Exacerbated Th2-mediated airway inflammation and hyperresponsiveness in autoimmune diabetes-prone NOD mice: A critical role for CD1d-dependent NKT cells

European Journal of Immunology

Volumn 34, Issue 2, 2004, Pages 327-335

  Araujo, Luisa M ^a   Lefort, Jean ^b   Nahori, Marie Anne ^b   Diem, Séverine ^a   Zhu, Ren ^a   Dy, Michel ^a   Leite de Moraes, Maria C ^a   Bach, J F ^a   Vargaftig, B Boris ^b,c   Herbelin, André ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Allergy; Autoimmunity; Cytokines; Diabetes; Th1; Th2

Indexed keywords

CD1 ANTIGEN; CD1D ANTIGEN; EOTAXIN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; OVALBUMIN; BETA CHEMOKINE; CYTOKINE; MONOCLONAL ANTIBODY;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; AUTOIMMUNE DISEASE; BRONCHUS HYPERREACTIVITY; BRONCHUS MUCUS; CELL COMPOSITION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DISEASE PREDISPOSITION; EOSINOPHILIA; IMMUNE RESPONSE; IMMUNOGENETICS; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE FUNCTION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; STRAIN DIFFERENCE; T LYMPHOCYTE SUBPOPULATION; TH2 CELL; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; BIOSYNTHESIS; BLOOD; CYTOLOGY; IMMUNOLOGY; LOEFFLER PNEUMONIA; LUNG LAVAGE; MALE; METABOLISM; MOUSE MUTANT; MUCUS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD1; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINES, CC; CYTOKINES; DIABETES MELLITUS, TYPE 1; IMMUNOGLOBULIN E; INTERLEUKIN-5; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, KNOCKOUT; MUCUS; OVALBUMIN; PULMONARY EOSINOPHILIA; TH2 CELLS;

EID: 1642291724     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324151     Document Type: Article

References (41)

