CD8+ CD122+ PD-1-effector cells promote the development of diabetes in NOD mice

Journal of Leukocyte Biology

Volumn 97, Issue 1, 2015, Pages 111-120

  Arndt, Borge ^a   Witkowski, Lukas ^a   Ellwart, Joachim ^b   Seissler, Jochen ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Autoimmunity; Inflammation; Insulitis; T cells

Indexed keywords

INTERLEUKIN 2 RECEPTOR BETA; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD122; PROGRAMMED DEATH 1 RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL INFILTRATION; CONTROLLED STUDY; DIABETES MELLITUS; EFFECTOR CELL; FEMALE; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOID ORGAN; MONONUCLEAR CELL; MOUSE; MOUSE STRAIN; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPLEEN CELL; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; FLOW CYTOMETRY; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; NONOBESE DIABETIC MOUSE;

MUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FEMALE; FLOW CYTOMETRY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NOD; PREDIABETIC STATE; T-LYMPHOCYTE SUBSETS;

EID: 84925285316     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlt.3A0613-344RR     Document Type: Article

References (43)

1. Atkinson, M. A., Leiter, E. H. (1999) The NOD mouse model of type 1 diabetes: as good as it gets? Nat. Med. 5, 601-604.
2. Anderson, M. S., Blucstone, J. A. (2005) The NOD mouse: a model of immune dysrcgulation. Annu. Rev. Immunol. 23, 447-485.
3. Wong, F. S., Visintin, I., Wen, L., FlavelL R. A., Janeway. Jr., C. A. (1996) CD8 T cell clones from young nonobcse diabetic (NÓD) Inlets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells.J. Exp. Med. 183, 67-76.
4. Brodie, G. M., Wallberg, M., Santamaria, P., Wong, F. S., Green, E. A. (2008) B-Cells promote intra-islet CD8+ ototoxic T-cell survival to enhance type 1 diabetes. Diabetes 57, 909-917.
5. DiLorenzo, T. P., Graser, R. T., Ono, T., Christianson, G. J., Chapman, H. D., Roopcnian, D. C., Nathenson, S. G., Scrrczc, D. V. (1998) Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobcse diabetic mice and use a prevalent T cell receptor alpha chain gene rearrangement. Proc. Nall Acad. Sri. USA 95, 12538-12543.
6. Emamaullce, J. A., Davis, J., Mcrani, S., Toso, C., Elliott, J. F., Thicscn, A., Shapiro, A. M. (2009) Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 58, 1302-1311.
7. Grinberg-Bleyer, Y., Baevens, A., You, S., Elhage, R., Fourcadc, G., Gregoire, S., Cagnard, N., Carpentier, W., Tang, Q., Bluestone, J., Chatenoud, L., Klatzmann, D., Salomon, B. L., Piaggio, E. (2010) IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatorv T cells. J. Exp. Med. 207, 1871-1878.
8. Tang, Q. Adams, J. Y., Penaranda, C. Melli, K., Piaggio, E., Sgouroudis, E., Piccirillo, C. A., Salomon, B. L., Bluestone, J. A. (2008) Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28, 687-697.
9. Bendelae A., Camaud, C., Boitard, C., Bach, J. F. (1987) Syngeneic transfer of autoimmune diabetes from diabetic NOD mice to healthy neonates. Requirement for both L3T4+ and Lyt-2+ T cells. J. Exp. Med. 166, 823-832.
10. Bedossa, P., Bcndelac, A., Bach, J. F., Camaud, C. (1989) Syngeneic T cell transfer of diabetes into NOD newborn mice: in situ studies of the autoimmune steps leading to insulin-producing cell destruction. Eur, J. Immunol 19, 1947-1951.
11. Miller, B. J., Appel, M. C., O'Neil, J. J., Wicker, L. S. (1988) Both the Lvt-2+ and L3T4+ T cell subsets arc required for the transfer of diabetes in nonobcse diabetic mice. J. Immunol. 140, 52-58.
