Does metabolic reprogramming underpin age-associated changes in T cell phenotype and function?

Free Radical Biology and Medicine

Volumn 71, Issue , 2014, Pages 26-35

  Torrão, Rita C ^a   Bennett, Stuart J ^a   Brown, James E ^a   Griffiths, Helen R ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

Aging; Free radicals; Mitochondria; Protein oxidation; Redox; Thioredoxin; Treg

Indexed keywords

INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; REACTIVE OXYGEN METABOLITE; SIGNAL PEPTIDE;

AGE ASSOCIATED DISEASE; CELL AGING; CELL MATURATION; CELL METABOLISM; CELL MIGRATION; CELL SURFACE; DEVELOPMENTAL DISORDER; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; LYMPHOCYTE FUNCTION; LYMPHOCYTE REJUVENATION; METABOLIC REPROGRAMMING; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATION REDUCTION STATE; PHENOTYPE; PRIORITY JOURNAL; PROPHYLAXIS; REDOX HOMEOSTASIS; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ADAPTIVE IMMUNITY; AGING; ANIMAL; AUTOIMMUNITY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ADAPTIVE IMMUNITY; AGING; ANIMALS; AUTOIMMUNITY; GENE EXPRESSION REGULATION; HUMANS; LYMPHOCYTE ACTIVATION; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION; PHENOTYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 84898725912     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.03.002     Document Type: Review

References (113)

1. DC Phillips, HK Dias, GD Kitas, and HR. Griffiths Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention Antioxid. Redox Signaling 12 2010 743 785
2. K Wing, and S. Sakaguchi Regulatory T cells exert checks and balances on self tolerance and autoimmunity Nat. Immunol. 11 2010 7 13
3. HJ Forman, M Maiorino, and F. Ursini Signaling functions of reactive oxygen species Biochemistry 49 2010 835 842
4. HR Griffiths, CR Dunston, SJ Bennett, MM Grant, DC Phillips, and GD. Kitas Free radicals and redox signalling in T-cells during chronic inflammation and ageing Biochem. Soc. Trans. 39 2011 1273 1278
5. KPT Murphy, and M. Walport Janeway's Immunobiology 7th edition 2007 Garland New York
6. CA Janeway Jr, and M Walport et al. Immunobiology: the Immune System in Health and Disease 5th ed. 2001 Garland New York
7. TM Lindstrom, and WH. Robinson Rheumatoid arthritis: a role for immunosenescence? J. Am. Geriatr. Soc 58 2010 1565 1575
8. O Joffre, MA Nolte, and R Sporri Reis e Sousa C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity Immunol. Rev. 227 2009 234 247
9. HR. Griffiths ROS as signalling molecules in T cells - evidence for abnormal redox signalling in the autoimmune disease, rheumatoid arthritis Redox Rep. 10 2005 273 280 (Pubitemid 44111122)
10. RJ Brownlie, and R. Zamoyska T cell receptor signalling networks: branched, diversified and bounded Nat. Rev. Immunol. 13 2013 257 269
11. J Lin, and A. Weiss T cell receptor signalling J. Cell Sci. 114 Pt 2 2001 243 244 (Pubitemid 32149568)
12. DA. Cantrell T-cell antigen receptor signal transduction Immunology 105 2002 369 374 (Pubitemid 34429683)
13. J Manning, B Mitchell, DA Appadurai, A Shakya, LJ Pierce, and H Wang et al. Vitamin C promotes maturation of T-cells Antioxid. Redox Signaling 19 2013 2054 2067
14. JD Ahlers, and IM. Belyakov Molecular pathways regulating CD4(+) T cell differentiation, anergy and memory with implications for vaccines Trends Mol. Med. 16 2010 478 491
15. M Feili-Hariri, DH Falkner, and PA. Morel Polarization of naive T cells into Th1 or Th2 by distinct cytokine-driven murine dendritic cell populations: implications for immunotherapy J. Leukocyte Biol. 78 2005 656 664 (Pubitemid 41292088)
