The Incomplete Glutathione Puzzle: Just Guessing at Numbers and Figures?

Antioxidants and Redox Signaling

Volumn 27, Issue 15, 2017, Pages 1130-1161

  Deponte, Marcel ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

compartmentalization; concentration; function; glutathione; kinetics; rate constant

Indexed keywords

CARRIER PROTEIN; ENZYME; GLUTATHIONE; GLUTATHIONE DISULFIDE; IRON SULFUR PROTEIN; IRON;

CELL COMPARTMENTALIZATION; CELL NUCLEUS; CYTOSOL; ENZYME KINETICS; GLUTATHIONE METABOLISM; IRON METABOLISM; METABOLITE; MITOCHONDRION; ORGANELLE BIOGENESIS; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GENE REGULATORY NETWORK; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; YEAST;

ANIMALS; CELL NUCLEUS; CYTOSOL; GENE REGULATORY NETWORKS; GLUTATHIONE; HUMANS; IRON; MITOCHONDRIA; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; YEASTS;

EID: 85031720644     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2017.7123     Document Type: Review

References (302)

1. Akerboom TP, Bilzer M, and Sies H. The relationship of biliary glutathione disulfide efflux and intracellular glutathione disulfide content in perfused rat liver. J Biol Chem 257: 4248-4252, 1982.
2. Akoachere M, Iozef R, Rahlfs S, Deponte M, Mannervik B, Creighton DJ, Schirmer H, and Becker K. Characterization of the glyoxalases of the malarial parasite Plasmodium falciparum and comparison with their human counterparts. Biol Chem 386: 41-52, 2005.
3. Alfonso-Prieto M, Vidossich P, and Rovira C. The reaction mechanisms of heme catalases: An atomistic view by ab initio molecular dynamics. Arch Biochem Biophys 525: 121-130, 2012.
4. Allen EM and Mieyal JJ. Protein-thiol oxidation and cell death: regulatory role of glutaredoxins. Antioxid Redox Signal 17: 1748-1763, 2012.
5. Allocati N, Federici L, Masulli M, and Di Ilio C. Glutathione transferases in bacteria. FEBS J 276: 58-75, 2009.
6. Ames BN, Profet M, and Gold LS. Nature's chemicals and synthetic chemicals: comparative toxicology. Proc Natl Acad Sci U S A 87: 7782-7786, 1990.
7. Antonenkov VD and Hiltunen JK. Peroxisomal membrane permeability and solute transfer. Biochim Biophys Acta 1763: 1697-1706, 2006.
8. Appenzeller-Herzog C and Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim Biophys Acta 1783: 535-548, 2008.
9. Armeni T, Cianfruglia L, Piva F, Urbanelli L, Luisa Caniglia M, Pugnaloni A, and Principato G. S-D-Lactoylglutathione can be an alternative supply of mitochondrial glutathione. Free Radic Biol Med 67: 451-459, 2014.
10. Aslund F, Berndt KD, and Holmgren A. Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J Biol Chem 272: 30780-30786, 1997.
11. Aslund F, Ehn B, Miranda-Vizuete A, Pueyo C, and Holmgren A. Two additional glutaredoxins exist in Escherichia coli: glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc Natl Acad Sci U S A 91: 9813-9817, 1994.
12. Atamna H and Ginsburg H. The malaria parasite supplies glutathione to its host cell-investigation of glutathione transport and metabolism in human erythrocytes infected with Plasmodium falciparum. Eur J Biochem 250: 670-679, 1997.
13. Atkins P and De Paula J. Atkins' Physical Chemistry, 8th ed. Oxford, United Kingdom: Oxford University Press, 2006.
14. Avery AM and Avery SV. Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. J Biol Chem 276: 33730-33735, 2001.
15. Bachhawat AK, Thakur A, Kaur J, and Zulkifli M. Glutathione transporters. Biochim Biophys Acta 1830: 3154-3164, 2013.
16. Bai M, Zhou JM, and Perrett S. The yeast prion protein Ure2 shows glutathione peroxidase activity in both native and fibrillar forms. J Biol Chem 279: 50025-50030, 2004.
17. Bandyopadhyay S, Gama F, Molina-NavarroMM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, and Rouhier N. Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27: 1122-1133, 2008.
18. Banhegyi G, Lusini L, Puskas F, Rossi R, Fulceri R, Braun L, Mile V, di Simplicio P, Mandl J, and Benedetti A. Preferential transport of glutathione versus glutathione disulfide in rat liver microsomal vesicles. J Biol Chem 274: 12213-12216, 1999.
19. Barrand MA, Winterberg M, Ng F, Nguyen M, Kirk K, and Hladky SB. Glutathione export from human erythrocytes and Plasmodium falciparum malaria parasites. Biochem J 448: 389-400, 2012.
20. Barreto L, Garcera A, Jansson K, Sunnerhagen P, and Herrero E. A peroxisomal glutathione transferase of Saccharomyces cerevisiae is functionally related to sulfur amino acid metabolism. Eukaryot Cell 5: 1748-1759, 2006.
21. Bedard K and Krause KH. The NOX family of ROSgenerating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007.
22. Begas P, Liedgens L, Moseler A, Meyer AJ, and Deponte M. Glutaredoxin catalysis requires two distinct glutathione interaction sites. Nat Commun 8: 14835, 2017.
23. Begas P, Staudacher V, and Deponte M. Systematic reevaluation of the bis(2-hydroxyethyl)disulfide (HEDS) assay reveals an alternative mechanism and activity of glutaredoxins. Chem Sci 6: 3788-3796, 2015.
24. Benhar M, Forrester MT, and Stamler JS. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10: 721-732, 2009.
25. Bermingham-McDonogh O, Gralla EB, and Valentine JS. The copper, zinc-superoxide dismutase gene of Saccharomyces cerevisiae: cloning, sequencing, and biological activity. Proc Natl Acad Sci U S A 85: 4789-4793, 1988.
26. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, and Riemer J. Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol Cell 37: 516-528, 2010.
27. Birk J, Meyer M, Aller I, Hansen HG, Odermatt A, Dick TP, Meyer AJ, and Appenzeller-Herzog C. Endoplasmic reticulum: reduced and oxidized glutathione revisited. J Cell Sci 126: 1604-1617, 2013.
28. Bisswanger H. Enzymkinetik. Weinheim, Deutschland: Wiley-VCH, 2000.
29. Bito A, Haider M, Hadler I, and Breitenbach M. Identification and phenotypic analysis of two glyoxalase II encoding genes from Saccharomyces cerevisiae, GLO2 and GLO4, and intracellular localization of the corresponding proteins. J Biol Chem 272: 21509-21519, 1997.
30. Board PG and Menon D. Glutathione transferases, regulators of cellular metabolism and physiology. Biochim Biophys Acta 1830: 3267-3288, 2013.
31. Bonnichsen RK, Chance B, and Theorell H. Catalase activity. Acta Chem Scand 1: 685-709, 1947.
32. Bourbouloux A, Shahi P, Chakladar A, Delrot S, and Bachhawat AK. Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. J Biol Chem 275: 13259-13265, 2000.
33. Brautigam L, Jensen LD, Poschmann G, Nystrom S, Bannenberg S, Dreij K, Lepka K, Prozorovski T, Montano SJ, Aktas O, Uhlen P, Stuhler K, Cao Y, Holmgren A, and Berndt C. Glutaredoxin regulates vascular development by reversible glutathionylation of sirtuin 1. Proc Natl Acad Sci U S A 110: 20057-20062, 2013.
