Quantitative measures for redox signaling

Free Radical Biology and Medicine

Volumn 96, Issue , 2016, Pages 290-303

  Pillay, Ché S ^a   Eagling, Beatrice D ^a   Driscoll, Scott R E ^a   Rohwer, Johann M ^b  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Computational models; Hydrogen peroxide; Kinetics; Oxidative stress; Peroxiredoxin; Redox; Systems biology

Indexed keywords

HYDROGEN PEROXIDE; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE;

ANALYSIS; CELL KINETICS; CONCENTRATION (PARAMETERS); CONCEPTUAL FRAMEWORK; HUMAN; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; QUALITATIVE RESEARCH; QUANTITATIVE STUDY; REDOX SIGNALING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SUPPLY DEMAND ANALYSIS; THERMODYNAMICS; TIME; CHEMISTRY; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; OXIDATIVE STRESS;

ANTIOXIDANTS; HYDROGEN PEROXIDE; KINETICS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84965097191     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.04.199     Document Type: Review

References (191)

1. U. Alon, An Introduction to Systems Biology: Design Principles of Biological Circuits, Chapman and Hall/CRC, 2006.
2. R. Heinrich, B.G. Neel, and T.A. Rapoport Mathematical models of protein kinase signal transduction Mol. Cell 9 2002 957 970
3. J.J. Hornberg, F.J. Bruggeman, B. Binder, C.R. Geest, A.J. de Vaate, J. Lankelma, R. Heinrich, and H.V. Westerhoff Principles behind the multifarious control of signal transduction. ERK phosphorylation and kinase/phosphatase control FEBS J. 272 2005 244 258
4. A. Goldbeter, and D.E. Koshland Jr. Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects J. Biol. Chem. 259 1984 14441 14447
5. J.J. Tyson, K.C. Chen, and B. Novak Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell Curr. Opin. Cell Biol. 15 2003 221 231
6. U. Alon Network motifs: theory and experimental approaches Nat. Rev. Genet. 8 2007 450 461
7. N. Rosenfeld, M.B. Elowitz, and U. Alon Negative autoregulation speeds the response times of transcription networks J. Mol. Biol. 323 2002 785 793
8. H.J. Forman, O. Augusto, R. Brigelius-Flohe, P.A. Dennery, B. Kalyanaraman, H. Ischiropoulos, G.E. Mann, R. Radi, L.J. Roberts 2nd, J. Vina, and K.J. Davies Even free radicals should follow some rules: a guide to free radical research terminology and methodology Free Radic. Biol. Med. 78 2015 233 235
9. K.J. Davies The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress IUBMB Life 48 1999 41 47
10. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 4 2008 278 286
11. T. Finkel Signal transduction by reactive oxygen species J. Cell Biol. 194 2011 7 15
12. H.J. Forman, F. Ursini, and M. Maiorino An overview of mechanisms of redox signaling J. Mol. Cell. Cardiol. 73 2014 2 9
13. M. Sundaresan, Z.X. Yu, V.J. Ferrans, K. Irani, and T. Finkel Requirement for generation of H2O2 for platelet-derived growth factor signal transduction Science 270 1995 296 299
14. Y.S. Bae, S.W. Kang, M.S. Seo, I.C. Baines, E. Tekle, P.B. Chock, and S.G. Rhee Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation J. Biol. Chem. 272 1997 217 221
15. B. D'Autreaux, and M.B. Toledano ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis Nat. Rev. Mol. Cell Biol. 8 2007 813 824
16. M.C. Gomez-Cabrera, A. Salvador-Pascual, H. Cabo, B. Ferrando, and J. Vina Redox modulation of mitochondriogenesis in exercise. Does antioxidant supplementation blunt thebenefits of exercise training? Free Radic. Biol. Med. 86 2015 37 46
17. V.I. Sayin, M.X. Ibrahim, E. Larsson, J.A. Nilsson, P. Lindahl, and M.O. Bergo Antioxidants accelerate lung cancer progression in mice Sci. Transl. Med. 6 2014 221ra215
18. D. Albanes, O.P. Heinonen, P.R. Taylor, J. Virtamo, B.K. Edwards, M. Rautalahti, A.M. Hartman, J. Palmgren, L.S. Freedman, J. Haapakoski, M.J. Barrett, P. Pietinen, N. Malila, E. Tala, K. Liippo, E.R. Salomaa, J.A. Tangrea, L. Teppo, F.B. Askin, E. Taskinen, Y. Erozan, P. Greenwald, and J.K. Huttunen Alpha-Tocopherol and beta-carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: effects of base-line characteristics and study compliance J. Natl. Cancer Inst. 88 1996 1560 1570
19. M. Ristow, K. Zarse, A. Oberbach, N. Kloting, M. Birringer, M. Kiehntopf, M. Stumvoll, C.R. Kahn, and M. Bluher Antioxidants prevent health-promoting effects of physical exercise in humans Proc. Natl. Acad. Sci. USA 106 2009 8665 8670
20. A. Bindoli, J.M. Fukuto, and H.J. Forman Thiol chemistry in peroxidase catalysis and redox signaling Antioxid. Redox Signal. 10 2008 1549 1564
