;48:4034-4037.
94. Ros-Lis JV, García B, Jiménez D, Martínez-Máñez R, Sancenón F, Soto J, et al. Squaraines as fluoro-chromogenic probes for thiol-containing compounds and their application to the detection of biorelevant thiols. J Am Chem Soc 2004;126:4064-4065.
95. Sreejith S, Divya KP, Ajayaghosh A. A near-infrared squaraine dye as a latent ratiometric fluorophore for the detection of aminothiol content in blood plasma. Angew Chem Int Ed Engl 2008;47:7883-7887.
96. Chen X, Ko SK, Kim MJ, Shin I, Yoon J. A thiol-specific fluorescent probe and its application for bioimaging. Chem Commun (Camb) 2010;46:2751-2753.
97. Nie L, Ma H, Sun M, Li X, Su M, Liang S. Direct chemiluminescence determination of cysteine in human serum using quinine-Ce(IV) system. Talanta 2003;59:959-964.
98. Wang S, Ma H, Li J, Chen X, Bao Z, Sun S. Direct determination of reduced glutathione in biological fluids by Ce(IV)-quinine chemiluminescence. Talanta 2006;70:518-521.
99. Rezaei B, Mokhtari AA. A simple and rapid flow injection chemiluminescence determination of cysteine with Ru(phen)3(2+)-Ce(IV) system. Spectrochim Acta A Mol Biomol Spectrosc 2007;66:359-363.
100. Han B, Yuan J, Wang E. Sensitive and selective sensor for biothiols in the cell based on the recovered fluorescence of the CdTe quantum dots-Hg(II) system. Anal Chem 2009;81:5569-5573.
101. Ji S, Guo H, Yuan X, Li X, Ding H, Gao P, et al. A highly selective OFF-ON red-emitting phosphorescent thiol probe with large stokes shift and long luminescent lifetime. Org Lett 2010;12:2876-2879.
102. Tang Y, Yang HR, Sun HB, Liu SJ, Wang JX, Zhao Q, et al. Rational design of an "OFF-ON" phosphorescent chemodosimeter based on an iridium(III) complex and its application for time-resolved luminescent detection and bioimaging of cysteine and homocysteine. Chemistry 2013;19:1311-1319.
103. Xu W, Zhao X, Lv W, Yang H, Liu S, Liang H, et al. Rational design of phosphorescent chemodosimeter for reaction-based one- and two-photon and time-resolved luminescent imaging of biothiols in living cells. Adv Healthc Mater 2014;3:658-669.
104. Huo FJ, Sun YQ, Su J, Chao JB, Zhi HJ, Yin CX. Colorimetric detection of thiols using a chromene molecule. Org Lett 2009;11:4918-4921.
105. Niwa K, Nakajima Y, Ohmiya Y. Applications of luciferin biosynthesis: bioluminescence assays for l-cysteine and luciferase. Anal Biochem 2010;396:316-318.
106. Watson WH, Jones DP. Oxidation of nuclear thioredoxin during oxidative stress. FEBS Lett 2003;543:144-147.
107. Halvey PJ, Watson WH, Hansen JM, Go YM, Samali A, Jones DP. Compartmental oxidation of thiol-disulphide redox couples during epidermal growth factor signalling. Biochem J 2005;386:215-219.
108. Chen Y, Go YM, Pohl J, Reed M, Cai J, Jones DP. Increased mitochondrial thioredoxin 2 potentiates Nethylmaleimide-induced cytotoxicity. Chem Res Toxicol 2008;21:1205-1210.
109. Go YM, Jones DP. Thioredoxin redox western analysis. Curr Protoc Toxicol 2009;41:17.12.1-17.12.12 (Chapter 17).
110. Du Y, Zhang H, Lu J, Holmgren A. Glutathione and glutaredoxin act as a backup of human thioredoxin reductase 1 to reduce thioredoxin 1 preventing cell death by aurothioglucose. J Biol Chem 2012;287:38210-38219.
