CD4+CD25+ regulatory T cells prevent type 1 diabetes preceded by dendritic cell-dominant invasive insulitis by affecting chemotaxis and local invasiveness of dendritic cells

Journal of Immunology

Volumn 185, Issue 4, 2010, Pages 2493-2501

  Lee, Mi Heon ^a   Lee, Wen Hui ^a   Todorov, Ivan ^a   Liu, Chih Pin ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL INVASION; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; DIABETOGENESIS; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; TISSUE DISTRIBUTION; ADOPTIVE TRANSFER; ANIMAL; CELL MOTION; FLOW CYTOMETRY; IMMUNOLOGY; IMPAIRED GLUCOSE TOLERANCE; INFLAMMATION; METABOLISM; NATURAL KILLER CELL; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PATHOLOGY; T LYMPHOCYTE; TIME; TRANSGENIC MOUSE; TRANSPLANTATION;

GLYCOPROTEIN P 15095; INTERLEUKIN 2 RECEPTOR ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD11C; CELL MOVEMENT; CHEMOKINE CCL19; CHEMOKINE CCL21; CHEMOTAXIS; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; FLOW CYTOMETRY; INFLAMMATION; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; ISLETS OF LANGERHANS; KILLER CELLS, NATURAL; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PREDIABETIC STATE; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TIME FACTORS;

EID: 77956931125     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001036     Document Type: Article

References (50)

