Induction of tolerance in type 1 diabetes via both CD4+CD25 + T regulatory cells and T regulatory type 1 cells

Diabetes

Volumn 55, Issue 6, 2006, Pages 1571-1580

  Battaglia, Manuela ^a   Stabilini, Angela ^a   Draghici, Elena ^b   Migliavacca, Barbara ^a   Gregori, Silvia ^a   Bonifacio, Ezio ^b   Roncarolo, Maria Grazia ^a,c  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

CFSE, carboxyfluorescein diacetate succinimidyl ester; FACS, fluorescence activated cell sorting; ICAM, intracellular adhesion molecule; IFN , interferon; IL, interleukin; mAb, monoclonal antibody; TGF, transforming growth factor

Indexed keywords

CYTOKINE; INTERLEUKIN 10; RAPAMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; MOUSE; NONHUMAN; PANCREAS FUNCTION; PRIORITY JOURNAL; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOKINES; DIABETES MELLITUS, TYPE 1; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED NOD; PANCREAS; POLYMERASE CHAIN REACTION; SIROLIMUS; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 33746368487     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db05-1576     Document Type: Article

References (43)

1. Stiller CR, Dupre J, Gent M, Jenner MR, Keown PA, Laupacis A, Martell R, Rodger NW, von Graffenried B, Wolfe BM: Effects of cyclosporine immunosuppression in insulin-dependent diabetes mellitus of recent onset. Science 223:1362-1367, 1984
2. Kahan BD, Camardo JS: Rapamycin: clinical results and future opportunities. Transplantation 72:1181-1193, 2001
3. Sehgal SN: Rapamune (RAPA, rapamycin, sirolimus): mechanism of action immunosuppressive effect results from blockade of signal transduction and inhibition of cell cycle progression. Clin Biochem 31:335-340, 1998
4. Roncarolo MG, Bacchetta R, Bordignon C, Narula S, Levings MK: Type 1 T regulatory cells. Immunol Rev 182:68-79, 2001
5. Shevach EM: CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2:389-400, 2002
6. Bacchetta R, Bigler M, Touraine JL, Parkman R, Tovo PA, Abrams J, de Waal Malefyt R, de Vries JE, Roncarolo MG: High levels of interleukin 10 production in vivo are associated with tolerance in SCID patients transplanted with HLA mismatched hematopoietic stem cells. J Exp Med 179:493-502, 1994
7. Cavani A, Nasorri F, Prezzi C, Sebastiani S, Albanesi C, Girolomoni G: Human CD4+ T lymphocytes with remarkable regulatory functions on dendritic cells and nickel-specific Th1 immune responses. J Invest Dermatol 114:295-302, 2000
8. Zuany-Amorim C, Sawicka E, Manlius C, Le Moine A, Brunet LR, Kemeny DM, Bowen G, Rook G, Walker C: Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat Med 8:625-629, 2002
9. Battaglia M, Gianfrani C, Gregori S, Roncarolo MG: IL-10-producing T regulatory type 1 cells and oral tolerance. Ann N Y Acad Sci 1029:142-153, 2004
10. Bluestone JA, Abbas AK: Natural versus adaptive regulatory T cells. Nat Rev Immunol 3:253-257, 2003
11. Delovitch TL, Singh B: The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7:727-738, 1997
12. Lyons AB, Parish CR: Determination of lymphocyte division by flow cytometry. J Immunol Methods 171:131-137, 1994
13. Gregori S, Giarratana N, Smiroldo S, Adorini L: Dynamics of pathogenic and suppressor T cells in development of autoimmune diabetes. J Immunol 171:4040-4047, 2003
14. Roncarolo MG, Battaglia M, Gregori S: The role of interleukin 10 in the control of autoimmunity. J Autoimmun 20:269-272, 2003
15. Rabinovitch A, Suarez-Pinzon WL, Shapiro AM, Rajotte RV, Power R: Combination therapy with sirolimus and interleukin-2 prevents spontaneous and recurrent autoimmune diabetes in NOD mice. Diabetes 51:638-645, 2002
16. Powrie F, Leach MW, Mauze S, Caddle LB, Coffman RL: Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5:1461-1471, 1993
17. Chen C, Lee WH, Yun P, Snow P, Liu CP: Induction of autoantigen-specific Th2 and Tr1 regulatory T cells and modulation of autoimmune diabetes. J Immunol 171:733-744, 2003
18. Blaha P, Bigenzahn S, Koporc Z, Schmid M, Langer F, Selzer E, Bergmeister H, Wrba F, Kurtz J, Kiss C, Roth E, Muehlbacher F, Sykes M, Wekerle T: The influence of immunosuppressive drugs on tolerance induction through bone marrow transplantation with costimulation blockade. Blood 101:2886-2893, 2003
19. Monk NJ, Hargreaves RE, Marsh JE, Farrar CA, Sacks SH, Millrain M, Simpson E, Dyson J, Jurcevic S: Fc-dependent depletion of activated T cells occurs through CD40L-specific antibody rather than costimulation blockade. Nat Med 9:1275-1280, 2003