111. Sakoh-Nakatogawa M, Nishikawa S, Endo T. Roles of protein-disulfide isomerase-mediated disulfide bond formation of yeast Mnl1p in endoplasmic reticulumassociated degradation. J Biol Chem 2009;284:11815-11825.
112. Denoncin K, Nicolaes V, Cho SH, Leverrier P, Collet JF. Protein disulfide bond formation in the periplasm: determination of the in vivo redox state of cysteine residues. Methods Mol Biol 2013;966:325-336.
113. Vertommen D, Depuydt M, Pan J, Leverrier P, Knoops L, Szikora JP, et al. The disulphide isomerase DsbC cooperates with the oxidase DsbA in a DsbD-independent manner. Mol Microbiol 2008;67:336-349.
114. Lee SR, Bar-Noy S, Kwon J, Levine RL, Stadtman TC, Rhee SG. Mammalian thioredoxin reductase: oxidation of the C-terminal cysteine/selenocysteine active site forms a thioselenide, and replacement of selenium with sulfur markedly reduces catalytic activity. Proc Natl Acad Sci USA 2000;97:2521-2526.
115. Kim JR, Lee SM, Cho SH, Kim JH, Kim BH, Kwon J, et al. Oxidation of thioredoxin reductase in HeLa cells stimulated with tumor necrosis factor-alpha. FEBS Lett 2004;567:189-196.
116. Lind C, Gerdes R, Hamnell Y, Schuppe-Koistinen I, von Lowenhielm HB, Holmgren A, Cotgreave IA. Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch Biochem Biophys 2002;406:229-240.
117. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, Salmona M, et al. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci USA 2002;99:3505-3510.
118. Shenton D, Grant CM. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 2003;374:513-519.
119. Brennan JP, Wait R, Begum S, Bell JR, Dunn MJ, Eaton P. Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J Biol Chem 2004;279:41352-41360.
120. Sethuraman M, McComb ME, Heibeck T, Costello CE, Cohen RA. Isotope-coded affinity tag approach to identify and quantify oxidant-sensitive protein thiols. Mol Cell Proteomics 2004;3:273-278.
121. Leichert LI, Jakob U. Protein thiol modifications visualized in vivo. PLoS Biol 2004;2:e333
122. Le Moan N, Clement G, Le Maout S, Tacnet F, Toledano MB. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J Biol Chem 2006;281:10420-10430.
123. Hagglund P, Bunkenborg J, Maeda K, Svensson B. Identification of thioredoxin disulfide targets using a quantitative proteomics approach based on isotopecoded affinity tags. J Proteome Res 2008;7:5270-5276.
124. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, et al. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA 2008;105:8197-8202.
125. Brandes N, Reichmann D, Tienson H, Leichert LI, Jakob U. Using quantitative redox proteomics to dissect the yeast redoxome. J Biol Chem 2011;286:41893-41903.
126. Lindemann C, Leichert LI. Quantitative redox proteomics: the NOxICAT method. Methods Mol Biol 2012;893:387-403.
127. Leonard SE, Reddie KG, Carroll KS. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol 2009;4:783-799.
128. Held JM, Danielson SR, Behring JB, Atsriku C, Britton DJ, Puckett RL, et al. Targeted quantitation of site-specific cysteine oxidation in endogenous proteins using a differential alkylation and multiple reaction monitoring mass spectrometry approach. Mol Cell Proteomics 2010;9:1400-1410.
129. Chouchani ET, Hurd TR, Nadtochiy SM, Brookes PS, Fearnley IM, Lilley KS, et al. Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible Snitrosation. Biochem J 2010;430:49-59.
130. Requejo R, Chouchani ET, James AM, Prime TA, Lilley KS, Fearnley IM, Murphy MP. Quantification and identification of mitochondrial proteins containing vicinal dithiols. Arch Biochem Biophys 2010;504:228-235.