12. Varey, A. M., Hutchings, P., O'Reilly, L., Hussell, T., Waldmann, H., Simpson, E., Cooke, A. (1991) The development of insulin-dependent diabetes mcllitus in non-obese diabetic mice: the role of CD4+ and CD8+ T cells. Biochem. Soc. Trans. 19, 187-191.
13. Peterson, J. D., Haskins, K. (1996) Transfer of diabetes in the NOD-scid mouse bv CD4 T-cell clones. Differential requirement for CD8 T-cells. Diabetes 45, 328-336.
14. Phillips, J. M., Haskins, K., Cooke, A. (2005) MAdCAM-1 is needed for diabetes development mediated bv the T cell clone. BDC-2.5. Immunology 116, 525-531.
15. Wang, B., Gonzalez, A., Benoist, C., Mathis, D. (1996) The role of CD8+ T cells in the initiation of insulin-dependent diabetes mcllitus. Eur, J. Immunol. 26, 1762-1769.
16. Walzer T., Arpin C., Beloeil L., Marvel J. (2002) Differential in vivo persistence of two subsets of memory phenotype CDS T cells defined bv CD44 and CD122 expression levels. J. Immunol. 168, 2704-2711.
17. Zhang, X., Sun, S., Hwang, I., Tough, D. F., Sprent.J. (1998) Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo bv IL-15 Immunity 8, 591-599.
18. Judge, A. D., Zhang, X., Fujii, H., Surh C. D., Sprent J. (2002) Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J. Exp. Med. 196, 935-946.
19. Takayama E., Seki S., Ohkawa T., Ami K., Habu Y., Yamaguchi T., Tadakuma T, Hiraide H. (2000) Mouse CD8+ CD122+ T cells with intermediate TCR increasing with age provide a source of early IEN gamma production. J. Immunol. 164, 5652-5658.
20. Motegi A., Kinoshita M., Inatsu A., Habu, Y., Saitoh, D. Seki, S. (2008) IL-15-induccd CDS+CD122+ T cells increase antibacterial and anti-tumor immune responses: implications for immune function in aged mice. J Leukoc. Biol. 84, 1047-1056.
21. Rifa'i, M., Kawamoto, Y., Nakashima, I., Suzuki, H. (2004) Essential roles of CD8+CD122+ regulatorv T cells in the maintenance of T cell homeostasis. J. Exp. Med. 200, 1123-1134.
22. Saitoh, O., Abiru, N., Nakahara, M., Nagayama, Y. (2007) CD8+CD122+ T cells, a newly identified regulatory T subset, negatively regulate Graves' hyperthyroidism in a murine model. Endocrinology 148, 6040-6046.
23. Endharti, A. T., Okuno, Y., Shi, Z., Misawa, N., Tovokuni, S., Ito, M., Isobe, K., Suzuki, H. (2011) CD8+CD122+ regulatory T cells (Tregs) and CD4+ Tregs cooperativelv prevent and cure CD4+ cell-induced colitis. J. Immunol. 186, 41-52.
24. Arndt, B., Kalinski, T., Rcinhold, D., Thielitz, A., Roessner, A., Schraven, B., Simeoni. L, (2013) Cooperative immunoregulatory function of the transmembrane adaptor proteins SIT and LAX. J. Leuhr. Biol. 93. 353-362.
25. Arndt, B., Poltorak, M., Kowtharapu, B. S., Reichardt, P., Philipsen, I., Lindquist, J. A., Schraven, B., Simeoni, L. (2013) Analysis of TCR activation kinetics in primary human T cells upon focal or soluble stimulation. J. Immunol. Methods 387, 276-283.
26. Ohly, P., Dohle, C., Abel.J., Seissler, J., Gleichmann, H. (2000) Zinc sulphate induces mctallothionein in pancreatic islets of mice and protects against diabetes induced by multiple low doses of streptozotocin. Diabetologia 43, 1020-1030.
27. Berzins, S. P., Venanzi, E. S., Benoist, C., Mathis, D. (2003) T-Cell compartments of prediabetic NOD mice. Diabetes 52, 327-334.
28. Dai, H., Wan, N., Zhang, S., Moore, Y., Wan, F., Dai, Z., (2010) Cutting edge: programmed death-1 defines CD8+CD122+ T cells as regulatory versus memory T cells. J. Immunol. 185, 803-807.
29. Groom, J. R., Luster, A. D. (2011) CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 89, 207-215.
