Aire deficiency causes increased susceptibility to streptozotocin-induced murine type 1 diabetes

Scandinavian Journal of Immunology

Volumn 67, Issue 6, 2008, Pages 569-580

  Hassler S ^a,b   Peltonen, L ^c,d   Sandler, S ^e   Winqvist, O ^b  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOIMMUNE REGULATOR PROTEIN; INTERLEUKIN 10; STREPTOZOCIN; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL CORTEX; AIRE GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE POLYENDOCRINOPATHY CANDIDIASIS ECTODERMAL DYSTROPHY; CELL ACTIVATION; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; EPITHELIUM CELL; GENE; GENE MUTATION; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PARATHYROID GLAND; PRIORITY JOURNAL; PROTEIN FUNCTION; STREPTOZOCIN DIABETES; THYMUS;

ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE SUSCEPTIBILITY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PANCREAS; POLYENDOCRINOPATHIES, AUTOIMMUNE; SPLEEN; STREPTOZOCIN; TRANSCRIPTION FACTORS;

EID: 43849088647     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/j.1365-3083.2008.02106.x     Document Type: Article

References (56)

1. Ahonen P, Myllärniemi S, Sipilä I, Perheentupa J. Clinical variation of autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) in a series of 68 patients. N Engl J Med 1990 322 : 1829 36.
2. Velloso LA, Winqvist O, Gustafsson J, Kampe O, Karlsson FA. Autoantibodies against a novel 51 kDa islet antigen and glutamate decarboxylase isoforms in autoimmune polyendocrine syndrome type I. Diabetologia 1994 37 : 61 9.
3. Bjork E, Velloso LA, Kampe O, Karlsson FA. GAD autoantibodies in IDDM, stiff-man syndrome, and autoimmune polyendocrine syndrome type I recognize different epitopes. Diabetes 1994 43 : 161 5.
4. Tuomi T, Bjorses P, Falorni A et al. Antibodies to glutamic acid decarboxylase and insulin-dependent diabetes in patients with autoimmune polyendocrine syndrome type I. J Clin Endocrinol Metab 1996 81 : 1488 94.
5. Gylling M, Tuomi T, Bjorses P et al. ss-cell autoantibodies, human leukocyte antigen II alleles, and type 1 diabetes in autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy. J Clin Endocrinol Metab 2000 85 : 4434 40.
6. Rorsman F, Husebye ES, Winqvist O, Bjork E, Karlsson FA, Kampe O. Aromatic-l-amino-acid decarboxylase, a pyridoxal phosphate-dependent enzyme, is a beta-cell autoantigen. Proc Natl Acad Sci U S A 1995 92 : 8626 9.
7. Halonen M, Eskelin P, Myhre AG et al. AIRE mutations and human leukocyte antigen genotypes as determinants of the autoimmune polyendocrinopathy- candidiasis-ectodermal dystrophy phenotype. J Clin Endocrinol Metab 2002 87 : 2568 74.
8. consortium TF-GA. An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Autoimmune Polyendocrinopathy-Candidiasis-Ectodermal Dystrophy. Nat Genet 1997 17 : 399 403.
9. Zuklys S, Balciunaite G, Agarwal A, Fasler-Kan E, Palmer E, Holländer G. Normal thymic architecture and negative selection are associated with Aire expression, the gene defective in the Autoimmune- Polyendocrinopathy-Candidiasis-Ectodermal Dystrophy (APECED). J Immunol 2000 165 : 1976 83.
10. Halonen M, Pelto-Huikko M, Eskelin P, Peltonen L, Ulmanen I, Kolmer M. Subcellular location and expression pattern of autoimmune reguator (Aire), the mouse orthologue for human gene defective in Autoimmune Polyendocrinopathy Candidiasis Ectodermal Dystrophy (APECED). J Histochem Cytochem 2001 49 : 197 208.
11. Heino M, Peterson P, Kudoh J et al. Autoimmune regulator is expressed in the cells regulating immune tolerance in thymus medulla. Biochem Biophys Res Commun 1999 257 : 821 5.
12. Heino M, Peterson P, Sillanpää N et al. RNA and protein expression of the murine autoimmune regulator gene (Aire) in normal, RelB-deficient and in NOD mouse. Eur J Immunol 2000 30 : 1884 93.
