Oxidative stress in rheumatoid arthritis

Studies on Arthritis and Joint Disorders

Volumn , Issue , 2013, Pages 145-167

  Szabó Taylor, Katalin É ^a   Nagy, György ^a   Eggleton, Paul ^b   Winyard, Paul G ^b  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85015793026     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-6166-1_8     Document Type: Chapter

References (134)

1. Hakim AJ, Clunie GPR, Haq I (2006) Oxford handbook of rheumatology. Oxford University Press, Oxford
2. Firestein GS (2003) Evolving concepts of rheumatoid arthritis. Nature 423:356-361
3. Bisoendial RJ, Stroes ESG, Kastelein JJP et al (2010) Targeting cardiovascular risk in rheumatoid arthritis: a dual role for statins. Nat Rev Rheumatol 6:157-164
4. Calvo-Alén J, Alarcón GS (2006) Epidemiology and determinants of susceptibility. In: Firestein GS, Panayi GS, Wollheim FA (eds) Rheumatoid arthritis, 2nd edn. Oxford University Press, Oxford
5. Altindag O, Karakoc M, Kocyigit A et al (2007) Increased DNA damage and oxidative stress in patients with rheumatoid arthritis. Clin Biochem 40:167-171
6. Gilston V, Blake DR, Winyard PG (1998) The rheumatoid joint: redox paradox? In: Montagnier L, Olivier R, Pasquier C (eds) Oxidative stress in cancer, AIDS, and neurodegenerative diseases. Marcel Dekker, New York
7. Ozkan Y, Yardým-Akaydýn S, Sepici A et al (2007) Oxidative status in rheumatoid arthritis. Clin Rheumatol 26:64-68
8. Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058-1071
9. Hurd TR, Murphy PM (2009) Biological systems relevant for redox signaling and control. In: Jacob C, Winyard PG (eds) Redox signaling and regulation in biology and medicine. Wiley-VCH, Weinheim
10. Bienert GP, Møller ALB, Kristiansen KA et al (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183-1192
11. Fisher AB (2009) Redox signaling across cell membranes. Antioxid Redox Signal 11:1349-1356
12. Bae YS, Kang SW, Seo MS et al (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 272:217-221
13. Sundaresan M, Yu ZX, Ferrans VJ et al (1995) Requirement for generation of H 2 O 2 for platelet-derived growth factor signal transduction. Science 270(5234):296-299
14. Ohba M, Shibanuma M, Kuroki T et al (1994) Production of hydrogen peroxide by transforming growth factor-beta 1 and its involvement in induction of egr-1 in mouse osteoblastic cells. J Cell Biol 126:1079-1088
15. Meier B, Radeke HH, Selle S et al (1989) Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumour necrosis factor-alpha. Biochem J 263:539-545
16. Finkel T (1998) Oxygen radicals and signaling. Curr Opin Cell Biol 10:248-253
17. Kang SW, Rhee SG, Chang TS et al (2005) 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med 11:571-578
18. Veal EA, Day AM, Morgan BA (2007) Hydrogen peroxide sensing and signaling. Mol Cell 26:1-14
19. Nisoli E, Clementi E, Paolucci C (2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299:896-899
20. Koncz A, Pásztói M, Mazan M et al (2007) Nitric oxide mediates T cell cytokine production and signal transduction in histidine decarboxylase knockout mice. J Immunol 179:6613-6619
21. Nagy G, Koncz A, Perl A et al (2003) T cell activation induced mitochondrial hyperpolarization is mediated by Ca2+ and redox-dependent production of nitric oxide. J Immunol 171:5188-5197
22. Mitsuhashi H, Yamashita S, Ikeuchi H et al (2005) Oxidative stress-dependent conversion of hydrogensulfide to sulfite by activated neutrophils. Shock 24:529-534
23. Whiteman M, Haigh R, Tarr JM et al (2010) Detection of hydrogen sulfide in plasma and knee-joint synovialfluid from rheumatoid arthritis patients: relation to clinical and laboratory measures of inflammation. Ann N Y Acad Sci 1203:146-150
24. Pattison DJ, Winyard PG (2008) Dietary antioxidants in inflammatory arthritis: do they have any role in etiology or therapy? Nat Clin Pract Rheumatol 4:590-596
25. Babior BM (2000) Phagocytes and oxidative stress. Am J Med 109:33-44
26. Hultqvist M, Olsson LM, Gelderman KA et al (2009) The protective role of ROS in autoimmune disease. Trends Immunol 30:201-208
27. Tak PP, Zvaifler NJ, Green DR et al (2000) Rheumatoid arthritis and p53: how oxidative stress might alter the course of inflammatory diseases. Immunol Today 21:78-82
