Superoxide production by macrophages and T cells is critical for the induction of autoreactivity and type 1 diabetes

Diabetes

Volumn 60, Issue 8, 2011, Pages 2144-2151

  Thayer, Terri C ^a,b   Delano, Matthew ^a   Liu, Chao ^a   Chen, Jing ^a   Padgett, Lindsey E ^c   Tse, Hubert M ^c   Annamali, Mani ^a   Piganelli, Jon D ^b   Moldawer, Lyle L ^a   Mathews, Clayton E ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANZYME B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME ACTIVITY; FEMALE; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN-PRESENTING CELLS; AUTOIMMUNITY; DIABETES MELLITUS, TYPE 1; FEMALE; MACROPHAGES; MICE; MICE, INBRED NOD; MICE, SCID; NADH, NADPH OXIDOREDUCTASES; NEUTROPHILS; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

EID: 80052841135     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-1222     Document Type: Article

References (49)

1. Bouma G, Coppens JM, Mourits S, et al. Evidence for an enhanced adhesion of DC to fibronectin and a role of CCL19 and CCL21 in the accumulation of DC around the pre-diabetic islets in NOD mice. Eur J Immunol 2005;35:2386-2396
2. Delovitch TL, Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 1997;7:727-738
3. Chen J, Gusdon AM, Thayer TC, Mathews CE. Role of increased ROS dissipation in prevention of T1D. Ann N Y Acad Sci 2008;1150:157-166
4. Griffiths HR. ROS as signalling molecules in T cells - evidence for abnormal redox signalling in the autoimmune disease, rheumatoid arthritis. Redox Rep 2005;10:273-280
5. Nauseef WM. Biological roles for the NOX family NADPH oxidases. J Biol Chem 2008;283:16961-16965
6. Rossi F, Zatti M. Biochemical aspects of phagocytosis in polymorphonuclear leucocytes. NADH and NADPH oxidation by the granules of resting and phagocytizing cells. Experientia 1964;20:21-23
7. Vignais PV. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 2002;59:1428-1459
8. Bäckdahl L, Guo JP, Jagodic M, et al. Definition of arthritis candidate risk genes by combining rat linkage-mapping results with human case-control association data. Ann Rheum Dis 2009;68:1925-1932
9. Hultqvist M, Olofsson P, Holmberg J, Bäckström BT, Tordsson J, 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 2004;101:12646-12651
10. Hultqvist M, Holmdahl R. Ncf1 (p47phox) polymorphism determines oxidative burst and the severity of arthritis in rats and mice. Cell Immunol 2005;233:97-101
11. Olofsson P, Holmdahl R. Positional cloning of Ncf1 - a piece in the puzzle of arthritis genetics. Scand J Immunol 2003;58:155-164
12. Olofsson P, Holmberg J, Tordsson J, Lu S, Akerström B, Holmdahl R. Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat Genet 2003;33:25-32
13. Babior BM, Kipnes RS, Curnutte JT. Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 1973;52:741-744
14. Lander HM, Milbank AJ, Tauras JM, et al. Redox regulation of cell signalling. Nature 1996;381:380-381
15. Sklavos MM, Tse HM, Piganelli JD. Redox modulation inhibits CD8 T cell effector function. Free Radic Biol Med 2008;45:1477-1486
16. Tse HM, Milton MJ, Schreiner S, Profozich JL, Trucco M, Piganelli JD. Disruption of innate-mediated proinflammatory cytokine and reactive oxygen species third signal leads to antigen-specific hyporesponsiveness. J Immunol 2007;178:908-917
17. Kwon J, Shatynski KE, Chen H, et al. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci Signal 2010;3:ra59
18. Laniewski NG, Grayson JM. Antioxidant treatment reduces expansion and contraction of antigen-specific CD8+ T cells during primary but not secondary viral infection. J Virol 2004;78:11246-11257
19. Tse HM, Thayer TC, Steele C, et al. NADPH oxidase deficiency regulates Th lineage commitment and modulates autoimmunity. J Immunol 2010;185:5247-5258
20. Mathews CE, Dunn BD, Hannigan MO, Huang CK, Leiter EH. Genetic control of neutrophil superoxide production in diabetes-resistant ALR/Lt mice. Free Radic Biol Med 2002;32:744-751
21. Ablamunits V, Elias D, Cohen IR. The pathogenicity of islet-infiltrating lymphocytes in the non-obese diabetic (NOD) mouse. Clin Exp Immunol 1999;115:260-267
22. Mathews CE, Graser RT, Savinov A, Serreze DV, Leiter EH. Unusual resistance of ALR/Lt mouse beta cells to autoimmune destruction: role for beta cell-expressed resistance determinants. Proc Natl Acad Sci USA 2001;98:235-240