16. J Zhu, and WE. Paul CD4 T cells: fates, functions, and faults Blood 112 2008 1557 1569
17. AK Marwaha, NJ Leung, AN McMurchy, and MK. Levings TH17 cells in autoimmunity and immunodeficiency: protective or pathogenic? Front Immunol 3 2012 129
18. KE Shatynski, H Chen, J Kwon, and MS. Williams Decreased STAT5 phosphorylation and GATA-3 expression in NOX2-deficient T cells: role in T helper development Eur. J. Immunol. 42 2012 3202 3211
19. MR King, AS Ismail, LS Davis, and DR. Karp Oxidative stress promotes polarization of human T cell differentiation toward a T helper 2 phenotype J. Immunol. 176 2006 2765 2772
20. AE Moghaddam, KH Gartlan, L Kong, and QJ. Sattentau Reactive carbonyls are a major Th2-inducing damage-associated molecular pattern generated by oxidative stress J. Immunol. 187 2011 1626 1633
21. T Hadzic, L Li, N Cheng, SA Walsh, DR Spitz, and CM. Knudson The role of low molecular weight thiols in T lymphocyte proliferation and IL-2 secretion J. Immunol. 175 2005 7965 7972 (Pubitemid 41798357)
22. Y Kamide, M Utsugi, K Dobashi, A Ono, T Ishizuka, and T Hisada et al. Intracellular glutathione redox status in human dendritic cells regulates IL-27 production and T-cell polarization Allergy 66 2011 1183 1192
23. A Martner, J Aurelius, A Rydstrom, K Hellstrand, and FB. Thoren Redox remodeling by dendritic cells protects antigen-specific T cells against oxidative stress J. Immunol. 187 2011 6243 6248
24. + effector T cells PLoS One 6 2011 e16013
25. D Mougiakakos, CC Johansson, R Jitschin, M Bottcher, and R. Kiessling Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress Blood 117 2011 857 861
26. Z Yan, SK Garg, and R. Banerjee Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells J. Biol. Chem. 285 2010 41525 41532
27. RK Shrimali, RD Irons, BA Carlson, Y Sano, VN Gladyshev, and JM Park et al. Selenoproteins mediate T cell immunity through an antioxidant mechanism J. Biol. Chem. 283 2008 20181 20185
28. + T cells in mice through a mechanism involving cellular free thiols J. Nutr. 140 2010 1155 1161
29. B Alberts, and JA Lewis Molecular Biology of the Cell 4th edition 2002 Garland New York (J, et al)
30. DD Taub, CS Hesdorffer, L Ferrucci, K Madara, JB Schwartz, and EJ. Goetzl Distinct energy requirements for human memory CD4 T-cell homeostatic functions FASEB J. 27 2013 342 349
31. SI. Rattan Increased molecular damage and heterogeneity as the basis of aging Biol. Chem. 389 2008 267 272 (Pubitemid 351329028)
32. MJ Smithey, G Li, V Venturi, MP Davenport, and J. Nikolich-Žugich Lifelong persistent viral infection alters the naive T cell pool, impairing CD8 T cell immunity in late life J. Immunol. 189 2012 5356 5366
33. SK Butcher, H Chahal, L Nayak, A Sinclair, NV Henriquez, and E Sapey et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans J. Leukocyte Biol. 70 2001 881 886 (Pubitemid 33151126)
34. AN Vallejo, E Bryl, K Klarskov, S Naylor, CM Weyand, and JJ. Goronzy Molecular basis for the loss of CD28 expression in senescent T cells J. Biol. Chem. 277 2002 46940 46949 (Pubitemid 36159198)
35. P Uciechowski, L Kahmann, B Plumakers, M Malavolta, E Mocchegiani, and G Dedoussis et al. TH1 and TH2 cell polarization increases with aging and is modulated by zinc supplementation Exp. Gerontol. 43 2008 493 498
36. S Koch, R Solana, OD Rosa, and G. Pawelec Human cytomegalovirus infection and T cell immunosenescence: a mini review Mech. Ageing Dev. 127 2006 538 543
