Hydrogen peroxide as an immunological transmitter regulating autoreactive T cells

Antioxidants and Redox Signaling

Volumn 18, Issue 12, 2013, Pages 1463-1474

  Holmdahl, Rikard ^a,b   Sareila, Outi ^b   Pizzolla, Angela ^a   Winter, Susann ^a   Hagert, Cecilia ^b   Jaakkola, Noora ^b   Kelkka, Tiina ^a,b   Olsson, Lina M ^a   Wing, Kajsa ^a   Bäckdahl, Liselotte ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BIOSYNTHESIS; CELL INTERACTION; CELL SELECTION; CELLULAR IMMUNITY; DOWN REGULATION; ENZYME ACTIVITY; GENETIC POLYMORPHISM; HUMAN; INFLAMMATION; INFLAMMATORY CELL; LYMPHOCYTE FUNCTION; MACROPHAGE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY BURST; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; ARTHRITIS, RHEUMATOID; HUMANS; HYDROGEN PEROXIDE; IMMUNOLOGIC FACTORS; LYMPHOID TISSUE; MACROPHAGES; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84875195550     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4734     Document Type: Review

References (91)

1. Angelini G, Gardella S, Ardy M, Ciriolo MR, Filomeni G, Di Trapani G, Clarke F, Sitia R, and Rubartelli A. Antigenpresenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc Natl Acad Sci USA 99: 1491-1496, 2002..
2. Arechiga AF, Habib T, He Y, Zhang X, Zhang Z-Y, Funk A, and Buckner JH. Cutting edge: The PTPN22 allelic variant associated with autoimmunity impairs B cell signaling. J Immunol 182: 3343-3347, 2009..
3. Auffray C, Sieweke MH, and Geissmann F. Blood monocytes: Development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol 27: 669-692, 2009..
4. Bayes M, Magano LF, Rivera N, Flores R, and Perez Jurado LA. Mutational mechanisms of Williams-Beuren syndrome deletions. Am J Hum Genet 73: 131-151, 2003..
5. Bedard K and Krause K-H. The NOX family of ROSgenerating NADPH oxidases: Physiology and pathophysiology. Physiol Rev 87: 245-313, 2008..
6. Begovich AB, Carlton VEH, Honigberg LA, Schrodi SJ, Chokkalingam AP, Alexander HC, Ardlie KG, Huang Q, Smith AM, Spoerke JM, Conn MT, Chang M, Chang SY, Saiki RK, Catanese JJ, Leong DU, Garcia VE, McAllister LB, Jeffery DA, Lee AT, Batliwalla F, Remmers E, Criswell LA, Seldin MF, Kastner DL, Amos CI, Sninsky JJ, and Gregersen PK. A missense single-nucleotide polymorphism in a gene encoding a protein tyrosine phosphatase (PTPN22) is associated with rheumatoid arthritis. Am J Hum Genet 75: 330-337, 2004..
7. Betten A, Bylund J, Christophe T, Cristophe T, Boulay F, Romero A, Hellstrand K, and Dahlgren C. A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis. J Clin Invest 108: 1221-1228, 2001..
8. Bridges RA, Berendes H, and Good RA. A fatal granulomatous disease of childhood; The clinical, pathological, and laboratory features of a new syndrome. AMA J Dis Child 97: 387-408, 1959..
9. Cale CM, Morton L, and Goldblatt D. Cutaneous and other lupus-like symptoms in carriers of X-linked chronic granulomatous disease: Incidence and autoimmune serology. Clin Exp Immunol 148: 79-84, 2007..
10. Castellani P, Angelini G, Delfino L, Matucci A, and Rubartelli A. The thiol redox state of lymphoid organs is modified by immunization: Role of different immune cell populations. Eur J Immunol 38: 2419-2425, 2008..
11. Chen K, Craige SE, and Keaney JF. Downstream targets and intracellular compartmentalization in Nox signaling. Antioxid Redox Signal 11: 2467-2480, 2009..
12. Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, Padhya T, McCaffrey TV, McCaffrey JC, and Gabrilovich DI. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182: 5693-5701, 2009..