34. Brigelius-Flohe R and Flohe L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 15: 2335-2381, 2011.
35. Brigelius-Flohe R and Maiorino M. Glutathione peroxidases. Biochim Biophys Acta 1830: 3289-3303, 2013.
36. Bulleid NJ and Ellgaard L. Multiple ways to make disulfides. Trends Biochem Sci 36: 485-492, 2011.
37. Can B, Kulaksiz Erkmen G, Dalmizrak O, Ogus IH, and Ozer N. Purification and characterisation of rat kidney glutathione reductase. Protein J 29: 250-256, 2010.
38. Carballal S, Bartesaghi S, and Radi R. Kinetic and mechanistic considerations to assess the biological fate of peroxynitrite. Biochim Biophys Acta 1840: 768-780, 2014.
39. Castro H, Teixeira F, Romao S, Santos M, Cruz T, Florido M, Appelberg R, Oliveira P, Ferreira-da-Silva F, and Tomas AM. Leishmania mitochondrial peroxiredoxin plays a crucial peroxidase-unrelated role during infection: insight into its novel chaperone activity. PLoS Pathog 7: e1002325, 2011.
40. Castro L, Rodriguez M, and Radi R. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 269: 29409-29415, 1994.
41. Cha MK, Choi YS, Hong SK, Kim WC, No KT, and Kim IH. Nuclear thiol peroxidase as a functional alkylhydroperoxide reductase necessary for stationary phase growth of Saccharomyces cerevisiae. J Biol Chem 278: 24636-24643, 2003.
42. Chae HZ, Kim IH, Kim K, and Rhee SG. Cloning, sequencing, and mutation of thiol-specific antioxidant gene of Saccharomyces cerevisiae. J Biol Chem 268: 16815-16821, 1993.
43. Chance B, Sies H, and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979.
44. Chang LY, Slot JW, Geuze HJ, and Crapo JD. Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J Cell Biol 107: 2169-2179, 1988.
45. Chapple SJ, Cheng X, and Mann GE. Effects of 4-hydroxynonenal on vascular endothelial and smooth muscle cell redox signaling and function in health and disease. Redox Biol 1: 319-331, 2013.
46. Cho CS, Yoon HJ, Kim JY, Woo HA, and Rhee SG. Circadian rhythm of hyperoxidized peroxiredoxin II is determined by hemoglobin autoxidation and the 20S proteasome in red blood cells. Proc Natl Acad Sci U S A 111: 12043-12048, 2014.
47. Choi JH, Lou W, and Vancura A. A novel membranebound glutathione S-transferase functions in the stationary phase of the yeast Saccharomyces cerevisiae. J Biol Chem 273: 29915-29922, 1998.
48. Chong YT, Koh JL, Friesen H, Duffy SK, Cox MJ, Moses A, Moffat J, Boone C, and Andrews BJ. Yeast proteome dynamics from single cell imaging and automated analysis. Cell 161: 1413-1424, 2015.
49. Chouchani ET, Hurd TR, Nadtochiy SM, Brookes PS, Fearnley IM, Lilley KS, Smith RA, and Murphy MP. Identification of S-nitrosated mitochondrial proteins by Snitrosothiol difference in gel electrophoresis (SNODIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation. Biochem J 430: 49-59, 2010.
50. Cohen G, Fessl F, Traczyk A, Rytka J, and Ruis H. Isolation of the catalase A gene of Saccharomyces cerevisiae by complementation of the cta1 mutation. Mol Gen Genet 200: 74-79, 1985.
51. Coleman JD, Prabhu KS, Thompson JT, Reddy PS, Peters JM, Peterson BR, Reddy CC, and Vanden Heuvel JP. The oxidative stress mediator 4-hydroxynonenal is an intracellular agonist of the nuclear receptor peroxisome proliferator-activated receptor-beta/delta (PPARbeta/delta). Free Radic Biol Med 42: 1155-1164, 2007.
52. Collinson EJ and Grant CM. Role of yeast glutaredoxins as glutathione S-transferases. J Biol Chem 278: 22492-22497, 2003.
53. Collinson EJ, Wheeler GL, Garrido EO, Avery AM, Avery SV, and Grant CM. The yeast glutaredoxins are active as glutathione peroxidases. J Biol Chem 277: 16712-16717, 2002.
54. Comini MA. Measurement and meaning of cellular thiol: disufhide redox status. Free Radic Res 50: 246-271, 2016.
55. Cordell PA, Futers TS, Grant PJ, and Pease RJ. The human hydroxyacylglutathione hydrolase (HAGH) gene encodes both cytosolic and mitochondrial forms of glyoxalase II. J Biol Chem 279: 28653-28661, 2004.
56. Couturier J, Przybyla-Toscano J, Roret T, Didierjean C, and Rouhier N. The roles of glutaredoxins ligating Fe-S clusters: sensing, transfer or repair functions Biochim Biophys Acta 1853: 1513-1527, 2015.
57. Dalziel K. Initial steady state velocities in the evaluation of enzyme-coenzyme-substrate reaction mechanisms. Acta Chem Scand 11: 1706-1723, 1957.
58. Dardalhon M, Kumar C, Iraqui I, Vernis L, Kienda G, Banach-Latapy A, He T, Chanet R, Faye G, Outten CE, and Huang ME. Redox-sensitive YFP sensors monitor dynamic nuclear and cytosolic glutathione redox changes. Free Radic Biol Med 52: 2254-2265, 2012.
59. Delaunay A, Pflieger D, Barrault MB, Vinh J, and Toledano MB. A thiol peroxidase is an H2O2 receptor and redoxtransducer in gene activation. Cell 111: 471-481, 2002.
60. Deponte M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 1830: 3217-3266, 2013.
61. Deponte M. Glyoxalase diversity in parasitic protists. Biochem Soc Trans 42: 473-478, 2014.
62. Deponte M and Becker K. Biochemical characterization of Toxoplasma gondii 1-Cys peroxiredoxin 2 with mechanistic similarities to typical 2-Cys Prx. Mol Biochem Parasitol 140: 87-96, 2005.
63. Deponte M, Becker K, and Rahlfs S. Plasmodium falciparum glutaredoxin-like proteins. Biol Chem 386: 33-40, 2005.
64. Deponte M and Hell K. Disulphide bond formation in the intermembrane space of mitochondria. J Biochem 146: 599-608, 2009.
65. Deponte M and Lillig CH. Enzymatic control of cysteinyl thiol switches in proteins. Biol Chem 396: 401-413, 2015.
66. Deponte M, Rahlfs S, and Becker K. Peroxiredoxin systems of protozoal parasites. Subcell Biochem 44: 219-229, 2007.
67. Deponte M, Sturm N, Mittler S, Harner M, Mack H, and Becker K. Allosteric coupling of two different functional active sites in monomeric Plasmodium falciparum glyoxalase I. J Biol Chem 282: 28419-28430, 2007.
68. Derakhshan B, Wille PC, and Gross SS. Unbiased identification of cysteine S-nitrosylation sites on proteins. Nat Protoc 2: 1685-1691, 2007.
69. Djuika CF, Fiedler S, Schnolzer M, Sanchez C, Lanzer M, and Deponte M. Plasmodium falciparum antioxidant protein as a model enzyme for a special class of glutaredoxin/ glutathione-dependent peroxiredoxins. Biochim Biophys Acta 1830: 4073-4090, 2013.
