Free radicals and redox signalling in T-cells during chronic inflammation and ageing

Biochemical Society Transactions

Volumn 39, Issue 5, 2011, Pages 1273-1278

  Griffiths, Helen R ^a   Dunston, Christopher R ^a   Bennett, Stuart J ^a   Grant, Melissa M ^a,c   Phillips, Darren C ^a,d   Kitas, George D ^b  

^a ASTON UNIVERSITY   (United Kingdom)

^b RUSSELLS HALL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d ABBOTT LABORATORIES   (United States)

Author keywords

Ageing; Glutathione; Inflammation; Reactive oxygen species (ROS); Redox signalling; Regulatory T cell (T reg cell)

Indexed keywords

ASCORBIC ACID; CONCANAVALIN A; CYSTEINE; FIBRINOGEN; FREE RADICAL; GLUCOSE TRANSPORTER 1; GLUTATHIONE; GLUTATHIONE REDUCTASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 2 RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; MULTIDRUG RESISTANCE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PEROXIREDOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN DISULFIDE ISOMERASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SERUM ALBUMIN; THIOL; THIOREDOXIN; THIOREDOXIN 1; TRANSFERRIN RECEPTOR;

AGING; ALBUMIN BLOOD LEVEL; AMINO ACID BLOOD LEVEL; BIOSYNTHESIS; CANCER CELL CULTURE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL GROWTH; CELL MATURATION; CELL METABOLISM; CELL MIGRATION; CELL PROLIFERATION; CHRONIC INFLAMMATION; COLON CANCER; CYTOTOXIC T LYMPHOCYTE; GENETIC TRANSCRIPTION; GLYCOLYSIS; GLYCOSYLATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID OXIDATION; LYMPHOCYTE FUNCTION; MITOCHONDRION; MODULATION; NONHUMAN; NUCLEUS ACCUMBENS; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH2 CELL; TUMOR GROWTH; VIRUS INFECTION; VITAMIN SUPPLEMENTATION;

AGING; FREE RADICALS; HUMANS; INFLAMMATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 80053363591     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0391273     Document Type: Review

References (45)