13. Cunninghame Graham DS, Morris DL, Bhangale TR, Criswell LA, Syvanen A-C, Ronnblom L, Behrens TW, Graham RR, and Vyse TJ. Association of NCF2, IKZF1, IRF8, IFIH1, and TYK2 with systemic lupus erythematosus. PLoS Genet 7: e1002341, 2011..
14. De Ravin SS, Naumann N, Cowen EW, Friend J, Hilligoss D, Marquesen M, Balow JE, Barron KS, Turner ML, Gallin JI, and Malech HL. Chronic granulomatous disease as a risk factor for autoimmune disease. J Allergy Clin Immunol 122: 1097-1103, 2008..
15. Devadas S, Zaritskaya L, Rhee SG, Oberley L, and Williams MS. 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 Exp Med 195: 59-70, 2002..
16. Ellson C, Davidson K, Anderson K, Stephens LR, and Hawkins PT. PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation. EMBO J 25: 4468-4478, 2006..
17. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, Ortmann W, Kosoy R, Ferreira RC, Nordmark G, Gunnarson I, Svenungsson E, Padyukow LS, Sturfelt G, Jonsen A, Bengtsson AA, Rantapaa-Dahlgvist S, Baechler EC, Brown EE, Alarcon GS, Edberg JC, Ramsey-Goldman R, McGwin G Jr, Reveille JD, Vila LM, Kimberly RP, Manzi S, Petri MA, Lee A, Gregersen PK, Seldin MF, Ronnblom L, Criswell LA, Syvanen AC, Behrens TW, and Graham RR. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41: 1228-1233, 2009..
18. Gelderman KA, Hultqvist M, Holmberg J, Olofsson P, and Holmdahl R. T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Natl Acad Sci USA 103: 12831-12836, 2006..
19. Gelderman KA, Hultqvist M, Pizzolla A, Zhao M, Nandakumar KS, Mattsson R, and Homdahl R. Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J Clin Invest 117: 3020-3028, 2007..
20. Gregersen PK and Olsson LM. Recent advances in the genetics of autoimmune disease. Annu Rev Immunol 27: 363-391, 2009..
21. Gringhuis SI, Leow A, Papendrecht-Van Der Voort EA, Remans PH, Breedveld FC, and Verweij CL. Displacement of linker for activation of T cells from the plasma membrane due to redox balance alterations results in hyporesponsiveness of synovial fluid T lymphocytes in rheumatoid arthritis. J Immunol 164: 2170-2179, 2000..
22. Gringhuis SI, Papendrecht-van der Voort EAM, Leow A, Nivine Levarht EW, Breedveld FC, and Verweij CL. Effect of redox balance alterations on cellular localization of LAT and downstream T-cell receptor signaling pathways. Mol Cell Biol 22: 400-411, 2002..
23. Go rlach A, Lee PL, Roesler J, Hopkins PJ, Christensen B, Green ED, Chanock SJ, and Curnutte JT. A p47-phox pseudogene carries the most common mutation causing p47-phox-deficient chronic granulomatous disease. J Clin Invest 100: 1907-1918, 1997..
24. Hagenow K, Gelderman KA, Hultqvist M, Merky P, Ba cklund J, Frey O, Kamradt T, and Holmdahl R. Ncf1-associated reduced oxidative burst promotes IL-33R + T cell-mediated adjuvant-free arthritis in mice. J Immunol 183: 874-881, 2009..
25. Hansson M, Romero A, Thoren F, Hermodsson S, and Hellstrand K. Activation of cytotoxic lymphocytes by interferon-alpha: Role of oxygen radical-producing mononuclear phagocytes. J Leukoc Biol 76: 1207-1213, 2004..
26. Himoudi N, Morgenstern DA, Yan M, Vernay B, Saraiva L, Wu Y, Cohen CJ, Gustafsson K, and Anderson J. Human cd T lymphocytes are licensed for professional antigen presentation by interaction with opsonized target cells. J Immunol 188: 1708-1716, 2012..