70. Djuika CF, Huerta-Cepas J, Przyborski JM, Deil S, Sanchez CP, Doerks T, Bork P, Lanzer M, and Deponte M. Prokaryotic ancestry and gene fusion of a dual localized peroxiredoxin in malaria parasites. Microbial Cell 2: 5-13, 2015.
71. Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, Dunbrack RL, and Ischiropoulos H. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci U S A 107: 16958-16963, 2010.
72. Draculic T, Dawes IW, and Grant CM. A single glutaredoxin or thioredoxin gene is essential for viability in the yeast Saccharomyces cerevisiae. Mol Microbiol 36: 1167-1174, 2000.
73. Eckers E, Bien M, Stroobant V, Herrmann JM, and Deponte M. Biochemical characterization of dithiol glutaredoxin 8 from Saccharomyces cerevisiae: The catalytic redox mechanism redux. Biochemistry 48: 1410-1423, 2009.
74. Edskes HK, Gray VT, and Wickner RB. The [URE3] prion is an aggregated form of Ure2p that can be cured by overexpression of Ure2p fragments. Proc Natl Acad Sci U S A 96: 1498-1503, 1999.
75. Eisenstein RS. Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 20: 627-662, 2000.
76. Elbaz-Alon Y, Morgan B, Clancy A, Amoako TN, Zalckvar E, Dick TP, Schwappach B, and Schuldiner M. The yeast oligopeptide transporter Opt2 is localized to peroxisomes and affects glutathione redox homeostasis. FEMS Yeast Res 14: 1055-1067, 2014.
77. Elgan TH and Berndt KD. Quantifying Escherichia coli glutaredoxin-3 substrate specificity using ligand-induced stability. J Biol Chem 283: 32839-32847, 2008.
78. Endo T, Yamano K, and Kawano S. Structural basis for the disulfide relay system in the mitochondrial intermembrane space. Antioxid Redox Signal 13: 1359-1373, 2010.
79. Fernandes AP, Fladvad M, Berndt C, Andresen C, Lillig CH, Neubauer P, Sunnerhagen M, Holmgren A, and Vlamis-Gardikas A. A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase. J Biol Chem 280: 24544-24552, 2005.
80. Fernando MR, Lechner JM, Lofgren S, Gladyshev VN, and Lou MF. Mitochondrial thioltransferase (glutaredoxin 2) has GSH-dependent and thioredoxin reductasedependent peroxidase activities in vitro and in lens epithelial cells. FASEB J 20: 2645-2647, 2006.
81. Ferrer-Sueta G and Radi R. Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 4: 161-177, 2009.
82. Fielden EM, Roberts PB, Bray RC, Lowe DJ, Mautner GN, Rotilio G, and Calabrese L. Mechanism of action of superoxide dismutase from pulse radiolysis and electron paramagnetic resonance. Evidence that only half the active sites function in catalysis. Biochem J 139: 49-60, 1974.
83. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, and Dietz KJ. The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280: 12168-12180, 2005.
84. Fischer M, Horn S, Belkacemi A, Kojer K, Petrungaro C, Habich M, Ali M, Kuttner V, Bien M, Kauff F, Dengjel J, Herrmann JM, and Riemer J. Protein import and oxidative folding in the mitochondrial intermembrane space of intact mammalian cells. Mol Biol Cell 24: 2160-2170, 2013.
85. Fleming T and Nawroth PP. Reactive metabolites as a cause of late diabetic complications. Biochem Soc Trans 42: 439-442, 2014.
86. Flint DH, Tuminello JF, and Emptage MH. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268: 22369-22376, 1993.
87. Flohe L. The fairytale of the GSSG/GSH redox potential. Biochim Biophys Acta 1830: 3139-3142, 2013.
88. Flohe L, Gunzler W, Jung G, Schaich E, and Schneider F. [Glutathione peroxidase. II. Substrate specificity and inhibitory effects of substrate analogues]. Hoppe Seylers Z Physiol Chem 352: 159-169, 1971.
89. Flohe L, Loschen G, Gunzler WA, and Eichele E. Glutathione peroxidase, V. The kinetic mechanism. Hoppe Seylers Z Physiol Chem 353: 987-999, 1972.
90. Flohe L, Toppo S, Cozza G, and Ursini F. A comparison of thiol peroxidase mechanisms. Antioxid Redox Signal 15: 763-780, 2011.
91. Forman HJ, Maiorino M, and Ursini F. Signaling functions of reactive oxygen species. Biochemistry 49: 835-842, 2010.
92. Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, and Stamler JS. Proteomic analysis of Snitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 27: 557-559, 2009.
93. Fridovich I. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem 264: 7761-7764, 1989.
94. Fuss JO, Tsai CL, Ishida JP, and Tainer JA. Emerging critical roles of Fe-S clusters in DNA replication and repair. Biochim Biophys Acta 1853: 1253-1271, 2015.
95. Gallogly MM, and Mieyal JJ. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr Opin Pharmacol 7: 381-391, 2007.
96. Gallogly MM, Starke DW, Leonberg AK, Ospina SM, and Mieyal JJ. Kinetic and mechanistic characterization and versatile catalytic properties of mammalian glutaredoxin 2: implications for intracellular roles. Biochemistry 47: 11144-11157, 2008.
97. Gallogly MM, Starke DW, and Mieyal JJ. Mechanistic and kinetic details of catalysis of thiol-disulfide exchangeby glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 11: 1059-1081, 2009.
98. Garcia-Gimenez JL, Markovic J, Dasi F, Queval G, Schnaubelt D, Foyer CH, and Pallardo FV. Nuclear glutathione. Biochim Biophys Acta 1830: 3304-3316, 2013.
99. Gellert M, Venz S, Mitlohner J, Cott C, Hanschmann EM, and Lillig CH. Identification of a dithiol-disulfide switch in collapsin response mediator protein 2 (CRMP2) that is toggled in a model of neuronal differentiation. J Biol Chem 288: 35117-35125, 2013.
100. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, and Weissman JS. Global analysis of protein expression in yeast. Nature 425: 737-741, 2003.
101. Gilbert HF. Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol 251: 8-28, 1995.
102. Giustarini D, Dalle-Donne I, Milzani A, Fanti P, and Rossi R. Analysis of GSH and GSSG after derivatization with N-ethylmaleimide. Nat Protoc 8: 1660-1669, 2013.
103. Godoy JR, Funke M, Ackermann W, Haunhorst P, Oesteritz S, Capani F, Elsasser HP, and Lillig CH. Redox atlas of the mouse. Immunohistochemical detection of glutaredoxin-, peroxiredoxin-, and thioredoxin-family proteins in various tissues of the laboratory mouse. Biochim Biophys Acta 1810: 2-92, 2011.
104. Gort AS and Imlay JA. Balance between endogenous superoxide stress and antioxidant defenses. J Bacteriol 180: 1402-1410, 1998.
105. Grant CM. Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39: 533-541, 2001.
106. Grant CM, Collinson LP, Roe JH, and Dawes IW. Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol Microbiol 21: 171-179, 1996.
107. Grant CM, Perrone G, and Dawes IW. Glutathione and catalase provide overlapping defenses for protection against hydrogen peroxide in the yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 253: 893-898, 1998.
108. Gravina SA and Mieyal JJ. Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase. Biochemistry 32: 3368-3376, 1993.