28. Halliwell B (1995) Oxygen radicals, nitric oxide and human inflammatory joint disease. Ann Rheum Dis 54:505-510
29. Hitchon C, El-Gabalawy H (2004) Oxidation in rheumatoid arthritis. Arthritis Res Ther 6:265-278
30. Phillips DC, Dias HKI, Kitas GD et al (2009) Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention. Antioxid Redox Signal 12:743-785
31. Jacob C, Ba LA (2011) Open season for hunting and trapping post-translational cysteine modifications in proteins and enzymes. ChemBioChem 12:841-844
32. Winyard PG, Ryan B, Eggleton P et al (2011) Measurement and meaning of markers of reactive species of oxygen, nitrogen and sulfur in healthy human subjects and patients with inflammatory joint disease. Biochem Soc Trans 39:1226-1232
33. Filippin LI, Vercelino R, Marroni NP et al (2008) Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol 152:415-422
34. Lemarechal H, Allanore Y, Chenevier-Gobeaux C et al (2006) High redox thioredoxin but low thioredoxin reductase activities in the serum of patients with rheumatoid arthritis. Clin Chim Acta 367:156-161
35. Bashir S, Harris G, Denman MA et al (1993) Oxidative DNA damage and cellular sensitivity to oxidative stress in human autoimmune diseases. Ann Rheum Dis 52:659-666
36. Firestein GS, Echeverri F, Yeo M et al (1997) Somatic mutations in the p53 tumor suppressor gene in rheumatoid arthritis synovium. Proc Natl Acad Sci USA 94:10895-10900
37. Eggleton P, Haigh R, Winyard PG (2008) Consequence of neo-antigenicity of the 'altered self'. Rheumatology 47:567-571
38. Dai L, Zhang Z, Winyard PG et al (1996) A modified form of low-density lipoprotein with increased electronegative charge is present in rheumatoid arthritis synovialfluid. Free Radic Biol Med 22:705-710
39. Winyard PG, Tatzber F, Esterbauer H et al (1993) Presence of foam cells containing oxidised low density lipoprotein in the synovial membrane from patients with rheumatoid arthritis. Ann Rheum Dis 52:677-680
40. Nissim A, Winyard PG, Corrigall V et al (2005) Generation of neoantigenic epitopes after posttranslational modification of type II collagen by factors present within the inflamed joint. Arthritis Rheum 52:3829-3838
41. Nagy G, Clark JM, Buzás E et al (2008) Nitric oxide production of T lymphocytes is increased in rheumatoid arthritis. Immunol Lett 118:55-58
42. Gupta B, Raghav SK, Das HR (2008) S-nitrosylation of mannose binding lectin regulates its functional activities and the formation of autoantibody in rheumatoid arthritis. Nitric Oxide 18:266-273
43. Grinnell S, Yoshida K, Jasin HE (2005) Responses of lymphocytes of patients with rheumatoid arthritis to IgG modified by oxygen radicals or peroxynitrite. Arthritis Rheum 52:80-83
44. Niethammer P, Grabher C, Look AT et al (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996-999
45. Yoo SK, Starnes TW, Deng Q et al (2012) Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature 480:109-112
46. Di A, Gao X-P, Qian F et al (2012) The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat Immunol 13:29-34
47. Reth M (2002) Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 3:1129-1134
48. Dröge W (2002) Free radicals in the physiological control of cell function. Phys Rev 82:47-95
49. Winyard PG, Moody CJ, Jacob C (2005) Oxidative activation of antioxidant defence. Trends Biochem Sci 30:453-461
50. Lee R, Westendorf J, Gold M (2007) Differential role of reactive oxygen species in the activation of mitogen-activated protein kinases and Akt by key receptors on B-lymphocytes: CD40, the B cell antigen receptor, and CXCR4. J Cell Commun Signal 1:33-43
51. Williams MS, Kwon J (2004) T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic Biol Med 37:1144-1151
52. Whiteman M, Winyard PG (2011) Hydrogen sulfide and inflammation: the good, the bad, the ugly and the promising. Exp Rev Clin Pharmacol 4:13-32
53. Fox B, Schantz JT, Haigh R et al (2012) Inducible hydrogen sulfide synthesis in chondrocytes and mesenchymal progenitor cells: is H 2 S a novel cytoprotective mediator in the inflamed joint? J Cell Mol Med 16:896-910
54. Szabó KÉ, Line K, Eggleton P et al (2009) Structure and function of the human peroxiredoxinbased antioxidant system: the interplay between peroxiredoxins, thioredoxins, thioredoxin reductases, sulfiredoxins and sestrins. In: Winyard PG, Jacob C (eds) Redox signaling and regulation in biology and medicine. Wiley-VCH, Weinheim
55. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499-511
56. Liew FY, Xu D, Brint EK et al (2005) Negative regulation of Toll-like receptor-mediated immune responses. Nat Rev Immunol 5:446-458
57. Abdollahi-Roodsaz S, Joosten LAB, Roelofs MF et al (2007) Inhibition of toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum 56:2957-2967
58. Asehnoune K, Strassheim D, Mitra S et al (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-k B. J Immunol 172:2522-2529
59. Yang CS, Lee DS, Song CH et al (2007) Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J Exp Med 204:583-594
60. Matsui M, Oshima M, Oshima H et al (1996) Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol 178:179-185
61. Hultqvist M, Olofsson P, Holmberg J et al (2004) Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc Natl Acad Sci USA 101:12646-12651
62. George-Chandy A, Nordström I, Nygren E et al (2008) Th17 development and autoimmune arthritis in the absence of reactive oxygen species. Eur J Immunol 38:1118-1126
63. Lawrence DA, Song R, Weber P (1996) Surface thiols of human lymphocytes and their changes after in vitro and in vivo activation. J Leukoc Biol 60:611-618
64. Szabó-Taylor KÉ, Eggleton P, Turner CAL et al (2012) Lymphocytes from rheumatoid arthritis patients have elevated levels of intracellular peroxiredoxin 2, and a greater frequency of cells with exofacial peroxiredoxin 2, compared with healthy human lymphocytes. Int J Biochem Cell Biol 44:1223-1231
65. Mougiakakos D, Johansson CC, Kiessling R (2009) Naturally occurring regulatory T cells show reduced sensitivity toward oxidative stress-induced cell death. Blood 113:3542-3545
66. Mougiakakos D, Johansson CC, Jitschin R et al (2011) Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress. Blood 117:857-861
67. Wruck CJ, Fragoulis A, Gurzynski A et al (2011) Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis 70:844-850
68. Gelderman KA, Hultqvist M, Olsson LM et al (2007) Rheumatoid arthritis: the role of reactive oxygen species in disease development and therapeutic strategies. Antioxid Redox Signal 9:1541-1568
69. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6055
70. Winkler H, Adam G, Mattes E et al (1988) Co-ordinate control of synthesis of mitochondrial and non-mitochondrial hemoproteins: a binding site for the HAP1 (CYP1) protein in the UAS region of the yeast catalase T gene (CTT1). EMBO J 7:1799-1804
71. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Phys Rev 59:527-605
72. Holmgren A, Björnstedt M (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol 252:199-208
73. Chae HZ, Chung SJ, Rhee SG (1994) Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269:27670-27678
74. Hofmann B, Hecht HJ, Flohe L (2002) Peroxiredoxins. Biol Chem 383:347-364
75. Edmonds SE (2000) Do antioxidants have a role in the therapy of human inflammatory diseases? In: Winyard PG, Blake DR, Evans CH (eds) Free radicals and inflammation. Birkhäuser, Basel
76. Kus ML, Fairburn K, Blake DR et al (1995) A vascular basis for free radical involvement in inflammatory joint disease. In: Blake DR, Winyard PG (eds) Immunopharmacology of free radical species. Academic, San Diego, CA
77. Arner ESJ, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102-6109
78. Hirota K, Matsui M, Iwata S et al (1997) AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci USA 94:3633-3638
79. Martin H, Dean M (1991) Identification of a thioredoxin-related protein associated with plasma membranes. Biochem Biophys Res Commun 175:123-128
80. Arner ESJ (1999) Superoxide production by dinitrophenyl-derivatized thioredoxin reductase-a model for the mechanism and correlation to immunostimulation by dinitrohalobenzenes. Biofactors 10:219-226
81. Yoshida S, Katoh T, Tetsuka T et al (1999) Involvement of thioredoxin in rheumatoid arthritis: its costimulatory roles in the TNF-α -induced production of IL-6 and IL-8 from cultured synovial fibroblasts. J Immunol 163:351-358
82. Jikimoto T, Nishikubo Y, Koshiba M et al (2001) Thioredoxin as a biomarker for oxidative stress in patients with rheumatoid arthritis. Mol Immunol 38:765-772
