Reactive oxygen species in the immune system

International Reviews of Immunology

Volumn 32, Issue 3, 2013, Pages 249-270

  Yang, Yuhui ^a   Bazhin, Alexandr V ^a   Werner, Jens ^a   Karakhanova, Svetlana ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Immune response; Immunoregulation; Innate immunity; Reactive oxygen species; T cells

Indexed keywords

INFLAMMASOME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ADAPTIVE IMMUNITY; ANTIGENICITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BONE MARROW CELL; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; DENDRITIC CELL; GENE EXPRESSION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; MITOCHONDRION; MOLECULE; NATURAL KILLER CELL; NONHUMAN; PATHOGEN CLEARANCE; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SENESCENCE; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADAPTIVE IMMUNITY; AGING; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; IMMUNITY, INNATE; NEOPLASMS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84879100023     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2012.755176     Document Type: Article

References (160)

1. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res 2010;44(5):479-496.
2. FreinbichlerW, ColivicchiMA, Stefanini C, et al. Highly reactive oxygen species: detection, formation, and possible functions. CellMol Life Sci 2011;68(12):2067-2079.
3. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002;82(1):47-95.
4. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 2002;3(12):1129-1134.
5. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011;194(1):7-15.
6. Lee SR, Yang KS, Kwon J, et al. Reversible inactivation of the tumor suppressor PTEN byH2O2. J Biol Chem 2002;277(23):20336-20342.
7. ChanDW, Liu VW, TsaoGS, et al. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 2008;29(9):1742-1750.
8. Miller EW, Dickinson BC, Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci USA 2010;107(36):15681-15686.
9. Woo HA, Yim SH, ShinDH, et al. Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 2010;140(4):517-528.
10. Saitoh M,Nishitoh H, FujiiM, et al.Mammalian thioredoxin is a direct inhibitor of apoptosis signalregulating kinase (ASK) 1. EMBO J 1998;17(9):2596-2606.
11. Zhou R, Tardivel A,Thorens B, et al.Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010;11(2):136-140.
12. Funato Y,Michiue T, AsashimaM,MikiH.The thioredoxin-related redox-regulating protein nucleoredoxin inhibitsWnt-beta-catenin signalling through dishevelled.Nat Cell Biol 2006;8(5):501-508.
13. Kim YJ, LeeWS, Ip C, et al. Prx1 suppresses radiation-induced c-JunNH2-terminal kinase signaling in lung cancer cells through interaction with the glutathione S-transferase Pi/c-Jun NH2-terminal kinase complex. Cancer Res 2006;66(14):7136-7142.
14. Rutault K, Alderman C, Chain BM, Katz DR. Reactive oxygen species activate human peripheral blood dendritic cells. Free Radic BiolMed 1999;26(1-2):232-238.
15. Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res 2001;61(12):4756-4760.
16. Malmberg KJ, Arulampalam V, Ichihara F, et al. Inhibition of activated/memory (CD45RO(+)) T cells by oxidative stress associated with block of NF-kappaB activation. J Immunol 2001;167(5):2595-2601.
17. Li W, Lidebjer C, Yuan XM, et al. NK cell apoptosis in coronary artery disease: relation to oxidative stress. Atherosclerosis 2008;199(1):65-72.
18. Babior BM, Kipnes RS, Curnutte JT. Biological defense mechanisms.The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 1973;52(3):741-744.
19. Babior BM.The respiratory burst of phagocytes. J Clin Invest 1984;73(3):599-601.
20. Lam GY, Huang J, Brumell JH.Themany roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin Immunopathol 2010;32(4):415-430.
21. Nauseef WM. Nox enzymes in immune cells. Semin Immunopathol 2008;30(3):195-208.
22. Lambeth JD.NOXenzymes and the biology of reactive oxygen.Nat Rev Immunol 2004;4(3):181-189.
23. Sareila O, Kelkka T, Pizzolla A, et al. NOX2 complex-derived ROS as immune regulators. Antioxid Redox Signal 2011;15(8):2197-2208.
24. Segal AW. The NADPH oxidase and chronic granulomatous disease. Mol Med Today 1996;2(3):129-135.
25. Roos D, van Bruggen R, Meischl C. Oxidative killing of microbes by neutrophils. Microbes Infect 2003;5(14):1307-1315.
