NADPH oxidase-derived superoxide provides a third signal for CD4 T cell effector responses

Journal of Immunology

Volumn 197, Issue 5, 2016, Pages 1733-1742

  Padgett, Lindsey E ^a   Tse, Hubert M ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; CYTOKINE; NEUTROPHIL CYTOSOLIC FACTOR 1; REACTIVE OXYGEN METABOLITE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; TH1 CELL; ANIMAL; DENDRITIC CELL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; METABOLISM; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; IMMUNITY, INNATE; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; MICE; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RECEPTORS, INTERLEUKIN-12; SIGNAL TRANSDUCTION; SUPEROXIDES; TH1 CELLS;

EID: 84983735850     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502581     Document Type: Article

References (38)

1. Lam, G. Y., J. Huang, and J. H. Brumell. 2010. The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin. Immunopathol. 32: 415-430.
2. Tse, H. M., M. J. Milton, and J. D. Piganelli. 2004. Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Radic. Biol. Med. 36: 233-247.
3. Tse, H. M., M. J. Milton, S. Schreiner, J. L. Profozich, M. Trucco, and J. D. Piganelli. 2007. Disruption of innate-mediated proinflammatory cytokine and reactive oxygen species third signal leads to antigen-specific hyporesponsiveness. J. Immunol. 178: 908-917.
4. Padgett, L. E., K. A. Broniowska, P. A. Hansen, J. A. Corbett, and H. M. Tse. 2013. The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann. N. Y. Acad. Sci. 1281: 16-35.
5. Sklavos, M. M., H. M. Tse, and J. D. Piganelli. 2008. Redox modulation inhibits CD8 T cell effector function. Free Radic. Biol. Med. 45: 1477-1486.
6. Tse, H. M., T. C. Thayer, C. Steele, C. M. Cuda, L. Morel, J. D. Piganelli, and C. E. Mathews. 2010. NADPH oxidase deficiency regulates Th lineage commitment and modulates autoimmunity. J. Immunol. 185: 5247-5258.
7. Khoruts, A., A. Mondino, K. A. Pape, S. L. Reiner, and M. K. Jenkins. 1998. A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL)-2-independent mechanism. J. Exp. Med. 187: 225-236.
8. + T cells. J. Immunol. 159: 591-598.
9. Batinić-Haberle, I., L. Benov, I. Spasojević, and I. Fridovich. 1998. The ortho effect makes manganese(III) meso-tetrakis(N-methylpyridinium-2-yl)porphyrin a powerful and potentially useful superoxide dismutase mimic. J. Biol. Chem. 273: 24521-24528.
10. Day, B. J., I. Batinic-Haberle, and J. D. Crapo. 1999. Metalloporphyrins are potent inhibitors of lipid peroxidation. Free Radic. Biol. Med. 26: 730-736.
11. Day, B. J., I. Fridovich, and J. D. Crapo. 1997. Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxidemediated injury. Arch. Biochem. Biophys. 347: 256-262.
12. Day, B. J., S. Shawen, S. I. Liochev, and J. D. Crapo. 1995. A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced endothelial cell injury, in vitro. J. Pharmacol. Exp. Ther. 275: 1227-1232.
13. Piganelli, J. D., S. C. Flores, C. Cruz, J. Koepp, I. Batinic-Haberle, J. Crapo, B. Day, R. Kachadourian, R. Young, B. Bradley, and K. Haskins. 2002. A metalloporphyrin-based superoxide dismutase mimic inhibits adoptive transfer of autoimmune diabetes by a diabetogenic T-cell clone. Diabetes 51: 347-355.
14. Delmastro, M. M., A. J. Styche, M. M. Trucco, C. J. Workman, D. A. Vignali, and J. D. Piganelli. 2012. Modulation of redox balance leaves murine diabetogenic TH1 T cells LAG-3-ing behind. Diabetes 61: 1760-1768.
15. Thayer, T. C., M. Delano, C. Liu, J. Chen, L. E. Padgett, H. M. Tse, M. Annamali, J. D. Piganelli, L. L. Moldawer, and C. E. Mathews. 2011. Superoxide production by macrophages and T cells is critical for the induction of autoreactivity and type 1 diabetes. Diabetes 60: 2144-2151.
16. Delmastro-Greenwood, M. M., H. M. Tse, and J. D. Piganelli. 2014. Effects of metalloporphyrins on reducing inflammation and autoimmunity. Antioxid. Redox Signal. 20: 2465-2477.
