Converting antigen-specific diabetogenic CD4 and CD8 T cells to TGF-beta producing non-pathogenic regulatory cells following FoxP3 transduction

Journal of Autoimmunity

Volumn 28, Issue 4, 2007, Pages 188-200

  Peng, Jian ^a   Dicker, Bridget ^a   Du, Wei ^a   Tang, Fengjuan ^a   Nguyen, Phuong ^b   Geiger, Terrence ^b   Wong, F Susan ^c   Wen, Li ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Diabetes; FoxP3; NOD mice; T cells; TGF

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DIABETOGENESIS; EX VIVO STUDY; FEMALE; GENETIC TRANSDUCTION; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FORKHEAD TRANSCRIPTION FACTORS; GENE THERAPY; INSULIN; MICE; MICE, INBRED NOD; MICE, SCID; RETROVIRIDAE; TRANSDUCTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 34248593473     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2007.02.015     Document Type: Article

References (45)

1. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4 (2003) 330-336
2. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299 (2003) 1057-1061
3. Khattri R., Cox T., Yasayko S.A., and Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 4 (2003) 337-342
4. Wraith D.C., Nicolson K.S., and Whitley N.T. Regulatory CD4+ T cells and the control of autoimmune disease. Curr Opin Immunol 16 (2004) 695-701
5. Gombert J.M., Herbelin A., Tancrede-Bohin E., Dy M., Carnaud C., and Bach J.F. Early quantitative and functional deficiency of NK1+-like thymocytes in the NOD mouse. Eur J Immunol 26 (1996) 2989-2998
6. Kukreja A., Cost G., Marker J., Zhang C., Sun Z., Lin-Su K., et al. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 109 (2002) 131-140
7. Pop S.M., Wong C.P., Culton D.A., Clarke S.H., and Tisch R. Single cell analysis shows decreasing FoxP3 and TGFbeta1 coexpressing CD4+CD25+ regulatory T cells during autoimmune diabetes. J Exp Med 201 (2005) 1333-1346
8. 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 199 (2004) 1479-1489
9. Tang Q., Henriksen K.J., Bi M., Finger E.B., Szot G., Ye J., et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 199 (2004) 1455-1465
10. Tarbell K.V., Yamazaki S., Olson K., Toy P., and Steinman R.M. CD25+CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J Exp Med 199 (2004) 1467-1477
11. Weber S.E., Harbertson J., Godebu E., Mros G.A., Padrick R.C., Carson B.D., et al. Adaptive islet-specific regulatory CD4 T cells control autoimmune diabetes and mediate the disappearance of pathogenic Th1 cells in vivo. J Immunol 176 (2006) 4730-4739
12. Battaglia M., Stabilini A., Draghici E., Gregori S., Mocchetti C., Bonifacio E., et al. Rapamycin and interleukin-10 treatment induces T regulatory type 1 cells that mediate antigen-specific transplantation tolerance. Diabetes 55 (2006) 40-49
13. Battaglia M., Stabilini A., Draghici E., Migliavacca B., Gregori S., Bonifacio E., et al. Induction of tolerance in type 1 diabetes via both CD4+CD25+ T regulatory cells and T regulatory type 1 cells. Diabetes 55 (2006) 1571-1580
14. Nakamura K., Kitani A., and Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 194 (2001) 629-644
15. Piccirillo C.A., Letterio J.J., Thornton A.M., McHugh R.S., Mamura M., Mizuhara H., et al. CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness. J Exp Med 196 (2002) 237-246
16. Green E.A., Gorelik L., McGregor C.M., Tran E.H., and Flavell R.A. CD4+CD25+ T regulatory cells control anti-islet CD8+ T cells through TGF-beta-TGF-beta receptor interactions in type 1 diabetes. Proc Natl Acad Sci U S A 100 (2003) 10878-10883
17. Peng Y., Laouar Y., Li M.O., Green E.A., and Flavell R.A. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc Natl Acad Sci U S A 101 (2004) 4572-4577
18. Fahlen L., Read S., Gorelik L., Hurst S.D., Coffman R.L., Flavell R.A., et al. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J Exp Med 201 (2005) 737-746
19. Oida T., Xu L., Weiner H.L., Kitani A., and Strober W. TGF-beta-mediated suppression by CD4+CD25+ T cells is facilitated by CTLA-4 signaling. J Immunol 177 (2006) 2331-2339
20. Chai J.G., Xue S.A., Coe D., Addey C., Bartok I., Scott D., et al. Regulatory T cells, derived from naive CD4+CD25- T cells by in vitro Foxp3 gene transfer, can induce transplantation tolerance. Transplantation 79 (2005) 1310-1316