1. Bach, J. F. 1994. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15: 516-542.
2. Robles, D. T., G. S. Eisenbarth, N. J. Dailey, L. B. Peterson, and L. S. Wicker. 2003. Insulin autoantibodies are associated with islet inflammation but not always related to diabetes progression in NOD congenic mice. Diabetes 52: 882-886.
3. Sakaguchi, S., and F. Powrie. 2007. Emerging challenges in regulatory T cell function and biology. Science 317: 627-629.
4. Herman, A. E., G. J. Freeman, D. Mathis, and C. Benoist. 2004. CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 199: 1479-1489.
5. Tang, Q., K. J. Henriksen, M. Bi, E. B. Finger, G. Szot, J. Ye, E. L. Masteller, H. McDevitt, M. Bonyhadi, and J. A. Bluestone. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199: 1455-1465.
6. Tarbell, K. V., S. Yamazaki, K. Olson, P. Toy, and R. M. Steinman. 2004. CD25+ CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199: 1467-1477.
7. Brusko, T. M., C. H. Wasserfall, M. J. Clare-Salzler, D. A. Schatz, and M. A. Atkinson. 2005. Functional defects and the influence of age on the frequency of CD4+ CD25+ T-cells in type 1 diabetes. Diabetes 54: 1407-1414.
8. Lindley, S., C. M. Dayan, A. Bishop, B. O. Roep, M. Peakman, and T. I. Tree. 2005. Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes 54: 92-99.
9. Tritt, M., E. Sgouroudis, E. d'Hennezel, A. Albanese, and C. A. Piccirillo. 2008. Functional waning of naturally occurring CD4+ regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes 57: 113-123.
10. Jansen, A., F. Homo-Delarche, H. Hooijkaas, P. J. Leenen, M. Dardenne, and H. A. Drexhage. 1994. Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and beta-cell destruction in NOD mice. Diabetes 43: 667-675.
11. Rosmalen, J. G., T. Martin, C. Dobbs, J. S. Voerman, H. A. Drexhage, K. Haskins, and P. J. Leenen. 2000. Subsets of macrophages and dendritic cells in nonobese diabetic mouse pancreatic inflammatory infiltrates: correlation with the development of diabetes. Lab. Invest. 80: 23-30.
12. Shinomiya, M., S. Nadano, H. Shinomiya, and M. Onji. 2000. In situ characterization of dendritic cells occurring in the islets of nonobese diabetic mice during the development of insulitis. Pancreas 20: 290-296.
13. Saxena, V., J. K. Ondr, A. F. Magnusen, D. H. Munn, and J. D. Katz. 2007. The countervailing actions of myeloid and plasmacytoid dendritic cells control autoimmune diabetes in the nonobese diabetic mouse. J. Immunol. 179: 5041-5053.
14. Martin, A. P., S. Rankin, S. Pitchford, I. F. Charo, G. C. Furtado, and S. A. Lira. 2008. Increased expression of CCL2 in insulin-producing cells of transgenic mice promotes mobilization of myeloid cells from the bone marrow, marked insulitis, and diabetes. Diabetes 57: 3025-3033.
15. von Boehmer, H. 2005. Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6: 338-344.
16. Serra, P., A. Amrani, J. Yamanouchi, B. Han, S. Thiessen, T. Utsugi, J. Verdaguer, and P. Santamaria. 2003. CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity 19: 877-889. (Pubitemid 37542307)
17. Houot, R., I. Perrot, E. Garcia, I. Durand, and S. Lebecque. 2006. Human CD4+ CD25high regulatory T cells modulate myeloid but not plasmacytoid dendritic cells activation. J. Immunol. 176: 5293-5298.
18. Tadokoro, C. E., G. Shakhar, S. Shen, Y. Ding, A. C. Lino, A. Maraver, J. J. Lafaille, and M. L. Dustin. 2006. Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 203: 505-511.
19. Tang, Q., J. Y. Adams, A. J. Tooley, M. Bi, B. T. Fife, P. Serra, P. Santamaria, R. M. Locksley, M. F. Krummel, and J. A. Bluestone. 2006. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 7: 83-92.
20. Yamazaki, S., K. Inaba, K. V. Tarbell, and R. M. Steinman. 2006. Dendritic cells expand antigen-specific Foxp3+ CD25+ CD4+ regulatory T cells including suppressors of alloreactivity. Immunol. Rev. 212: 314-329.
21. Zhang, N., B. Schröppel, G. Lal, C. Jakubzick, X. Mao, D. Chen, N. Yin, R. Jessberger, J. C. Ochando, Y. Ding, and J. S. Bromberg. 2009. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 30: 458-469.
22. Haskins, K., and M. McDuffie. 1990. Acceleration of diabetes in young NOD mice with a CD4+ islet-specific T cell clone. Science 249: 1433-1436. (Pubitemid 20341909)
23. Katz, J. D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74: 1089-1100.
24. Chen, Z., A. E. Herman, M. Matos, D. Mathis, and C. Benoist. 2005. Where CD4+ CD25+ T reg cells impinge on autoimmune diabetes. J. Exp. Med. 202: 1387-1397.
25. Lee, M. H., W.-H. Lee, Y. Van, C. H. Contag, and C.-P. Liu. 2007. Image-guided analyses reveal that non-CD4 splenocytes contribute to CD4+ T cell-mediated inflammation leading to islet destruction by altering their local function and not systemic trafficking patterns. Mol. Imaging 6: 369-383.