1. Makino, S., Kunimoto, K., Muraoka, Y., Mizushima, Y., Katagiri, K. and Tochino, Y., Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 1980. 29: 1-13.
2. Bach, J. F., Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 1994. 15: 516-542.
3. Bach, J. F. and Chatenoud, L., Tolerance to islet autoantigens in type 1 diabetes. Annu. Rev. Immunol. 2001. 19: 131-161.
4. Delovitch, T. L. and Singh, B., The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 1997. 7: 727-738.
5. Katz, J. D., Benoist, C. and Mathis, D., T helper cell subsets in insulin-dependent diabetes. Science 1995. 268: 1185-1188.
6. Liblau, R. S., Singer, S. M. and McDevitt, H. O., Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today 1995. 16: 34-38.
7. + islet-specific T cell clone. Science 1990. 249: 1433-1436.
8. + Th1 and Th2 cells derived from the spleens of diabetic NOD mice. J. Clin. Invest. 1995. 95: 2979-2985.
9. Trembleau, S., Penna, G., Bosi, E., Mortara, A., Gately, M. K. and Adorini, L., Interleukin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 1995. 2: 817-821.
10. Rabinovitch, A., Suarez-Pinzon, W. L., Sorensen, O., Bleackley, R. C. and Power, R. F., IFN-gamma gene expression in pancreatic islet-infiltrating mononuclear cells correlates with autoimmune diabetes in nonobese diabetic mice. J. Immunol. 1995. 154: 4874-4882.
11. Fox, C. J. and Danska, J. S., IL-4 expression at the onset of islet inflammation predicts nondestructive insulitis in nonobese diabetic mice. J. Immunol. 1997. 158: 2414-2424.
12. Debray-Sachs, M., Carnaud, C., Boitard, C., Debray-Sachs, M., Carnaud, Boitard, C. C., Gresser, I., Cohen, H., Bedossa, P. and Bach, J. F., Prevention of diabetes in NOD mice treated with antibody to murine IFN gamma. J. Autoimmun. 1991. 4: 237-248.
13. Trembleau, S., Penna, G., Gregori, S., Gately, M. K. and Adorini, L., Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur. J. Immunol. 1997. 27: 2330-2339.
14. Rapoport, M. J., Jaramillo, A., Zipris, D., Lazarus, A. H., Serraze, D. V., Leiter, E. H., Cyopick, P., Danska, J. S. and Delovitch, T. L., Interleukin 4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J. Exp. Med. 1993. 178: 87-99.
15. Mueller, R., Krahl, T. and Sarvetnick, N., Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in nonobese diabetic (NOD) mice. J. Exp. Med. 1996. 184: 1093-1099.
16. Tian, J., Olcott, P. A. and Kaufman, L. D., Antigen-based immunotherapy drives the precocious development of autoimmunity. J. Immunol. 2002. 169: 6564-6569.
17. Tian, J., Lehmann, V. P. and Kaufman, L. D., Determinant spreading of T helper cell 2 (Th2) responses to pancreatic islet autoantigens. J. Exp. Med. 1997. 186: 2039-2043.
18. Haile, S., Lefort, J., Joseph, D., Gounon, P., Huerre, M. and Vargaftig, B. B., Mucous-cell metaplasia and inflammatory-cell recruitment are dissociated in allergic mice after antibody- and drug-dependent cell depletion in a murine model of asthma. Am. J. Resp. Cell Mol. Biol. 1999. 20: 891-902.
19. Vargaftig, B. B., What can we learn from murine models of asthma? Clin. Exp. Allergy 1999. 29 Suppl 1: 9-13.
20. Proust, B., Ruffie, C., Lefort, J. and Vargaftig, B.B., Bronchopulmonary hyperreactivity and lung eosinophil sequestration but not their migration to the alveolar compartment are independent of interleukin-5 in allergic mice. Eur. Cytokine Netw. 2002. 13: 340-349.
21. Matsukura, S., Stellato, C., Georas, S. N., Casolaro, V., Plitt, J. R., Miura, K. Kurosawa, S., Schindler, U. and Schleimer, R. P., Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 2001. 24: 755-761.
22. Snapper, C. M., Finkelman, F. D. and Paul, W. E., Differential regulation of IgG1 and IgE synthesis by interleukin 4. J. Exp. Med. 1988. 167: 183-196.
23. Wills-Karp, M., Luyimbazi, J., Xu, X., Schofield, B., Neben, T. Y., Karp, C. L. and Donaldson, D. D., Interleukin-13: central mediator of allergic asthma. Science 1998. 282: 2258-2261.
24. Akbari, O., Stock, P., Meyer, E., Kronenberg, M., Sidobre, S., Nakayama, T., Taniguchi, M., Grusby, M. J., DeKruyff, R. H. and Umetsu, D. T., Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 2003. 9: 582-588.
25. Lisbonne, M., Diem, S., de Castro Keller, A., Lefort, J., Araujo L. M., Hachem, P., Fourneau, J. M., Sidobre, S., Kronenberg, M., Taniguchi, M., et al. Cutting edge: invariant Valpha14 NKT cells are required for allergen-induced airway inflammation and hyperreactivity in an experimental asthma model. J. Immunol. 2003. 171: 1637-1641.
26. +-like thymocytes in the NOD mouse. Eur. J. Immunol. 1996. 26: 2989-2998.
27. - T cell deficiency and IDDM in NOD/Lt mice. Diabetes 1997. 46: 572-582.
28. Sharif, S., Arreaza, G. A., Zucker, P., Mi, Q. S., Sondhi, J., Naidenko, O. V., Kronenberg, M., Koezuka, Y., Delovitch, T. L., Gombert, T. L. et al., Activation of natural killer T cells by alpha-galactosylceramide treatment prevents the onset and recurrence of autoimmune Type 1 diabetes. Nat. Med. 2001. 7: 1057-1062.
29. Scott, B., Liblau, R., Degermann, S., Marconi, L. A., Ogata, L., Caton, A. J., McDevitt, H. O. and Lo, D., A role for non-MHC genetic polymorphism in susceptibility to spontaneous autoimmunity. Immunity 1994. 1: 73-83.
30. Hogan, S. P., Matthaei, K. I., Young, J. M., Koskinen, A., Young, I. G. and Foster, P. S., A novel T cell-regulated mechanism modulating allergen-induced airway hyperreactivity in BALB/c mice independently of IL-4 and IL-5. J. Immunol. 1998. 161: 1501-1509.
31. Gavett, S. H, O'Hearn, D. J., Li, X., Huang, S. K., Finkelman, F. D. and Wills-Karp, M., Interleukin 12 inhibits antigen-induced airway hyperresponsiveness, inflammation, and Th2 cytokine expression in mice. J. Exp. Med. 1995. 182: 1527-1536.
32. Huang, T. J., MacAry, P. A., Eynott, P., Moussavi, A., Daniel, K. C., Askenase, P. W., Kemeny, D. M. and Chung, K. F., Allergen-specific Th1 cells counteract efferent Th2 cell-dependent bronchial hyperresponsiveness and eosinophilic inflammation partly via IFN-gamma. J. Immunol. 2001. 166: 207-217.
33. Randolph, D. A., Stephens, R., Carruthers, C. J. and Chaplin, D. D., Cooperation between Th1 and Th2 cells in a murine model of eosinophilic airway inflammation. J. Clin. Invest. 1999. 104: 1021-1029.
34. Akbari, O., Freeman, G. J., Meyer, E. H., Greenfield, E. A., Chang, T. T., Sharpe, A. H., Berry, G., DeKruyff, R. H., Umetsu, D. T., et al., Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 2002. 8: 1024-1032.
35. Yssel, H., Lécart, S. and Pène, J., Regulatory T cells and allergic asthma. Microbes Infect. 2001. 3: 899-904.
36. Umetsu, D. T., McIntire, J. J., Akbari, O., Macaubas, C. and Dekruyff, R. H., Asthma: an epidemic of dysregulated immunity. Nat. Immunol. 2002. 3: 713-720.
37. Zuany-Amorim, C., Sawicka, E., Manlius, C., Le Moine, A., Brunet, L. R., Kemeny, D. M., Bowen, G., Rook, G. and Walker, C., Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T cells. Nat. Med. 2002. 8: 625-629.
38. Mars, L. T., Laloux, V., Goude, K., Desbois, S., Saoudi, A., Van Kaer, L., Lassmann, H., Herbelin, A., Lehuen, A. and Liblau, R. S., Cutting edge: V alpha 14-J alpha 281 NKT cells naturally regulate experimental autoimmune encephalomyelitis in nonobese diabetic mice. J. Immunol. 2002. 168: 6007-6011.
39. Hong, S., Wilson, M. T., Serizawa, I., Wu, L., Singh, N., Naidenko, O. V., Miura, T., Haba, T., Scherer, D. C., Wei, J., et al., The natural killer T cell ligand alpha-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat. Med. 2001. 7: 1052-1056
40. Stene, L. C. and Nafstad, P., Relation between occurrence of type 1 diabetes and asthma. Lancet 2001. 357: 607-608.
41. Serreze, D. V. and Leiter, E. H., Genes and cellular requirements for autoimmune diabetes susceptibility in nonobese diabetic mice. Curr. Dir. Autoimmun. 2001. 4: 31-67.