27. Hinterberger M, Aichinger M, Prazeres da Costa O, Voehringer D, Hoffmann R, and Klein L. Autonomous role of medullary thymic epithelial cells in central CD4( + ) T cell tolerance. Nat Immunol 11: 512-519, 2010..
28. Hultqvist M, Backlund J, Bauer K, Gelderman KA, and Holmdahl R. Lack of reactive oxygen species breaks T cell tolerance to collagen type II and allows development of arthritis in mice. J Immunol 179: 1431-1437, 2007..
29. Hultqvist M, Olofsson P, Gelderman KA, Holmberg J, and Holmdahl R. A new arthritis therapy with oxidative burst inducers. PLoS Med 3: e348, 2006..
30. Hultqvist M, Olofsson P, Holmberg J, Ba ckstrom BT, Tordsson J, and Holmdahl R. 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, 2004..
31. Hultqvist M, Sareila O, Vilhardt F, Norin U, Olsson LM, Olofsson P, Hellman U, and Holmdahl R. Positioning of a polymorphic quantitative trait nucleotide in the Ncf1 gene controlling oxidative burst response and arthritis severity in rats. Antioxid Redox Signal 14: 2373-2383, 2011..
32. Huang Z, Rose AH, and Hoffmann PR. The role of selenium in inflammation and immunity: From molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16: 705-743, 2012..
33. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, Ermolaeva M, Veldhuizen R, Leung YH, Wang H, Liu H, Sun Y, Pasparakis M, Kopf M, Mech C, Bavari S, Peiris JS, Slutsky AS, Akira S, Hultqvist M, Holmdahl R, Nicholls J, Jiang C, Binder CJ, Penninger JM. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249, 2008..
34. International Multiple Sclerosis Genetics Consortium; Wellcome Trust Case Control Consortium 2, Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, Freeman C, Hunt SE, Edkins S, Gray E, Booth DR, Potter SC, Goris A, Band G, Oturai AB, Strange A, Saarela J, Bellenguez C, Fontaine B, Gillman M, Hemmer B, Gwilliam R, Zipp F, Jayakumar A, Martin R, Leslie S, Hawkins S, Giannoulatou E, D'alfonso S, Blackburn H, Martinelli Boneschi F, Liddle J, Harbo HF, Perez ML, Spurkland A, Waller MJ, Mycko MP, Ricketts M, Comabella M, Hammond N, Kockum I, McCann OT, Ban M, Whittaker P, Kemppinen A, Weston P, Hawkins C, Widaa S, Zajicek J, Dronov S, Robertson N, Bumpstead SJ, Barcellos LF, Ravindrarajah R, Abraham R, Alfredsson L, Ardlie K, Aubin C, Baker A, Baker K, Baranzini SE, Bergamaschi L, Bergamaschi R, Bernstein A, Berthele A, Boggild M, Bradfield JP, Brassat D, Broadley SA, Buck D, Butzkueven H, Capra R, Carroll WM, Cavalla P, Celius EG, Cepok S, Chiavacci R, Clerget-Darpoux F, Clysters K, Comi G, Cossburn M, Cournu-Rebeix I, Cox MB, Cozen W, Cree BA, Cross AH, Cusi D, Daly MJ, Davis E, de Bakker PI, Debouverie M, D'hooghe MB, Dixon K, Dobosi R, Dubois B, Ellinghaus D, Elovaara I, Esposito F, Fontenille C, Foote S, Franke A, Galimberti D, Ghezzi A, Glessner J, Gomez R, Gout O, Graham C, Grant SF, Guerini FR, Hakonarson H, Hall P, Hamsten A, Hartung HP, Heard RN, Heath S, Hobart J, Hoshi M, Infante-Duarte C, Ingram G, Ingram W, Islam T, Jagodic M, Kabesch M, Kermode AG, Kilpatrick TJ, Kim C, Klopp N, Koivisto K, Larsson M, Lathrop M, Lechner-Scott JS, Leone MA, Leppa V, Liljedahl U, Bomfim IL, Lincoln RR, Link J, Liu J, Lorentzen AR, Lupoli S, Macciardi F, Mack