NADPH oxidase deficiency regulates Th lineage commitment and modulates autoimmunity

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5247-5258

  Tse, Hubert M ^a,d   Thayer, Terri C ^a,b   Steele, Chad ^c   Cuda, Carla M ^b   Morel, Laurence ^b   Piganelli, Jon D ^a,e   Mathews, Clayton E ^a,b  

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

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

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

^e CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIBODY; CD3 ANTIBODY; CELL ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 23; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; REACTIVE OXYGEN METABOLITE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CELL LINEAGE; CELL MEMBRANE DEPOLARIZATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; FEMALE; HELPER CELL; IMMUNOMODULATION; IN VIVO STUDY; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RESPIRATORY BURST; T LYMPHOCYTE; TH1 CELL; TH17 CELL; VALIDATION STUDY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL SEPARATION; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYMOLOGY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; AUTOIMMUNITY; BLOTTING, WESTERN; CELL LINEAGE; CELL SEPARATION; CYTOKINES; DIABETES MELLITUS, TYPE 1; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; INTERLEUKIN-17; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, TRANSGENIC; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDES; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 78149485627     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001472     Document Type: Article

References (67)

1. Cantor, J., and K. Haskins. 2005. Effector function of diabetogenic CD4 Th1 T cell clones: a central role for TNF-alpha. J. Immunol. 175:7738-7745.
2. Corbett, J. A., M. A. Sweetland, J. L. Wang, J. R. Lancaster, Jr., and M. L. McDaniel. 1993. Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc. Natl. Acad. Sci. USA 90:1731-1735.
3. Gusdon, A. M., J. A. Corbett, and C. E. Mathews. 2006. Type 1 diabetes: islet inflammation-the contribution of cytokines and beta cells. Drug Discov. Today 3:367-372.
4. Mathews, C. E., R. T. Graser, A. Y. Savinov, D. V. Serreze, and E. H. Leiter. 2001. Unusual resistance of ALR/Lt mouse beta cells to autoimmune destruction: role for beta cell-expressed resistance determinants. Proc. Natl. Acad. Sci. USA 98:235-240.
5. 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.
6. Babior, B. M., R. S. Kipnes, and J. T. Curnutte. 1973. Biological defense mechanisms: the production by leukocytes of superoxide, a potential bactericidal agent. J. Clin. Invest. 52:741-744.
7. Lander, H. M., A. J. Milbank, J. M. Tauras, D. P. Hajjar, B. L. Hempstead, G. D. Schwartz, R. T. Kraemer, U. A. Mirza, B. T. Chait, S. C. Burk, and L. A. Quilliam. 1996. Redox regulation of cell signalling. Nature 381:380-381.
8. Snelgrove, R. J., L. Edwards, A. J. Rae, and T. Hussell. 2006. An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur. J. Immunol. 36:1364-1373.
9. Snelgrove, R. J., L. Edwards, A. E. Williams, A. J. Rae, and T. Hussell. 2006. In the absence of reactive oxygen species, T cells default to a Th1 phenotype and mediate protection against pulmonary Cryptococcus neoformans infection. J. Immunol. 177:5509-5516.
10. 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.
11. Hultqvist, M., P. Olofsson, J. Holmberg, B. T. Bäckström, J. Tordsson, and R. Holmdahl. 2004. 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.
12. Mathews, C. E., B. D. Dunn, M. O. Hannigan, C. K. Huang, and E. H. Leiter. 2002. Genetic control of neutrophil superoxide production in diabetes-resistant ALR/Lt mice. Free Radic. Biol. Med. 32:744-751.
13. Mathews, C. E., R. T. Graser, R. J. Bagley, J. W. Caldwell, R. Li, G. A. Churchill, D. V. Serreze, and E. H. Leiter. 2003. Genetic analysis of resistance to type-1 diabetes in ALR/Lt mice, a NOD-related strain with defenses against autoimmune-mediated diabetogenic stress. Immunogenetics 55:491-496.
14. 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.
15. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240.
16. Gusdon, A. M., T. V. Votyakova, I. J. Reynolds, and C. E. Mathews. 2007. Nuclear and mitochondrial interaction involving mt-Nd2 leads to increased mitochondrial reactive oxygen species production. J. Biol. Chem. 282:5171-5179.
17. Gerling, I. C., D. V. Serreze, S. W. Christianson, and E. H. Leiter. 1992. Intrathymic islet cell transplantation reduces beta-cell autoimmunity and prevents diabetes in NOD/Lt mice. Diabetes 41:1672-1676.