21. Y.M. Janssen-Heininger, B.T. Mossman, N.H. Heintz, H.J. Forman, B. Kalyanaraman, T. Finkel, J.S. Stamler, S.G. Rhee, and A. van der Vliet Redox-based regulation of signal transduction: principles, pitfalls, and promises Free Radic. Biol. Med. 45 2008 1 17
22. S. Garcia-Santamarina, S. Boronat, and E. Hidalgo Reversible cysteine oxidation in hydrogen peroxide sensing and signal transduction Biochemistry 53 2014 2560 2580
23. C.C. Winterbourn Are free radicals involved in thiol-based redox signaling? Free Radic. Biol. Med. 80 2015 164 170
24. K.M. Holmstrom, and T. Finkel Cellular mechanisms and physiological consequences of redox-dependent signalling Nat. Rev. Mol. Cell Biol. 15 2014 411 421
25. C.C. Winterbourn The biological chemistry of hydrogen peroxide Methods Enzymol. 528 2013 3 25
26. H.Z. Chae, H. Oubrahim, J.W. Park, S.G. Rhee, and P.B. Chock Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators Antioxid. Redox Signal. 16 2012 506 523
27. S.G. Rhee, and H.A. Woo Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H(2)O(2), and protein chaperones Antioxid. Redox Signal. 15 2011 781 794
28. J.R. Stone, and S. Yang Hydrogen peroxide: a signaling messenger Antioxid. Redox Signal. 8 2006 243 270
29. J.A. Imlay Pathways of oxidative damage Annu. Rev. Microbiol. 57 2003 395 418
30. S. Mishra, and J. Imlay Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch. Biochem. Biophys. 525 2012 145 160
31. J.M. Dubbs, and S. Mongkolsuk Peroxide-sensing transcriptional regulators in bacteria J. Bacteriol. 194 2012 5495 5503
32. H.S. Marinho, C. Real, L. Cyrne, H. Soares, and F. Antunes Hydrogen peroxide sensing, signaling and regulation of transcription factors Redox Biol. 2 2014 535 562
33. K. Mahadev, H. Motoshima, X. Wu, J.M. Ruddy, R.S. Arnold, G. Cheng, J.D. Lambeth, and B.J. Goldstein The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction Mol. Cell. Biol. 24 2004 1844 1854
34. Y.A. Suh, R.S. Arnold, B. Lassegue, J. Shi, X. Xu, D. Sorescu, A.B. Chung, K.K. Griendling, and J.D. Lambeth Cell transformation by the superoxide-generating oxidase Mox1 Nature 401 1999 79 82
35. M.B. Hampton, A.J. Kettle, and C.C. Winterbourn Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing Blood 92 1998 3007 3017
36. B.J. Goldstein, K. Mahadev, X. Wu, L. Zhu, and H. Motoshima Role of insulin-induced reactive oxygen species in the insulin signaling pathway Antioxid. Redox Signal. 7 2005 1021 1031
37. S.G. Rhee Cell signaling. H2O2, a necessary evil for cell signaling Science 312 2006 1882 1883
38. T.H. Truong, and K.S. Carroll Redox regulation of protein kinases Crit. Rev. Biochem. Mol. Biol. 48 2013 332 356
39. J.R. Godoy, M. Funke, W. Ackermann, P. Haunhorst, S. Oesteritz, F. Capani, H.P. Elsasser, and C.H. Lillig 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 2011 2 92
40. G.P. Bienert, J.K. Schjoerring, and T.P. Jahn Membrane transport of hydrogen peroxide Biochim. Biophys. Acta 1758 2006 994 1003
41. G.P. Bienert, and F. Chaumont Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide Biochim. Biophys. Acta 1840 2014 1596 1604
42. J.A. Imlay The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium Nat. Rev. Microbiol. 11 2013 443 454
43. J.A. Imlay Cellular defenses against superoxide and hydrogen peroxide Annu. Rev. Biochem. 77 2008 755 776
44. V.D. Petrov, and F. Van Breusegem Hydrogen peroxide-a central hub for information flow in plant cells AoB Plants 2012 2012 pls014
45. R. Mittler, S. Vanderauwera, N. Suzuki, G. Miller, V.B. Tognetti, K. Vandepoele, M. Gollery, V. Shulaev, and F. Van Breusegem ROS signaling: the new wave? Trends Plant Sci. 16 2011 300 309
46. S. Gilroy, N. Suzuki, G. Miller, W.G. Choi, M. Toyota, A.R. Devireddy, and R. Mittler A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling Trends Plant Sci. 19 2014 623 630
47. P.M. Wood The potential diagram for oxygen at pH 7 Biochem. J. 253 1988 287 289
48. M. Giorgio, M. Trinei, E. Migliaccio, and P.G. Pelicci Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8 2007 722 728
49. C.C. Winterbourn, and D. Metodiewa Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide Free Radic. Biol. Med. 27 1999 322 328
50. J.M. Sobota, M. Gu, and J.A. Imlay Intracellular hydrogen peroxide and superoxide poison 3-deoxy-d-arabinoheptulosonate 7-phosphate synthase, the first committed enzyme in the aromatic biosynthetic pathway of Escherichia coli J. Bacteriol. 196 2014 1980 1991
51. M. Deponte, and C. Horst Lillig Enzymatic control of cysteinyl thiol switches in proteins Biol. Chem. 396 2015 401 413
52. N. Le Moan, G. Clement, S. Le Maout, F. Tacnet, and M.B. Toledano The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways J. Biol. Chem. 281 2006 10420 10430