109. Greetham D and Grant CM. Antioxidant activity of the yeast mitochondrial one-Cys peroxiredoxin is dependent on thioredoxin reductase and glutathione in vivo. Mol Cell Biol 29: 3229-3240, 2009.
110. Greetham D, Kritsiligkou P, Watkins RH, Carter Z, Parkin J, and Grant CM. Oxidation of the yeast mitochondrial thioredoxin promotes cell death. Antioxid Redox Signal 18: 376-385, 2013.
111. Gupta V and Carroll KS. Sulfenic acid chemistry, detection and cellular lifetime. Biochim Biophys Acta 1840: 847-875, 2014.
112. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, and Dick TP. Real-time imaging of the intracellular glutathione redox potential. Nat Methods 5: 553-559, 2008.
113. Hall A, Nelson K, Poole LB, and Karplus PA. Structurebased insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid Redox Signal 15: 795-815, 2011.
114. Han YH, Kim SU, Kwon TH, Lee DS, Ha HL, Park DS, Woo EJ, Lee SH, Kim JM, Chae HB, Lee SY, Kim BY, Yoon do Y, Rhee SG, Fibach E, and Yu DY. Peroxiredoxin II is essential for preventing hemolytic anemia from oxidative stress through maintaining hemoglobin stability. Biochem Biophys Res Commun 426: 427-432, 2012.
115. Hatahet F, Boyd D, and Beckwith J. Disulfide bond formation in prokaryotes: history, diversity and design. Biochim Biophys Acta 1844: 1402-1414, 2014.
116. Hausladen A and Fridovich I. Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J Biol Chem 269: 29405-29408, 1994.
117. Hayes JD, Flanagan JU, and Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol 45: 51-88, 2005.
118. Hentze MW, Muckenthaler MU, Galy B, and Camaschella C. Two to tango: regulation of Mammalian iron metabolism. Cell 142: 24-38, 2010.
119. Herrero E, Ros J, Belli G, and Cabiscol E. Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780: 1217-1235, 2008.
120. Hildebrandt T, Knuesting J, Berndt C, Morgan B, and Scheibe R. Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub Biol Chem 396: 523-537, 2015.
121. Hiller N, Fritz-Wolf K, Deponte M, Wende W, Zimmermann H, and Becker K. Plasmodium falciparum glutathione S-transferase-structural and mechanistic studies on ligand binding and enzyme inhibition. Protein Sci 15: 281-289, 2006.
122. Hirrlinger J, Konig J, Keppler D, Lindenau J, Schulz JB, and Dringen R. The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J Neurochem 76: 627-636, 2001.
123. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, and O'Shea EK. Global analysis of protein localization in budding yeast. Nature 425: 686-691, 2003.
124. Hwang C, Sinskey AJ, and Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502, 1992.
125. Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776, 2008.
126. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443-454, 2013.
127. Imlay JA and Fridovich I. Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266: 6957-6965, 1991.
128. Inoue Y and Kimura A. Identification of the structural gene for glyoxalase I from Saccharomyces cerevisiae. J Biol Chem 271: 25958-25965, 1996.
129. Inoue Y, Maeta K, and Nomura W. Glyoxalase system in yeasts: structure, function, and physiology. Semin Cell Dev Biol 22: 278-284, 2011.
130. Inoue Y, Matsuda T, Sugiyama K, Izawa S, and Kimura A. Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J Biol Chem 274: 27002-27009, 1999.
131. Iwai K, Naganuma A, and Kuge S. Peroxiredoxin Ahp1 acts as a receptor for alkylhydroperoxides to induce disulfide bond formation in the Cad1 transcription factor. J Biol Chem 285: 10597-10604, 2010.
132. Izquierdo A, Casas C, Muhlenhoff U, Lillig CH, and Herrero E. Saccharomyces cerevisiae Grx6 and Grx7 are monothiol glutaredoxins associated with the early secretory pathway. Eukaryot Cell 7: 1415-1426, 2008.
133. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, and Snyder SH. Protein S-nitrosylation: A physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197, 2001.
134. Jakobsson PJ, Mancini JA, Riendeau D, and Ford-Hutchinson AW. Identification and characterization of a novel microsomal enzyme with glutathione-dependent transferase and peroxidase activities. J Biol Chem 272: 22934-22939, 1997.
135. Jakobsson PJ, Morgenstern R, Mancini J, Ford-Hutchinson A, and Persson B. Common structural features of MAPEG-a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci 8: 689-692, 1999.
136. Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, Choi YO, KimWY, Kang JS, Cheong GW, Yun DJ, Rhee SG, Cho MJ, and Lee SY. Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117: 625-635, 2004.
137. Jarvis RM, Hughes SM, and Ledgerwood EC. Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med 53: 1522-1530, 2012.
138. Johansson AS and Mannervik B. Human glutathione transferase A3-3, a highly efficient catalyst of doublebond isomerization in the biosynthetic pathway of steroid hormones. J Biol Chem 276: 33061-33065, 2001.
139. Johansson C, Lillig CH, and Holmgren A. Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. J Biol Chem 279: 7537-7543, 2004.
140. Johnson RM, Goyette G, Jr., Ravindranath Y, and Ho YS. Hemoglobin autoxidation and regulation of endogenous H2O2 levels in erythrocytes. Free Radic Biol Med 39: 1407-1417, 2005.
141. Johnson WM, Golczak M, Choe K, Currran PL, Gorelenkova Miller O, Yao C, Wang W, Lin J, Milkovic NM, Ray A, Ravindranath V, Zhu X, Wilson MA, Wilson-Delfosse AL, Chen SG, and Mieyal JJ. Regulation of DJ-1 by glutaredoxin 1 in vivo-implications for Parkinson's disease. Biochemistry 55: 4512-4532, 2016.
142. Jones CM, Lawrence A, Wardman P, and Burkitt MJ. Electron paramagnetic resonance spin trapping investigation into the kinetics of glutathione oxidation by the superoxide radical: re-evaluation of the rate constant. Free Radic Biol Med 32: 982-990, 2002.
143. Kehr S, Jortzik E, Delahunty C, Yates JR, 3rd, Rahlfs S, and Becker K. Protein S-glutathionylation in malaria parasites. Antioxid Redox Signal 15: 2855-2865, 2011.
144. Kelner MJ and Montoya MA. Structural organization of the human glutathione reductase gene: determination of correct cDNA sequence and identification of a mitochondrial leader sequence. Biochem Biophys Res Commun 269: 366-368, 2000.
145. Keyer K and Imlay JA. Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J Biol Chem 272: 27652-27659, 1997.
146. Kim IH, Kim K, and Rhee SG. Induction of an antioxidant protein of Saccharomyces cerevisiae by O2, Fe3+, or 2-mercaptoethanol. Proc Natl Acad Sci U S A 86: 6018-6022, 1989.
147. Kirsch M, Lehnig M, Korth HG, Sustmann R, and de Groot H. Inhibition of peroxynitrite-induced nitration of tyrosine by glutathione in the presence of carbon dioxide through both radical repair and peroxynitrate formation. Chemistry 7: 3313-3320, 2001.
148. Knockenhauer KE and Schwartz TU. The nuclear pore complex as a flexible and dynamic gate. Cell 164: 1162-1171, 2016.
149. Kodali VK and Thorpe C. Oxidative protein folding and the quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal 13: 1217-1230, 2010.
150. Kojer K, Bien M, Gangel H, Morgan B, Dick TP, and Riemer J. Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state. EMBO J 31: 3169-3182, 2012.