18. Tse, H. M., S. I. Josephy, E. D. Chan, D. Fouts, and A. M. Cooper. 2002. 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. 168:825-833.
19. Martinon, F., X. Chen, A. H. Lee, and L. H. Glimcher. 2010. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11:411-418.
20. 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.
21. Greve, B., L. Vijayakrishnan, A. Kubal, R. A. Sobel, L. B. Peterson, L. S. Wicker, and V. K. Kuchroo. 2004. The diabetes susceptibility locus Idd5.1 on mouse chromosome 1 regulates ICOS expression and modulates murine experimental autoimmune encephalomyelitis. J. Immunol. 173:157-163.
22. Ichikawa, M., C. S. Koh, A. Inoue, J. Tsuyusaki, M. Yamazaki, Y. Inaba, Y. Sekiguchi, M. Itoh, H. Yagita, and A. Komiyama. 2000. Anti-IL-12 antibody prevents the development and progression of multiple sclerosis-like relapsing-remitting demyelinating disease in NOD mice induced with myelin oligodendrocyte glycoprotein peptide. J. Neuroimmunol. 102:56-66.
23. Mathur, A. N., H. C. Chang, D. G. Zisoulis, G. L. Stritesky, Q. Yu, J. T. O'Malley, R. Kapur, D. E. Levy, G. S. Kansas, and M. H. Kaplan. 2007. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J. Immunol. 178:4901-4907.
24. Yang, X. O., A. D. Panopoulos, R. Nurieva, S. H. Chang, D. Wang, S. S. Watowich, and C. Dong. 2007. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282:9358-9363.
25. Karin, M. 1998. The NF-kappa B activation pathway: its regulation and role in inflammation and cell survival. Cancer J. Sci. Am. 4 (Suppl. 1): S92-S99.
26. Torres, M., and H. J. Forman. 2003. Redox signaling and the MAP kinase pathways. Biofactors 17:287-296.
27. 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.
28. Curtsinger, J. M., C. S. Schmidt, A. Mondino, D. C. Lins, R. M. Kedl, M. K. Jenkins, and M. F. Mescher. 1999. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162:3256-3262.
29. Pape, K. A., A. Khoruts, A. Mondino, and M. K. Jenkins. 1997. Inflammatory cytokines enhance the in vivo clonal expansion and differentiation of antigenactivated CD4+ T cells. J. Immunol. 159:591-598.
30. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179-189.
31. Zhou, L., J. E. Lopes, M. M. Chong, I. I. Ivanov, R. Min, G. D. Victora, Y. Shen, J. Du, Y. P. Rubtsov, A. Y. Rudensky, et al. 2008. TGF-beta-induced Foxp3 inhibits T (H) 17 cell differentiation by antagonizing RORgammat function. Nature 453:236-240.
32. Tzartos, J. S., M. A. Friese, M. J. Craner, J. Palace, J. Newcombe, M. M. Esiri, and L. Fugger. 2008. Interleukin-17 production in central nervous systeminfiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 172:146-155.
33. Jäger, A., V. Dardalhon, R. A. Sobel, E. Bettelli, and V. K. Kuchroo. 2009. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 183:7169-7177.
34. Hultqvist, M., and R. Holmdahl. 2005. Ncf1 (p47phox) polymorphism determines oxidative burst and the severity of arthritis in rats and mice. Cell. Immunol. 233:97-101.
35. Chen, J., A. M. Gusdon, T. C. Thayer, and C. E. Mathews. 2008. Role of increased ROS dissipation in prevention of T1D. Ann. NY Acad. Sci. 1150:157-166.
36. Chen, J., Y. Lu, C. H. Lee, R. Li, E. H. Leiter, and C. E. Mathews. 2008. Commonalities of genetic resistance to spontaneous autoimmune and free radical-mediated diabetes. Free Radic. Biol. Med. 45:1263-1270.
37. Gusdon, A. M., T. V. Votyakova, and C. E. Mathews. 2008. mt-Nd2a suppresses reactive oxygen species production by mitochondrial complexes I and III. J. Biol. Chem. 283:10690-10697.
38. Mathews, C. E., and E. H. Leiter. 1999. Constitutive differences in antioxidant defense status distinguish alloxan-resistant and alloxan-susceptible mice. Free Radic. Biol. Med. 27:449-455.
39. Mathews, C. E., and E. H. Leiter. 1999. Resistance of ALR/Lt islets to free radical-mediated diabetogenic stress is inherited as a dominant trait. Diabetes 48:2189-2196.
40. Mathews, C. E., W. L. Suarez-Pinzon, J. J. Baust, K. Strynadka, E. H. Leiter, and A. Rabinovitch. 2005. Mechanisms underlying resistance of pancreatic islets from ALR/Lt mice to cytokine-induced destruction. J. Immunol. 175:1248-1256.
41. Piganelli, J. D., T. Martin, and K. Haskins. 1998. Splenic macrophages from the NOD mouse are defective in the ability to present antigen. Diabetes 47:1212-1218.
42. Tiedge, M., S. Lortz, R. Munday, and S. Lenzen. 1999. Protection against the co-operative toxicity of nitric oxide and oxygen free radicals by overexpression of antioxidant enzymes in bioengineered insulin-producing RINm5F cells. Diabetologia 42:849-855.
43. Tiedge, M., S. Lortz, R. Munday, and S. Lenzen. 1998. Complementary action of antioxidant enzymes in the protection of bioengineered insulin-producing RINm5F cells against the toxicity of reactive oxygen species. Diabetes 47:1578-1585.