37. A Jagger, Y Shimojima, JJ Goronzy, and CM. Weyand Regulatory T cells and the immune aging process: a mini-review Gerontology 60 2014 130 137
38. L Arranz, JH Caamano, JM Lord, and M. De la Fuente Preserved immune functions and controlled leukocyte oxidative stress in naturally long-lived mice: possible role of nuclear factor kappa B J. Gerontol. A Biol. Sci. Med. Sci 65 2010 941 950
39. DE Lewis, M Merched-Sauvage, JJ Goronzy, CM Weyand, and AN. Vallejo Tumor necrosis factor-α and CD80 modulate CD28 expression through a similar mechanism of T-cell receptor-independent inhibition of transcription J. Biol. Chem. 279 2004 29130 29138 (Pubitemid 38915785)
40. A Kenessary, Z Zhumadilov, T Nurgozhin, D Kipling, M Yeoman, and L Cox et al. Biomarkers, interventions and healthy ageing New Biotechnol 30 2013 373 377
41. S Henis-Korenblit, P Zhang, M Hansen, M McCormick, SJ Lee, and M Cary et al. Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity Proc. Natl. Acad. Sci. USA 107 2010 9730 9735
42. DP Jones, YM Go, CL Anderson, TR Ziegler, JM Kinkade Jr., and WG. Kirlin Cysteine/cystine couple is a newly recognized node in the circuitry for biologic redox signaling and control FASEB J. 18 2004 1246 1248 (Pubitemid 39561565)
43. DP Jones, and YM. Go Redox compartmentalization and cellular stress Diabetes Obes. Metab. 12 Suppl. 2 2010 116 125
44. YC Jang, and H. Van Remmen The mitochondrial theory of aging: insight from transgenic and knockout mouse models Exp. Gerontol. 44 2009 256 260
45. G Powis, and WR. Montfort Properties and biological activities of thioredoxins Annu. Rev. Biophys. Biomol. Struct. 30 2001 421 455 (Pubitemid 32566170)
46. A Mitsui, J Hamuro, H Nakamura, N Kondo, Y Hirabayashi, and S Ishizaki-Koizumi et al. Overexpression of human thioredoxin in transgenic mice controls oxidative stress and life span Antioxid. Redox Signaling 4 2002 693 696 (Pubitemid 35001454)
47. VI Perez, LA Cortez, CM Lew, M Rodriguez, CR Webb, and H Van Remmen et al. Thioredoxin 1 overexpression extends mainly the earlier part of life span in mice J. Gerontol. A Biol. Sci. Med. Sci 66 2011 1286 1299
48. J Ungerstedt, Y Du, H Zhang, D Nair, and A. Holmgren in vivo redox state of human thioredoxin and redox shift by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) Free Radic. Biol. Med. 53 2012 2002 2007
49. A Holmgren, and J. Lu Thioredoxin and thioredoxin reductase: current research with special reference to human disease Biochem. Biophys. Res. Commun. 396 2010 120 124
50. SI Hashemy, and A. Holmgren Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues J. Biol. Chem. 283 2008 21890 21898
51. A. Holmgren Thioredoxin Annu. Rev. Biochem. 54 1985 237 271 (Pubitemid 15073647)
52. M Kaimul Ahsan, H Nakamura, M Tanito, K Yamada, H Utsumi, and J. Yodoi Thioredoxin-1 suppresses lung injury and apoptosis induced by diesel exhaust particles (DEP) by scavenging reactive oxygen species and by inhibiting DEP-induced downregulation of Akt Free Radic. Biol. Med. 39 2005 1549 1559 (Pubitemid 41642586)
53. H Nakamura, LA Herzenberg, J Bai, S Araya, N Kondo, and Y Nishinaka et al. Circulating thioredoxin suppresses lipopolysaccharide-induced neutrophil chemotaxis Proc. Natl. Acad. Sci. USA 98 2001 15143 15148 (Pubitemid 34013983)
54. H Tamaki, H Nakamura, A Nishio, H Nakase, S Ueno, and N Uza et al. Human thioredoxin-1 ameliorates experimental murine colitis in association with suppressed macrophage inhibitory factor production Gastroenterology 131 2006 1110 1121 (Pubitemid 44498706)