131. Hu Q, Guo G, Yang Z, Li Y, Xia Y. Stable isotope metabolic labeling-based quantitative thiol redox proteomic analysis of hydrogen peroxidetreated Arabidopsis plant. J Proteomics Bioinform 2014;7:121-133.
132. Chouchani ET, James AM, Fearnley IM, Lilley KS, Murphy MP. Proteomic approaches to the characterization of protein thiol modification. Curr Opin Chem Biol 2011;15:120-128.
133. Baez NO, Reisz JA, Furdui CM. Mass spectrometry in studies of protein thiol chemistry and signaling: opportunities and caveats. Free Radic Biol Med 2015;80:191-211.
134. Izquierdo-Álvarez A, Martínez-Ruiz A. Thiol redox proteomics seen with fluorescent eyes: the detection of cysteine oxidative modifications by fluorescence derivatization and 2-DE. J Proteomics 2011;75:329-338.
135. Ratnayake S, Dias IH, Lattman E, Griffiths HR. Stabilising cysteinyl thiol oxidation and nitrosation for proteomic analysis. J Proteomics 2013;92:160-170.
136. Hurd TR, Prime TA, Harbour ME, Lilley KS, Murphy MP. Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J Biol Chem 2007;282:22040-22051.
137. Hurd TR, James AM, Lilley KS, Murphy MP. Chapter 19 Measuring redox changes to mitochondrial protein thiols with redox difference gel electrophoresis (redox-DIGE). Methods Enzymol 2009;456:343-361.
138. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 2004;279:13044-13053.
139. Björnberg O, Ostergaard H, Winther JR. Measuring intracellular redox conditions using GFP-based sensors. Antioxid Redox Signal 2006;8:354-361.
140. Meyer AJ, Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 2010;13:621-650.
141. Pal R, Basu Thakur P, Li S, Minard C, Rodney GG. Realtime imaging of NADPH oxidase activity in living cells using a novel fluorescent protein reporter. PLoS One 2013;8:e63989
142. Pal R, Monroe TO, Palmieri M, Sardiello M, Rodney GG. Rotenone induces neurotoxicity through Rac1-dependent activation of NADPH oxidase in SHSY-5Y cells. FEBS Lett 2014;588:472-481.
143. Pal R, Palmieri M, Loehr JA, Li S, Abo-Zahrah R, Monroe TO, et al. Src-dependent impairment of autophagy by oxidative stress in a mouse model of Duchenne muscular dystrophy. Nat Commun 2014;5:4425
144. Brach T, Soyk S, Müller C, Hinz G, Hell R, Brandizzi F, Meyer AJ. Noninvasive topology analysis of membrane proteins in the secretory pathway. Plant J 2009;57:534-541
145. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, Surmeier DJ. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 2010;468:696-700.
146. Albrecht SC, Barata AG, Grosshans J, Teleman AA, Dick TP. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab 2011;14:819-829.
147. Goldberg JA, Guzman JN, Estep CM, Ilijic E, Kondapalli J, Sanchez-Padilla J, Surmeier DJ. Calcium entry induces mitochondrial oxidant stress in vagal neurons at risk in Parkinson's disease. Nat Neurosci 2012;15:1414-1421.
148. Seiler C, Davuluri G, Abrams J, Byfield FJ, Janmey PA, Pack M. Smooth muscle tension induces invasive remodeling of the zebrafish intestine. PLoS Biol 2012;10:e1001386
149. Back P, De Vos WH, Depuydt GG, Matthijssens F, Vanfleteren JR, Braeckman BP. Exploring real-time in vivo redox biology of developing and aging Caenorhabditis elegans. Free Radic Biol Med 2012;52:850-859.
150. O'Donnell KC, Vargas ME, Sagasti A. WldS and PGC-1a regulate mitochondrial transport and oxidation state after axonal injury. J Neurosci 2013;33:14778-14790.