151. Kojer K, Peleh V, Calabrese G, Herrmann JM, and Riemer J. Kinetic control by limiting glutaredoxin amounts enables thiol oxidation in the reducing mitochondrial intermembrane space. Mol Biol Cell 26: 195-204, 2015.
152. Kulak NA, Pichler G, Paron I, Nagaraj N, and Mann M. Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat Methods 11: 319-324, 2014.
153. Kumar C, Igbaria A, D'Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, and Toledano MB. Glutathione revisited: A vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 30: 2044-2056, 2011.
154. Kussmaul L and Hirst J. The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A 103: 7607-7612, 2006.
155. Kwak HS, Yim HS, Chock PB, and Yim MB. Endogenous intracellular glutathionyl radicals are generated in neuroblastoma cells under hydrogen peroxide oxidative stress. Proc Natl Acad Sci U S A 92: 4582-4586, 1995.
156. Le Moan N, Clement G, Le Maout S, Tacnet F, and Toledano MB. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J Biol Chem 281: 10420-10430, 2006.
157. Lee J, Spector D, Godon C, Labarre J, and Toledano MB. A new antioxidant with alkyl hydroperoxide defense properties in yeast. J Biol Chem 274: 4537-4544, 1999.
158. Lee JY, Yang JG, Zhitnitsky D, Lewinson O, and Rees DC. Structural basis for heavy metal detoxification by an Atm1-type ABC exporter. Science 343: 1133-1136, 2014.
159. Lee TH, Kim SU, Yu SL, Kim SH, Park DS, Moon HB, Dho SH, Kwon KS, Kwon HJ, Han YH, Jeong S, Kang SW, Shin HS, Lee KK, Rhee SG, and Yu DY. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 101: 5033-5038, 2003.
160. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, and Jakob U. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A 105: 8197-8202, 2008.
161. Li H, Mapolelo DT, Dingra NN, Naik SG, Lees NS, Hoffman BM, Riggs-Gelasco PJ, Huynh BH, Johnson MK, and Outten CE. The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation. Biochemistry 48: 9569-9581, 2009.
162. Li ZS, Szczypka M, Lu YP, Thiele DJ, and Rea PA. The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J Biol Chem 271: 6509-6517, 1996.
163. Lillig CH, Berndt C, and Holmgren A. Glutaredoxin systems. Biochim Biophys Acta 1780: 1304-1317, 2008.
164. Lillig CH, Berndt C, Vergnolle O, Lonn ME, Hudemann C, Bill E, and Holmgren A. Characterization of human glutaredoxin 2 as iron-sulfur protein: A possible role as redox sensor. Proc Natl Acad Sci U S A 102: 8168-8173, 2005.
165. Little C and O'Brien PJ. Mechanism of peroxideinactivation of the sulphydryl enzyme glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 10: 533-538, 1969.
166. Lopreiato R, Facchin S, Sartori G, Arrigoni G, Casonato S, Ruzzene M, Pinna LA, and Carignani G. Analysis of the interaction between piD261/Bud32, an evolutionarily conserved protein kinase of Saccharomyces cerevisiae, and the Grx4 glutaredoxin. Biochem J 377: 395-405, 2004.
167. Lu SC. Glutathione synthesis. Biochim Biophys Acta 1830: 3143-3153, 2013.
168. Luikenhuis S, Perrone G, Dawes IW, and Grant CM. The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. Mol Biol Cell 9: 1081-1091, 1998.
169. Luo M, Jiang YL, Ma XX, Tang YJ, He YX, Yu J, Zhang RG, Chen Y, and Zhou CZ. Structural and biochemical characterization of yeast monothiol glutaredoxin Grx6. J Mol Biol 398: 614-622, 2010.
170. Maiorino M, Bosello-Travain V, Cozza G, Miotto G, Roveri A, Toppo S, Zaccarin M, and Ursini F. Understanding mammalian glutathione peroxidase 7 in the light of its homologs. Free Radic Biol Med 83: 352-360, 2015.
171. Maiorino M, Scapin M, Ursini F, Biasolo M, Bosello V, and Flohe L. Distinct promoters determine alternative transcription of gpx-4 into phospholipid-hydroperoxide glutathione peroxidase variants. J Biol Chem 278: 34286-34290, 2003.
172. Maiorino M, Ursini F, Bosello V, Toppo S, Tosatto SC, Mauri P, Becker K, Roveri A, Bulato C, Benazzi L, De Palma A, and Flohe L. The thioredoxin specificity of Drosophila GPx: A paradigm for a peroxiredoxin-like mechanism of many glutathione peroxidases. J Mol Biol 365: 1033-1046, 2007.
173. Malik SI, Hussain A, Yun BW, Spoel SH, and Loake GJ. GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181: 540-544, 2011.
174. Manta B, Hugo M, Ortiz C, Ferrer-Sueta G, Trujillo M, and Denicola A. The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch Biochem Biophys 484: 146-154, 2009.
175. Martinez-Ruiz A, Araujo IM, Izquierdo-Alvarez A, Hernansanz-Agustin P, Lamas S, and Serrador JM. Specificity in S-nitrosylation: A short-range mechanism for NO signaling Antioxid Redox Signal 19: 1220-1235, 2013.
176. Martinez Molina D, Eshaghi S, and Nordlund P. Catalysis within the lipid bilayer-structure and mechanism of the MAPEG family of integral membrane proteins. Curr Opin Struct Biol 18: 442-449, 2008.
177. Martins AM, Mendes P, Cordeiro C, and Freire AP. In situ kinetic analysis of glyoxalase I and glyoxalase II in Saccharomyces cerevisiae. Eur J Biochem 268: 3930-3936, 2001.
178. Massey V. Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 269: 22459-22462, 1994.
179. Mattevi A. To be or not to be an oxidase: challenging the oxygen reactivity of flavoenzymes. Trends Biochem Sci 31: 276-283, 2006.
180. McLaggan D, Rufino H, Jaspars M, and Booth IR. Glutathione-dependent conversion of N-ethylmaleimide to the maleamic acid by Escherichia coli: An intracellular detoxification process. Appl Environ Microbiol 66: 1393-1399, 2000.
181. McLellan AC, Phillips SA, and Thornalley PJ. The assay of S-D-lactoylglutathione in biological systems. Anal Biochem 211: 37-43, 1993.
182. Meinecke M, Cizmowski C, Schliebs W, Kruger V, Beck S, Wagner R, and Erdmann R. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat Cell Biol 12: 273-277, 2010.
183. Mesecke N, Mittler S, Eckers E, Herrmann JM, and Deponte M. Two novel monothiol glutaredoxins from Saccharomyces cerevisiae provide further insight into ironsulfur cluster binding, oligomerization, and enzymatic activity of glutaredoxins. Biochemistry 47: 1452-1463, 2008.
184. Mesecke N, Spang A, Deponte M, and Herrmann JM. A novel group of glutaredoxins in the cis-Golgi critical for oxidative stress resistance. Mol Biol Cell 19: 2673-2680, 2008.
185. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, and Herrmann JM. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121: 1059-1069, 2005.
186. Messner KR and Imlay JA. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J Biol Chem 274: 10119-10128, 1999.
187. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, and Shelton MD. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941-1988, 2008.
188. Molina MM, Belli G, de la Torre MA, Rodriguez-Manzaneque MT, and Herrero E. Nuclear monothiol glutaredoxins of Saccharomyces cerevisiae can function as mitochondrial glutaredoxins. J Biol Chem 279: 51923-51930, 2004.