53. E.M. Allen, and J.J. Mieyal Protein-thiol oxidation and cell death: regulatory role of glutaredoxins Antioxid. Redox Signal. 17 2012 1748 1763
54. M.M. Gallogly, and J.J. Mieyal Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress Curr. Opin. Pharmacol. 7 2007 381 391
55. I. Dalle-Donne, R. Rossi, G. Colombo, D. Giustarini, and A. Milzani Protein S-glutathionylation: a regulatory device from bacteria to humans Trends Biochem. Sci. 34 2009 85 96
56. C.H. Lillig, and C. Berndt Glutaredoxins in thiol/disulfide exchange Antioxid. Redox Signal. 18 2013 1654 1665
57. H.J. Forman, M. Maiorino, and F. Ursini Signaling functions of reactive oxygen species Biochemistry 49 2010 835 842
58. J.J. Mieyal, M.M. Gallogly, S. Qanungo, E.A. Sabens, and M.D. Shelton Molecular mechanisms and clinical implications of reversible protein S-glutathionylation Antioxid. Redox Signal. 10 2008 1941 1988
59. H.A. Woo, S.H. Yim, D.H. Shin, D. Kang, D.Y. Yu, and S.G. Rhee Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling Cell 140 2010 517 528
60. M. Kemp, Y.M. Go, and D.P. Jones Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology Free Radic. Biol. Med. 44 2008 921 937
61. S. Ashfaq, J.L. Abramson, D.P. Jones, S.D. Rhodes, W.S. Weintraub, W.C. Hooper, V. Vaccarino, D.G. Harrison, and A.A. Quyyumi The relationship between plasma levels of oxidized and reduced thiols and early atherosclerosis in healthy adults J. Am. College Cardiol. 47 2006 1005 1011
62. G.R. Buettner, B.A. Wagner, and V.G. Rodgers Quantitative redox biology: an approach to understand the role of reactive species in defining the cellular redox environment Cell Biochem. Biophys. 67 2013 477 483
63. R. Banerjee Redox outside the box: linking extracellular redox remodeling with intracellular redox metabolism J. Biol. Chem. 287 2012 4397 4402
64. D.P. Jones Extracellular redox state: refining the definition of oxidative stress in aging Rejuvenation Res. 9 2006 169 181
65. L. Flohe The fairytale of the GSSG/GSH redox potential Biochim. Biophys. Acta 1830 2013 3139 3142
66. C.S. Pillay, J.H. Hofmeyr, L.N. Mashamaite, and J.M. Rohwer From top-down to bottom-up: computational modeling approaches for cellular redoxin networks Antioxid. Redox Signal. 18 2013 2075 2086
67. A.I. Derman, W.A. Prinz, D. Belin, and J. Beckwith Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli Science 262 1993 1744 1747
68. M. Ralser, M.M. Wamelink, A. Kowald, B. Gerisch, G. Heeren, E.A. Struys, E. Klipp, C. Jakobs, M. Breitenbach, H. Lehrach, and S. Krobitsch Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress J. Biol. 6 2007 10
69. S. Toppo, L. Flohe, F. Ursini, S. Vanin, and M. Maiorino Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme Biochim. Biophys. Acta 1790 2009 1486 1500
70. L. Flohe, S. Toppo, G. Cozza, and F. Ursini A comparison of thiol peroxidase mechanisms Antioxid. Redox Signal. 15 2011 763 780
71. M.J. Picklo, E.K. Long, and E.E. Vomhof-DeKrey Glutathionyl systems and metabolic dysfunction in obesity Nutr. Rev. 73 2015 858 868
72. S.G. Rhee, H.A. Woo, I.S. Kil, and S.H. Bae Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides J. Biol. Chem. 287 2012 4403 4410
73. B. Manta, M. Hugo, C. Ortiz, G. Ferrer-Sueta, M. Trujillo, and A. Denicola The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2 Arch. Biochem. Biophys. 484 2009 146 154
74. K.J. Nelson, S.T. Knutson, L. Soito, C. Klomsiri, L.B. Poole, and J.S. Fetrow Analysis of the peroxiredoxin family: using active-site structure and sequence information for global classification and residue analysis Proteins 79 2011 947 964
75. A.V. Peskin, P.E. Pace, J.B. Behring, L.N. Paton, M. Soethoudt, M.M. Bachschmid, and C.C. Winterbourn Glutathionylation of the active site cysteines of peroxiredoxin 2 and recycling by glutaredoxin J. Biol. Chem. 291 2016 3053 3062
76. N. Rouhier, E. Gelhaye, and J.P. Jacquot Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism J. Biol. Chem. 277 2002 13609 13614
77. F. Pauwels, B. Vergauwen, F. Vanrobaeys, B. Devreese, and J.J. Van Beeumen Purification and characterization of a chimeric enzyme from Haemophilus influenzae Rd that exhibits glutathione-dependent peroxidase activity J. Biol. Chem. 278 2003 16658 16666
78. A.A. Sayed, and D.L. Williams Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni J. Biol. Chem. 279 2004 26159 26166
79. A. Perkins, L.B. Poole, and P.A. Karplus Tuning of peroxiredoxin catalysis for various physiological roles Biochemistry 53 2014 7693 7705
80. L.B. Poole, A. Hall, K.J. Nelson, Overview of peroxiredoxins in oxidant defense and redox regulation. (Current) (protocols in toxicology/editorial board, Mahin D. Maines), (Chapter 7), (Unit7 9), 2011.