17. Barnden, M. J., J. Allison, W. R. Heath, and F. R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha-and betachain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76: 34-40.
18. Huang, C. K., L. Zhan, M. O. Hannigan, Y. Ai, and T. L. Leto. 2000. P47(phox)-deficient NADPH oxidase defect in neutrophils of diabetic mouse strains, C57BL/6J-m db/db and db/+. J. Leukoc. Biol. 67: 210-215.
19. Cheng, G., J. C. Salerno, Z. Cao, P. J. Pagano, and J. D. Lambeth. 2008. Identification and characterization of VPO1, a new animal heme-containing peroxidase. Free Radic. Biol. Med. 45: 1682-1694.
20. Dahlgren, C., P. Follin, A. Johansson, R. Lock, and K. Orselius. 1989. Localization of the luminol-dependent chemiluminescence reaction in human granulocytes. J. Biolumin. Chemilumin. 4: 263-266.
21. Seleme, M. C., W. Lei, A. R. Burg, K. Y. Goh, A. Metz, C. Steele, and H. M. Tse. 2012. Dysregulated TLR3-dependent signaling and innate immune activation in superoxide-deficient macrophages from nonobese diabetic mice. Free Radic. Biol. Med. 52: 2047-2056.
22. Lokesh, B. R., and M. L. Cunningham. 1986. Further studies on the formation of oxygen radicals by potassium superoxide in aqueous medium for biochemical investigations. Toxicol. Lett. 34: 75-84.
23. Ishiyama, M., Y. Miyazono, K. Sasamoto, Y. Ohkura, and K. Ueno. 1997. A highly water-soluble disulfonated tetrazolium salt as a chromogenic indicator for NADH as well as cell viability. Talanta 44: 1299-1305.
24. Padgett, L. E., A. R. Burg, W. Lei, and H. M. Tse. 2014. Loss of NADPH oxidase-derived superoxide skews macrophage phenotypes to delay type 1 diabetes. Diabetes 64: 937-946.
25. Johansson, A., and C. Dahlgren. 1989. Characterization of the luminol-amplified lightgenerating reaction induced in human monocytes. J. Leukoc. Biol. 45: 444-451.
26. Jackson, S. H., S. Devadas, J. Kwon, L. A. Pinto, and M. S. Williams. 2004. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 5: 818-827.
27. Athie-Morales, V., H. H. Smits, D. A. Cantrell, and C. M. Hilkens. 2004. Sustained IL-12 signaling is required for Th1 development. J. Immunol. 172: 61-69.
28. Suzuki, Y. J., H. J. Forman, and A. Sevanian. 1997. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 22: 269-285.
29. Katz, J. D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulindependent diabetes. Science 268: 1185-1188.
30. Rabinovitch, A. 1994. Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM. Therapeutic intervention by immunostimulation? Diabetes 43: 613-621.
31. von Herrath, M. G., and M. B. Oldstone. 1997. Interferon-gamma is essential for destruction of beta cells and development of insulin-dependent diabetes mellitus. J. Exp. Med. 185: 531-539.
32. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
33. Ghoreschi, K., C. Weigert, and M. Röcken. 2007. Immunopathogenesis and role of T cells in psoriasis. Clin. Dermatol. 25: 574-580.
34. Curtsinger, J. M., J. O. Valenzuela, P. Agarwal, D. Lins, and M. F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174: 4465-4469.
35. Curtsinger, J. M., C. M. Johnson, and M. F. Mescher. 2003. CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J. Immunol. 171: 5165-5171.
36. Gelderman, K. A., M. Hultqvist, J. Holmberg, P. Olofsson, and R. Holmdahl. 2006. T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc. Natl. Acad. Sci. USA 103: 12831-12836.
37. Richter, C., M. H. Juan, J. Will, R. P. Brandes, U. Kalinke, S. Akira, J. M. Pfeilschifter, M. Hultqvist, R. Holmdahl, and H. H. Radeke. 2009. Ncf1 provides a reactive oxygen species-independent negative feedback regulation of TLR9-induced IL-12p70 in murine dendritic cells. J. Immunol. 182: 4183-4191.
38. Takeshita, F., K. J. Ishii, K. Kobiyama, Y. Kojima, C. Coban, S. Sasaki, N. Ishii, D. M. Klinman, K. Okuda, S. Akira, and K. Suzuki. 2005. TRAF4 acts as a silencer in TLR-mediated signaling through the association with TRAF6 and TRIF. Eur. J. Immunol. 35: 2477-2485.