Abrogation of ICOS/ICOS ligand costimulation in NOD mice results in autoimmune deviation toward the neuromuscular system

European Journal of Immunology

Volumn 40, Issue 8, 2010, Pages 2267-2276

  Prevot, Nicolas ^a,b   Briet, Claire ^a,b   Lassmann, Hans ^c   Tardivel, Isabelle ^b   Roy, Edwige ^d   Morin, Joëlle ^b   Mak, Tak W ^e   Tafuri, Anna ^d   Boitard, Christian ^a,b  

^a HÔPITAL SAINT VINCENT DE PAUL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c Medical University of Vienna   (Austria)

^d INSERM   (France)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Autoimmunity; Costimulation; ICOS; ICOS ligand; Type 1 diabetes

Indexed keywords

CD28 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; INDUCIBLE T CELL CO STIMULATOR LIGAND; INDUCIBLE T CELL COSTIMULATOR; LIGAND; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; EFFECTOR CELL; IMMUNOLOGICAL TOLERANCE; INFLAMMATORY INFILTRATE; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; MYOSITIS; NEUROMUSCULAR SYSTEM; NONHUMAN; NONOBESE DIABETIC MOUSE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SENSORY GANGLION; T LYMPHOCYTE SUBPOPULATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; AUTOIMMUNITY; DIABETES MELLITUS, TYPE 1; FACIAL NERVE DISEASES; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MYOSITIS; PROTEINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 77956096397     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040416     Document Type: Article

References (40)