81. G. Monteiro, B.B. Horta, D.C. Pimenta, O. Augusto, and L.E. Netto Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C Proc. Natl. Acad. Sci. USA 104 2007 4886 4891
82. Y. Manevich, S.I. Feinstein, and A.B. Fisher Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST Proc. Natl. Acad. Sci. USA 101 2004 3780 3785
83. J.R. Pedrajas, B. McDonagh, F. Hernandez-Torres, A. Miranda-Vizuete, R. Gonzalez, E. Martinez-Galisteo, C.A. Padilla, J.A. Barcena, Glutathione is the resolving thiol for thioredoxin peroxidase activity of 1-Cys peroxiredoxin without being consumed during the catalytic cycle, Antioxid. Redox Signal, 2015.
84. S. Barranco-Medina, J.J. Lazaro, and K.J. Dietz The oligomeric conformation of peroxiredoxins links redox state to function FEBS Lett. 583 2009 1809 1816
85. Z.A. Wood, E. Schroder, J. Robin Harris, and L.B. Poole Structure, mechanism and regulation of peroxiredoxins Trends Biochem. Sci. 28 2003 32 40
86. Z.A. Wood, L.B. Poole, R.R. Hantgan, and P.A. Karplus Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins Biochemistry 41 2002 5493 5504
87. H.H. Jang, K.O. Lee, Y.H. Chi, B.G. Jung, S.K. Park, J.H. Park, J.R. Lee, S.S. Lee, J.C. Moon, J.W. Yun, Y.O. Choi, W.Y. Kim, J.S. Kang, G.W. Cheong, D.J. Yun, S.G. Rhee, M.J. Cho, and S.Y. Lee Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function Cell 117 2004 625 635
88. H.A. Woo, H.Z. Chae, S.C. Hwang, K.S. Yang, S.W. Kang, K. Kim, and S.G. Rhee Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation Science 300 2003 653 656
89. B. Biteau, J. Labarre, and M.B. Toledano ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin Nature 425 2003 980 984
90. M.B. Pascual, A. Mata-Cabana, F.J. Florencio, M. Lindahl, and F.J. Cejudo Overoxidation of 2-Cys peroxiredoxin in prokaryotes: cyanobacterial 2-Cys peroxiredoxins sensitive to oxidative stress J. Biol. Chem. 285 2010 34485 34492
91. K.J. Nelson, D. Parsonage, P.A. Karplus, and L.B. Poole Evaluating peroxiredoxin sensitivity toward inactivation by peroxide substrates Methods Enzymol. 527 2013 21 40
92. Z.A. Wood, L.B. Poole, and P.A. Karplus Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling Science 300 2003 650 653
93. R.S. Edgar, E.W. Green, Y. Zhao, G. van Ooijen, M. Olmedo, X. Qin, Y. Xu, M. Pan, U.K. Valekunja, K.A. Feeney, E.S. Maywood, M.H. Hastings, N.S. Baliga, M. Merrow, A.J. Millar, C.H. Johnson, C.P. Kyriacou, J.S. O'Neill, and A.B. Reddy Peroxiredoxins are conserved markers of circadian rhythms Nature 485 2012 459 464
94. J.S. O'Neill, and A.B. Reddy Circadian clocks in human red blood cells Nature 469 2011 498 503
95. J.S. O'Neill, G. van Ooijen, L.E. Dixon, C. Troein, F. Corellou, F.Y. Bouget, A.B. Reddy, and A.J. Millar Circadian rhythms persist without transcription in a eukaryote Nature 469 2011 554 558
96. C.S. Cho, H.J. Yoon, J.Y. Kim, H.A. Woo, and S.G. Rhee Circadian rhythm of hyperoxidized peroxiredoxin II is determined by hemoglobin autoxidation and the 20S proteasome in red blood cells Proc. Natl. Acad. Sci. USA 111 2014 12043 12048
97. T.J. Phalen, K. Weirather, P.B. Deming, V. Anathy, A.K. Howe, A. van der Vliet, T.J. Jonsson, L.B. Poole, and N.H. Heintz Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery J. Cell Biol. 175 2006 779 789
98. R.M. Jarvis, S.M. Hughes, and E.C. Ledgerwood Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells Free Radic. Biol. Med. 53 2012 1522 1530
99. M.H. Choi, I.K. Lee, G.W. Kim, B.U. Kim, Y.H. Han, D.Y. Yu, H.S. Park, K.Y. Kim, J.S. Lee, C. Choi, Y.S. Bae, B.I. Lee, S.G. Rhee, and S.W. Kang Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II Nature 435 2005 347 353
100. M. Thamsen, C. Kumsta, F. Li, and U. Jakob Is overoxidation of peroxiredoxin physiologically significant? Antioxid. Redox Signal. 14 2011 725 730
101. S.J. Rawat, C.L. Creasy, J.R. Peterson, and J. Chernoff The tumor suppressor Mst1 promotes changes in the cellular redox state by phosphorylation and inactivation of peroxiredoxin-1 protein J. Biol. Chem. 288 2013 8762 8771