20. Zheng XX, Sanchez-Fueyo A, Sho M, Domenig C, Sayegh MH, Strom TB: Favorably tipping the balance between cytopathic and regulatory T cells to create transplantation tolerance. Immunity 19:503-514, 2003
21. Tian L, Lu L, Yuan Z, Lamb JR, Tam PK: Acceleration of apoptosis in CD4+CD8+ thymocytes by rapamycin accompanied by increased CD4+CD25+ T cells in the periphery. Transplantation 77:183-189, 2004
22. Battaglia M, Stabilini A, Roncarolo MG: Rapamycin selectively expands CD4+CD25+FOXP3+ regulatory T cells. Blood 105:4743-4748, 2005
23. Green EA, Choi Y, Flavell RA: Pancreatic lymph node-derived CD4(+)CD25(+) Treg cells: highly potent regulators of diabetes that require TRANCE-RANK signals. Immunity 16:183-191, 2002
24. 3 analog enhances regulatory T-cells and arrests autoimmune diabetes in NOD mice. Diabetes 51:1367-1374, 2002
25. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L: TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 9:1202-1208, 2003
26. Peng Y, Laouar Y, Li MO, Green EA, Flavell RA: 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 101:4572-4577, 2004
27. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM: 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 198:1875-1886, 2003
28. Zheng SG, Wang JH, Gray JD, Soucier H, Horwitz DA: 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 172:5213-5221, 2004
29. Wogensen L, Lee MS, Sarvetnick N: Production of interleukin 10 by islet cells accelerates immune-mediated destruction of beta cells in nonobese diabetic mice. J Exp Med 179:1379-1384, 1994
30. Balasa B, La Cava A, Van Gunst K, Mocnik L, Balakrishna D, Nguyen N, Tucker L, Sarvetnick N: A mechanism for IL-10-mediated diabetes in the nonobese diabetic (NOD) mouse: ICAM-1 deficiency blocks accelerated diabetes. J Immunol 165:7330-7337, 2000
31. van de Stolpe A, van der Saag PT: Intercellular adhesion molecule-1. J Mol Med 74:13-33, 1996
32. Hasegawa Y, Yokono K, Taki T, Amano K, Tominaga Y, Yoneda R, Yagi N, Maeda S, Yagita H, Okumura K, et al.: Prevention of autoimmune insulin-dependent diabetes in non-obese diabetic mice by anti-LFA-1 and anti-ICAM-1 mAb. Int Immunol 6:831-838, 1994
33. Fabien N, Bergerot I, Orgiazzi J, Thivolet C: Lymphocyte function associated antigen-1, integrin alpha 4, and Lselectin mediate T-cell homing to the pancreas in the model of adoptive transfer of diabetes in NOD mice. Diabetes 45:1181-1186, 1996
34. Cameron MJ, Arreaza GA, Grattan M, Meagher C, Sharif S, Burdick MD, Strieter RM, Cook DN, Delovitch TL: Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J Immunol 165:1102-1110, 2000
35. Sarween N, Chodos A, Raykundalia C, Khan M, Abbas AK, Walker LS: CD4+CD25+ cells controlling a pathogenic CD4 response inhibit cytokine differentiation, CXCR-3 expression, and tissue invasion. J Immunol 173:2942-2951, 2004
36. Ninova D, Dean PG, Stegall MD: Immunomodulation through inhibition of multiple adhesion molecules generates resistance to autoimmune diabetes in NOD mice. J Autoimmun 23:201-209, 2004
37. Kim SH, Cleary MM, Fox HS, Chantry D, Sarvetnick N: CCR4-bearing T cells participate in autoimmune diabetes. J Clin Invest 110:1675-1686, 2002
38. Groux H: Type 1 T-regulatory cells: their role in the control of immune responses. Transplantation 75:8S-12S, 2003
39. Battaglia M, Stabilini A, Draghici E, Gregori S, Mocchetti C, Bonifacio E, Roncarolo MG: Rapamycin and interleukin-10 treatment induces T regulatory type 1 cells that mediate antigen-specific transplantation tolerance. Diabetes 55:40-49, 2006
40. Li Y, Li XC, Zheng XX, Wells AD, Turka LA, Strom TB: Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat Med 5:1298-1302, 1999
41. Taylor PA, Lees CJ, Wilson JM, Ehrhardt MJ, Campbell MT, Noelle RJ, Blazar BR: Combined effects of calcineurin inhibitors or sirolimus with anti-CD40L mAb on alloengraftment under nonmyeloablative conditions. Blood 100:3400-3407, 2002
42. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A, Bluestone JA: B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431-440, 2000
43. Goudy KS, Burkhardt BR, Wasserfall C, Song S, Campbell-Thompson ML, Brusko T, Powers MA, Clare-Salzler MJ, Sobel ES, Ellis TM, Flotte TR, Atkinson MA: Systemic overexpression of IL-10 induces CD4+CD25+ cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol 171:2270-2278, 2003