13. Kogawa K, Nagafuchi S, Katsuta H et al. Expression of AIRE gene in peripheral monocyte/dendritic cell lineage. Immunol Lett 2002 1 : 80.
14. Ramsey C, Winqvist O, Puhakka L et al. Aire deficient mice develop multiple features of APECED phenotype and show altered immune response. Hum Mol Genet 2002 11 : 397 409.
15. Anderson M, Venanzi ES, Klein L et al. Projection of an immunological self shadow within the thymus by the Aire protein. Science 2002 298 : 1395 401.
16. Liston A, Lesage S, Wilson J, Peltonen L, Goodnow CG. Aire regulates negative selection of organ-specific T cells. Nature Immunology 2003 4 : 350 4.
17. Ramsey C, Hässler S, Marits P et al. Increased antigen presenting cell-mediated T cell activation in mice and patients without the autoimmune regulator. Eur J Immunol 2006 36 : 305 17.
18. Kuroda N, Mitani T, Takeda N et al. Development of autoimmunity against transcriptionally unrepressed target antigen in the thymus of Aire-deficient mice. J Immunol 2005 15 : 174.
19. Jiang W, Anderson MS, Bronson R, Mathis D, Benoist C. Modifier loci condition autoimmunity provoked by Aire deficiency. J Exp Med 2005 19 : 202.
20. Anderson MS, Venanzi ES, Chen Z, Berzins SP, Benoist C, Mathis D. The cellular mechanism of Aire control of T cell tolerance. Immunity 2005 23 : 227 39.
21. Liston A, Gray DH, Lesage S et al. Gene dosage - limiting role of Aire in thymic expression, clonal deletion, and organ-specific autoimmunity. J Exp Med 2004 200 : 1015 26.
22. Johnnidis JB, Venanzi ES, Taxman DJ, Ting JP, Benoist CO, Mathis DJ. Chromosomal clustering of genes controlled by the Aire transcription factor. Proc Natl Acad Sci U S A 2005 102 : 7233 8.
23. Niki S, Oshikawa K, Mouri Y et al. Alteration of intra-pancreatic target-organ specificity by abrogation of Aire in NOD mice. J Clin Invest 2006 116 : 1292 301.
24. Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 1976 30 : 193.
25. Slingsby J, MB H, E S, MJ W, BJ M. New microsatellite polymorphisms identified between C57BL/6, C57BL/10, and C57BL/KsJ inbred mouse strains. Immunogenetics 1996 43 : 72 5.
26. Holstad M, Sandler S. Aminoguanidine, an inhibitor of nitric oxide formation, fails to protect against insulitis and hyperglycemia induced by multiple low dose streptozotocin injections in mice. Autoimmunity 1993 15 : 311 4.
27. Sandler S, Andersson A, Hellerstrom C. Inhibitory effects of interleukin 1 on insulin secretion, insulin biosynthesis, and oxidative metabolism of isolated rat pancreatic islets. Endocrinology 1987 121 : 1424 31.
28. Lau J, Borjesson A, Holstad M, Sandler S. Prolactin regulation of the expression of TNF-alpha, IFN-gamma and IL-10 by splenocytes in murine multiple low dose streptozotocin diabetes. Immunol Lett 2006 102 : 20 35.
29. Rossini AA, Appel MC, Williams RM, Like AA. Genetic influence of the streptozotocin-induced insulitis and hyperglycemia. Diabetes 1977 26 : 916 20.
30. Schnedl WJ, Ferber S, Johnson JH, Newgard CB. STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 1994 43 : 1326 33.
31. Bonnevie-Nielsen V, Steffes MW, Lernmark A. A major loss in islet mass and B-cell function precedes hyperglycemia in mice given multiple low doses of streptozotocin. Diabetes 1981 30 : 424 9.
32. Ihm SH, Lee KU, Rhee BD, Min HK. Initial role of macrophage in the development of anti-beta-cell cellular autoimmunity in multiple low-dose streptozotocin-induced diabetes in mice. Diabetes Res Clin Pract 1990 10 : 123 6.
33. + T cells. Chem Res Toxicol 2005 18 : 872 9.
34. Yamamoto H, Uchigata Y, Okamoto H. Streptozotocin and alloxan induce DNA strand breaks and poly(ADP-ribose) synthetase in pancreatic islets. Nature 1981 294 : 284 6.