102. T.A. Zykova, F. Zhu, T.I. Vakorina, J. Zhang, L.A. Higgins, D.V. Urusova, A.M. Bode, and Z. Dong T-LAK cell-originated protein kinase (TOPK) phosphorylation of Prx1 at Ser-32 prevents UVB-induced apoptosis in RPMI7951 melanoma cells through the regulation of Prx1 peroxidase activity J. Biol. Chem. 285 2010 29138 29146
103. M.C. Sobotta, W. Liou, S. Stocker, D. Talwar, M. Oehler, T. Ruppert, A.N. Scharf, and T.P. Dick Peroxiredoxin-2 and STAT3 form a redox relay for H2O2 signaling Nat. Chem. Biol. 11 2015 64 70
104. A. Delaunay, D. Pflieger, M.B. Barrault, J. Vinh, and M.B. Toledano A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation Cell 111 2002 471 481
105. K. Gulshan, S.A. Rovinsky, S.T. Coleman, and W.S. Moye-Rowley Oxidant-specific folding of Yap1p regulates both transcriptional activation and nuclear localization J. Biol. Chem. 280 2005 40524 40533
106. E.A. Veal, S.J. Ross, P. Malakasi, E. Peacock, and B.A. Morgan Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor J. Biol. Chem. 278 2003 30896 30904
107. S. Kuge, T. Toda, N. Iizuka, and A. Nomoto Crm1 (XpoI) dependent nuclear export of the budding yeast transcription factor yAP-1 is sensitive to oxidative stress Genes Cells: Devoted Mol. Cell. Mech. 3 1998 521 532
108. C. Yan, L.H. Lee, and L.I. Davis Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor EMBO J. 17 1998 7416 7429
109. H. Liu, H. Zhang, K.E. Iles, A. Rinna, G. Merrill, J. Yodoi, M. Torres, and H.J. Forman The ADP-stimulated NADPH oxidase activates the ASK-1/MKK4/JNK pathway in alveolar macrophages Free Radic. Res. 40 2006 865 874
110. A.M. Day, J.D. Brown, S.R. Taylor, J.D. Rand, B.A. Morgan, and E.A. Veal Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival Mol. Cell. 45 2012 398 408
111. L.M. Randall, G. Ferrer-Sueta, and A. Denicola Peroxiredoxins as preferential targets in H2O2-induced signaling Methods Enzymol. 527 2013 41 63
112. A. Morinaka, Y. Funato, K. Uesugi, and H. Miki Oligomeric peroxiredoxin-I is an essential intermediate for p53 to activate MST1 kinase and apoptosis Oncogene 30 2011 4208 4218
113. F. Aslund, M. Zheng, J. Beckwith, and G. Storz Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status Proc. Natl. Acad. Sci. USA 96 1999 6161 6165
114. M. Zheng, F. Aslund, and G. Storz Activation of the OxyR transcription factor by reversible disulfide bond formation Science 279 1998 1718 1721
115. Q. Wei, P.N. Minh, A. Dotsch, F. Hildebrand, W. Panmanee, A. Elfarash, S. Schulz, S. Plaisance, D. Charlier, D. Hassett, S. Haussler, and P. Cornelis Global regulation of gene expression by OxyR in an important human opportunistic pathogen Nucl. Acids Res. 40 2012 4320 4333
116. M. Zheng, X. Wang, B. Doan, K.A. Lewis, T.D. Schneider, and G. Storz Computation-directed identification of OxyR DNA binding sites in Escherichia coli J. Bacteriol. 183 2001 4571 4579
117. M. Zheng, X. Wang, L.J. Templeton, D.R. Smulski, R.A. LaRossa, and G. Storz DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide J. Bacteriol. 183 2001 4562 4570
118. M.B. Toledano, I. Kullik, F. Trinh, P.T. Baird, T.D. Schneider, and G. Storz Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection Cell 78 1994 897 909
119. L. Jacquamet, D.A. Traore, J.L. Ferrer, O. Proux, D. Testemale, J.L. Hazemann, E. Nazarenko, A. El Ghazouani, C. Caux-Thang, V. Duarte, and J.M. Latour Structural characterization of the active form of PerR: insights into the metal-induced activation of PerR and Fur proteins for DNA binding Mol. Microbiol. 73 2009 20 31
120. A.F. Herbig, and J.D. Helmann Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA Mol. Microbiol. 41 2001 849 859
121. B. Halliwell, and J.M. Gutteridge Free Radicals in Biology and Medicine 1999 Oxford University Press Oxford
122. L. Wu, and A.B. Reddy Rethinking the clockwork: redox cycles and non-transcriptional control of circadian rhythms Biochem. Soc. Trans. 42 2014 1 10
123. L.E. Netto, F. Antunes, The Roles of Peroxiredoxin and Thioredoxin in Hydrogen Peroxide Sensing and in Signal Transduction, Mol. Cells, 2016.
