In vivo diabetogenic action of CD4+ T lymphocytes requires Fas expression and is independent of IL-1 and IL-18

European Journal of Immunology

Volumn 41, Issue 5, 2011, Pages 1344-1351

  Wen, Li ^a   Green, Elizabeth A ^b   Stratmann, Thomas ^c   Panosa, Anaïs ^d   Gomis, Ramon ^c   Eynon, Elizabeth E ^a   Flavell, Richard A ^a   Mezquita, Jovita A ^c   Mora, Conchi ^d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF BARCELONA   (Spain)

^d UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Autoimmune diabetes; B cell apoptosis; CD4+ T cells; Fas

Indexed keywords

FAS ANTIGEN; INTERLEUKIN 18; INTERLEUKIN 1BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL DAMAGE; DIABETOGENESIS; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD95; CD4-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FAS LIGAND PROTEIN; GENOTYPE; INSULIN-SECRETING CELLS; INTERLEUKIN-18; INTERLEUKIN-1BETA; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC;

EID: 79955158277     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041216     Document Type: Article

References (40)

1. Delovitch, T. L. and Singh, B., The nonobese diabetic mouse as a model of autoimmune diabetes: dysregulation gets the NOD. Immunity 1997. 7: 727-738.
2. Itoh, N., Imagawa, A., Hanafusa, T., Waguri, M., Yamamoto, K., Iwasahi, H., Moriwaki, M. et al., Requirement of Fas for the Development of Autoimmune Diabetes in Nonobese Diabetic Mice. J. Exp. Med. 1997. 186: 613-618.
3. Kagi, D., Odermatt, B., Seiler, P., Zinkernagel, R. M., Mak, T. W. and Hengartner, H., Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice. J. Exp. Med. 1997. 186: 989-997.
4. Heitmeier, M. R., Scarin, A. L. and Corbett, J. A., Interferon-γ increases the sensitivity of islets of Langerhans for inducible nitric-oxide synthase expression induced by interleukin 1. J. Biol. Chem. 1997. 272: 13697-13704.
5. Darville, M. I. and Eizirik, D. L., Cytokine induction of Fas gene expression in insulin-producing cells requires the transcription factors NF-kappaB and C/EBP. Diabetes 2001. 50: 1741-1748.
6. Yamada, K., Takane-Gyotoku, X., Yuan, X., Ichikawa, F., Inada, C. and Nonaka, K., Mouse islet cell lysis mediated by interleukin-1-induced Fas. Diabetologia 1996. 39: 1306-1312.
7. Augstein, P., Bahr, J., Wachlin, G., Heinke, P., Berg, S., Salzsieder, E. and Harrison, L. C., Cytokines activate caspase-3 in insulinoma cells of diabetes-prone NOD mice directly and via upregulation of Fas. J. Autoimmun. 2004. 23: 301-309.
8. Amrani, A., Verdaguer, J., Thiessen, S., Bou, S. and Santamaria, P., IL-1 alpha, IL-1 beta, and IFN-gamma mark beta cells for Fas-dependent destruction by diabetogenic CD4 (+) T lymphocytes. J. Clin. Invest. 2000. 105: 459-468.
9. Jun, H.-S., Yoon, C.-S., Zbytnuik, L., van Rooijen, N. and Yoon, J.-W., The role of macrophages in T-cell mediated autoimmune diabetes in Non Obese Diabetic mice. J. Exp. Med. 1999. 189: 347-358.
10. Suarez-Pinzón, W., Sorensen, O., Bleackley, R. C., Elliot, J. F., Rajotte, R. V. and Rabinovitch, A., Beta.cell destruction in NOD mice correlates with Fas (CD95) expression on beta cells and pro-inflammatory cytokine expression in islets. Diabetes 1999. 48: 21-28.
11. Zumsteg, U., Frigerio, S. and Hollander, G. A., Nitric oxide production and Fas surface expression mediate two independent pathways of cytokine-induced murine beta-cell damage. Diabetes 2000. 49: 39-47.
12. Kurrer, M. O., Pakala, S. V., Hanson, H. L. and Katz, J. D., β Cell Apoptosis in T-cell-mediated Autoimmune Diabetes. Proc. Natl. Acad. Sci. USA 1997. 94: 213-218.
13. Dhein, J., Walczak, H., Baumler, C., Debatin, K. M. and Krammer, P. H., Autocrine T cell suicide mediated by APO-1/(Fas/CD95). Nature 1995. 375: 78-81.
14. Chervonsky, A. V., Wang, Y., Wong, F. S., Visintin, I., Flavell, R. A., Janeway Jr, C. A. and Matis, L. A., The role of Fas in autoimmune diabetes. Cell 1997. 89: 17-24.
15. Su, X., Hu, Q., Kristan, J. M., Costa, C., Shen, Y., Gero, D., Matis, L. A. and Wang, Y., Significant role for Fas in the pathogenesis of autoimmune diabetes. J. Immunol. 2000. 164: 2523-2532.
16. Savinov, A. Y., Tcherepanov, A., Green, E. A., Flavell, R.A. and Chervonsky, A. V., Contribution of Fas to diabetes development. Proc. Natl. Acad. Sci. USA 2003. 100: 628-632.
17. Allison, J., Thomas, H. E., Catterall, T., Kay, T. W. and Strasser, A., Transgenic expression of dominant-negative Fas-associated death domain protein in beta cells protects against Fas ligand-induced apoptosis and reduces spontaneous diabetes in nonobese diabetic mice. J. Immunol. 2005. 175: 293-301.