T, Marriott M, Martinelli V, Mason D, McCauley JL, Mentch F, Mero IL, Mihalova T, Montalban X, Mottershead J, Myhr KM, Naldi P, Ollier W, Page A, Palotie A, Pelletier J, Piccio L, Pickersgill T, Piehl F, Pobywajlo S, Quach HL, Ramsay PP, Reunanen M, Reynolds R, Rioux JD, Rodegher M, Roesner S, Rubio JP, Ru ckert IM, Salvetti M, Salvi E, Santaniello A, Schaefer CA, Schreiber S, Schulze C, Scott RJ, Sellebjerg F, Selmaj KW, Sexton D, Shen L, Simms-Acuna B, Skidmore S, Sleiman PM, Smestad C, Sørensen PS, Søndergaard HB, Stankovich J, Strange RC, Sulonen AM, Sundqvist E, Syvanen AC, Taddeo F, Taylor B, Blackwell JM, Tienari P, Bramon E, Tourbah A, Brown MA, Tronczynska E, Casas JP, Tubridy N, Corvin A, Vickery J, Jankowski J, Villoslada P, Markus HS, Wang K, Mathew CG, Wason J, Palmer CN, Wichmann HE, Plomin R, Willoughby E, Rautanen A, Winkelmann J, Wittig M, Trembath RC, Yaouanq J, Viswanathan AC, Zhang H, Wood NW, Zuvich R, Deloukas P, Langford C, Duncanson A, Oksenberg JR, Pericak-Vance MA, Haines JL, Olsson T, Hillert J, Ivinson AJ, De Jager PL, Peltonen L, Stewart GJ, Hafler DA, Hauser SL, McVean G, Donnelly P, and Compston A. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476: 214-219, 2011
35. Jackson SH, Devadas S, Kwon J, Pinto LA, and Williams MS. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 5: 818-827, 2004..
36. Jackson SH, Gallin JI, and Holland SM. The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med 182: 751-758, 1995..
37. Jacob CO, Eisenstein M, Dinauer MC, Ming W, Liu Q, John S, Quismorio FP Jr, Myones BL, Kaufman KM, McCurdy D, Harley JB, Silverman E, Kimberly RP, Vyse TJ, Gaffney PM, Moser KL, Klein-Gitelman M, Wagner-Weiner L, Langefeld CD, Armstrong DL, and Zidovetzki R. Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase. Proc Natl Acad Sci USA 109: 59-67, 2011..
38. Jendrysik MA, Vasilevsky S, Yi L, Wood A, Zhu N, Zhao Y, Koontz SM, and Jackson SH. NADPH oxidase-2 derived ROS dictates murine DC cytokine-mediated cell fate decisions during CD4 T helper-cell commitment. PLoS ONE 6: e28198, 2011..
39. Kang EM, Marciano BE, DeRavin S, Zarember KA, Holland SM, and Malech HL. Chronic granulomatous disease: Overview and hematopoietic stem cell transplantation. J Allergy Clin Immunol 127: 1319-1326, 2011.
40. Kielland A, Blom T, Nandakumar KS, Holmdahl R, Blomhoff R, and Carlsen H. In vivo imaging of reactive oxygen and nitrogen species in inflammation using the luminescent probe L-012. Free Radic Biol Med Elsevier Inc 47: 760-766, 2009..
41. Kraaij MD, Savage NDL, van der Kooij SW, Koekkoek K, Wang J, van den Berg JM, Ottenhoff TH, Kuijpers TW, Holmdahl R, van Kooten C, and Gelderman KA. Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc Natl Acad Sci USA 107: 17686-17691, 2010..
42. Kraaij MD, van der Kooij SW, Reinders MEJ, Koekkoek K, Rabelink TJ, van Kooten C, and Gelderman KA. Dexamethasone increases ROS production and T cell suppressive capacity by anti-inflammatory macrophages. Mol Immunol 49: 549-557, 2011..
43. Kwon J, Devadas S, and Williams MS. T cell receptorstimulated generation of hydrogen peroxide inhibits MEKERK activation and lck serine phosphorylation. Free Radic Biol Med 35: 406-417, 2003..