189. Montero D, Tachibana C, Rahr Winther J, and Appenzeller-Herzog C. Intracellular glutathione pools are heterogeneously concentrated. Redox Biol 1: 508-513, 2013.
190. Moore RB, Mankad MV, Shriver SK, Mankad VN, and Plishker GA. Reconstitution of Ca(2+)-dependent K+ transport in erythrocyte membrane vesicles requires a cytoplasmic protein. J Biol Chem 266: 18964-18968, 1991.
191. Morel F, Rauch C, Petit E, Piton A, Theret N, Coles B, and Guillouzo A. Gene and protein characterization of the human glutathione S-transferase kappa and evidence for a peroxisomal localization. J Biol Chem 279: 16246-16253, 2004.
192. Morgan B, Ezerina D, Amoako TN, Riemer J, Seedorf M, and Dick TP. Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat Chem Biol 9: 119-125, 2013.
193. Morgan B, Van Laer K, Owusu TN, Ezerina D, Pastor-Flores D, Amponsah PS, Tursch A, and Dick TP. Real-time monitoring of basal H2O2 levels with peroxiredoxinbased probes. Nat Chem Biol 12: 437-443, 2016.
194. Muhlenhoff U, Molik S, Godoy JR, UzarskaMA, Richter N, SeubertA, ZhangY, Stubbe J, Pierrel F, Herrero E, LilligCH, and Lill R. Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound ironsulfur cluster. Cell Metab 12: 373-385, 2010.
195. Muller EG. A glutathione reductase mutant of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol Biol Cell 7: 1805-1813, 1996.
196. Muller S. Role and Regulation of glutathione metabolism in Plasmodium falciparum. Molecules 20: 10511-10534, 2015.
197. Munday R. Toxicity of thiols and disulphides: involvement of free-radical species. Free Radic Biol Med 7: 659-673, 1989.
198. Nagy P. Kinetics and mechanisms of thiol-disulfide exchange covering direct substitution and thiol oxidationmediated pathways. Antioxid Redox Signal 18: 1623-1641, 2013.
199. Nagy P and Ashby MT. Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. J Am Chem Soc 129: 14082-14091, 2007.
200. Nelson KJ, Klomsiri C, Codreanu SG, Soito L, Liebler DC, Rogers LC, Daniel LW, and Poole LB. Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol 473: 95-115, 2010.
201. Netto LE, de Oliveira MA, Tairum CA, and da Silva Neto JF. Conferring specificity in redox pathways by enzymatic thiol/disulfide exchange reactions. Free Radic Res 50: 206-245, 2016.
202. Nicholls P. Classical catalase: Ancient and modern. Arch Biochem Biophys 525: 95-101, 2012.
203. Nickel C, Rahlfs S, Deponte M, Koncarevic S, and Becker K. Thioredoxin networks in the malarial parasite Plasmodium falciparum. Antioxid Redox Signal 8: 1227-1239, 2006.
204. Nordlund P and Reichard P. Ribonucleotide reductases. Annu Rev Biochem 75: 681-706, 2006.
205. Ogino N, Miyamoto T, Yamamoto S, and Hayaishi O. Prostaglandin endoperoxide E isomerase from bovine vesicular gland microsomes, a glutathione-requiring enzyme. J Biol Chem 252: 890-895, 1977.
206. Ogura Y. Catalase activity at high concentration of hydrogen peroxide. Arch Biochem Biophys 57: 288-300, 1955.
207. Ogusucu R, Rettori D, Munhoz DC, Netto LE, and Augusto O. Reactions of yeast thioredoxin peroxidases I and II with hydrogen peroxide and peroxynitrite: rate constants by competitive kinetics. Free Radic Biol Med 42: 326-334, 2007.
208. Ohdate T and Inoue Y. Involvement of glutathione peroxidase 1 in growth and peroxisome formation in Saccharomyces cerevisiae in oleic acid medium. Biochim Biophys Acta 1821: 1295-1305, 2012.
209. Okumura M, Kadokura H, and Inaba K. Structures and functions of protein disulfide isomerase family members involved in proteostasis in the endoplasmic reticulum. Free Radic Biol Med 83: 314-322, 2015.
210. Osawa H, Stacey G, and Gassmann W. ScOPT1 and AtOPT4 function as proton-coupled oligopeptide transporters with broad but distinct substrate specificities. Biochem J 393: 267-275, 2006.
211. Oshino N, Chance B, Sies H, and Bucher T. The role of H2O2 generation in perfused rat liver and the reaction of catalase compound I and hydrogen donors. Arch Biochem Biophys 154: 117-131, 1973.
212. Ostergaard H, Tachibana C, and Winther JR. Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166: 337-345, 2004.
213. Ott C, Jacobs K, Haucke E, Navarrete Santos A, Grune T, and Simm A. Role of advanced glycation end products in cellular signaling. Redox Biol 2: 411-429, 2014.
214. Outten CE and Albetel AN. Iron sensing and regulation in Saccharomyces cerevisiae: ironing out the mechanistic details. Curr Opin Microbiol 16: 662-668, 2013.
215. Outten CE and Culotta VC. Alternative start sites in the Saccharomyces cerevisiae GLR1 gene are responsible for mitochondrial and cytosolic isoforms of glutathione reductase. J Biol Chem 279: 7785-7791, 2004.
216. Outten CE, Falk RL, and Culotta VC. Cellular factors required for protection from hyperoxia toxicity in Saccharomyces cerevisiae. Biochem J 388: 93-101, 2005.
217. Ozyamak E, Black SS, Walker CA, Maclean MJ, Bartlett W, Miller S, and Booth IR. The critical role of Slactoylglutathione formation during methylglyoxal detoxification in Escherichia coli. Mol Microbiol 78: 1577-1590, 2010.
218. Park JW, Piszczek G, Rhee SG, and Chock PB. Glutathionylation of peroxiredoxin I induces decamer to dimers dissociation with concomitant loss of chaperone activity. Biochemistry 50: 3204-3210, 2011.
219. Park SG, Cha MK, Jeong W, and Kim IH. Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J Biol Chem 275: 5723-5732, 2000.
220. Parsonage D, Karplus PA, and Poole LB. Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci U S A 105: 8209-8214, 2008.
221. Pedrajas JR, Kosmidou E, Miranda-Vizuete A, Gustafsson JA, Wright AP, and Spyrou G. Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem 274: 6366-6373, 1999.
222. Pedrajas JR, Miranda-Vizuete A, Javanmardy N, Gustafsson JA, and Spyrou G. Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J Biol Chem 275: 16296-16301, 2000.
223. Pedrajas JR, Porras P, Martinez-Galisteo E, Padilla CA, Miranda-Vizuete A, and Barcena JA. Two isoforms of Saccharomyces cerevisiae glutaredoxin 2 are expressed in vivo and localize to different subcellular compartments. Biochem J 364: 617-623, 2002.
224. Peltoniemi MJ, Karala AR, Jurvansuu JK, Kinnula VL, and Ruddock LW. Insights into deglutathionylation reactions. Different intermediates in the glutaredoxin and protein disulfide isomerase catalyzed reactions are defined by the gamma-linkage present in glutathione. J Biol Chem 281: 33107-33114, 2006.
225. Peralta D, Bronowska AK, Morgan B, Doka E, Van Laer K, Nagy P, Grater F, and Dick TP. A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat Chem Biol 11: 156-163, 2015.