1. Wing, K. and Sakaguchi, S. (2010) Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11, 7-13
2. Gersovitz, M., Munro, H.N., Udall, J. and Young, V.R. (1980) Albumin synthesis in young and elderly subjects using a new stable isotope methodology: response to level of protein intake. Metab., Clin. Exp. 29, 1075-1086 (Pubitemid 11232204)
3. Thalacker-Mercer, A.E. and Campbell, W.W. (2008) Dietary protein intake affects albumin fractional synthesis rate in younger and older adults equally. Nutr. Rev. 66, 91-95 (Pubitemid 351666654)
4. Leto, S., Yiengst, M.J. and Barrows, C.H. (1970) The effect of age and protein deprivation on the sulfhydryl content of serum albumin. J. Gerontol. 25, 4-8
5. Dröge, W. (2005) Oxidative stress and ageing: is ageing a cysteine deficiency syndrome? Philos. Trans. R. Soc. Ser. B 360, 2355-2372
6. Jones, D.P., Carlson, J.L., Mody, V.C., Cai, J., Lynn, M.J. and Sternberg, P. (2000) Redox state of glutathione in human plasma. Free Radical Biol. Med. 28, 625-635 (Pubitemid 30136044)
7. - : cystine supplier and beyond. Amino Acids, doi:10.1007/s00726-011-0867-5
8. Bi, S., Hong, P.W., Lee, B. and Baum, L.G. (2011) Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance T-cell migration and HIV entry. Proc. Natl. Acad. Sci. U.S.A. 108, 10650-10655
9. Laragione, T., Bonetto, V., Casoni, F., Massignan, T., Bianchi, G., Gianazza, E. and Ghezzi, P. (2003) Redox regulation of surface protein thiols: identification of integrin α4 as a molecular target by using redox proteomics. Proc. Natl. Acad. Sci. 100, 14737-14741 (Pubitemid 37517960)
10. Aon, M.A., Cortassa, S. and O'Rourke, B. (2010) Redox-optimized ROS balance: a unifying hypothesis. Biochim. Biophys. Acta 1797, 865-877
11. Wild, A.C., Moinova, H.R. and Mulcahy, R.T. (1999) Regulation of γ -glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274, 33627-33636 (Pubitemid 129511675)
12. Benhar, M., Thompson, J.W., Moseley, M.A. and Stamler, J.S. (2010) Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49, 6963-6969
13. Keppler, D. (1999) Export pumps for glutathione S-conjugates. Free Radical Biol. Med. 27, 985-991
14. Mårtensson, J., Lai, J.C. and Meister, A. (1990) High-affinity transport of glutathione is part of a multicomponent system essential for mitochondrial function. Proc. Natl. Acad. Sci. U.S.A. 87, 7185-7189
15. Diaz Vivancos, P., Wolff, T., Markovic, J., Pallardó, F.V. and Foyer, C.H. (2010) A nuclear glutathione cycle within the cell cycle. Biochem. J. 431, 169-178
16. Adimora, N.J., Jones, D.P. and Kemp, M.L. (2010) A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses. Antioxid. Redox Signaling 13, 731-743
17. Mougiakakos, D., Johansson, C.C., Jitschin, R., Böttcher, M. and Kiessling, R. (2011) Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress. Blood 117, 857-861
18. Phillips, D.C., Dias, H.K.I., Kitas, G.D. and Griffiths, H.R. (2010) 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, 743-785
19. Lacombe, P., Kraus, L., Fay, M. and Pocidalo, J.-J. (1985) Lymphocyte glutathione status in relation to their Con A proliferative response. FEBS Lett. 191, 227-230 (Pubitemid 16230674)
20. Los, M., Schenk, H., Hexel, K., Baeuerle, P.A., Dröge, W. and Schulze-Osthoff, K. (1995) IL-2 gene expression and NF-κB activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 14, 3731-3740
21. Williams, M.S. and Kwon, J. (2004) T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radical Biol. Med. 37, 1144-1151 (Pubitemid 39296739)
22. Griffiths, H.R. (2005) ROS as signalling molecules in T cells: evidence for abnormal redox signalling in the autoimmune disease, rheumatoid arthritis. Redox Rep. 10, 273-280
23. Cemerski, S., van Meerwijk, J.P.M. and Romagnoli, P. (2003) Oxidative-stress-induced T lymphocyte hyporesponsiveness is caused by structural modification rather than proteasomal degradation of crucial TCR signaling molecules. Eur. J. Immunol. 33, 2178-2185 (Pubitemid 37010035)
24. Reference deleted