44. Kwon J, Shatynski KE, Chen H, Morand S, de Deken X, Miot F, Leto TL, and Williams MS. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Science Signal 3: ra59, 2010..
45. Lee K, Won HY, Bae MA, Hong J-H, and Hwang ES. Spontaneous and aging-dependent development of arthritis in NADPH oxidase 2 deficiency through altered differentiation of CD11b + and Th/Treg cells. Proc Natl Acad Sci USA 108: 9548-9553, 2011..
46. Lillemeier BF, Mo rtelmaier MA, Forstner MB, Huppa JB, Groves JT, and Davis MM. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 11: 90-96, 2010..
47. Mantegazza AR, Savina A, Vermeulen M, Perez L, Geffner J, Hermine O, Rosenzweig SD, Faure F, and Amigorena S. NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 112: 4712-4722, 2008..
48. Martinez FO, Helming L, and Gordon S. Alternative activation of macrophages: An immunologic functional perspective. Annu Rev Immunol 27: 451-483, 2009..
49. Martner A, Aurelius J, Rydstrom A, Hellstrand K, and Thoren FB. Redox remodeling by dendritic cells protects antigen-specific T cells against oxidative stress. J Immunol 187: 6243-6248, 2011..
50. Mattsson R, Mattsson A, Holmdahl R, Whyte A, and Rook GA. Maintained pregnancy levels of oestrogen afford complete protection from post-partum exacerbation of collageninduced arthritis. Clin Exp Immunol 85: 41-47, 1991..
51. Matute JD, Arias AA, Wright NAM, Wrobel I, Waterhouse CCM, Li XJ, Marchal CC, Stull ND, LewisDB, Steele M, Kellner JD, Yu W, Meroueh SO, Nauseef WM, and Dinauer MC. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40phox and selective defects in neutrophil NADPH oxidase activity. Blood 114: 3309-3315, 2009..
52. Moon E-Y, Han YH, Lee D-S, Han Y-M, and Yu D-Y. Reactive oxygen species induced by the deletion of peroxiredoxin II (PrxII) increases the number of thymocytes resulting in the enlargement of PrxII-null thymus. Eur J Immunol 34: 2119-2128, 2004..
53. Muise AM, Xu W, Guo C-H, Walters TD, Wolters VM, Fattouh R, Lam GY, Hu P, Murchie R, Sherlock M, Gana JC, NEOPICS, Russel RK, Glogauer M, Duerr RH, Cho JH, Lees CW, Satsangi J, Wilson DC, Paterson AD, Griffiths AM, Silverberg MS, and Brumell JH. NADPH oxidase complex and IBD candidate gene studies: Identification of a rare variant in NCF2 that results in reduced binding to RAC2. Gut 61: 1028-1035, 2011..
54. Olofsson P, Holmberg J, Tordsson J, Lu S, Akerstrom B, and Holmdahl R. Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat Genet 33: 25-32, 2003..
55. Olofsson P, Johansson A, Wedekind D, Klo ting I, Klinga-Levan K, Lu S, and Holmdahl R. Inconsistent susceptibility to autoimmunity in inbred LEW rats is due to genetic crossbreeding involving segregation of the arthritis-regulating gene Ncf1. Genomics 83: 765-771, 2004..
56. Olsson LM, Lindqvist A-K, Ka llberg H, Padyukov L, Burkhardt H, Alfredsson L, Klareskog L, and Holmdahl R. A case-control study of rheumatoid arthritis identifies an associated single nucleotide polymorphism in the NCF4 gene, supporting a role for the NADPH-oxidase complex in autoimmunity. Arthritis Res Ther 9: 98, 2007..
57. Olsson LM, Nerstedt A, Lindqvist A-K, Johansson AC, Medstrand P, Olofsson P, and Holmdahl R. Copy number variation of the gene NCF1 is associated with Rheumatoid Arthritis. Antioxid Redox Signal 16: 71-78, 2011..