226. Peskin AV, Pace PE, Behring JB, Paton LN, Soethoudt M, Bachschmid MM, and Winterbourn CC. Glutathionylation of the active site cysteines of peroxiredoxin 2 and recycling by glutaredoxin. J Biol Chem 291: 3053-3062, 2016.
227. Petrova VY, Drescher D, Kujumdzieva AV, and Schmitt MJ. Dual targeting of yeast catalase A to peroxisomes and mitochondria. Biochem J 380: 393-400, 2004.
228. Picciocchi A, Saguez C, Boussac A, Cassier-Chauvat C, and Chauvat F. CGFS-type monothiol glutaredoxins from the cyanobacterium Synechocystis PCC6803 and other evolutionary distant model organisms possess a glutathioneligated [2Fe-2S] cluster. Biochemistry 46: 15018-15026, 2007.
229. Prohaska JR and Ganther HE. Glutathione peroxidase activity of glutathione-s-transferases purified from rat liver. Biochem Biophys Res Commun 76: 437-445, 1976.
230. Puigpinos J, Casas C, and Herrero E. Altered intracellular calcium homeostasis and endoplasmic reticulum redox state in Saccharomyces cerevisiae cells lacking Grx6 glutaredoxin. Mol Biol Cell 26: 104-116, 2015.
231. Pujol-Carrion N, Belli G, Herrero E, Nogues A, and de la Torre-Ruiz MA. Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci 119: 4554-4564, 2006.
232. Rabbani N and Thornalley PJ. Glyoxalase in diabetes, obesity and related disorders. Semin Cell Dev Biol 22: 309-317, 2011.
233. Rabbani N and Thornalley PJ. Measurement of methylglyoxal by stable isotopic dilution analysis LC-MS/MS with corroborative prediction in physiological samples. Nat Protoc 9: 1969-1979, 2014.
234. Rabenstein DL, and Millis KK. Nuclear magnetic resonance study of the thioltransferase-catalyzed glutathione/ glutathione disulfide interchange reaction. Biochim Biophys Acta 1249: 29-36, 1995.
235. Rahlfs S, Nickel C, Deponte M, Schirmer RH, and Becker K. Plasmodium falciparum thioredoxins and glutaredoxins as central players in redox metabolism. Redox Rep 8: 246-250, 2003.
236. Reeves SA, Parsonage D, Nelson KJ, and Poole LB. Kinetic and thermodynamic features reveal that Escherichia coli BCP is an unusually versatile peroxiredoxin. Biochemistry 50: 8970-8981, 2011.
237. Reisz JA, Bechtold E, King SB, Poole LB, and Furdui CM. Thiol-blocking electrophiles interfere with labeling and detection of protein sulfenic acids. FEBS J 280: 6150-6161, 2013.
238. Rhee SG, Chae HZ, and Kim K. Peroxiredoxins: A historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 38: 1543-1552, 2005.
239. Riemer J, Bulleid N, and Herrmann JM. Disulfide formation in the ER and mitochondria: Two solutions to a common process. Science 324: 1284-1287, 2009.
240. Rodriguez-Manzaneque MT, Ros J, Cabiscol E, Sorribas A, and Herrero E. Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol Cell Biol 19: 8180-8190, 1999.
241. Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, and Herrero E. Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121, 2002.
242. Rouhier N, Gelhaye E, Sautiere PE, Brun A, Laurent P, Tagu D, Gerard J, de Fay E, Meyer Y, and Jacquot JP. Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol 127: 1299-1309, 2001.
243. Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP, and Wingsle G. Identification of plant glutaredoxin targets. Antioxid Redox Signal 7: 919-929, 2005.
244. Sato M, Sato K, and Nakano A. Endoplasmic reticulum quality control of unassembled iron transporter depends on Rer1p-mediated retrieval from the golgi. Mol Biol Cell 15: 1417-1424, 2004.
245. Schaedler TA, Thornton JD, Kruse I, Schwarzlander M, Meyer AJ, van Veen HW, and Balk J. A conserved mitochondrial ATP-binding cassette transporter exports glutathione polysulfide for cytosolic metal cofactor assembly. J Biol Chem 289: 23264-23274, 2014.
246. Schuppe-Koistinen I, Moldeus P, Bergman T, and Cotgreave IA. S-thiolation of human endothelial cell glyceraldehyde-3-phosphate dehydrogenase after hydrogen peroxide treatment. Eur J Biochem 221: 1033-1037, 1994.
247. Schutte LD, Baumeister S, Weis B, Hudemann C, Hanschmann EM, and Lillig CH. Identification of potential protein dithiol-disulfide substrates of mammalian Grx2. Biochim Biophys Acta 1830: 4999-5005, 2013.
248. Schwarzlander M, Dick TP, Meyer AJ, and Morgan B. Dissecting redox biology using fluorescent protein sensors. Antioxid Redox Signal 24: 680-712, 2016.
249. Seaver LC and Imlay JA. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183: 7182-7189, 2001.
250. Segel I. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady State Enzyme Systems. New York: John Wiley & Sons, Inc., 1993.
251. Shenton D and Grant CM. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374: 513-519, 2003.
252. Sies H. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem 289: 8735-8741, 2014.
253. Sies H and Chance B. The steady state level of catalase compound I in isolated hemoglobin-free perfused rat liver. FEBS Lett 11: 172-176, 1970.
254. SobottaMC, Barata AG, Schmidt U, Mueller S, Millonig G, and Dick TP. Exposing cells to H2O2: A quantitative comparison between continuous low-dose and one-time highdose treatments. Free Radic Biol Med 60: 325-335, 2013.
255. Sobotta MC, Liou W, Stocker S, Talwar D, Oehler M, Ruppert T, Scharf AN, and Dick TP. Peroxiredoxin-2 and STAT3 form a redox relay for HO signaling. Nat Chem Biol 11: 64-70, 2014.
256. Sousa Silva M, Gomes RA, Ferreira AE, Ponces Freire A, and Cordeiro C. The glyoxalase pathway: The first hundred years. And beyond. Biochem J 453: 1-15, 2013.
257. Spickett CM. The lipid peroxidation product 4-hydroxy-2-nonenal: Advances in chemistry and analysis. Redox Biol 1: 145-152, 2013.
258. Srinivasan U, Mieyal PA, and Mieyal JJ. pH profiles indicative of rate-limiting nucleophilic displacement in thioltransferase catalysis. Biochemistry 36: 3199-3206, 1997.
259. Srinivasan V, Pierik AJ, and Lill R. Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter Atm1. Science 343: 1137-1140, 2014.
260. Staab CA, Hellgren M, and Hoog JO. Medium-and shortchain dehydrogenase/reductase gene and protein families: dual functions of alcohol dehydrogenase 3: implications with focus on formaldehyde dehydrogenase and Snitrosoglutathione reductase activities. Cell Mol Life Sci 65: 3950-3960, 2008.
261. Staudacher V, Djuika CF, Koduka J, Schlossarek S, Kopp J, Buchler M, Lanzer M, and Deponte M. Plasmodium falciparum antioxidant protein reveals a novel mechanism for balancing turnover and inactivation of peroxiredoxins. Free Radic Biol Med 85: 228-236, 2015.
262. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, and Dancis A. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271: 1552-1557, 1996.
263. Stone JR and Yang S. Hydrogen peroxide: A signaling messenger. Antioxid Redox Signal 8: 243-270, 2006.
264. Sturm N, Jortzik E, Mailu BM, Koncarevic S, Deponte M, Forchhammer K, Rahlfs S, and Becker K. Identification of proteins targeted by the thioredoxin superfamily in Plasmodium falciparum. PLoS Pathog 5: e1000383, 2009.