55. RB Carilho Torrao, IH Dias, SJ Bennett, CR Dunston, and HR. Griffiths Healthy ageing and depletion of intracellular glutathione influences T cell membrane thioredoxin-1 levels and cytokine secretion. Chem Cent. J. 7 2013 150
56. CC Winterbourn, and MB. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 45 2008 549 561
57. CH Lillig, and A. Holmgren Thioredoxin and related molecules - from biology to health and disease Antioxid. Redox Signaling 9 2007 25 47 (Pubitemid 44901873)
58. K Hirota, M Matsui, S Iwata, A Nishiyama, K Mori, and J. Yodoi AP-1 transcriptional activity is regulated by a direct association between thioredoxin and-Ref-1 Proc. Natl. Acad. Sci. USA 94 1997 3633 3638 (Pubitemid 27180424)
59. Y Kabe, K Ando, S Hirao, M Yoshida, and H. Handa Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus Antioxid. Redox Signaling 7 2005 395 403 (Pubitemid 40279807)
60. TC Zschauer, K Kunze, S Jakob, J Haendeler, and J. Altschmied Oxidative stress-induced degradation of thioredoxin-1 and apoptosis is inhibited by thioredoxin-1-actin interaction in endothelial cells Arterioscler. Thromb. Vasc. Biol. 31 2011 650 656
61. L Meng, JH Wong, LJ Feldman, PG Lemaux, and BB. Buchanan A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication Proc. Natl. Acad. Sci. USA 107 2010 3900 3905
62. A Rubartelli, A Bajetto, G Allavena, E Wollman, and R. Sitia Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway J. Biol. Chem. 267 1992 24161 24164
63. S Curbo, R Gaudin, M Carlsten, K-J Malmberg, M Troye-Blomberg, and N Ahlborg et al. Regulation of interleukin-4 signaling by extracellular reduction of intramolecular disulfides Biochem. Biophys. Res. Commun. 390 2009 1272 1277
64. N Kondo, Y Ishii, YW Kwon, M Tanito, J Sakakura-Nishiyama, and M Mochizuki et al. Lipid raft-mediated uptake of cysteine-modified thioredoxin-1: apoptosis enhancement by inhibiting the endogenous thioredoxin-1 Antioxid. Redox Signaling 9 2007 1439 1448
65. DP. Jones Extracellular redox state: refining the definition of oxidative stress in aging Rejuvenation Res 9 2006 169 181 (Pubitemid 43856805)
66. D Mougiakakos, CC Johansson, R Jitschin, M Böttcher, and R. Kiessling Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress Blood 117 2011 857 861
67. KA Gelderman, M Hultqvist, J Holmberg, P Olofsson, and R. Holmdahl T cell surface redox levels determine T cell reactivity and arthritis susceptibility Proc. Natl. Acad. Sci. USA 103 2006 12831 12836 (Pubitemid 44298647)
68. GJ van der Windt, D O'Sullivan, B Everts, SC Huang, MD Buck, and JD Curtis et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability Proc. Natl. Acad. Sci. USA 110 2013 14336 14341
69. M Chehtane, and AR. Khaled Interleukin-7 mediates glucose utilization in lymphocytes through transcriptional regulation of the hexokinase II gene Am. J. Physiol. Cell Physiol 298 2010 C1560 C1571
70. L Swainson, S Kinet, C Mongellaz, M Sourisseau, T Henriques, and N. Taylor IL-7-induced proliferation of recent thymic emigrants requires activation of the PI3K pathway Blood 109 2007 1034 1042 (Pubitemid 46220649)
71. + T cell subsets J. Immunol. 186 2011 3299 3303
72. MA Aon, S Cortassa, B. O'Rourke, and ROS Redox-optimized balance: a unifying hypothesis Biochim. Biophys. Acta Bioenerg 1797 2010 865 877
73. AC Wild, HR Moinova, and RT. Mulcahy Regulation of γ- glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2 J. Biol. Chem. 274 1999 33627 33636 (Pubitemid 129511675)
74. D. Keppler Export pumps for glutathione S-conjugates Free Radic. Biol. Med. 27 1999 985 991 (Pubitemid 29507471)