151. Kasozi D, Mohring F, Rahlfs S, Meyer AJ, Becker K. Realtime imaging of the intracellular glutathione redox potential in the malaria parasite Plasmodium falciparum. PLoS Pathog 2013;9:e1003782
152. Breckwoldt MO, Pfister FM, Bradley PM, Marinkovic P, Williams PR, Brill MS, et al. Multiparametric optical analysis of mitochondrial redox signals during neuronal physiology and pathology in vivo. Nat Med 2014;20:555-560.
153. Wolf AM, Nishimaki K, Kamimura N, Ohta S. Realtime monitoring of oxidative stress in live mouse skin. J Invest Dermatol 2014;134:1701-1709.
154. Albrecht SC, Sobotta MC, Bausewein D, Aller I, Hell R, Dick TP, Meyer AJ. Redesign of genetically encoded biosensors for monitoring mitochondrial redox status in a broad range of model eukaryotes. J Biomol Screen 2014;19:379-386.
155. Bhaskar A, Chawla M, Mehta M, Parikh P, Chandra P, Bhave D, et al. Reengineering redox sensitive GFP to measure mycothiol redox potential of Mycobacterium tuberculosis during infection. PLoS Pathog 2014;10: e1003902
156. Bhaskar A, Munshi M, Khan SZ, Fatima S, Arya R, Jameel S, Singh A. Measuring glutathione redox potential of HIV-1 infected macrophages. J Biol Chem 2015;290: 1020-1038.
157. Lohman JR, Remington SJ. Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry 2008;47:8678-8688.
158. Aller I, Rouhier N, Meyer AJ. Development of roGFP2-derived redox probes for measurement of the glutathione redox potential in the cytosol of severely glutathione-deficient rml1 seedlings. Front Plant Sci 2013;4:506
159. Sugiura K, Nagai T, Nakano M, Ichinose H, Nakabayashi T, Ohta N, Hisabori T. Redox sensor proteins for highly sensitive direct imaging of intracellular redox state. Biochem Biophys Res Commun 2015;457:242-248.
160. Su T, Zhang Z, Luo Q. Ratiometric fluorescence imaging of dual bio-molecular events in single living cells using a new FRET pair mVenus/mKOk-based biosensor and a single fluorescent protein biosensor. Biosens Bioelectron 2012;31:292-298.
161. Fan Y, Chen Z, Ai HW. Monitoring redox dynamics in living cells with a redox-sensitive red fluorescent protein. Anal Chem 2015;87:2802-2810.
162. Kolossov VL, Spring BQ, Sokolowski A, Conour JE, Clegg RM, Kenis PJ, Gaskins HR. Engineering redox-sensitive linkers for genetically encoded FRET-based biosensors. Exp Biol Med (Maywood) 2008;233:238-248.
163. Kolossov VL, Spring BQ, Clegg RM, Henry JJ, Sokolowski A, Kenis PJ, Gaskins HR. Development of a high-dynamic range, GFP-based FRET probe sensitive to oxidative microenvironments. Exp Biol Med (Maywood) 2011;236:681-691.
164. Kolossov VL, Leslie MT, Chatterjee A, Sheehan BM, Kenis PJ, Gaskins HR. Förster resonance energy transferbased sensor targeting endoplasmic reticulum reveals highly oxidative environment. Exp Biol Med 2012;237: 652-662.
165. Yano T, Oku M, Akeyama N, Itoyama A, Yurimoto H, Kuge S, et al. A novel fluorescent sensor protein for visualization of redox states in the cytoplasm and in peroxisomes. Mol Cell Biol 2010;30:3758-3766.
166. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J 2000;19:5157-5166.
167. 2 with roGFP2-based redox probes. Free Radic Biol Med 2011;51:1943-1951.
168. Maulucci G, Labate V, Mele M, Panieri E, Arcovito G, Galeotti T, et al. High-resolution imaging of redox signaling in live cells through an oxidation-sensitive yellow fluorescent protein. Sci Signal 2008;1:13-28.
169. Ezeriņa D, Morgan B, Dick TP. Imaging dynamic redox processes with genetically encoded probes. J Mol Cell Cardiol 2014;73:43-49.