26. Haas A, Goebel W. Microbial strategies to prevent oxygen-dependent killing by phagocytes. Free Radic Res Commun 1992;16(3):137-157.
27. Reeves EP, Lu H, Jacobs HL, et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 2002;416(6878):291- 297.
28. Segal AW. How neutrophils killmicrobes. Annu Rev Immunol 2005;23:197-223.
29. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303(5663):1532-1535.
30. Wartha F, Henriques-Normark B. ETosis: a novel cell death pathway. Sci Signal 2008;1(21):pe25.
31. Amulic B, Hayes G. Neutrophil extracellular traps. Curr Biol 2011;21(9):R297-R298.
32. Bianchi M, Hakkim A, Brinkmann V, et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009;114(13):2619-2622.
33. Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 2011;51(7):1289-1301.
34. Gross O,Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev 2011;243(1):136-151.
35. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature 2012;481(7381):278-286.
36. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol 2012;13(4):325-332.
37. Tschopp J, Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 2010;10(3):210-215.
38. Dostert C, Petrilli V, Van Bruggen R, et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008;320(5876):674-677.
39. Petrilli V, Papin S, Dostert C, et al. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ 2007;14(9):1583-1589.
40. Masters SL, Dunne A, Subramanian SL, et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 2010;11(10):897-904.
41. Cruz CM, Rinna A, Forman HJ, et al. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 2007;282(5):2871-2879.
42. Hornung V, Bauernfeind F, Halle A, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008;9(8):847-856.
43. van de Veerdonk FL, Smeekens SP, Joosten LA, et al. Reactive oxygen species-independent activation of the IL-1beta inflammasome in cells from patients with chronic granulomatous disease. Proc Natl Acad Sci USA 2010;107(7):3030-3033.
44. Nakahira K, Haspel JA, Rathinam VA, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011;12(3):222-230.
45. Zhou R, Yazdi AS,Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011;469(7329):221-225.
46. Naik E, Dixit VM. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J ExpMed 2011;208(3):417-420.
47. Bulua AC, Simon A,Maddipati R, et al.Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J ExpMed 2011;208(3):519-533.
48. Veal EA, Day AM,Morgan BA. Hydrogen peroxide sensing and signaling.Mol Cell 2007;26(1):1-14.
49. West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol 2011;11(6):389-402.
50. Koshiba T. Mitochondrial-mediated antiviral immunity. Biochim Biophys Acta 2013;1833(1):225-232.
51. West AP, Brodsky IE, Rahner C, et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011;472(7344):476-480.
52. Dalton DK, Pitts-Meek S, Keshav S, et al. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 1993;259(5102):1739-1742.
53. Sonoda J, Laganiere J, Mehl IR, et al. Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense. Genes Dev 2007;21(15):1909-1920.
54. Vats D, Mukundan L, Odegaard JI, et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. CellMetab 2006;4(1):13-24.
55. Loo YM, Gale M, Jr. Immune signaling by RIG-I-like receptors. Immunity 2011;34(5):680-692.
56. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005;122(5):669-682.
57. Kawai T, Takahashi K, Sato S, et al. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 2005;6(10):981-988.
58. Meylan E, Curran J, Hofmann K, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005;437(7062):1167-1172.
59. Xu LG, Wang YY, Han KJ, et al. VISA is an adapter protein required for virus-triggered IFN-beta signaling.Mol Cell 2005;19(6):727-740.
60. Tal MC, SasaiM, Lee HK, et al. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci USA 2009;106(8):2770-2775.
61. Soucy-Faulkner A,Mukawera E, Fink K, et al. Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PLoS Pathog 2010;6(6):e1000930.
62. Doughan AK, Harrison DG, Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linkingmitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 2008;102(4):488-496.
63. Dikalova AE, Bikineyeva AT, Budzyn K, et al.Therapeutic targeting ofmitochondrial superoxide in hypertension. Circ Res 2010;107(1):106-116.
64. Daiber A. Redox signaling (cross-talk) from and tomitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta 2010;1797(6-7):897-906.
65. Malhotra A, Shanker A.NK cells: immune cross-talk and therapeutic implications. Immunotherapy 2011;3(10):1143-66.
66. Roder JC, Helfand SL,Werkmeister J, et al. Oxygen intermediates are triggered early in the cytolytic pathway of human NK cells. Nature 1982;298(5874):569-572.