75. DC Phillips, HKI Dias, GD Kitas, and HR. Griffiths Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention Antioxid. Redox Signaling 12 2009 743 785
76. LA Sena, S Li, A Jairaman, M Prakriya, T Ezponda, and DA Hildeman et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling Immunity 38 2013 225 236
77. MR von Essen, M Kongsbak, TB Levring, AK Hansen, L Boding, and JP Lauritsen et al. PKC-theta exists in an oxidized inactive form in naive human T cells Eur. J. Immunol. 43 2013 1659 1666
78. MM Grant, and HR. Griffiths Cell passage-associated transient high oxygenation causes a transient decrease in cellular glutathione and affects T cell responses to apoptotic and mitogenic stimuli Environ. Toxicol. Pharmacol. 23 2007 335 339 (Pubitemid 46274485)
79. RT Kolamunne, M Clare, and HR. Griffiths Mitochondrial superoxide anion radicals mediate induction of apoptosis in cardiac myoblasts exposed to chronic hypoxia Arch. Biochem. Biophys. 505 2011 256 265
80. R Checker, D Sharma, SK Sandur, G Subrahmanyam, S Krishnan, and TB Poduval et al. Plumbagin inhibits proliferative and inflammatory responses of T cells independent of ROS generation but by modulating intracellular thiols J. Cell. Biochem. 110 2010 1082 1093
81. JP Messina, and DA. Lawrence Cell cycle progression of glutathione-depleted human peripheral blood mononuclear cells is inhibited at S phase J. Immunol. 143 1989 1974 1981 (Pubitemid 19241216)
82. JP Messina, and DA. Lawrence Effects of 2-mercaptoethanol and buthionine sulfoximine on cystine metabolism by and proliferation of mitogen-stimulated human and mouse lymphocytes Int. J. Immunopharmacol. 14 1992 1221 1234
83. S Roth, and W. Droge Regulation of interleukin 2 production, interleukin 2 mRNA expression and intracellular glutathione levels in ex vivo derived T lymphocytes by lactate Eur. J. Immunol. 21 1991 1933 1937
84. P Jeannin, Y Delneste, S Lecoanet-Henchoz, JF Gauchat, P Life, and D Holmes et al. Thiols decrease human interleukin (IL) 4 production and IL-4-induced immunoglobulin synthesis J. Exp. Med. 182 1995 1785 1792
85. C Metcalfe, P Cresswell, L Ciaccia, B Thomas, and AN. Barclay Labile disulfide bonds are common at the leucocyte cell surface Open Biol 1 2011 110010
86. MM Grant, N Mistry, J Lunec, and HR. Griffiths Dose-dependent modulation of the T cell proteome by ascorbic acid Br. J. Nutr. 97 2007 19 26 (Pubitemid 46662055)
87. HR Griffiths, RS Willetts, MM Grant, N Mistry, J Lunec, and RJ. Bevan in vivo vitamin C supplementation increases phosphoinositol transfer protein expression in peripheral blood mononuclear cells from healthy individuals Br. J. Nutr. 101 2009 1432 1439
88. M Tatar, A Kopelman, D Epstein, MP Tu, CM Yin, and RS. Garofalo A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function Science 292 2001 107 110 (Pubitemid 32289137)
89. R Schillaci, MG Brocardo, A Galeano, and A. Roldan Downregulation of insulin-like growth factor-1 receptor (IGF-1 R) expression in human T lymphocyte activation Cell. Immunol. 183 1998 157 161 (Pubitemid 28222272)
90. K Yang, and H. Chi mTOR and metabolic pathways in T cell quiescence and functional activation Semin. Immunol. 24 2012 421 428
91. Z Yang, H Fujii, SV Mohan, JJ Goronzy, and CM. Weyand Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells J. Exp. Med. 210 2013 2119 2134
92. FM Marelli-Berg, H Fu, and C. Mauro Molecular mechanisms of metabolic reprogramming in proliferating cells: implications for T-cell-mediated immunity Immunology 136 2012 363 369
