IFN-γ-dependent regulatory circuits in immune inflammation highlighted in diabetes

Journal of Immunology

Volumn 181, Issue 10, 2008, Pages 6964-6974

  Calderon, Boris ^a   Suri, Anish ^a   Pan, Xiaoou O ^a   Mills, Jason C ^a   Unanue, Emil R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; NEUTRALIZING ANTIBODY; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DIABETES MELLITUS; EXPERIMENTAL MODEL; FOXP3+ CD4+ T LYMPHOCYTE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INFLAMMATION; LEUKOCYTE; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS ISLET; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SCID MOUSE; T LYMPHOCYTE; ADOPTIVE TRANSFER; ANIMAL; DNA MICROARRAY; FLOW CYTOMETRY; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; LASER; MICRODISSECTION; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PATHOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FLOW CYTOMETRY; INFLAMMATION; INTERFERON-GAMMA; ISLETS OF LANGERHANS; LASERS; MACROPHAGES; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MICRODISSECTION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ANTIGEN, T-CELL;

EID: 58149192146     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.10.6964     Document Type: Article

References (58)

1. Tisch, R., and H. McDevitt. 1996. Insulin-dependent diabetes mellitus. Cell 85: 291-297.
2. Anderson, M. S., and J. A. Bluestone. 2005. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23: 447-485.
3. Shoda, L. K., D. L. Young, S. Ramanujan, C. C. Whiting, M. A. Atkinson, J. A. Bluestone, G. S. Eisenbarth, D. Mathis, A. A. Rossini, S. E. Campbell, et al. 2005. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity 23: 115-126.
4. Schoenborn, J. R., and C. B. Wilson. 2007. Regulation of interferon-γ during innate and adaptive immune responses. Adv. Immunol. 96: 41-101. (Pubitemid 350018717)
5. Bach, E. A., M. Aguet, and R. D. Schreiber. 1997. The IFNγ receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15: 563-591.
6. Schreiber, R. D., J. L. Pace, S. W. Russell, A. Altman, and D. H. Katz. 1983. Macrophage-activating factor produced by a T cell hybridoma: physiochemical and biosynthetic resemblance to gamma-interferon. J. Immunol. 131: 826-832.
7. Katz, J. D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74: 1089-1100. (Pubitemid 23289465)
8. + T cells in autoimmune diabetes through the use of TCR transgenic mice. Immunol. Rev. 169: 55-65.
9. + T-cell-induced diabetes, macrophages are the final effector cells that mediate islet β-cell killing: studies from an acute model. Am. J. Pathol. 169: 2137-2147.
10. Hultgren, B., X. Huang, N. Dybdal, and T. A. Stewart. 1996. Genetic absence of γ-interferon delays but does not prevent diabetes in NOD mice. Diabetes 45: 812-817. (Pubitemid 26166778)
11. Serreze, D. V., C. M. Post, H. D. Chapman, E. A. Johnson, B. Lu, and P. B. Rothman. 2000. Interferon-γ receptor signaling is dispensable in the development of autoimmune type 1 diabetes in NOD mice. Diabetes 49: 2007-2011.
12. Kanagawa, O., G. Xu, A. Tevaarwerk, and B. A. Vaupel. 2000. Protection of nonobese diabetic mice from diabetes by gene(s) closely linked to IFN-γ receptor loci. J. Immunol. 164: 3919-3923. (Pubitemid 30169852)
13. Wang, B., I. Andre, A. Gonzalez, J. D. Katz, M. Aguet, C. Benoist, and D. Mathis. 1997. Interferon-γ impacts at multiple points during the progression of autoimmune diabetes. Proc. Natl. Acad. Sci. USA 94: 13844-13849. (Pubitemid 28009672)
14. Nicoletti, F., P. Zaccone, R. Di Marco, M. Di Mauro, G. Magro, S. Grasso, L. Mughini, P. Meroni, and G. Garotta. 1996. The effects of a nonimmunogenic form of murine soluble interferon-γ receptor on the development of autoimmune diabetes in the NOD mouse. Endocrinology 137: 5567-5575.
15. Debray-Sachs, M., C. Carnaud, C. Boitard, H. Cohen, I. Gresser, P. Bedossa, and J. F. Bach. 1991. Prevention of diabetes in NOD mice treated with antibody to murine IFN gamma. J. Autoimmun. 4: 237-248.