83. Maurice MM, Nakamura H, Gringhuis S et al (1999) Expression of the thioredoxin-thioredoxin reductase system in the inflamed joints of patients with rheumatoid arthritis. Arthritis Rheum 42:2430-2439
84. Lemarechal H, Anract P, Beaudeux J-L et al (2007) Expression and extracellular release of Trx80, the truncated form of thioredoxin, by TNF-α and IL-1β-stimulated human synoviocytes from patients with rheumatoid arthritis. Clin Sci 113:149-155
85. Pekkari K, Gurunath R, Arner ESJ et al (2000) Truncated thioredoxin is a mitogenic cytokine for resting human peripheral blood mononuclear cells and is present in human plasma. J Biol Chem 275:37474-37480
86. Pekkari K, Goodarzi MT, Scheynius A et al (2005) Truncated thioredoxin (Trx80) induces differentiation of human CD14+ monocytes into a novel cell type (TAMs) via activation of the MAP kinases p38, ERK, and JNK. Blood 105:1598-1605
87. Kabuyama Y, Kitamura T, Yamaki J et al (2008) Involvement of thioredoxin reductase 1 in the regulation of redox balance and viability of rheumatoid synovial cells. Biochem Biophys Res Commun 367:491-496
88. Kim CW, Cho EH, Lee YJ et al (2006) Disease specific proteins from rheumatoid arthritis patients. J Korean Med Sci 21:478-484
89. Bo GP, Zhou LN, He WF et al (2009) Analyses of differential proteome of human synovial fibroblasts obtained from arthritis. Clin Rheumatol 28:191-199
90. Ali IU, Hynes RO (1978) Role of disulfide bonds in the attachment and function of large, external, transformation-sensitive glycoprotein at the cell surface. Biochim Biophys Acta 510:140-150
91. Laragione T, Gianazza E, Tonelli R et al (2006) Regulation of redox-sensitive exofacial protein thiols in CHO cells. Biol Chem 387:1371-1376
92. Freed BM, Mozayeni B, Lawrence DA et al (1986) Differential inhibition of human T-lymphocyte activation by maleimide probes. Cell Immunol 101:181-194
93. Pedersen-Lane JH, Zurier RB, Lawrence DA (2007) Analysis of the thiol status of peripheral blood leukocytes in rheumatoid arthritis patients. J Leukoc Biol 81:934-941
94. Gelderman KA, Hultqvist M, Holmberg J et al (2006) T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Natl Acad Sci USA 103:12831-12836
95. Wessels JAM, Huizinga TWJ, Guchelaar HJ (2008) Recent insights in the pharmacological actions of methotrexate in the treatment of rheumatoid arthritis. Rheumatology 47:249-255
96. Sahaf B, Söderberg A, Spyrou G et al (1997) Thioredoxin expression and localization in human cell lines: detection of full-length and truncated species. Exp Cell Res 236:181-192
97. Cortes-Bratti X, Basseres E, Herrera-Rodriguez F et al (2011) Thioredoxin 80-activatedmonocytes (TAMs) inhibit the replication of intracellular pathogens. PLoS One 6:e16960
98. Hara T, Kondo N, Nakamura H et al (2007) Cell-surface thioredoxin-1: possible involvement in thiol-mediated leukocyte-endothelial cell interaction through lipid rafts. Antioxid Redox Signal 9:1427-1438
99. Angelini G, Gardella S, Ardy M et al (2002) Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc Natl Acad Sci USA 99:1491-1496
100. Rubartelli A, Bajetto A, Allavena G et al (1992) Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 267:24161-24164
101. Soderberg A, Sahaf B, Rosen A (2000) Thioredoxin reductase, a redox-active selenoprotein, is secreted by normal and neoplastic cells: presence in human plasma. Cancer Res 60:2281-2289
102. Chang JW, Lee SH, Lu Y et al (2006) Transforming growth factor-b 1 includes the non-classical secretion of peroxiredoxin-I in A549 cells. Biochem Biophys Res Commun 345:118-123
103. Keller M, Rüegg A, Werner S et al (2008) Active caspase-1 is a regulator of unconventional protein secretion. Cell 132:818-831
104. Wakasugi N, Tagaya Y, Wakasugi H et al (1990) Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein-Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc Natl Acad Sci USA 87:8282-8286
105. Miller LA, Usachenko J, McDonald RJ et al (2000) Trafficking of neutrophils across airway epithelium is dependent upon both thioredoxin- and pertussis toxin-sensitive signaling mechanisms. J Leukoc Biol 68:201-208
106. Nakamura H, Hoshino Y, Okuyama H et al (2009) Thioredoxin 1 delivery as new therapeutics. Adv Drug Deliv Rev 61:303-309