93. A Silva, A Girio, I Cebola, CI Santos, F Antunes, and JT. Barata Intracellular reactive oxygen species are essential for PI3K/Akt/mTOR-dependent IL-7-mediated viability of T-cell acute lymphoblastic leukemia cells Leukemia 25 2011 960 967
94. S Winer, Y Chan, G Paltser, D Truong, H Tsui, and J Bahrami et al. Normalization of obesity-associated insulin resistance through immunotherapy Nat. Med 15 2009 921 929
95. JM Han, SJ Patterson, M Speck, JA Ehses, and MK. Levings Insulin inhibits IL-10-mediated regulatory T cell function: implications for obesity J. Immunol. 192 2014 623 629
96. K Eller, A Kirsch, AM Wolf, S Sopper, A Tagwerker, and U Stanzl et al. Potential role of regulatory T cells in reversing obesity-linked insulin resistance and diabetic nephropathy Diabetes 60 2011 2954 2962
97. G Matarese, C Procaccini, and V. De Rosa At the crossroad of T cells, adipose tissue, and diabetes Immunol. Rev. 249 2012 116 134
98. HS Kwon, HW Lim, J Wu, M Schnolzer, E Verdin, and M. Ott Three novel acetylation sites in the Foxp3 transcription factor regulate the suppressive activity of regulatory T cells J. Immunol. 188 2012 2712 2721
99. J van Loosdregt, Y Vercoulen, T Guichelaar, YY Gent, JM Beekman, and O van Beekum et al. Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization Blood 115 2010 965 974
100. + T cell activation by enhancing the expression and activity of Sirt1 PLoS One 8 2013 e75139
101. JE Brown, DJ Onyango, M Ramanjaneya, AC Conner, ST Patel, and SJ Dunmore et al. Visfatin regulates insulin secretion, insulin receptor signalling and mRNA expression of diabetes-related genes in mouse pancreatic beta-cells J. Mol. Endocrinol. 44 2010 171 178
102. 2+ by cyclic ADP-ribose-dependent TRPM2 channel gating in human T lymphocytes J. Biol. Chem. 287 2012 21067 21081
103. EL Pearce, MC Walsh, PJ Cejas, GM Harms, H Shen, and LS Wang et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism Nature 460 2009 103 107
104. EL Pearce, MC Poffenberger, CH Chang, and RG. Jones Fueling immunity: insights into metabolism and lymphocyte function Science 342 2013 1242454
105. JD Mezrich, JH Fechner, X Zhang, BP Johnson, WJ Burlingham, and CA. Bradfield An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells J. Immunol. 185 2010 3190 3198
106. HR Griffiths, J Lunec, and DR. Blake Oxygen radical induced fluorescence in proteins; identification of the fluorescent tryptophan metabolite, N-formyl kynurenine, as a biological index of radical damage Amino Acids 3 1992 183 194
107. M Dodson, V Darley-Usmar, and J. Zhang Cellular metabolic and autophagic pathways: traffic control by redox signaling Free Radic. Biol. Med. 63 2013 207 221
108. JD Powell, and GM. Delgoffe The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism Immunity 33 2010 301 311
109. R Wang, and DR. Green Metabolic checkpoints in activated T cells Nat. Immunol. 13 2012 907 915
110. Y Samstag, I John, and GH. Wabnitz Cofilin: a redox sensitive mediator of actin dynamics during T-cell activation and migration Immunol. Rev. 256 2013 30 47
111. KE Szabo-Taylor, P Eggleton, CA Turner, ML Faro, JM Tarr, and S Toth et al. 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 2012 1223 1231
112. C Metcalfe, P Cresswell, and AN. Barclay Interleukin-2 signalling is modulated by a labile disulfide bond in the CD132 chain of its receptor Open Biol 2 2012 110036
113. FB Thoren, A Betten, AI Romero, and K. Hellstrand Cutting edge: antioxidative properties of myeloid dendritic cells: protection of T cells and NK cells from oxygen radical-induced inactivation and apoptosis J. Immunol. 179 2007 21 25 (Pubitemid 46986511)