16. Campbell, I. L., T. W. Kay, L. Oxbrow, and L. C. Harrison. 1991. Essential role for interferon-gamma and interleukin-6 in autoimmune insulin-dependent diabetes in NOD/Wehi mice. J. Clin. Invest. 87: 739-742.
17. Trembleau, S., G. Penna, S. Gregori, N. Giarratana, and L. Adorini. 2003. IL-12 administration accelerates autoimmune diabetes in both wild-type and IFN-γ- deficient nonobese diabetic mice, revealing pathogenic and protective effects of IL-12-induced IFN-γ. J. Immunol. 170: 5491-5501. (Pubitemid 36617837)
18. Schadt, E. E., C. Li, B. Ellis, and W. H. Wong. 2001. Feature extraction and normalization algorithms for high-density oligonucleotide gene expression array data. J. Cell. Biochem. (Suppl. 37): 120-125.
19. Zhong, S., C. Li, and W. H. Wong. 2003. ChipInfo: software for extracting gene annotation and gene ontology information for microarray analysis. Nucleic Acids Res. 31: 3483-3486. (Pubitemid 37442181)
20. Doherty, J. M., L. K. Carmichael, and J. C. Mills. 2006. GOurmet: a tool for quantitative comparison and visualization of gene expression profiles based on gene ontology (GO) distributions. BMC Bioinform. 7: 151.
21. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57: 289-300.
22. Mills, J. C., N. Andersson, T. S. Stappenbeck, C. C. Chen, and J. I. Gordon. 2003. Molecular characterization of mouse gastric zymogenic cells. J. Biol. Chem. 278: 46138-46145. (Pubitemid 37432764)
23. Schreiber, R. D., L. J. Hicks, A. Celada, N. A. Buchmeier, and P. W. Gray. 1985. Monoclonal antibodies to murine gamma-interferon which differentially modulate macrophage activation and antiviral activity. J. Immunol. 134: 1609-1618.
24. Harris, M. A., J. Clark, A. Ireland, J. Lomax, M. Ashburner, R. Foulger, K. Eilbeck, S. Lewis, B. Marshall, C. Mungall, et al. 2004. The gene ontology (GO) database and informatics resource. Nucleic Acids Res. 32: D258-D261.
25. Lang, R., D. Patel, J. J. Morris, R. L. Rutschman, and P. J. Murray. 2002. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 169: 2253-2263. (Pubitemid 34920965)
26. Pull, S. L., J. M. Doherty, J. C. Mills, J. I. Gordon, and T. S. Stappenbeck. 2005. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc. Natl. Acad. Sci. USA 102: 99-104.
27. Mosser, D. M. 2003. The many faces of macrophage activation. J. Leukocyte Biol. 73: 209-212.
28. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
29. Welch, J. S., L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass. 2002. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J. Biol. Chem. 277: 42821-42829.
30. H2-mediated pulmonary inflammation leads to the differential expression of ribonuclease genes by alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 27: 678-687.
31. Mantovani, A., A. Sica, and M. Locati. 2005. Macrophage polarization comes of age. Immunity 23: 344-346.
32. Rauh, M. J., V. Ho, C. Pereira, A. Sham, L. M. Sly, V. Lam, L. Huxham, A. I. Minchinton, A. Mui, and G. Krystal. 2005. SHIP represses the generation of alternatively activated macrophages. Immunity 23: 361-374.
33. Herbert, D. R., C. Holscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, et al. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20: 623-635. (Pubitemid 38659504)
34. Zhu, Z., T. Zheng, R. J. Homer, Y. K. Kim, N. Y. Chen, L. Cohn, Q. Hamid, and J. A. Elias. 2004. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682. (Pubitemid 38765861)
35. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686. (Pubitemid 39457982)
36. Kanagawa, O., A. Militech, and B. A. Vaupel. 2002. Regulation of diabetes development by regulatory T cells in pancreatic islet antigen-specific TCR transgenic nonobese diabetic mice. J. Immunol. 168: 6159-6164. (Pubitemid 34620034)
37. Suri, A., J. Shimizu, J. D. Katz, S. Sakaguchi, E. R. Unanue, and O. Kanagawa. 2004. Regulation of autoimmune diabetes by non-islet-specific T cells: a role for the glucocorticoid-induced TNF receptor. Eur. J. Immunol. 34: 447-454. (Pubitemid 39255955)
