Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice

Journal of Experimental Medicine

Volumn 204, Issue 1, 2007, Pages 191-201

  Tarbell, Kristin V ^a   Petit, Lucine ^a   Zuo, Xiaopan ^a   Toy, Priscilla ^a   Luo, Xunrong ^b,c   Mqadmi, Amina ^a   Yang, Hua ^b   Suthanthiran, Manikkam ^b   Mojsov, Svetlana ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; L SELECTIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DENDRITIC CELL; DIABETES MELLITUS; DISEASE COURSE; FEMALE; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULITIS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

ANIMALS; BLOOD GLUCOSE; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; INSULIN; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; ISLETS OF LANGERHANS; L-SELECTIN; MALE; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PREDIABETIC STATE; T-LYMPHOCYTES, REGULATORY;

EID: 33846410255     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061631     Document Type: Article

References (50)

1. Shoda, L.K., D.L. Young, S. Ramanujan, C.C. Whiting, M.A. Atkinson, J.A. Bluestone, G.S. Eisenbarth, D. Mathis, A.A. Rossini, S.E. Campbell, et al. 2005. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity. 23:115-126.
2. Herold, K.C., W. Hagopian, J.A. Auger, E. Poumian-Ruiz, L. Taylor, D. Donaldson, S.E. Gitelman, D.M. Harlan, D. Xu, R.A. Zivin, and J.A. Bluestone. 2002. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 346:1692-1698.
3. Chatenoud, L., E. Thervet, J. Primo, and J.F. Bach. 1994. Anti-CD3 antibody induces long-term remission of overt autoimmunity in non-obese diabetic mice. Proc. Natl. Acad. Sci. USA. 91:123-127.
4. Luo, X., H. Yang, I.S. Kim, F. Saint-Hilaire, D.A. Thomas, B.P. De, E. Ozkaynak, T. Muthukumar, W.W. Hancock, R.G. Crystal, and M. Suthanthiran. 2005. Systemic transforming growth factor-beta1 gene therapy induces Foxp3+ regulatory cells, restores self-tolerance, and facilitates regeneration of beta cell function in overtly diabetic non-obese diabetic mice. Transplantation. 79:1091-1096.
5. Ogawa, N., J.F. List, J.F. Habener, and T. Maki. 2004. Cure of overt diabetes in NOD mice by transient treatment with anti-lymphocyte serum and exendin-4. Diabetes. 53:1700-1705.
6. Bresson, D., L. Togher, E. Rodrigo, Y. Chen, J.A. Bluestone, K.C. Herold, and M. von Herrath. 2006. Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J. Clin. Invest. 116:1371-1381.
7. Keymeulen, B., E. Vandemeulebroucke, A.G. Ziegler, C. Mathieu, L. Kaufman, G. Hale, F. Gorus, M. Goldman, M. Walter, S. Candon, et al. 2005. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 352:2598-2608.
8. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198:235-247.
9. + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199:1467-1477.
10. + regulatory T cells by dendritic cells during the mixed leukocyte reaction. Proc. Natl. Acad. Sci. USA. 103:2758-2763.
11. 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.
12. 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.
13. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor foxp3. Science. 299:1057- 1061.
14. 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 auto immune diabetes. J. Exp. Med. 199:1455-1465.
15. Masteller, E.L., M.R. Warner, Q. Tang, K.V. Tarbell, H. McDevitt, and J.A. Bluestone. 2005. Expansion of functional endogenous antigen-specific CD4+CD25+ regulatory T cells from nonobese diabetic mice. J. Immunol. 175:3053-3059.
16. Jaeckel, E., H. von Boehmer, and M.P. Manns. 2005. Antigen-specific FoxP3-transduced T-cells can control established type 1 diabetes. Diabetes. 54:306-310.
17. + splenocytes that delays adoptive transfer of diabetes expresses l-selectin and high levels of CCR7. J. Immunol. 169:2461-2465.
18. You, S., G. Slehoffer, S. Barriot, J.F. Bach, and L. Chatenoud. 2004. Unique role of CD4+CD62L+ regulatory T cells in the control of autoimmune diabetes in T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA. 101:14580-14585.
19. Hoglund, P., J. Mintern, C. Waltzinger, W. Heath, C. Benoist, and D. Mathis. 1999. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 189:331-339.
20. Turley, S., L. Poirot, M. Hattori, C. Benoist, and D. Mathis. 2003. Physiological β cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198:1527-1537.
21. 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 non-obese diabetic mice. Nat. Immunol. 7:83-92.
22. Gregori, S., N. Giarratana, S. Smiroldo, and L. Adorini. 2003. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J. Immunol. 171:4040-4047.
23. Pop, S.M., C.P. Wong, D.A. Culton, S.H. Clarke, and R. Tisch. 2005. Single cell analysis shows decreasing FoxP3 and TGFβ1 coexpressing CD4+CD25+ regulatory T cells during autoimmune diabetes. J. Exp. Med. 201:1333-1346.