265. Sturtz LA, Diekert K, Jensen LT, Lill R, and Culotta VC. A fraction of yeast Cu, Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276: 38084-38089, 2001.
266. Szajewski RP and Whitesides GM. Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J Am Chem Soc 102: 2011-2026, 1980.
267. Takanishi CL, Ma LH, and Wood MJ. A genetically encoded probe for cysteine sulfenic acid protein modification in vivo. Biochemistry 46: 14725-14732, 2007.
268. Tang Y, Zhang J, Yu J, Xu L, Wu J, Zhou CZ, and Shi Y. Structure-guided activity enhancement and catalytic mechanism of yeast grx8. Biochemistry 53: 2185-2196, 2014.
269. Terziyska N, Grumbt B, Kozany C, and Hell K. Structural and functional roles of the conserved cysteine residues of the redox-regulated import receptor Mia40 in the intermembrane space of mitochondria. J Biol Chem 284: 1353-1363, 2009.
270. Thornalley PJ. The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269: 1-11, 1990.
271. Thornalley PJ and Rabbani N. Glyoxalase in tumourigenesis and multidrug resistance. Semin Cell Dev Biol 22: 318-325, 2011.
272. Toledano MB, Delaunay-Moisan A, Outten CE, and Igbaria A. Functions and cellular compartmentation of the thioredoxin and glutathione pathways in yeast. Antioxid Redox Signal 18: 1699-1711, 2013.
273. Toppo S, Flohe L, Ursini F, Vanin S, and Maiorino M. Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. Biochim Biophys Acta 1790: 1486-1500, 2009.
274. Trotter EW and Grant CM. Overlapping roles of the cytoplasmic and mitochondrial redox regulatory systems in the yeast Saccharomyces cerevisiae. Eukaryot Cell 4: 392-400, 2005.
275. Trujillo M, Clippe A, Manta B, Ferrer-Sueta G, Smeets A, Declercq JP, Knoops B, and Radi R. Pre-steady state kinetic characterization of human peroxiredoxin 5: Taking advantage of Trp84 fluorescence increase upon oxidation. Arch Biochem Biophys 467: 95-106, 2007.
276. Turell L, Botti H, Carballal S, Ferrer-Sueta G, Souza JM, Duran R, Freeman BA, Radi R, and Alvarez B. Reactivity of sulfenic acid in human serum albumin. Biochemistry 47: 358-367, 2008.
277. Uchida M, Sun Y, McDermott G, Knoechel C, Le Gros MA, Parkinson D, Drubin DG, and Larabell CA. Quantitative analysis of yeast internal architecture using soft Xray tomography. Yeast 28: 227-236, 2011.
278. Urade Y, Ujihara M, Horiguchi Y, Igarashi M, Nagata A, Ikai K, and Hayaishi O. Mast cells contain spleen-type prostaglandin D synthetase. J Biol Chem 265: 371-375, 1990.
279. Urscher M, Alisch R, and Deponte M. The glyoxalase system of malaria parasites-Implications for cell biology and general glyoxalase research. Semin Cell Dev Biol 22: 262-270, 2011.
280. Urscher M and Deponte M. Plasmodium falciparum glyoxalase II: Theorell-Chance product inhibition patterns, rate-limiting substrate binding via Arg(257)/ Lys(260), and unmasking of acid-base catalysis. Biol Chem 390: 1171-1183, 2009.
281. Urscher M, Przyborski JM, Imoto M, and Deponte M. Distinct subcellular localization in the cytosol and apicoplast, unexpected dimerization and inhibition of Plasmodium falciparum glyoxalases. Mol Microbiol 76: 92-103, 2010.
282. Ursini F, Heim S, Kiess M, Maiorino M, Roveri A, Wissing J, and Flohe L. Dual function of the selenoprotein PHGPx during sperm maturation. Science 285: 1393-1396, 1999.
283. Vall-Llaura N, Reverter-Branchat G, Vived C, Weertman N, Rodriguez-Colman MJ, and Cabiscol E. Reversible glutathionylation of Sir2 by monothiol glutaredoxins Grx3/4 regulates stress resistance. Free Radic Biol Med 96: 45-56, 2016.
284. Wachter A, Wolf S, Steininger H, Bogs J, and Rausch T. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41: 15-30, 2005.
285. Wallace MA, Liou LL, Martins J, Clement MH, Bailey S, Longo VD, Valentine JS, andGralla EB. Superoxide inhibits 4Fe-4S cluster enzymes involved in amino acid biosynthesis. Cross-compartment protection by CuZn-superoxide dismutase. J Biol Chem 279: 32055-32062, 2004.
286. Wang L, Wang X, and Wang CC. Protein disulfideisomerase, a folding catalyst and a redox-regulated chaperone. Free Radic Biol Med 83: 305-313, 2015.
287. Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO, and von Mering C. PaxDb, a database of protein abundance averages across all three domains of life. Mol Cell Proteomics 11: 492-500, 2012.
288. Wang Y, Armando AM, Quehenberger O, Yan C, and Dennis EA. Comprehensive ultra-performance liquid chromatographic separation and mass spectrometric analysis of eicosanoid metabolites in human samples. J Chromatogr A 1359: 60-69, 2014.
289. Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K, Bodra N, Van Molle I, De Smet B, Vertommen D, Gevaert K, De Jaeger G, Van Montagu M, Messens J, and Van Breusegem F. Sulfenome mining in Arabidopsis thaliana. Proc Natl Acad Sci U S A 111: 11545-11550, 2014.
290. Wendler A, Irsch T, Rabbani N, Thornalley PJ, and Krauth-Siegel RL. Glyoxalase II does not support methylglyoxal detoxification but serves as a general trypanothione thioesterase in African trypanosomes. Mol Biochem Parasitol 163: 19-27, 2009.
291. Weydert CJ and Cullen JJ. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc 5: 51-66, 2010.
292. Wickner RB. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569, 1994.
293. Winterbourn CC. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim Biophys Acta 1840: 730-738, 2014.
294. Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549-561, 2008.
295. Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322-328, 1999.
296. Winther JR and Thorpe C. Quantification of thiols and disulfides. Biochim Biophys Acta 1840: 838-846, 2014.
297. Wolfe KH and Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713, 1997.
298. Wong CM, Siu KL, and Jin DY. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J Biol Chem 279: 23207-23213, 2004.
299. Wood ZA, Poole LB, and Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653, 2003.
300. Zaffagnini M, Bedhomme M, Marchand CH, Couturier JR, Gao XH, Rouhier N, Trost P, and Lemaire SP. Glutaredoxin s12: unique properties for redox signaling. Antioxid Redox Signal 16: 17-32, 2012.
301. Zahedi Avval F and Holmgren A. Molecular mechanisms of thioredoxin and glutaredoxin as hydrogen donors for Mammalian s phase ribonucleotide reductase. J Biol Chem 284: 8233-8240, 2009.
302. Zhang B, Bandyopadhyay S, Shakamuri P, Naik SG, Huynh BH, Couturier J, Rouhier N, and Johnson MK. Monothiol glutaredoxins can bind linear [Fe3S4]+ and [Fe4S4]2+ clusters in addition to [Fe2S2]2+ clusters: spectroscopic characterization and functional implications. J Am Chem Soc 135: 15153-15164, 2013.