35. Kroncke KD, Fehsel K, Sommer A, Rodriguez ML, Kolb-Bachofen V. Nitric oxide generation during cellular metabolization of the diabetogenic N-methyl-N-nitroso-urea streptozotozin contributes to islet cell DNA damage. Biol Chem Hoppe Seyler 1995 376 : 179 85.
36. Bolzan AD, Bianchi MS. Genotoxicity of streptozotocin. Mutat Res 2002 512 : 121 34.
37. Heller B, Wang ZQ, Wagner EF et al. Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells. J Biol Chem 1995 270 : 11176 80.
38. Burkart V, Wang ZQ, Radons J et al. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat Med 1999 5 : 314 9.
39. Kallmann B, Burkart V, Kroncke KD, Kolb-Bachofen V, Kolb H. Toxicity of chemically generated nitric oxide towards pancreatic islet cells can be prevented by nicotinamide. Life Sci 1992 51 : 671 8.
40. Herold KC, Vezys V, Sun Q et al. Regulation of cytokine production during development of autoimmune diabetes induced with multiple low doses of streptozotocin. J Immunol 1996 156 : 3521 7.
41. Muller A, Schott-Ohly P, Dohle C, Gleichmann H. Differential regulation of Th1-type and Th2-type cytokine profiles in pancreatic islets of C57BL/6 and BALB/c mice by multiple low doses of streptozotocin. Immunobiology 2002 205 : 35 50.
42. Thorvaldson L, Holstad M, Sandler S. Cytokine release by murine spleen cells following multiple low dose streptozotocin-induced diabetes and treatment with a TNFalpha transcriptional inhibitor. Int Immunopharmacol 2003 3 : 1609 17.
43. Cvetkovic I, Al-Abed Y, Miljkovic D et al. Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes. Endocrinology 2005 146 : 2942 51.
44. Kusterer K, Ludwig R, Hochschulz P, Stegmuller M, Bojunga J, von Minckwitz G. Macrophage and lymphocyte homing in experimental diabetes. Exp Clin Endocrinol Diabetes 1999 107 (Suppl. 3 S102 7.
45. McEvoy RC, Andersson J, Sandler S, Hellerstrom C. Multiple low-dose streptozotocin-induced diabetes in the mouse. Evidence for stimulation of a cytotoxic cellular immune response against an insulin-producing beta cell line. J Clin Invest 1984 74 : 715 22.
46. Kolb-Bachofen V, Epstein S, Kiesel U, Kolb H. Low-dose streptozocin-induced diabetes in mice. Electron microscopy reveals single-cell insulitis before diabetes onset. Diabetes 1988 37 : 21 7.
47. Kantwerk-Funke G, Burkart V, Kolb H. Low dose streptozotocin causes stimulation of the immune system and of anti-islet cytotoxicity in mice. Clin Exp Immunol 1991 86 : 266 70.
48. Lukic ML, Stosic-Grujicic S, Shahin A. Effector mechanisms in low-dose streptozotocin-induced diabetes. Dev Immunol 1998 6 : 119 28.
49. Jansen A, Homo-Delarche F, Hooijkaas H, Leenen PJ, Dardenne M, Drexhage HA. Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and beta-cell destruction in NOD mice. Diabetes 1994 43 : 667 75.
50. Welsh M, Welsh N, Bendtzen K et al. Comparison of mRNA contents of interleukin-1 beta and nitric oxide synthase in pancreatic islets isolated from female and male nonobese diabetic mice. Diabetologia 1995 38 : 153 60.
51. 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 2.
52. 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 8.
53. Trembleau S, Penna G, Gregori S, Gately MK, Adorini L. Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur J Immunol 1997 27 : 2330 9.
54. Cameron MJ, Arreaza GA, Zucker P et al. IL-4 prevents insulitis and insulin-dependent diabetes mellitus in nonobese diabetic mice by potentiation of regulatory T helper-2 cell function. J Immunol 1997 159 : 4686 92.
55. Hassler S, Ramsey C, Karlsson MC et al. Aire deficient mice develop hematopoetic irregularities and marginal zone B cell lymphoma. Blood 2006 108 : 1941 8.
56. Turunen JA, Wessman M, Forsblom C et al. Association analysis of the AIRE and insulin genes in Finnish type 1 diabetic patients. Immunogenetics 2006 58 : 331 8.