21. Albert M.H., Liu Y., Anasetti C., and Yu X.Z. Antigen-dependent suppression of alloresponses by Foxp3-induced regulatory T cells in transplantation. Eur J Immunol 35 (2005) 2598-2607
22. Loser K., Hansen W., Apelt J., Balkow S., Buer J., and Beissert S. In vitro-generated regulatory T cells induced by Foxp3-retrovirus infection control murine contact allergy and systemic autoimmunity. Gene Ther 12 (2005) 1294-1304
23. Jaeckel E., von Boehmer H., and Manns M.P. Antigen-specific FoxP3-transduced T-cells can control established type 1 diabetes. Diabetes 54 (2005) 306-310
24. Nguyen P., and Geiger T.L. Antigen-specific targeting of CD8+ T cells with receptor-modified T lymphocytes. Gene Ther 10 (2003) 594-604
25. Wong F.S., Visintin I., Wen L., Flavell R.A., and Janeway Jr. C.A. 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 183 (1996) 67-76
26. Wong F.S., Karttunen J., Dumont C., Wen L., Visintin I., Pilip I.M., et al. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat Med 5 (1999) 1026-1031
27. Birebent B., Lorho R., Lechartier H., de Guibert S., Alizadeh M., Vu N., et al. Suppressive properties of human CD4+CD25+ regulatory T cells are dependent on CTLA-4 expression. Eur J Immunol 34 (2004) 3485-3496
28. Read S., Greenwald R., Izcue A., Robinson N., Mandelbrot D., Francisco L., et al. Blockade of CTLA-4 on CD4+CD25+ regulatory T cells abrogates their function in vivo. J Immunol 177 (2006) 4376-4383
29. Shimizu J., Yamazaki S., Takahashi T., Ishida Y., and Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 3 (2002) 135-142
30. Kishimoto H., and Sprent J. A defect in central tolerance in NOD mice. Nat Immunol 2 (2001) 1025-1031
31. Strid J., Lopes L., Marcinkiewicz J., Petrovska L., Nowak B., Chain B.M., et al. A defect in bone marrow derived dendritic cell maturation in the nonobesediabetic mouse. Clin Exp Immunol 123 (2001) 375-381
32. Grohmann U., Fallarino F., Bianchi R., Orabona C., Vacca C., Fioretti M.C., et al. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J Exp Med 198 (2003) 153-160
33. Zucchelli S., Holler P., Yamagata T., Roy M., Benoist C., and Mathis D. Defective central tolerance induction in NOD mice: genomics and genetics. Immunity 22 (2005) 385-396
34. Anderson M.S., and Bluestone J.A. The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 23 (2005) 447-485
35. Gambineri E., Torgerson T.R., and Ochs H.D. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol 15 (2003) 430-435
36. Ochs H.D., Ziegler S.F., and Torgerson T.R. FOXP3 acts as a rheostat of the immune response. Immunol Rev 203 (2005) 156-164
37. Bacchetta R., Passerini L., Gambineri E., Dai M., Allan S.E., Perroni L., et al. Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J Clin Invest 116 (2006) 1713-1722
38. Chen Z., Herman A.E., Matos M., Mathis D., and Benoist C. Where CD4+CD25+ T reg cells impinge on autoimmune diabetes. J Exp Med 202 (2005) 1387-1397
39. You S., Belghith M., Cobbold S., Alyanakian M.A., Gouarin C., Barriot S., et al. Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes 54 (2005) 1415-1422
40. Alard P., Manirarora J.N., Parnell S.A., Hudkins J.L., Clark S.L., and Kosiewicz M.M. 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 (2006) 2098-2105
41. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198 (2003) 1875-1886
42. Fantini M.C., Becker C., Monteleone G., Pallone F., Galle P.R., and Neurath M.F. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 172 (2004) 5149-5153
43. Schramm C., Huber S., Protschka M., Czochra P., Burg J., Schmitt E., et al. TGFbeta regulates the CD4+CD25+ T-cell pool and the expression of Foxp3 in vivo. Int Immunol 16 (2004) 1241-1249
44. Zheng S.G., Wang J.H., Gray J.D., Soucier H., and Horwitz D.A. Natural and induced CD4+CD25+ cells educate CD4+CD25- cells to develop suppressive activity: the role of IL-2, TGF-beta, and IL-10. J Immunol 172 (2004) 5213-5221
45. Marie J.C., Letterio J.J., Gavin M., and Rudensky A.Y. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J Exp Med 201 (2005) 1061-1067