124. B. Knoops, V. Argyropoulou, S. Becker, L. Ferte, O. Kuznetsova, Multiple roles of peroxiredoxins in inflammation, Mol. Cells, 2016.
125. S. Donnelly, S.M. O'Neill, M. Sekiya, G. Mulcahy, and J.P. Dalton Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages Infect. Immun. 73 2005 166 173
126. S. Donnelly, C.M. Stack, S.M. O'Neill, A.A. Sayed, D.L. Williams, and J.P. Dalton Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages FASEB J. 22 2008 4022 4032
127. M.W. Robinson, A.T. Hutchinson, J.P. Dalton, and S. Donnelly Peroxiredoxin: a central player in immune modulation Parasite Immunol. 32 2010 305 313
128. T. Furuta, S. Imajo-Ohmi, H. Fukuda, S. Kano, K. Miyake, and N. Watanabe Mast cell-mediated immune responses through IgE antibody and Toll-like receptor 4 by malarial peroxiredoxin Eur. J. Immunol. 38 2008 1341 1350
129. P. Checconi, S. Salzano, L. Bowler, L. Mullen, M. Mengozzi, E.M. Hanschmann, C.H. Lillig, R. Sgarbanti, S. Panella, L. Nencioni, A.T. Palamara, and P. Ghezzi Redox proteomics of the inflammatory secretome identifies a common set of redoxins and other glutathionylated proteins released in inflammation, influenza virus infection and oxidative stress PloS One 10 2015 e0127086
130. L. Mullen, E.M. Hanschmann, C.H. Lillig, L.A. Herzenberg, and P. Ghezzi Cysteine oxidation targets peroxiredoxins 1 and 2 for exosomal release through a novel mechanism of redox-dependent secretion Mol. Med. 21 2015 98 108
131. S. Salzano, P. Checconi, E.M. Hanschmann, C.H. Lillig, L.D. Bowler, P. Chan, D. Vaudry, M. Mengozzi, L. Coppo, S. Sacre, K.R. Atkuri, B. Sahaf, L.A. Herzenberg, L.A. Herzenberg, L. Mullen, and P. Ghezzi Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal Proc. Natl. Acad. Sci. USA 111 2014 12157 12162
132. J. Zhang, N. Jin, Y. Liu, and R.A. Rhoades Hydrogen peroxide stimulates extracellular signal-regulated protein kinases in pulmonary arterial smooth muscle cells Am. J. Respir. Cell Mol. Biol. 19 1998 324 332
133. R. Colavitti, G. Pani, B. Bedogni, R. Anzevino, S. Borrello, J. Waltenberger, and T. Galeotti Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR J. Biol. Chem. 277 2002 3101 3108
134. K.C. Chen, Y. Zhou, K. Xing, K. Krysan, and M.F. Lou Platelet derived growth factor (PDGF)-induced reactive oxygen species in the lens epithelial cells: the redox signaling Exp. Eye Res. 78 2004 1057 1067
135. C.S. Pillay, J.H. Hofmeyr, and J.M. Rohwer The logic of kinetic regulation in the thioredoxin system BMC Syst. Biol. 5 2011 15
136. D. Fell Understanding the Control of Metabolism 1997 Portland Press London
137. J.H. Hofmeyr, A. Cornish-Bowden, and J.M. Rohwer Taking enzyme kinetics out of control; putting control into regulation Eur. J. Biochem./FEBS 212 1993 833 837
138. M. Adler, A. Mayo, and U. Alon Logarithmic and power law input-output relations in sensory systems with fold-change detection PLoS Comput. Biol. 10 2014 e1003781
139. G. Dwivedi, and M.L. Kemp Systemic redox regulation of cellular information processing Antioxid. Redox Signal. 16 2012 374 380
140. E. Klipp, W. Liebermeister, C. Wierling, A. Kowald, H. Lehrach, and R. Herwig Systems Biology: A Textbook 2009 Wiley-VCH Weinheim
141. A.A. Sablina, A.V. Budanov, G.V. Ilyinskaya, L.S. Agapova, J.E. Kravchenko, and P.M. Chumakov The antioxidant function of the p53 tumor suppressor Nat. Med. 11 2005 1306 1313
142. J.A. Imlay, and S. Linn Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide J. Bacteriol. 166 1986 519 527
143. S. Iwakami, H. Misu, T. Takeda, M. Sugimori, S. Matsugo, S. Kaneko, and T. Takamura Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes PloS One 6 2011 e27401
144. M. Gulden, A. Jess, J. Kammann, E. Maser, and H. Seibert Cytotoxic potency of H2O2 in cell cultures: impact of cell concentration and exposure time Free Radic. Biol. Med. 49 2010 1298 1305
145. E. Linley, S.P. Denyer, G. McDonnell, C. Simons, and J.Y. Maillard Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action J. Antimicrob. Chemother. 67 2012 1589 1596