23. Mathews CE, Suarez-Pinzon WL, Baust JJ, Strynadka K, Leiter EH, Rabinovitch A. Mechanisms underlying resistance of pancreatic islets from ALR/Lt mice to cytokine-induced destruction. J Immunol 2005;175:1248-1256
24. Walker JM. Molecular diagnosis of genetic diseases. In Methods in Molecular Medicine, Elles E, Ed. Totowa, NJ, Humana Press, 1996.
25. Christianson SW, Shultz LD, Leiter EH. Adoptive transfer of diabetes into immunodeficient NOD-scid/scid mice. Relative contributions of CD4+ and CD8+ T-cells from diabetic versus prediabetic NOD.NON-Thy-1a donors. Diabetes 1993;42:44-55
26. Piganelli JD, Flores SC, Cruz C, et al. A metalloporphyrin-based superoxide dismutase mimic inhibits adoptive transfer of autoimmune diabetes by a diabetogenic T-cell clone. Diabetes 2002;51:347-355
27. Tse HM, Josephy SI, Chan ED, Fouts D, Cooper AM. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages. J Immunol 2002;168:825-833
28. Huang CK, Zhan L, Hannigan MO, Ai Y, Leto TL. P47(phox)-deficient NADPH oxidase defect in neutrophils of diabetic mouse strains, C57BL/6J-m db/db and db/+. J Leukoc Biol 2000;67:210-215
29. Morgan D, Oliveira-Emilio HR, Keane D, et al. Glucose, palmitate and proinflammatory cytokines modulate production and activity of a phagocyte-like NADPH oxidase in rat pancreatic islets and a clonal beta cell line. Diabetologia 2007;50:359-369
30. Newsholme P, Morgan D, Rebelato E, et al. Insights into the critical role of NADPH oxidase(s) in the normal and dysregulated pancreatic beta cell. Diabetologia 2009;52:2489-2498
31. Oliveira HR, Verlengia R, Carvalho CR, Britto LR, Curi R, Carpinelli AR. Pancreatic beta-cells express phagocyte-like NAD(P)H oxidase. Diabetes 2003;52:1457-1463
32. Lee KU, Amano K, Yoon JW. Evidence for initial involvement of macrophage in development of insulitis in NOD mice. Diabetes 1988;37:989-991
33. Lee KU, Kim MK, Amano K, et al. Preferential infiltration of macrophages during early stages of insulitis in diabetes-prone BB rats. Diabetes 1988;37:1053-1058
34. Lee KU, Pak CY, Amano K, Yoon JW. Prevention of lymphocytic thyroiditis and insulitis in diabetes-prone BB rats by the depletion of macrophages. Diabetologia 1988;31:400-402
35. Oschilewski U, Kiesel U, Kolb H. Administration of silica prevents diabetes in BB-rats. Diabetes 1985;34:197-199
36. Calderon B, Suri A, Unanue ER. In CD4+ T-cell-induced diabetes, macrophages are the final effector cells that mediate islet beta-cell killing: studies from an acute model. Am J Pathol 2006;169:2137-2147
37. Jun HS, Yoon CS, Zbytnuik L, van Rooijen N, Yoon JW. The role of macrophages in T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Exp Med 1999;189:347-358
38. Cantor J, Haskins K. Recruitment and activation of macrophages by pathogenic CD4 T cells in type 1 diabetes: evidence for involvement of CCR8 and CCL1. J Immunol 2007;179:5760-5767
39. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 2008;83:64-70
40. Jackson SH, Devadas S, Kwon J, Pinto LA, Williams MS. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 2004;5:818-827
41. Mathews CE, Leiter EH. Constitutive differences in antioxidant defense status distinguish alloxan-resistant and alloxan-susceptible mice. Free Radic Biol Med 1999;27:449-455
42. Mathews CE, Graser RT, Bagley RJ, et al. Genetic analysis of resistance to Type-1 Diabetes in ALR/Lt mice, a NOD-related strain with defenses against autoimmune-mediated diabetogenic stress. Immunogenetics 2003;55:491-496
43. DiLorenzo TP, Lieberman SM, Takaki T, et al. During the early prediabetic period in NOD mice, the pathogenic CD8(+) T-cell population comprises multiple antigenic specificities. Clin Immunol 2002;105:332-341
44. Graser RT, DiLorenzo TP, Wang F, et al. Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J Immunol 2000;164:3913-3918
45. Gloire G, Piette J. Redox regulation of nuclear post-translational modifications during NF-kappaB activation. Antioxid Redox Signal 2009;11:2209-2222
46. Oliveira-Marques V, Marinho HS, Cyrne L, Antunes F. Role of hydrogen peroxide in NF-kappaB activation: from inducer to modulator. Antioxid Redox Signal 2009;11:2223-2243
47. Sun Y, Oberley LW. Redox regulation of transcriptional activators. Free Radic Biol Med 1996;21:335-348
48. Donaldson M, Antignani A, Milner J, et al. p47phox-deficient immune microenvironment signals dysregulate naive T-cell apoptosis. Cell Death Differ 2009;16:125-138
49. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 2001;11:173-186