26. Chen, C., W.-H. Lee, P. Yun, P. Snow, and C.-P. Liu. 2003. Induction of autoantigen-specific Th2 and Tr1 regulatory T cells and modulation of autoimmune diabetes. J. Immunol. 171: 733-744. (Pubitemid 36871383)
27. You, S., C. Chen, W.-H. Lee, C.-H. Wu, V. Judkowski, C. Pinilla, D. B. Wilson, and C.-P. Liu. 2003. Detection and characterization of T cells specific for BDC2.5 T cell-stimulating peptides. J. Immunol. 170: 4011-4020.
28. Contag, P. R., I. N. Olomu, D. K. Stevenson, and C. H. Contag. 1998. Bioluminescent indicators in living mammals. Nat. Med. 4: 245-247.
29. Tang, Q., and M. F. Krummel. 2006. Imaging the function of regulatory T cells in vivo. Curr. Opin. Immunol. 18: 496-502.
30. Onishi, Y., Z. Fehervari, T. Yamaguchi, and S. Sakaguchi. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA 105: 10113-10118.
31. Feuerer, M., Y. Shen, D. R. Littman, C. Benoist, and D. Mathis. 2009. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 31: 654-664.
32. Shultz, L. D., P. A. Schweitzer, S. W. Christianson, B. Gott, I. B. Schweitzer, B. Tennent, S. McKenna, L. Mobraaten, T. V. Rajan, D. L. Greiner, et al. 1995. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 154: 180-191.
33. Serreze, D. V., H. R. Gaskins, and E. H. Leiter. 1993. Defects in the differentiation and function of antigen presenting cells in NOD/Lt mice. J. Immunol. 150: 2534-2543.
34. Jansen, A., M. van Hagen, and H. A. Drexhage. 1995. Defective maturation and function of antigen-presenting cells in type 1 diabetes. Lancet 345: 491-492.
35. Alard, P., J. N. Manirarora, S. A. Parnell, J. L. Hudkins, S. L. Clark, and M. M. Kosiewicz. 2006. Deficiency in NOD antigen-presenting cell function may be responsible for suboptimal CD4+CD25+ T-cell-mediated regulation and type 1 diabetes development in NOD mice. Diabetes 55: 2098-2105.
36. Judkowski, V., C. Pinilla, K. Schroder, L. Tucker, N. Sarvetnick, and D. B. Wilson. 2001. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol. 166: 908-917.
37. Rossi, D., and A. Zlotnik. 2000. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18: 217-242.
38. Giarratana, N., G. Penna, S. Amuchastegui, R. Mariani, K. C. Daniel, and L. Adorini. 2004. A vitamin D analog down-regulates proinflammatory chemokine production by pancreatic islets inhibiting T cell recruitment and type 1 diabetes development. J. Immunol. 173: 2280-2287.
39. Raine, T., P. Zaccone, P. Mastroeni, and A. Cooke. 2006. Salmonella typhimurium infection in nonobese diabetic mice generates immunomodulatory dendritic cells able to prevent type 1 diabetes. J. Immunol. 177: 2224-2233.
40. Martin, A. P., T. Marinkovic, C. Canasto-Chibuque, R. Latif, J. C. Unkeless, T. F. Davies, Y. Takahama, G. C. Furtado, and S. A. Lira. 2009. CCR7 deficiency in NOD mice leads to thyroiditis and primary hypothyroidism. J. Immunol. 183: 3073-3080.
41. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33.
42. Gunn, M. D., S. Kyuwa, C. Tam, T. Kakiuchi, A. Matsuzawa, L. T. Williams, and H. Nakano. 1999. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189: 451-460.
43. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Förster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21: 279-288.
44. Tang, Q., J. Y. Adams, C. Penaranda, K. Melli, E. Piaggio, E. Sgouroudis, C. A. Piccirillo, B. L. Salomon, and J. A. Bluestone. 2008. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28: 687-697.
45. Cantor, J., and K. Haskins. 2005. Effector function of diabetogenic CD4 Th1 T cell clones: a central role for TNF-alpha. J. Immunol. 175: 7738-7745.
46. Cantor, J., and K. Haskins. 2007. Recruitment and activation of macrophages by pathogenic CD4 T cells in type 1 diabetes: evidence for involvement of CCR8 and CCL1. J. Immunol. 179: 5760-5767.
47. Ghiringhelli, F., C. Ménard, M. Terme, C. Flament, J. Taieb, N. Chaput, P. E. Puig, S. Novault, B. Escudier, E. Vivier, et al. 2005. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J. Exp. Med. 202: 1075-1085.
48. Terme, M., N. Chaput, B. Combadiere, A. Ma, T. Ohteki, and L. Zitvogel. 2008. Regulatory T cells control dendritic cell/NK cell cross-talk in lymph nodes at the steady state by inhibiting CD4+ self-reactive T cells. J. Immunol. 180: 4679-4686.
49. Melli, K., R. S. Friedman, A. E. Martin, E. B. Finger, G. Miao, G. L. Szot, M. F. Krummel, and Q. Tang. 2009. Amplification of autoimmune response through induction of dendritic cell maturation in inflamed tissues. J. Immunol. 182: 2590-2600.
50. Rivas-Caicedo, A., G. Soldevila, T. I. Fortoul, A. Castell- Rodríguez, L. Flores-Romo, and E. A. García-Zepeda. 2009. Jak3 is involved in dendritic cell maturation and CCR7-dependent migration. PLoS ONE 4: e7066.