67. Duwe AK, Roder JC. Involvement of hydroxyl free radical, but not superoxide, in the cytolytic pathway of natural killer cells. Revision of an earlier hypothesis.Med Biol 1984;62(2):95-100.
68. Duwe AK, Werkmeister J, Roder JC, et al. Natural killer cell-mediated lysis involves an hydroxyl radical-dependent step. J Immunol 1985;134(4):2637-2644.
69. SuthanthiranM, Solomon SD,Williams PS, et al.Hydroxyl radical scavengers inhibit human natural killer cell activity. Nature 1984;307(5948):276-278.
70. KayHD, SmithDL, SullivanG, et al. Evidence for a nonoxidative mechanism of human natural killer (NK) cell cytotoxicity by using mononuclear effector cells from healthy donors and from patients with chronic granulomatous disease. J Immunol 1983;131(4):1784-1788.
71. Ramstedt U, Rossi P, Kullman C, et al. Free oxygen radicals are not detectable by chemiluminescence during human natural killer cell cytotoxicity. Scand J Immunol 1984;19(5):457-464.
72. StorkusWJ,Dawson JR.Oxygen-reactive metabolites are not detected at the effector-target interface during natural killing. J Leukoc Biol 1986;39(5):547-557.
73. Gibboney JJ, Haak RA, Kleinhans FW, Brahmi Z. Electron spin resonance spectroscopy does not reveal hydroxyl radical production in activated natural killer lymphocytes. J Leukoc Biol 1988;44(6):545-550.
74. HanssonM, RomeroA,Thoren F, et al.Activation of cytotoxic lymphocytes by interferon-alpha: role of oxygen radical-producing mononuclear phagocytes. J Leukoc Biol 2004;76(6):1207-1213.
75. Hellstrand K, Asea A, Dahlgren C, Hermodsson S. Histaminergic regulation of NK cells. Role of monocyte-derived reactive oxygen metabolites. J Immunol 1994;153(11):4940-4947.
76. Asea A, Hansson M, Czerkinsky C, et al. Histaminergic regulation of interferon-gamma (IFNgamma) production by human natural killer (NK) cells. Clin Exp Immunol 1996;105(2):376-382.
77. Seaman WE, Gindhart TD, Blackman MA, et al. Suppression of natural killing in vitro bymonocytes and polymorphonuclear leukocytes: requirement for reactive metabolites of oxygen. J Clin Invest 1982;69(4):876-888.
78. Kono K, Salazar-Onfray F, Petersson M, et al. Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing zeta molecules and inhibits tumor-specific T cell-and natural killer cell-mediated cytotoxicity. Eur J Immunol 1996;26(6):1308-1313.
79. Corsi MM, Maes HH, Wasserman K, et al. Protection by L-2-oxothiazolidine- 4-carboxylic acid of hydrogen peroxide-induced CD3zeta and CD16zeta chain down-regulation in human peripheral blood lymphocytes and lymphokine-activated killer cells. Biochem Pharmacol 1998;56(5):657-662.
80. BruneM,HanssonM,Mellqvist UH, et al.NK cell-mediated killing ofAMLblasts: role of histamine, monocytes and reactive oxygen metabolites. Eur J Haematol 1996;57(4):312-319.
81. Houze TA, Larsson PA, Hellstrand K, Gustavsson B.The role of reactive oxygen metabolites in the transcriptional regulation of IFN-gamma gene expression by histamine in NK cells following IL-2 stimulation. Cell Biol Int 1996;20(9):589-598.
82. Asea A,Hermodsson S,Hellstrand K.Histaminergic regulation of natural killer cell-mediated clearance of tumour cells in mice. Scand J Immunol 1996;43(1):9-15.
83. Brune M, Castaigne S, Catalano J, et al. Improved leukemia-free survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acutemyeloid leukemia: results of a randomized phase 3 trial. Blood 2006;108(1):88-96.
84. HanssonM,AseaA, ErssonU, et al. Induction of apoptosis inNKcells by monocyte-derived reactive oxygen metabolites. J Immunol 1996;156(1):42-47.
85. Aurelius J, Thoren FB, Akhiani AA, et al.Monocytic AML cells inactivate antileukemic lymphocytes: role of NADPH oxidase/gp91(phox) expression and the PARP-1/PAR pathway of apoptosis. Blood 2012;119(24):5832-5837.