58. Pizzolla A, Gelderman KA, Hultqvist M, Vestberg M, Gustafsson K, Mattsson R, and Holmdahl R. CD68-expressing cells can prime T cells and initiate autoimmune arthritis in the absence of reactive oxygen species. Eur J Immunol 41: 403-412, 2011..
59. Pizzolla A, Hultqvist M, Nilson B, Grimm M, Enelung T, Jonsson I, Verdrengh M, Kelkka T, Gjertsson I, Segal BH, and Holmdahl R. Reactive oxygen species produced by the NOX2 complex in monocytes protect mice from bacterial infections. J Immunol 188: 5003-5011, 2012..
60. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 3: 1129-1134, 2002..
61. Rieck M, Arechiga A, Onengut-Gumuscu S, Greenbaum C, Concannon P, and Buckner JH. Genetic variation in PTPN22 corresponds to altered function of T and B lymphocytes. J Immunol 179: 4704-4710, 2007..
62. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A, Green T, Kuballa P, Barmada MM, Datta LW, Shugart YY, Griffiths AM, Targan SR, Ippoliti AF, Bernard EJ, Mei L, Nicolae DL, Regueiro M, Schumm LP, Steinhart AH, Rotter JI, Duerr RH, Cho JH, Daly MJ, and Brant SR. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 39: 596-604, 2007..
63. Roberts RL, Hollis-Moffatt JE, Gearry RB, Kennedy MA, Barclay ML, and Merriman TR. Confirmation of association of IRGM and NCF4 with ileal Crohn's disease in a population-based cohort. Genes Immun 9: 561-565, 2008..
64. Rosenzweig SD. Inflammatory manifestations in chronic granulomatous disease (CGD). J Clin Immunol 1: 67-72, 2008..
65. Rybicka JM, Balce DR, Chaudhuri S, Allan ERO, and Yates RM. Phagosomal proteolysis in dendritic cells is modulated by NADPH oxidase in a pH-independent manner. EMBO J 31: 932-944, 2012..
66. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru S, and Sakaguchi S. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 426: 454-460, 2003..
67. Sakaguchi S, Tanaka S, Tanaka A, Ito Y, Maeda S, Sakaguchi N, and Hashimoto M. Thymus, innate immunity and autoimmune arthritis: Interplay of gene and environment. FEBS Lett 585: 3633-3639, 2011..
68. Salmeen A, Andersen JN, Myers MP, Meng T-C, Hinks JA, Tonks NK, and Barford D. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769-773, 2003..
69. Sareila O, Kelkka T, Pizzolla A, Hultqvist M, and Holmdahl R. NOX2 Complex-derived ROS as Immune Regulators. Antioxid Redox Signal 15: 2197-2208, 2011.
70. Savina A, Jancic C, Hugues S, Guermonprez P, Vargas P, Moura IC, Lennon-Dumenil AM, Seabra MC, Raposo G, and Amigorena S. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126: 205-218, 2006..
71. Schappi M, Deffert C, Fiette L, Gavazzi G, Herrmann F, Belli D, and Krause KH. Branched fungal beta-glucan causes hyperinflammation and necrosis in phagocyte NADPH oxidase-deficient mice. J Pathol 214: 434-444, 2008..
72. Segal BH, Veys P, Malech H, and Cowan MJ. Chronic granulomatous disease: Lessons from a rare disorder. Biol Blood Marrow Transplant 17: 123-131, 2011..
73. Sironi M, Guerini FR, Agliardi C, Biasin M, Cagliani R, Fumagalli M, Caputo D, Cassinotti A, Ardizzone S, Zanzottera M, Bolognesi E, Riva S, Kanari Y, Miyazawa M, and Clerici M. An evolutionary analysis of RAC2 identifies haplotypes associated with human autoimmune diseases. Mol Biol Evol 28: 3319-3329, 2011..
74. Snelgrove RJ, Edwards L, Rae AJ, and Hussell T. An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur J Immunol 36: 1364-1373, 2006..
75. Somasundaram R, Deuring JJ, van der Woude CJ, Peppelenbosch MP, and Fuhler GM. Linking risk conferring mutations in NCF4 to functional consequences in Crohn's disease. Gut 61: 1097, 2011..