30. Oghumu, S., Dong, R., Varikuti, S., Shawler, T., Kampfrath, T., Terrazas, C. A., Lezama-Davila, C., Ahmer, B. M., Whitaere. C, C., Rajagopalan, S., Locksley, R., Sharpe, A. H., Satoskar, A. R. (2013) Distinct populations of innate CDS+ T cells revealed in a CXCR3 reporter mouse. J. Immunol. 190, 2229-2240.
31. Sato, K., Kinoshita, M., Motegi, A., Habu, Y., Takavama, E., Nonoyama, S., Hiraide, H., Seki, S. (2005) Critical role of the liver CDS+ CD122+ T cells in the generalized Shwartzman reaction of mice. Eur, J. Immunol. 35, 593-602.
32. Rifa'i, M., Shi, Z., Zhang, S. Y., Lee, Y. H., Shika, H., Isobe, K., Suzuki, H. (2008) CD8+CD122+ regulatory T cells recognize activated T cells via conventional MHC class I-alphabetaTCR interaction and become IL-10- producing active regulatory cells. Int. ImmunoL 20, 937-947.
33. Endharti, A. T., Rifa'i, M., Shi, Z., Fukuoka, Y., Nakahara, Y., Kawamoto, Y., Takeda, K., Isobe, K., Suzuki, H. (2005) Cutdng edge: CD8+CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. J. ImmunoL 175, 7093-7097.
34. Shamcli, A., Yamanouchi, J., Tsai, S., Yang, Y., Clcmcnte-Casares, X., Moore, A., Serra, P., Santamaria, P. (2013) ILr2 promotes the function of memory-like autorcgulatory CD8+ T cells but suppresses their development via FoxP3r Treg cells. Eur, J. ImmunoL 43, 394-403.
35. Yamanouchi, J., Rainbow, D., Serra, P., Howlett, S., Hunter, K., Gamer, V. E., Gonzalez-M unoz, A., Clark, J., Veijola, R., Cubbon, R., Chen, S. L., Rosa, R., Cumiskcy, A. M., Serreze, D. V., Gregory, S., Rogers, J., Lyons, P. A., Healy, B., Smink, L. J., Todd, J. A., Peterson, L. B., Wicker, L. S., Santamaria, P. (2007) Intcrleukin-2 gene variation impairs regulatory T cell funcüon and causes autoimmunity'. Sat. Genet. 39, 329-337.
36. Beilke, J. N., Meagher, C. T., Hosiawa, K., Champsaur, M., Bluestone, J. A., Lanier, L. L. (2012) NK cells are not required for spontaneous autoimmune diabetes in NOD mice. PLoS ONE 7, e36011.
37. Campanella, G. S., Grimm, J., Manice, L. A., Colvin, R. A., Medoff, B. D., Wojtkiewicz, G. R., Weissleder, R., Luster, A. D. (2006) Oligomerization of CXCL10 is necessary for endothelial cell presentation and in vivo activity. J. ImmunoL 177,6991-6998.
38. Cole, K. E., Strick, C. A., Paradis, T. J., Ogborne, K. T., Loetscher, M., Gladue, R. P., Lin, W., Boyd, J. G., Moser, B., Wood, D. E., Sahagan, B. G., Neote, K. (1998) Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J. Exp. Med. 187, 2000-2021.
39. Loetschcr, M., Loetscher, P., Brass, N., Meesc, E., Moser, B. (1998) Lymphocyte-specific chemokine receptor CXCR3: regulation, chemokine binding and gene localization. Eur, J. ImmunoL 28, 3696-3705.
40. Lu, B., Humbles, A., Bota, D., Gerard, C., Moser, B., Soler, D., Luster, A D., Gerard, N. P. (1999) Structure and function of the murine chemokine receptor CXCR3. Eur, J. ImmunoL 29, 3804-3812.
41. Frigerio, S., Junt, T., Lu, B., Gerard, C., Zumsteg, U., Hollander, G. .V, Piali, L. (2002) Beta cells arc responsible for CXCR3-mcdiated T cell infiltration in insulitis. Slut. Med. 8, 1414-1420.
42. Rhode, A., Pauza, M. E., Barral, A. M., Rodrigo, E., Oldstonc, M. B., von Herrath, M. G., Christen, U. (2005) Islet-specific expression of CXCL10 causes spontaneous islet infiltration and accelerates diabetes development. J. ImmunoL 175, 3516-3524.
43. Tanaka, S., Nishida, Y., Aida, K., Maruyama, T., Shimada, A., Suzuki, M., Shimura, H., Takizawa, S., Takahashi, M., Akiyama, D., Arai-Yamashita, S., Furuya, F., Kawaguchi, A, Kaneshige, M., Katoh, R., Endo, T., Kobayashi, T. (2009) Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated beta-cell failure in fulminant type 1 diabetes. Diabetes 58, 2285-2291.