86. Li W, Johnson H, Yuan XM, Jonasson L. 7beta-hydroxycholesterol induces natural killer cell death via oxidative lysosomal destabilization. Free Radic Res 2009;43(11):1072-1079.
87. Huang Y, Lei Y, Zhang H, et al. Interleukin-12 treatment down-regulates STAT4 and induces apoptosis with increasing ROS production in human natural killer cells. J Leukoc Biol 2011;90(1): 87-97.
88. Romero AI,Thoren FB, Brune M, Hellstrand K. NKp46 and NKG2D receptor expression in NK cells with CD56dim and CD56bright phenotype: regulation by histamine and reactive oxygen species. Br J Haematol 2006;132(1):91-98.
89. Harlin H, Hanson M, Johansson CC, et al. The CD16-CD56(bright) NK cell subset is resistant to reactive oxygen species produced by activated granulocytes and has higher antioxidative capacity than the CD16+ CD56(dim) subset. J Immunol 2007;179(7):4513-4519.
90. Thoren FB, Romero AI, Hermodsson S, Hellstrand K.The CD16-/CD56bright subset of NK cells is resistant to oxidant-induced cell death. J Immunol 2007;179(2):781-785.
91. Izawa S, Kono K, Mimura K, et al. H(2)O(2) production within tumor microenvironment inversely correlatedwith infiltration of CD56(dim) NK cells in gastric and esophageal cancer: possiblemechanisms of NK cell dysfunction. Cancer Immunol Immunother 2011;60(12):1801-1810.
92. Del Prete A, Zaccagnino P, Di Paola M, et al. Role of mitochondria and reactive oxygen species in dendritic cell differentiation and functions. Free Radic BiolMed 2008;44(7):1443-1451.
93. Sheng KC, Pietersz GA, Tang CK, et al. Reactive oxygen species level defines two functionally distinctive stages of inflammatory dendritic cell development from mouse bone marrow. J Immunol 2010;184(6):2863-2872.
94. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processingmachines. Cell 2001;106(3):255-258.
95. Kantengwa S, Jornot L,DevenogesC,Nicod LP. Superoxide anions induce thematuration of human dendritic cells. AmJ Respir Crit CareMed 2003;167(3):431-437.
96. Lahiri A, Das P, Vani J, et al. TLR 9 activation in dendritic cells enhances salmonella killing and antigen presentation via involvement of the reactive oxygen species. PLoS One 2010;5(10):e13772.
97. Ogasawara N, Oguro T, Sakabe T, et al. Hemoglobin induces the expression of indoleamine 2,3-dioxygenase in dendritic cells through the activation of PI3K, PKC, and NF-kappaB and the generation of reactive oxygen species. J Cell Biochem 2009;108(3):716-725.
98. Rock KL, Shen L. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol Rev 2005;207:166-183.
99. Elsen S, Doussiere J, Villiers CL, et al. Cryptic O2-generating NADPH oxidase in dendritic cells. J Cell Sci 2004;117(Pt 11):2215-2226.
100. Mantegazza AR, SavinaA,Vermeulen M, et al.NADPHoxidase controls phagosomal pHand antigen cross-presentation in human dendritic cells. Blood 2008;112(12):4712-4722.
101. Kotsias F, Hoffmann E, Amigorena S, Savina A. Reactive oxygen species production in the phagosome: impact on antigen presentation in dendritic cells. Antioxid Redox Signal 2012 (September 11) [Epub ahead of print].
102. Savina A, Jancic C, Hugues S, et al. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006;126(1):205-218.
103. Fidelus RK, Ginouves P, Lawrence D, Tsan MF.Modulation of intracellular glutathione concentrations alters lymphocyte activation and proliferation. Exp Cell Res 1987;170(2):269-275.
104. Novogrodsky A, Ravid A, Rubin AL, Stenzel KH.Hydroxyl radical scavengers inhibit lymphocytemitogenesis. Proc Natl Acad Sci USA 1982;79(4):1171-1174.
105. Chaudhri G, Hunt NH, Clark IA, Ceredig R. Antioxidants inhibit proliferation and cell surface expression of receptors for interleukin-2 and transferrin in T lymphocytes stimulated with phorbol myristate acetate and ionomycin. Cell Immunol 1988;115(1):204-213.
106. Chaudhri G, Clark IA, Hunt NH, et al. Effect of antioxidants on primary alloantigen-induced T cell activation and proliferation. J Immunol 1986;137(8):2646-2652.