1. Faideau, B., Larger, E., Lepault, F., Carel, J. C. and Boitard, C., Role of betacells in type 1 diabetes pathogenesis. Diabetes 2005. 54: S87-S96. (Pubitemid 43343336)
2. Anderson, M. S. and Bluestone, J. A., The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 2005. 23: 447-485.
3. Jones, E. Y., Fugger, L., Strominger, J. L. and Siebold, C., MHC class II proteins and disease: a structural perspective. Nat. Rev. Immunol. 2006. 6: 271-282.
4. Toma, A., Haddouk, S., Briand, J. P., Camoin, L., Gahery, H., Connan, F., Dubois-Laforgue, D. et al., Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. Proc. Natl. Acad. Sci. USA 2005. 102: 10581-10586.
5. Wong, F. S., Visintin, I., Wen, L., Flavell, R. A. and Janeway, C. A., Jr., CD8 T cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells. J. Exp. Med. 1996. 183: 67-76.
6. Hara, T., Fu, S. M. and Hansen, J. A., Human T cell activation. II. A new activation pathway used by a major T cell population via a disulfide-bonded dimer of a 44 kilodalton polypeptide (9.3 antigen). J. Exp. Med. 1985. 161: 1513-1524.
7. Gross, J. A., St John, T. and Allison, J. P., The murine homologue of the T lymphocyte antigen CD28. Molecular cloning and cell surface expression. J. Immunol. 1990. 144: 3201-3210.
8. Brunet, J. F., Denizot, F., Luciani, M. F., Roux-Dosseto, M., Suzan, M., Mattei, M. G. and Golstein, P., A new member of the immunoglobulin superfamily - CTLA-4. Nature 1987. 328: 267-270. (Pubitemid 17108278)
9. Yoshinaga, S. K., Whoriskey, J. S., Khare, S. D., Sarmiento, U., Guo, J., Horan, T., Shih, G. et al., T-cell co-stimulation through B7RP-1 and ICOS. Nature 1999. 402: 827-832. (Pubitemid 129638129)
10. Hutloff, A., Dittrich, A. M., Beier, K. C., Eljaschewitsch, B., Kraft, R., Anagnostopoulos, I. and Kroczek, R. A., ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999. 397: 263-266.
11. Todd, J. A. and Wicker, L. S., Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity 2001. 15: 387-395.
12. Ueda, H., Howson, J.M., Esposito, L., Heward, J., Snook, H., Chamberlain, G., Rainbow, D. B. et al., Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 2003. 423: 506-511. (Pubitemid 36648570)
13. Lenschow, D. J., Ho, S. C., Sattar, H., Rhee, L., Gray, G., Nabavi, N., Herold, K. C. et al., Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 1995. 181: 1145-1155.
14. Lenschow, D. J., Herold, K. C., Rhee, L., Patel, B., Koons, A., Qin, H. Y., Fuchs, E. et al., CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 1996. 5: 285-293.
15. Salomon, B., Lenschow, D. J., Rhee, L., Ashourian, N., Singh, B., Sharpe, A. and Bluestone, J. A., B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000. 12: 431-440.
16. Luhder, F., Hoglund, P., Allison, J. P., Benoist, C. and Mathis, D., Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes. J. Exp. Med. 1998. 187: 427-432.
17. Ansari, M. J., Salama, A. D., Chitnis, T., Smith, R. N., Yagita, H., Akiba, H., Yamazaki, T. et al., The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J. Exp. Med. 2003. 198: 63-69.
18. Ansari, M. J., Fiorina, P., Dada, S., Guleria, I., Ueno, T., Yuan, X., Trikudanathan, S. et al., Role of ICOS pathway in autoimmune and alloimmune responses in NOD mice. Clin. Immunol. 2008. 126: 140-147.
19. Nanji, S. A., Hancock,W.W., Luo, B., Schur, C. D., Pawlick, R. L., Zhu, L. F., Anderson, C. C. et al., Costimulation blockade of both inducible costimulator and CD40 ligand induces dominant tolerance to islet allografts and prevents spontaneous autoimmune diabetes in the NOD mouse. Diabetes 2006. 55: 27-33. (Pubitemid 43343296)
20. Hawiger, D., Tran, E., Du,W., Booth, C. J.,Wen, L., Dong, C. and Flavell, R. A., ICOS mediates the development of insulin-dependent diabetes mellitus in nonobese diabetic mice. J. Immunol. 2008. 180: 3140-3147.
21. Herman, A. E., Freeman, G. J., Mathis, D. and Benoist, C., CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 2004. 199: 1479-1489.
22. Tafuri, A., Shahinian, A., Bladt, F., Yoshinaga, S. K., Jordana, M., Wakeham, A., Boucher, L. M. et al., ICOS is essential for effective T-helper-cell responses. Nature 2001. 409: 105-109.
23. Rottman, J. B., Smith, T., Tonra, J. R., Ganley, K., Bloom, T., Silva, R., Pierce, B. et al., The costimulatory molecule ICOS plays an important role in the immunopathogenesis of EAE. Nat. Immunol. 2001. 2: 605-611.
24. Dong, C., Juedes, A. E., Temann, U. A., Shresta, S., Allison, J. P., Ruddle, N. H. and Flavell, R. A., ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 2001. 409: 97-101.
25. McAdam, A. J., Greenwald, R. J., Levin, M. A., Chernova, T., Malenkovich, N., Ling, V., Freeman, G. J. et al., ICOS is critical for CD40-mediated antibody class switching. Nature 2001. 409: 102-105. (Pubitemid 32098633)
26. Gigoux, M., Shang, J., Pak, Y., Xu, M., Choe, J., Mak, T.W. and Suh, W. K., Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. USA 2009. 106: 20371-20376.
27. Serreze, D. V., Fleming, S. A., Chapman, H. D., Richard, S. D., Leiter, E. H. and Tisch, R. M., B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 1998. 161: 3912-3918.
28. Noorchashm, H., Noorchashm, N., Kern, J., Rostami, S. Y., Barker, C. F. and Naji, A., B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes 1997. 46: 941-946. (Pubitemid 27220992)
29. Serreze, D. V., Chapman, H. D., Varnum, D. S., Hanson, M. S., Reifsnyder, P. C., Richard, S. D., Fleming, S. A. et al., B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J. Exp. Med. 1996. 184: 2049-2053.
30. Hu, Y., Nakagawa, Y., Purushotham, K. R. and Humphreys-Beher, M. G., Functional changes in salivary glands of autoimmune disease-prone NOD mice. Am. J. Physiol. 1992. 263: E607-E614.
31. Many, M. C., Maniratunga, S. and Denef, J. F., The non-obese diabetic (NOD) mouse: an animal model for autoimmune thyroiditis. Exp. Clin. Endocrinol. Diabetes 1996. 104: 17-20.
32. Oldenborg, P. A., Gresham, H. D., Chen, Y., Izui, S. and Lindberg, F. P., Lethal autoimmune hemolytic anemia in CD47-deficient nonobese diabetic (NOD) mice. Blood 2002. 99: 3500-3504.
33. Rivero, V. E., Cailleau, C., Depiante-Depaoli, M., Riera, C. M. and Carnaud, C., Non-obese diabetic (NOD) mice are genetically susceptible to experimental autoimmune prostatitis (EAP). J. Autoimmun. 1998. 11: 603-610. (Pubitemid 29016118)
34. Salomon, B., Rhee, L., Bour-Jordan, H., Hsin, H., Montag, A., Soliven, B., Arcella, J. et al., Development of spontaneous autoimmune peripheral polyneuropathy in B7-2-deficient NOD mice. J. Exp. Med. 2001. 194: 677-684.
35. Robinson, C. P., Yamachika, S., Bounous, D. I., Brayer, J., Jonsson, R., Holmdahl, R., Peck, A. B. et al., A novel NOD-derived murine model of primary Sjogren's syndrome. Arthritis Rheum. 1998. 41: 150-156. (Pubitemid 28041933)
36. Girvin, A. M., Dal Canto, M. C., Rhee, L., Salomon, B., Sharpe, A., Bluestone, J. A. and Miller, S. D., A critical role for B7/CD28 costimulation in experimental autoimmune encephalomyelitis: a comparative study using costimulatory molecule-deficient mice and monoclonal antibody blockade. J. Immunol. 2000. 164: 136-143.
37. Louvet, C., Kabre, B. G., Davini, D. W., Martinier, N., Su, M. A., DeVoss, J. J., Rosenthal, W. L. et al., A novel myelin P0-specific T cell receptor transgenic mouse develops a fulminant autoimmune peripheral neuropathy. J. Exp. Med. 2009. 206: 507-514.
38. Mak, T.W., Shahinian, A., Yoshinaga, S. K.,Wakeham, A., Boucher, L. M., Pintilie, M., Duncan, G. et al., Costimulation through the inducible costimulator ligand is essential for both T helper and B cell functions in T cell-dependent B cell responses. Nat. Immunol. 2003. 4: 765-772.
39. Halbout, P., Briand, J. P., Becourt, C., Muller, S. and Boitard, C., T cell response to preproinsulin I and II in the nonobese diabetic mouse. J. Immunol. 2002. 169: 2436-2443. (Pubitemid 34920987)
40. Boitard, C., Yasunami, R., Dardenne, M. and Bach, J. F., T cell-mediated inhibition of the transfer of autoimmune diabetes in NOD mice. J. Exp. Med. 1989. 169: 1669-1680.