24. Berzins, S.P., E.S. Venanzi, C. Benoist, and D. Mathis. 2003. T-cell compartments of prediabetic NOD mice. Diabetes. 52:327-334.
25. Andre, I., A. Gonzalez, B. Wang, J. Katz, C. Benoist, and D. Mathis. 1996. Checkpoints in the progression of autoimmune disease: lessons from diabetes models. Proc. Natl. Acad. Sci. USA. 93:2260-2263.
26. Mojsov, S., G.C. Weir, and J.F. Habener. 1987. Insulinotropin: glucagon-like peptide 1 [7-37] co-encoded in the glucagon gene is a potent stimulator of insulin release in the perfused rat pancreas. J. Clin. Invest. 79:616-619.
27. Nathan, D.M., E. Screiber, H. Fogel, S. Mojsov, and J.F. Habener. 1992. Insulinotropic actions of glucagon-like peptide-I [7-37] administered to diabetic and non-diabetic human subjects. Diabetes Care. 15:270-276.
28. Gutniak, M., C. Orskov, J.J. Holst, B. Ahren, and S. Efendic. 1992. Antidiabetogenic effect of glucagon-like peptide-I [7-36] amide in normal subjects and patients with diabetes mellitus. N. Engl. J. Med. 326:1316-1322.
29. Li, Y., T. Hansotia, B. Yusta, F. Ris, P.A. Halban, and D.J. Drucker. 2003. Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J. Biol. Chem. 278:471-478.
30. Xu, G., D.A. Stoffers, J.F. Habener, and S. Bonner-Weir. 1999. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes. 48:2270-2276.
31. Amrani, A., S. Durant, M. Throsby, J. Coulaud, M. Dardenne, and F. Homo-Delarche. 1998. Glucose homeostasis in the nonobese diabetic mouse at the prediabetic stage. Endocrinology. 139:1115-1124.
32. Achenbach, P., K. Koczwara, A. Knopff , H. Naserke, A.G. Ziegler, and E. Bonifacio. 2004. Mature high-affinity immune responses to (pro)insulin anticipate the autoimmune cascade that leads to type 1 diabetes. J. Clin. Invest. 114:589-597.
33. Gianani, R., and G.S. Eisenbarth. 2005. The stages of type 1A diabetes: 2005. Immunol. Rev. 204:232-249.
34. Couper, J.J., I. Hudson, G.A. Werther, G.L. Warne, J.M. Court, and L.C. Harrison. 1991. Factors predicting residual beta-cell function in the first year after diagnosis of childhood type 1 diabetes. Diabetes Res. Clin. Pract. 11:9-16.
35. + regulatory T cells. J. Immunol. 170:3939-3943.
36. Liu, H., B. Hu, D. Xu, and F.Y. Liew. 2003. CD4+CD25+ regulatory T cells cure murine colitis: the role of IL-10, TGF-beta, and CTLA4. J. Immunol. 171:5012-5017.
37. McGeachy, M.J., L.A. Stephens, and S.M. Anderton. 2005. Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. J. Immunol. 175:3025-3032.
38. Naftanel, M.A., and D.M. Harlan. 2004. Pancreatic islet transplantation. PLoS Med. 1:e58.
39. Egan, J.M., A. Bulotta, H. Hui, and R. Perfetti. 2003. GLP-1 receptor agonists are growth and differentiation factors for pancreatic islet beta cells. Diabetes Metab. Res. Rev. 19:115-123.
40. Yang, Z., M. Chen, J.D. Carter, C.S. Nunemaker, J.C. Garmey, S.D. Kimble, and J.L. Nadler. 2006. Combined treatment with lisofylline and exendin-4 reverses autoimmune diabetes. Biochem. Biophys. Res. Commun. 344:1017-1022.
41. Deacon, C.F., A.H. Johnsen, and J.J. Holst. 1995. Degradation of glucagon-like peptide-1 by human plasma in vitro yields an N-terminally truncated peptide that is a major endogenous metabolite in vivo. J. Clin. Endocrinol. Metab. 80:952-957.
42. Rooman, I., and L. Bouwens. 2004. Combined gastrin and epidermal growth factor treatment induces islet regeneration and restores normoglycaemia in C57Bl6/J mice treated with alloxan. Diabetologia. 47:259-265.
43. Brand, S.J., S. Tagerud, P. Lambert, S.G. Magil, K. Tatarkiewicz, K. Doiron, and Y. Yan. 2002. Pharmacological treatment of chronic diabetes by stimulating pancreatic beta-cell regeneration with systemic co-administration of EGF and gastrin. Pharmacol. Toxicol. 91:414-420.
44. + regulatory T cells responsible for protection against diabetes. Proc. Natl. Acad. Sci. USA. 101:4572-4577.
45. + regulatory T cells in the regional lymph node. J. Exp. Med. 202:771-781.
46. Hori, S., M. Haury, J.J. Lafaille, J. Demengeot, and A. Coutinho. 2002. Peripheral expansion of thymus-derived regulatory cells in antimyelin basic protein T cell receptor transgenic mice. Eur. J. Immunol. 32:3729-3735.
47. - cells to develop suppressive activity: the role of IL-2, TGF-β, and IL-10. J. Immunol. 172:5213-5221.
48. Waldmann, H., E. Adams, P. Fairchild, and S. Cobbold. 2006. Infectious tolerance and the long-term acceptance of transplanted tissue. Immunol. Rev. 212:301-313.
49. + regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172:6003-6010.
50. Bisikirska, B., J. Colgan, J. Luban, J.A. Bluestone, and K.C. Herold. 2005. TCR stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8+CD25+ Tregs. J. Clin. Invest. 115:2904-2913.