25. Kaur, N., Naga, O.S., Norell, H., Al-Khami, A.A., Scheffel, M.J., Chakraborty, N.G., Voelkel-Johnson, C., Mukherji, B. and Mehrotra, S. (2011) T cells expanded in presence of IL-15 exhibit increased antioxidant capacity and innate effector molecules. Cytokine 55, 307-317
26. Lawrence, D.A., Song, R. and Weber, P. (1996) Surface thiols of human lymphocytes and their changes after in vitro and in vivo activation. J. Leukocyte Biol. 60, 611-618 (Pubitemid 26400418)
27. Jonas, C.R., Ziegler, T.R., Gu, L.i. H. and Jones, D.P. (2002) Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma (Caco2) cell line. Free Radical Biol. Med. 33, 1499-1506 (Pubitemid 35351593)
28. Lukosz, M., Jakob, S., Büchner, N., Zschauer, T.-C., Altschmied, J. and Haendeler, J. (2010) Nuclear redox signaling. Antioxid. Redox Signaling 12, 713-742
29. Go, Y.-M. and Jones, D.P. (2010) Redox control systems in the nucleus: mechanisms and functions. Antioxid. Redox Signaling 13, 489-509
30. hi T lymphocytes accumulate with age in mice and respond poorly to concanavalin A. Eur. J. Immunol. 19, 977-982
31. Franklin, R.A., Arkins, S. and Kelley, K.W. (1990) The proliferative response of rat T cells to calcium ionophores increases with age. Cell. Immunol. 130, 416-428 (Pubitemid 20368059)
32. Grant, M.M. and Griffiths, H.R. (2007) 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, 335-339 (Pubitemid 46274485)
33. Checker, R., Sharma, D., Sandur, S.K., Subrahmanyam, G., Krishnan, S., Poduval, T.B. and Sainis, K.B. (2010) Plumbagin inhibits proliferative and inflammatory responses of T cells independent of ROS generation but by modulating intracellular thiols. J. Cell. Biochem. 110, 1082-1093
34. Sareila, O., Kelkka, T., Pizzolla, A., Hultqvist, M. and Holmdahl, R. (2011) NOX2 complex-derived ROS as immune regulators. Antioxid. Redox Signaling 15, 2197-2208
35. phox) is essential for direct regulatory T cell mediated suppression of CD4+ effector T cells. PLoS ONE 6, e16013
36. Yan, Z., Garg, S.K. and Banerjee, R. (2010) Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J. Biol. Chem. 285, 41525-41532
37. Grant, M.M., Mistry, N., Lunec, J. and Griffiths, H.R. (2007) Dose-dependent modulation of the T cell proteome by ascorbic acid. Br. J. Nutr. 97, 19-26 (Pubitemid 46662055)
38. Griffiths, H.R., Willetts, R.S., Grant, M.M., Mistry, N., Lunec, J. and Bevan, R.J. (2009) In vivo vitamin C supplementation increases phosphoinositol transfer protein expression in peripheral blood mononuclear cells from healthy individuals. Br. J. Nutr. 101, 1432-1439
39. Carty, J.L., Bevan, R., Waller, H., Mistry, N., Cooke, M., Lunec, J. and Griffiths, H.R. (2000) The effects of vitamin C supplementation on protein oxidation in healthy volunteers. Biochem. Biophys. Res. Commun. 273, 729-735 (Pubitemid 30599052)
40. Wilankar, C., Sharma, D., Checker, R., Khan, N.M., Patwardhan, R., Patil, A., Sandur, S.K. and Devasagayam, T.P. A. (2011) Role of immunoregulatory transcription factors in differential immunomodulatory effects of tocotrienols. Free Radical Biol. Med. 51, 129-143
41. Sinclair, L.V., Finlay, D., Feijoo, C., Cornish, G.H., Gray, A., Ager, A., Okkenhaug, K., Hagenbeek, T.J., Spits, H. and Cantrell, D.A. (2008) Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat. Immunol. 9, 513-521 (Pubitemid 351560520)
42. Michalek, R.D., Gerriets, V.A., Jacobs, S.R., Macintyre, A.N., MacIver, N.J., Mason, E.F., Sullivan, S.A., Nichols, A.G. and Rathmell, J.C. (2011) Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 186, 3299-3303
43. Wahl, D.R., Petersen, B., Warner, R., Richardson, B.C., Glick, G.D. and Opipari, A.W. (2010) Characterization of the metabolic phenotype of chronically activated lymphocytes. Lupus 19, 1492-1501
44. Pike, L.S., Smift, A.L., Croteau, N.J., Ferrick, D.A. and Wu, M. (2010) Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim. Biophys. Acta 1807, 726-734
45. Toms, T.E., Panoulas, V.F., Douglas, K.M.J., Nightingale, P., Smith, J.P., Griffiths, H., Sattar, N., Symmons, D.P. M. and Kitas, G.D. (2011) Are lipid ratios less susceptible to change with systemic inflammation than individual lipid components in patients with rheumatoid arthritis? Angiology 62, 167-175