146. K. Nose, M. Shibanuma, K. Kikuchi, H. Kageyama, S. Sakiyama, and T. Kuroki Transcriptional activation of early-response genes by hydrogen peroxide in a mouse osteoblastic cell line Eur. J. Biochem./FEBS 201 1991 99 106
147. A. Delaunay, A.D. Isnard, and M.B. Toledano H2O2 sensing through oxidation of the Yap1 transcription factor EMBO J. 19 2000 5157 5166
148. Y.Y. Wang, S.M. Chen, and H. Li Hydrogen peroxide stress stimulates phosphorylation of FoxO1 in rat aortic endothelial cells Acta Pharmacol. Sin. 31 2010 160 164
149. F. Antunes, and E. Cadenas Estimation of H2O2 gradients across biomembranes FEBS Lett. 475 2000 121 126
150. B.K. Huang, and H.D. Sikes Quantifying intracellular hydrogen peroxide perturbations in terms of concentration Redox Biol. 2C 2014 955 962
151. H.S. Marinho, L. Cyrne, E. Cadenas, and F. Antunes H2O2 delivery to cells: steady-state versus bolus addition Methods Enzymol. 526 2013 159 173
152. M.C. Sobotta, A.G. Barata, U. Schmidt, S. Mueller, G. Millonig, and T.P. Dick Exposing cells to H2O2: a quantitative comparison between continuous low-dose and one-time high-dose treatments Free Radic. Biol. Med. 60 2013 325 335
153. S. Mueller, G. Millonig, and G.N. Waite The GOX/CAT system: a novel enzymatic method to independently control hydrogen peroxide and hypoxia in cell culture Adv. Medic. Sci. 54 2009 121 135
154. P.M. Brito, and F. Antunes Estimation of kinetic parameters related to biochemical interactions between hydrogen peroxide and signal transduction proteins Front. Chem. 2 2014 82
155. J.E. Ferrell Jr., and E.M. Machleder The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes Science 280 1998 895 898
156. G.J. Melen, S. Levy, N. Barkai, and B.Z. Shilo Threshold responses to morphogen gradients by zero-order ultrasensitivity Mol. Syst. Biol. 1 2005 2005 0028
157. M.K. Malleshaiah, V. Shahrezaei, P.S. Swain, and S.W. Michnick The scaffold protein Ste5 directly controls a switch-like mating decision in yeast Nature 465 2010 101 105
158. P.S. Swain, and E.D. Siggia The role of proofreading in signal transduction specificity Biophys. J. 82 2002 2928 2933
159. A.R. Asthagiri, and D.A. Lauffenburger A computational study of feedback effects on signal dynamics in a mitogen-activated protein kinase (MAPK) pathway model Biotechnol. Prog. 17 2001 227 239
160. M. Thattai, and A. van Oudenaarden Attenuation of noise in ultrasensitive signaling cascades Biophys. J. 82 2002 2943 2950
161. S.O. Kim, K. Merchant, R. Nudelman, W.F. Beyer Jr., T. Keng, J. DeAngelo, A. Hausladen, and J.S. Stamler OxyR: a molecular code for redox-related signaling Cell 109 2002 383 396
162. C. Lee, S.M. Lee, P. Mukhopadhyay, S.J. Kim, S.C. Lee, W.S. Ahn, M.H. Yu, G. Storz, and S.E. Ryu Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path Nat. Struct. Mol. Biol. 11 2004 1179 1185
163. J.R. Banga Optimization in computational systems biology BMC Syst. Biol. 2 2008 47
164. R. Schuetz, N. Zamboni, M. Zampieri, M. Heinemann, and U. Sauer Multidimensional optimality of microbial metabolism Science 336 2012 601 604
165. J.H. Hofmeyr The harmony of the cell: the regulatory design of cellular processes Essays Biochem. 45 2008 57 66
166. J.H. Hofmeyr, and J.M. Rohwer Supply-demand analysis a framework for exploring the regulatory design of metabolism Methods Enzymol. 500 2011 533 554
167. J.S. Hofmeyr, and A. Cornish-Bowden Regulating the cellular economy of supply and demand FEBS Lett. 476 2000 47 51
168. L.C. Seaver, and J.A. Imlay Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli J. Bacteriol. 183 2001 7173 7181
169. Y. Yamamoto, D. Ritz, A.G. Planson, T.J. Jonsson, M.J. Faulkner, D. Boyd, J. Beckwith, and L.B. Poole Mutant AhpC peroxiredoxins suppress thiol-disulfide redox deficiencies and acquire deglutathionylating activity Mol. Cell. 29 2008 36 45