44. Chen, H., X. Li, and P. N. Epstein. 2005. MnSOD and catalase transgenes demonstrate that protection of islets from oxidative stress does not alter cytokine toxicity. Diabetes 54:1437-1446.
45. Li, X., H. Chen, and P. N. Epstein. 2006. Metallothionein and catalase sensitize to diabetes in nonobese diabetic mice: reactive oxygen species may have a protective role in pancreatic beta-cells. Diabetes 55:1592-1604.
46. Hotta, M., F. Tashiro, H. Ikegami, H. Niwa, T. Ogihara, J. Yodoi, and J. Miyazaki. 1998. Pancreatic beta cell-specific expression of thioredoxin, an antioxidative and antiapoptotic protein, prevents autoimmune and streptozotocin-induced diabetes. J. Exp. Med. 188:1445-1451.
47. Backdahl, L., J. P. Guo, M. Jagodic, K. Becanovic, B. Ding, T. Olsson, and J. C. Lorentzen. 2009. Definition of arthritis candidate risk genes by combining rat linkage-mapping results with human case control association data. Ann. Rheum. Dis. 68:1925-1932.
48. Olofsson, P., J. Holmberg, J. Tordsson, S. Lu, B. Akerström, and R. Holmdahl. 2003. Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat. Genet. 33:25-32.
49. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177:566-573.
50. Hofstetter, H. H., S. M. Ibrahim, D. Koczan, N. Kruse, A. Weishaupt, K. V. Toyka, and R. Gold. 2005. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell. Immunol. 237:123-130.
51. Kelchtermans, H., E. Schurgers, L. Geboes, T. Mitera, J. Van Damme, J. Van Snick, C. Uyttenhove, and P. Matthys. 2009. Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res. Ther. 11: R122.
52. Geboes, L., L. Dumoutier, H. Kelchtermans, E. Schurgers, T. Mitera, J. C. Renauld, and P. Matthys. 2009. Proinflammatory role of the Th17 cytokine interleukin-22 in collagen-induced arthritis in C57BL/6 mice. Arthritis Rheum. 60:390-395.
53. Katz, J. D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulindependent diabetes. Science 268:1185-1188.
54. Dietlin, T. A., D. J. Cua, K. A. Burke, B. T. Lund, and R. C. van der Veen. 2009. Role of IL-23 in mobilization of immunoregulatory nitric oxide-or superoxideproducing Gr-1+ cells from bone marrow. Free Radic. Biol. Med. 47:357-363.
55. Fossiez, F., O. Djossou, P. Chomarat, L. Flores-Romo, S. Ait-Yahia, C. Maat, J. J. Pin, P. Garrone, E. Garcia, S. Saeland, et al. 1996. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 183:2593-2603.
56. Wuyts, W. A., B. M. Vanaudenaerde, L. J. Dupont, D. E. Van Raemdonck, M. G. Demedts, and G. M. Verleden. 2005. Interleukin-17-induced interleukin-8 release in human airway smooth muscle cells: role for mitogen-activated kinases and nuclear factor-kappaB. J. Heart Lung Transplant. 24:875-881.
57. Laan, M., Z. H. Cui, H. Hoshino, J. Lötvall, M. Sjöstrand, D. C. Gruenert, B. E. Skoogh, and A. Lindén. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162:2347-2352.
58. Liblau, R. S., S. M. Singer, and H. O. McDevitt. 1995. Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today 16:34-38.
59. Serreze, D. V., and E. H. Leiter. 1988. Defective activation of T suppressor cell function in nonobese diabetic mice: potential relation to cytokine deficiencies. J. Immunol. 140:3801-3807.
60. Koarada, S., Y. Wu, and W. M. Ridgway. 2001. Increased entry into the IFN-gamma effector pathway by CD4+ T cells selected by I-Ag7 on a nonobese diabetic versus C57BL/6 genetic background. J. Immunol. 167:1693-1702.
61. Knaus, U. G., P. G. Heyworth, T. Evans, J. T. Curnutte, and G. M. Bokoch. 1991. Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science 254:1512-1515.
62. Roberts, A. W., C. Kim, L. Zhen, J. B. Lowe, R. Kapur, B. Petryniak, A. Spaetti, J. D. Pollock, J. B. Borneo, G. B. Bradford, et al. 1999. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10:183-196.
63. Li, B., H. Yu, W. Zheng, R. Voll, S. Na, A. W. Roberts, D. A. Williams, R. J. Davis, S. Ghosh, and R. A. Flavell. 2000. Role of the guanosine triphosphatase Rac2 in T helper 1 cell differentiation. Science 288:2219-2222.
64. Yu, H., D. Leitenberg, B. Li, and R. A. Flavell. 2001. Deficiency of small GTPase Rac2 affects T cell activation. J. Exp. Med. 194:915-926.
65. Bending, D., H. De La Peña, M. Veldhoen, J. M. Phillips, C. Uyttenhove, B. Stockinger, and A. Cooke. 2009. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest.
66. Martin-Orozco, N., Y. Chung, S. H. Chang, Y. H. Wang, and C. Dong. 2009. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur. J. Immunol. 39:216-224.
67. Wilson, C. B., E. Rowell, and M. Sekimata. 2009. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 9:91-105.