107. Williams MS, Kwon J. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic BiolMed 2004;37(8):1144-1151.
108. Devadas S, Zaritskaya L, Rhee SG, et al. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J ExpMed 2002;195(1):59-70.
109. Jackson SH, Devadas S, Kwon J, et al. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 2004;5(8):818-827.
110. Kwon J, Devadas S, Williams MS. T cell receptor-stimulated generation of hydrogen peroxide inhibitsMEK-ERKactivation andlck serinephosphorylation. FreeRadicBiolMed2003;35(4):406-417.
111. Kaminski MM, Sauer SW, Klemke CD, et al. Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression:mechanism of ciprofloxacin-mediated immunosuppression. J Immunol 2010;184(9):4827-4841.
112. Yi JS, Holbrook BC, Michalek RD, et al. Electron transport complex I is required for CD8+ T cell function. J Immunol 2006;177(2):852-862.
113. Kaminski M, Kiessling M, Suss D, et al. Novel role for mitochondria: protein kinase Cthetadependent oxidative signaling organelles in activation-induced T-cell death. Mol Cell Biol 2007;27(10):3625-3639.
114. Gelderman KA, Hultqvist M, Pizzolla A, et al. Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J Clin Invest 2007;117(10):3020-3028.
115. Matsue H, Edelbaum D, Shalhevet D, et al. Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J Immunol 2003;171(6):3010-3018.
116. Fooksman DR, Vardhana S, Vasiliver-Shamis G, et al. Functional anatomy of T cell activation and synapse formation. Annu Rev Immunol 2010;28:79-105.
117. Hultqvist M, Olsson LM, Gelderman KA, Holmdahl R. The protective role of ROS in autoimmune disease. Trends Immunol 2009;30(5):201-208.
118. Case AJ, McGill JL, Tygrett LT, et al. Elevated mitochondrial superoxide disrupts normal T cell development, impairing adaptive immune responses to an influenza challenge. Free Radic Biol Med 2011;50(3):448-458.
119. Lahdenpohja N, Savinainen K, Hurme M. Pre-exposure to oxidative stress decreases the nuclear factor-kappa B-dependent transcription in T lymphocytes. J Immunol 1998;160(3):1354-1358.
120. Tripathi P, Hildeman D. Sensitization of T cells to apoptosis-a role for ROS? Apoptosis 2004;9(5):515-523.
121. Diebold SS. Determination of T-cell fate by dendritic cells. Immunol Cell Biol 2008;86(5):389-397.
122. Krueger A, Fas SC, Baumann S, Krammer PH.Therole of CD95 in the regulation of peripheral T-cell apoptosis. Immunol Rev 2003;193:58-69.
123. Green DR, Droin N, Pinkoski M. Activation-induced cell death in T cells. Immunol Rev 2003;193:70-81.
124. Hildeman DA. Regulation of T-cell apoptosis by reactive oxygen species. Free Radic Biol Med 2004;36(12):1496-1504.
125. Li-Weber M, Krammer PH. The death of a T-cell: expression of the CD95 ligand. Cell Death Differ 2002;9(2):101-103.
126. Bauer MK, VogtM, Los M, et al. Role of reactive oxygen intermediates in activation-induced CD95 (APO-1/Fas) ligand expression. J Biol Chem 1998;273(14):8048-8055.
127. Li-Weber M, Weigand MA, Giaisi M, et al. Vitamin E inhibits CD95 ligand expression and protects T cells from activation-induced cell death. J Clin Invest 2002;110(5):681-690.
128. Zhang N, Hartig H, Dzhagalov I, et al.The role of apoptosis in the development and function of T lymphocytes. Cell Res 2005;15(10):749-769.
129. Martinou JC, Youle RJ. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 2011;21(1):92-101.
130. KroemerG,Galluzzi L, BrennerC.Mitochondrialmembrane permeabilization in cell death. Physiol Rev 2007;87(1):99-163.
131. Ott M, Robertson JD, Gogvadze V, et al. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 2002;99(3):1259-1263.
132. Cheng EH, Wei MC, Weiler S, et al. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX-and BAK-mediated mitochondrial apoptosis.Mol Cell 2001;8(3):705-711.
133. Hildeman DA, Zhu Y, Mitchell TC, et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 familymember bim. Immunity 2002;16(6):759-767.