170. R.L. Moore, C.O. Cook, R. Williams, and D.C. Goodwin Substitution of strictly conserved Y111 in catalase-peroxidases: impact of remote interdomain contacts on active site structure and catalytic performance J. Inorg. Biochem. 102 2008 1819 1824
171. B. Gonzalez-Flecha, and B. Demple Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli J. Biol. Chem. 270 1995 13681 13687
172. Y. Zhang, O. Marcillat, C. Giulivi, L. Ernster, and K.J. Davies The oxidative inactivation of mitochondrial electron transport chain components and ATPase J. Biol. Chem. 265 1990 16330 16336
173. L.C. Seaver, and J.A. Imlay Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli J. Bacteriol. 183 2001 7182 7189
174. B. Gonzalez-Flecha, and B. Demple Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli J. Bacteriol. 179 1997 382 388
175. R. Benfeitas, G. Selvaggio, F. Antunes, P.M. Coelho, and A. Salvador Hydrogen peroxide metabolism and sensing in human erythrocytes: a validated kinetic model and reappraisal of the role of peroxiredoxin II Free Radic. Biol. Med. 74 2014 35 49
176. N.J. Adimora, D.P. Jones, and M.L. Kemp A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses Antioxid. Redox Signal. 13 2010 731 743
177. Z. Gonzalez-Chavez, V. Olin-Sandoval, J.S. Rodiguez-Zavala, R. Moreno-Sanchez, and E. Saavedra Metabolic control analysis of the Trypanosoma cruzi peroxide detoxification pathway identifies tryparedoxin as a suitable drug target Biochim. Biophys. Acta 1850 2015 263 273
178. V. Olin-Sandoval, Z. Gonzalez-Chavez, M. Berzunza-Cruz, I. Martinez, R. Jasso-Chavez, I. Becker, B. Espinoza, R. Moreno-Sanchez, and E. Saavedra Drug target validation of the trypanothione pathway enzymes through metabolic modelling FEBS J. 279 2012 1811 1833
179. J.M. Rohwer, and J.H. Hofmeyr Identifying and characterising regulatory metabolites with generalised supply-demand analysis J. Theor. Biol. 252 2008 546 554
180. D.P. Jones, and Y.M. Go Mapping the cysteine proteome: analysis of redox-sensing thiols Curr. Opin. Chem. Biol. 15 2011 103 112
181. M. Lindahl, A. Mata-Cabana, and T. Kieselbach The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance Antioxid. Redox Signal. 14 2011 2581 2642
182. M. Thamsen, and U. Jakob The redoxome: proteomic analysis of cellular redox networks Curr. Opin. Chem. Biol. 15 2011 113 119
183. U. Sauer Metabolic networks in motion: 13C-based flux analysis Mol. Syst. Biol. 2 2006 62
184. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, L.J. Roberts 2nd, and H. Ischiropoulos Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic. Biol. Med. 52 2012 1 6
185. H. Link, D. Christodoulou, and U. Sauer Advancing metabolic models with kinetic information Curr. Opin. Biotechnol. 29 2014 8 14
186. R. Milo, S. Shen-Orr, S. Itzkovitz, N. Kashtan, D. Chklovskii, and U. Alon Network motifs: simple building blocks of complex networks Science 298 2002 824 827
187. L. Padayachee, C.S. Pillay, The thioredoxin system and not the Michaelis-Menten equation should be fitted to substrate saturation datasets from the thioredoxin insulin assay, Redox Report: (communications) (in free radical research), (2016), http://dx.doi.org/10.1179/1351000215Y.0000000024, Available at: http://www.tandfonline.com/doi/abs/10.1179/1351000215Y.0000000024?journalCode=yrer20
188. C.S. Pillay, J.H. Hofmeyr, B.G. Olivier, J.L. Snoep, and J.M. Rohwer Enzymes or redox couples? The kinetics of thioredoxin and glutaredoxin reactions in a systems biology context Biochem. J. 417 2009 269 275
189. L.N. Mashamaite, J.M. Rohwer, and C.S. Pillay The glutaredoxin mono- and di-thiol mechanisms for deglutathionylation are functionally equivalent: implications for redox systems biology Biosci. Rep. 35 2015 (pii: e00173)
190. A. Perkins, K.J. Nelson, D. Parsonage, L.B. Poole, and P.A. Karplus Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling Trends Biochem. Sci. 40 2015 435 445
191. B.G. Olivier, J.M. Rohwer, and J.H. Hofmeyr Modelling cellular systems with PySCeS Bioinformatics 21 2005 560 561