38. Pakala, S. V., M. Chivetta, C. B. Kelly, and J. D. Katz. 1999. In autoimmune diabetes the transition from benign to pernicious insulitis requires an islet cell response to tumor necrosis factor α. J. Exp. Med. 189: 1053-1062.
39. Morimoto, J., H. Yoneyama, A. Shimada, T. Shigihara, S. Yamada, Y. Oikawa, K. Matsushima, T. Saruta, and S. Narumi. 2004. CXC chemokine ligand 10 neutralization suppresses the occurrence of diabetes in nonobese diabetic mice through enhanced β cell proliferation without affecting insulitis. J. Immunol. 173: 7017-7024. (Pubitemid 39541091)
40. Orlofsky, A., E. Y. Lin, and M. B. Prystowsky. 1994. Selective induction of the beta chemokine C10 by IL-4 in mouse macrophages. J. Immunol. 152: 5084-5091. (Pubitemid 24139104)
41. Orlofsky, A., Y. Wu, and M. B. Prystowsky. 2000. Divergent regulation of the murine CC chemokine C10 by Th1 and Th2 cytokines. Cytokine 12: 220-228.
42. Heitmeier, M. R., A. L. Scarim, and J. A. Corbett. 1997. Interferon-γ increases the sensitivity of islets of Langerhans for inducible nitric-oxide synthase expression induced by interleukin 1. J. Biol. Chem. 272: 13697-13704.
43. + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 212: 8-27.
44. Fallarino, F., R. Bianchi, C. Orabona, C. Vacca, M. L. Belladonna, M. C. Fioretti, D. V. Serreze, U. Grohmann, and P. Puccetti. 2004. CTLA-4-Ig activates forkhead transcription factors and protects dendritic cells from oxidative stress in nonobese diabetic mice. J. Exp. Med. 200: 1051-1062. (Pubitemid 39431129)
45. Luhder, F., C. Chambers, J. P. Allison, C. Benoist, and D. Mathis. 2000. Pin-pointing when T cell costimulatory receptor CTLA-4 must be engaged to dampen diabetogenic T cells. Proc. Natl. Acad. Sci. USA 97: 12204-12209. (Pubitemid 30815163)
46. + immunoregulatory T cells is antigen nonspecific. J. Immunol. 164: 183-190.
47. Taylor, P. A., C. J. Lees, S. Fournier, J. P. Allison, A. H. Sharpe, and B. R. Blazar. 2004. B7 expression on T cells down-regulates immune responses through CTLA-4 ligation via T-T interactions. J. Immunol. 172: 34-39.
48. + regulatory T cell function. Eur. J. Immunol. 34: 2996-3005.
49. Grohmann, U., F. Fallarino, R. Bianchi, C. Orabona, C. Vacca, M. C. Fioretti, and P. Puccetti. 2003. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J. Exp. Med. 198: 153-160. (Pubitemid 36870195)
50. Puccetti, P., and U. Grohmann. 2007. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-κB activation. Nat. Rev. Immunol. 7: 817-823. (Pubitemid 47480306)
51. Keskin, D. B., B. Marshall, D. Munn, A. L. Mellor, and D. A. Gearhart. 2007. Decreased protein nitration in macrophages that overexpress indoleamine 2,3- dioxygenase. Cell. Mol. Biol. Lett. 12: 82-102.
52. Mellor, A. L., P. Chandler, B. Baban, A. M. Hansen, B. Marshall, J. Pihkala, H. Waldmann, S. Cobbold, E. Adams, and D. H. Munn. 2004. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. Int. Immunol. 16: 1391-1401.
53. Mellor, A. L., B. Baban, P. Chandler, B. Marshall, K. Jhaver, A. Hansen, P. A. Koni, M. Iwashima, and D. H. Munn. 2003. Cutting edge: Induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J. Immunol. 171: 1652-1655.
54. Mellor, A. L., and D. H. Munn. 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4: 762-774.
55. Ulaeto, D., P. E. Lacy, D. M. Kipnis, O. Kanagawa, and E. R. Unanue. 1992. A T-cell dormant state in the autoimmune process of nonobese diabetic mice treated with complete Freund's adjuvant. Proc. Natl. Acad. Sci. USA 89: 3927-3931.
56. Mori, Y., T. Kato, T. Kodaka, E. M. Kanagawa, S. Hori, and O. Kanagawa. 2008. Protection of IFN-γ signaling-deficient NOD mice from diabetes by cyclophosphamide. Int. Immunol. 20: 1231-1237.
57. Matos, M., R. Park, D. Mathis, and C. Benoist. 2004. Progression to islet destruction in a cyclophosphamide-induced transgenic model: a microarray overview. Diabetes 53: 2310-2321. (Pubitemid 39145584)
58. Cain, J. A., J. A. Smith, J. K. Ondr, B. Wang, and J. D. Katz. 2006. NKT cells and IFN-γ establish the regulatory environment for the control of diabetogenic T cells in the nonobese diabetic mouse. J. Immunol. 176: 1645-1654.