134. Orrenius S, Gogvadze V, Zhivotovsky B.Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 2007;47:143-83.
135. Vene R, Delfino L, Castellani P, et al. Redox remodeling allows and controls B-cell activation and differentiation. Antioxid Redox Signal 2010;13(8):1145-1155.
136. Bertolotti M, Yim SH, Garcia-Manteiga JM, et al. B-to plasma-cell terminal differentiation entails oxidative stress and profound reshaping of the antioxidant responses. Antioxid Redox Signal 2010;13(8):1133-1144.
137. Yang Y, Karakhanova S, Soltek S, et al. In vivo immunoregulatory properties of the novel mitochondria-targeted antioxidant SkQ1.Mol Immunol 2012;52(1):19-29.
138. Wentworth AD, Jones LH, Wentworth P, Jr., et al. Antibodies have the intrinsic capacity to destroy antigens. Proc Natl Acad Sci USA 2000;97(20):10930-10935.
139. Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997;272(33):20313-20316.
140. Sheikh Z, Ahmad R, Sheikh N, Ali R. Enhanced recognition of reactive oxygen species damaged human serum albumin by circulating systemic lupus erythematosus autoantibodies. Autoimmunity 2007;40(7):512-520.
141. Chiang CL, Ledermann JA,Aitkens E, et al.Oxidation of ovarian epithelial cancer cells byhypochlorous acid enhances immunogenicity and stimulates T cells that recognize autologous primary tumor. Clin Cancer Res 2008;14(15):4898-4907.
142. Weiskopf D, Schwanninger A, Weinberger B, et al. Oxidative stress can alter the antigenicity of immunodominant peptides. J Leukoc Biol 2010;87(1):165-172.
143. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008;8(7):523-532.
144. Efimova O, Szankasi P, Kelley TW. Ncf1 (p47phox) is essential for direct regulatory T cellmediated suppression of CD4+ effector T cells. PLoS One 2011;6(1):e16013.
145. Lahdenpohja N,HurmeM.Naive (CD45RA+) T lymphocytes are more sensitive to oxidative stressinduced signals than memory (CD45RO+) cells. Cell Immunol 1996;173(2):282-286.
146. Takahashi A, Hanson MG, Norell HR, et al. Preferential cell death of CD8 +effector memory (CCR7-CD45RA-) T cells by hydrogen peroxide-induced oxidative stress. J Immunol 2005;174(10):6080-6087.
147. Gupta S, Young T, Yel L, et al. Differential sensitivity of naive and subsets of memory CD4+ and CD8+ T cells to hydrogen peroxide-induced apoptosis. Genes Immun 2007;8(7):560-569.
148. Mougiakakos D, Johansson CC, Kiessling R. Naturally occurring regulatory T cells show reduced sensitivity toward oxidative stress-induced cell death. Blood 2009;113(15):3542-3545.
149. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9(3):162-174.
150. Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008;27(45):5904-5912.
151. Condamine T, Gabrilovich DI.Molecular mechanisms regulatingmyeloid- derived suppressor cell differentiation and function. Trends Immunol 2011;32(1):19-25.
152. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12(4):253-268.
153. Cheng P, Corzo CA, Luetteke N, et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med 2008;205(10):2235-2249.
154. Gorlin RJ, Koutlas IG. Multiple schwannomas, multiple nevi, and multiple vaginal leiomyomas: a new dominant syndrome. Am JMed Genet 1998;78(1):76-81.
155. JiaW, Jackson-Cook C, Graf MR. Tumor-infiltrating,myeloid-derived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma + vaccination model. J Neuroimmunol 2010;223(1-2):20-30.
156. Harari O, Liao JK. Inhibition of MHC II gene transcription by nitric oxide and antioxidants. Curr PharmDes 2004;10(8):893-898.
157. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol 2004;172(2):989-999.
158. Nagaraj S, Gupta K, Pisarev V, et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. NatMed 2007;13(7):828-835.
159. Kraaij MD, Savage ND, van der Kooij SW, et al. Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc Natl Acad Sci USA 2010;107(41):17686-17691.
160. Centuori SM, Trad M, Lacasse CJ, et al.Myeloid-derived suppressor cells from tumor-bearingmice impair TGF-beta-induced differentiation of CD4+CD25+FoxP3+Tregs fromCD4+CD25-FoxP3-T cells. J Leukoc Biol 2012;92(5):987-997.