107. Bertini R, Howard OMZ, Dong HF et al (1999) Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes and T cells. J Exp Med 189:1783-1789
108. Powis G, Mustacich D, Coon A (2000) The role of the redox protein thioredoxin in cell growth and cancer. Free Radic Biol Med 29:312-322
109. Matthias LJ, Yam PTW, Jiang X-M et al (2002) Disulfide exchange in domain 2 of CD4 is required for entry of HIV-1. Nat Immunol 3:727-732
110. Schwertassek U, Balmer Y, Gutscher M et al (2007) Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1. EMBO J 26:3086-3097
111. Geiben-Lynn R, Kursar M, Brown NV et al (2003) HIV-1 antiviral activity of recombinant natural killer cell enhancing factors, NKEF-A and NKEF-B, members of the peroxiredoxin family. J Biol Chem 278:1569-1574
112. Chen JH, Chang YW, Yao CW et al (2004) Plasma proteome of severe acute respiratory syndrome analyzed by two-dimensional gel electrophoresis and mass spectrometry. Proc Natl Acad Sci USA 101:17039-17044
113. Chang JW, Lee SH, Jeong JY et al (2005) Peroxiredoxin-I is an autoimmunogenic tumor antigen in non-small cell lung cancer. FEBS Lett 579:2873
114. Liu H, Pope RM (2003) The role of apoptosis in rheumatoid arthritis. Curr Opin Pharmacol 3:317-322
115. Korb A, Pavenstädt H, Pap T (2009) Cell death in rheumatoid arthritis. Apoptosis 14:447-454
116. Peng SL (2006) Fas (CD95)-related apoptosis and rheumatoid arthritis. Rheumatology 45:26-30
117. Chung HT, Pae HO, Choi BM et al (2001) Nitric oxide as a bioregulator of apoptosis. Biochem Biophys Res Commun 282:1075-1079
118. Kim YM, Bombeck CA, Billiar TR (1999) Nitric oxide as a bifunctional regulator of apoptosis. Circ Res 84:253-256
119. Leist M, Single B, Castoldi AF et al (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185:1481-1486
120. Cross A, Barnes T, Bucknall RC et al (2006) Neutrophil apoptosis in rheumatoid arthritis is regulated by local oxygen tensions within joints. J Leukoc Biol 80:521-528
121. Zhang P, Liu B, Kang SW et al (1997) Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J Biol Chem 272:30615-30618
122. Wang T, Tamae D, LeBon T et al (2005) The role of peroxiredoxin II in radiation-resistant MCF-7 breast cancer cells. Cancer Res 65:10338-10346
123. Moon JC, Hah YS, Kim WY et al (2005) Oxidative stress-dependent structural and functional switching of a human 2-Cys peroxiredoxin isotype II that enhances HeLa cell resistance to H 2 O 2 -induced cell death. J Biol Chem 280:28775-28784
124. Shau H, Kim AT, Hedrick CC et al (1997) Endogenous natural killer enhancing factor-B increases cellular resistance to oxidative stresses. Free Radic Biol Med 22:497-507
125. Chang TS, Cho CS, Park S et al (2004) Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J Biol Chem 279:41975-41984
126. Shih SF, Wu YH, Hung CH et al (2001) Abrin triggers cell death by inactivating a thiolspecific antioxidant protein. J Biol Chem 276:21870-21877
127. Cox AG, Pullar JM, Hughes G et al (2008) Oxidation of mitochondrial peroxiredoxin 3 during the initiation of receptor-mediated apoptosis. Free Radic Biol Med 44:1001-1009
128. Wonsey DR, Zeller KI, Dang CV (2002) The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc Natl Acad Sci USA 99:6649-6654
129. Ueda S, Nakamura T, Yamada A et al (2006) Recombinant human thioredoxin suppresses lipopolysaccharide-induced bronchoalveolar neutrophil infiltration in rat. Life Sci 79:1170-1177
130. Ichiki H, Hoshino T, Kinoshita T et al (2005) Thioredoxin suppresses airway hyperresponsiveness and airway inflammation in asthma. Biochem Biophys Res Commun 334:1141-1148
131. Tsuji G, Koshiba M, Nakamura H et al (2006) Thioredoxin protects against joint destruction in a murine arthritis model. Free Radic Biol Med 40:1721-1731
132. Ohashi S, Nishio A, Nakamura H et al (2006) Protective roles of redox-active protein thioredoxin-1 for severe acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 290:G772-G781
133. Schröder E, Littlechild JA, Lebedev AA et al (2000) Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 Å resolution. Structure 8:605-615
134. Maicas N, Ferrándiz ML, Brines R, Ibáñes L, Cuadrado A, Koenders MI, van den Berg WB, Alcaraz MJ (2011) Deficiency of Nrf2 accelerates the effector phase of arthritis and aggravates joint disease. Antioxid Redox Signal 15:889-901