18. Silva, D. G., Petrovsky, N., Socha, L., Slattery, R., Gatenby, P. and Charlton, B., Mechanisms of accelerated immune-mediated diabetes resulting from islet beta cell expression of a Fas ligand transgene. J. Immunol. 2003. 170: 4996-5002.
19. Mora, C., Wong, F. S., Chang, C. H. and Flavell, R. A., Pancreatic infiltration but not diabetes occurs in the relative absence of MHC Class II- restricted CD4 T cells: studies using NOD/CIITA-deficient mice. J. Immunol. 1999. 162: 4576-4588.
20. Thomas, H. E., Darwiche, R., Corbett, J. A. and Kay, T. W., Evidence that beta cell death in the nonobese diabetic mouse is Fas independent. J. Immunol. 1999. 163: 1562-1569.
21. Apostolou, I., Hao, Z., Rajewsky, K. and von Boehmer, H., Effective destruction of Fas-deficient insulin-producing beta cells in type 1 diabetes. J. Exp. Med. 2003. 198: 1103-1106.
22. Angstetra, E., Graham, K. L., Emmett, S., Dudek, N. L., Darwiche, R., Ayala-Perez, R., Allison, J. et al., In vivo effects of cytokines on pancreatic beta-cells in models of type I diabetes dependent on CD4 (+) T lymphocytes. Immunol. Cell Biol. 2009. 87: 178-185.
23. Vence, L., Benoist, C. and Mathis, D., Fas deficiency prevents Type 1 Diabetes by inducing hyporesponsiveness in islet-cell reactive T cells. Diabetes 2004. 53: 2797-2803.
24. Adachi, M., Watanabe-Fukunaga, R. and Nagata, S., Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Proc. Natl. Acad. Sci. USA 1990. 90: 1756-1760.
25. Kim, S., Kim, K. A., Hwang, D. Y., Lee, T. H., Kayagaki, N., Yagita, H. and Lee, M. S., Inhibition of autoimmune diabetes by Fas ligand: the paradox is solved. J. Immunol. 2000. 164: 2931-2936.
26. Kikutani, H. and Makino, S., The murine autoimmune diabetes model: NOD and related strains. Adv. Immunol. 1992. 51: 285-322.
27. Takahashi, T., Tanaka, M., Brannan, C. I., Jenkins, N. A., Copeland, N. G., Suda, T. and Nagata, S., Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 1994. 76: 969-976.
28. Fukunaga, R., Brannan, C. I., Itoh, N., Yonehara, S., Copeland, N. G., Jenkins, N. A. and Nagata, S., The cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen. J Immunol. 1992. 148: 1274-1279.
29. Kuida, K., Lippke, J. A., Ku, G., Harding, M. W., Livingston, D. J., Su, M. S. and Flavell, R. A., Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 1995. 267: 2000-2003.
30. Schott, W. H., Haskell, B. D., Tse, H. M., Milton, M. J., Piganelli, J. D., Choisy-Rossy, C. M., Reifsnyder, P. C. et al., Caspase-1 is not required for type 1 diabetes in the NOD mouse. Diabetes 2004. 53: 99-104.
31. Redd, S., Ginn, S. and Ross, J. M., Fas and Fas ligand immunolocalization in pancreatic islets of NOD mice during spontaneous and cyclophosphamide-accelerated diabetes. Histochem. J. 2002. 34: 1-12.
32. Darwiche, R., Chong, M. M., Santamaria, P., Thomas, H. E. and Kay, T. W., Fas is detectable on beta cells in accelerated, but not spontaneous, diabetes in nonobese diabetic mouse. J. Immunol. 2003. 170: 6292-6297.
33. Nakayama, M., Nagata, M., Yasuda, H., Arisawa, K., Kotani, R., Yamada, K. and Chowdhury, S. A., Fas/Fas ligand interactions play an essential role in the initiation of murine autoimmune diabetes. Diabetes 2002. 51: 1391-1397.
34. Thomas, H. E., Irawaty, W., Darwiche, R., Brodnicki, T. C., Santamaria, P., Allison, J. and Kay, T. W., IL-1 receptor deficiency slows progression to diabetes in the NOD mouse. Diabetes 2004. 53: 113-121.
35. Sandberg, J. O., Eizirik, D. L. and Sandler, S., IL-1 receptor antagonist inhibits recurrence of disease after syngeneic pancreatic islet transplantation to spontaneously diabetic non-obese diabetic (NOD) mice. Clin. Exp. Immunol. 1997. 108: 314-317.
36. KB repressor. J. Biol. Chem. 2000. 275: 36509-36513.
37. Téllez, N., Montolio, M., Biarnes, M., Castaño, E., Soler, J. and Montanya, E., Adenoviral overexpression of interleukin-1 receptor antagonist protein increases beta-cell replication in rat pancreatic islets. Gene Ther. 2005. 12: 120-128.
38. Mandrup-Poulsen, T., Pickersgill, L. and Donath, M. Y., Blockade of interleukin 1 in type 1 diabetes mellitus. Nat. Rev. Endocrinol. 2010. 6: 158-166.
39. Zheng, H., Fletcher, D., Kozak, W., Jiang, M., Hofmann, K. J., Conn, C. A., Soszynski, D. et al., Resistance to fever induction and impaired acute-phase response in interleukin-1β-deficient mice. Immunity 1995. 3: 9-19.
40. Blunt, T., Gell, D., Fox, M., Taccioli, G. E., Lehmann, A. R., Jackson, S. P. and Jeggo, P. A., Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc Natl Acad Sci USA 1996. 93: 10285-10290.