76. Suthanthiran M, Anderson ME, Sharma VK, and Meister A. Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lymphocytes stimulated via the CD2 and CD3 antigens. Proc Natl Acad Sci 87: 3343-3377, 1990..
77. Thoren FB, Betten A, Romero AI, and Hellstrand K. Cutting edge: Antioxidative properties of myeloid dendritic cells: protection of T cells and NK cells from oxygen radicalinduced inactivation and apoptosis. J Immunol 179: 21-25, 2007..
78. Thoren F, Romero A, Lindh M, Dahlgren C, and Hellstrand K. A hepatitis C virus-encoded, nonstructural protein (NS3) triggers dysfunction and apoptosis in lymphocytes: Role of NADPH oxidase-derived oxygen radicals. J Leukoc Biol 76: 1180-1186, 2004..
79. Tsai SJ, Sen U, Zhao L, Greenleaf WB, Dasgupta J, Fiorillo E, Orru V, Bottini N, and Chen XS. Crystal structure of the human lymphoid tyrosine phosphatase catalytic domain: Insights into redox regulation. Biochemistry 48: 4838-4845, 2009..
80. Vasilevsky S, Liu Q, Koontz SM, Kastenmayer R, Shea K, and Jackson SH. Role of p47phox in antigen-presenting cellmediated regulation of humoral immunity in mice. Am J Pathol 178: 2774-2782, 2011..
81. Verreck FAW, de Boer T, Langenberg DML, van der Zanden L, and Ottenhoff THM. Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma-and CD40L-mediated costimulation. J Leukoc Biol 79: 285-293, 2006..
82. Vingsbo-Lundberg C, Nordquist N, Olofsson P, Sundvall M, Saxne T, Pettersson U, and Holmdahl R. Genetic control of arthritis onset, severity and chronicity in a model for rheumatoid arthritis in rats. Nat Genet 20: 401-404, 1998..
83. Weiskopf D, Schwanninger A, Weinberger B, Almanzar G, Parson W, Buus S, Lindner H, and Grubeck-Loebenstein B. Oxidative stress can alter the antigenicity of immunodominant peptides. J Leukoc Biol 87: 165-172, 2010..
84. Wiede F, Shields BJ, Chew SH, Kyparissoudis K, van Vliet C, Galic S, Tremblay ML, Russell SM, Godfrey DI, and Tiganis T. T cell protein tyrosine phosphatase attenuates T cell signaling to maintain tolerance in mice. J Clin Invest 121: 4758-4774, 2011..
85. Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549-561, 2008..
86. Won HY, Sohn JH, Min HJ, Lee K, Woo HA, Ho Y-S, Park JW, Rhee SG, and Hwang ES. Glutathione peroxidase 1 deficiency attenuates allergen-induced airway inflammation by suppressing Th2 and Th17 cell development. Antioxid Redox Signal 13: 575-587, 2010..
87. Woo HA, Yim SH, Shin DH, Kang D, Yu D-Y, and Rhee SG. Inactivation of peroxiredoxin I by phosphorylation allows localized H2O2 accumulation for cell signaling. Cell 140: 517-528, 2010..
88. Yan Z and Banerjee R. Redox remodeling as an immunoregulatory strategy. Biochemistry 49: 1059-1066, 2010..
89. Yan Z, Garg SK, and Banerjee R. Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J Biol Chem 285: 41525-41532, 2010..
90. Yan Z, Garg SK, Kipnis J, and Banerjee R. Extracellular redox modulation by regulatory T cells. Nat Chem Biol 5: 721-723, 2009..
91. Zhang J, Zahir N, Jiang Q, Miliotis H, Heyraud S, Meng X, Dong B, Xie G, Qiu F, Hao Z, McCulloch CA, Keystone EC, Peterson AC, and Siminovitch KA.. The autoimmune disease-associated PTPN22 variant promotes calpain-mediated Lyp/Pep degradation associated with lymphocyte and dendritic cell hyperresponsiveness. Nat Genet 43: 902-907, 2011..