Treg-therapy allows mixed chimerism and transplantation tolerance without cytoreductive conditioning

American Journal of Transplantation

Volumn 10, Issue 4, 2010, Pages 751-762

  Pilat, N ^a   Baranyi, U ^a   Klaus, C ^a   Jaeckel, E ^b   Mpofu, N ^b   Wrba, F ^a   Golshayan, D ^c   Muehlbacher, F ^a   Wekerle, T ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Mixed chimerism; Tolerance; Transplantation

Indexed keywords

ABATACEPT; CD40 LIGAND MONOCLONAL ANTIBODY; GREEN FLUORESCENT PROTEIN; RAPAMYCIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BONE MARROW TRANSPLANTATION; CELL POPULATION; CELL PROLIFERATION; CHIMERA; CONTROLLED STUDY; CYTOREDUCTIVE CONDITIONING; FEMALE; GRAFT SURVIVAL; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SKIN GRAFT; SURVIVAL TIME; TRANSPLANTATION TOLERANCE;

ADAPTIVE IMMUNITY; ANIMALS; BASE SEQUENCE; CELL TRANSPLANTATION; CHIMERA; DNA PRIMERS; FEMALE; LYMPHOCYTE CULTURE TEST, MIXED; MICE; MICE, INBRED STRAINS; POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION CONDITIONING;

EID: 77949852097     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2010.03018.x     Document Type: Article

References (50)

1. Wekerle T, Sykes M. Mixed chimerism and transplantation tolerance. Annu Rev Med 2001 52 : 353 370.
2. Sykes M, Szot GL, Swenson K, Pearson DA. Induction of high levels of allogeneic hematopoietic reconstitution and donor-specific tolerance without myelosuppressive conditioning. Nat Med 1997 3 : 783 787.
3. Wekerle T, Sayegh MH, Hill J et al. Extrathymic T cell deletion and allogeneic stem cell engraftment induced with costimulatory blockade is followed by central T cell tolerance. J Exp Med 1998 187 : 2037 2044.
4. Wekerle T, Kurtz J, Ito H et al. Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment. Nat Med 2000 6 : 464 469.
5. Shirasugi N, Adams AB, Durham MM et al. Prevention of chronic rejection in murine cardiac allografts: A comparison of chimerism- and nonchimerism-inducing costimulation blockade-based tolerance induction regimens. J Immunol 2002 169 : 2677 2684.
6. Blaha P, Bigenzahn S, Koporc Z et al. The influence of immunosuppressive drugs on tolerance induction through bone marrow transplantation with costimulation blockade. Blood 2003 101 : 2886 2893.
7. Domenig C, Sanchez-Fueyo A, Kurtz J et al. Roles of deletion and regulation in creating mixed chimerism and allograft tolerance using a nonlymphoablative irradiation-free protocol. J Immunol 2005 175 : 51 60.
8. Hamby K, Trexler A, Pearson TC, Larsen CP, Rigby MR, Kean LS. NK cells rapidly reject allogeneic bone marrow in the spleen through a perforin- and Ly49D-dependent, but NKG2D-independent mechanism. Am J Transplant 2007 7 : 1884 1896.
9. Kawai T, Cosimi AB, Spitzer TR et al. HLA-mismatched renal transplantation without maintenance immunosuppression. N Engl J Med 2008 358 : 353 361.
10. Ildstad ST, Sachs DH. Reconstitution with syngeneic plus allogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature 1984 307 : 168 170.
11. Joffre O, Santolaria T, Calise D et al. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med 2008 14 : 88 92.
12. Westerhuis G, Maas WGE, Willemze R, Toes REM, Fibbe WE. Long-term mixed chimerism after immunologic conditioning and MHC-mismatched stem-cell transplantation is dependent on NK-cell tolerance. Blood 2005 106 : 2215 2220.
13. Graca L, Daley S, Fairchild P, Cobbold S, Waldmann H. Co-receptor and co-stimulation blockade for mixed chimerism and tolerance without myelosuppressive conditioning. BMC Immunol 2006 7 : 9.
14. Durham MM, Bingaman AW, Adams AB et al. Administration of anti-CD40 ligand and donor bone marrow leads to hematopoietic chimerism and donor-specific tolerance without cytoreductive conditioning. J Immunol 2000 165 : 1 4.
15. Lambert JF, Colvin GA, Zhong S et al. H2-mismatched transplantation with repetitive cell infusions and CD40 ligand antibody infusions without myeloablation. Br J Haematol 2002 119 : 155 163.
16. Jaeckel E, von Boehmer H, Manns M. Antigen-specific Foxp3 transduced T cells can control established Type 1 diabetes. Diabetes 2005 54 : 306 310.
17. Tsang JY, Tanriver Y, Jiang S et al. Conferring indirect allospecificity on CD4+CD25+ Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest 2008 118 : 3619 3628.
18. Golshayan D, Jiang S, Tsang J, Garin MI, Mottet C, Lechler RI. In vitro-expanded donor alloantigen-specific CD4+CD25+ regulatory T cells promote experimental transplantation tolerance. Blood 2007 109 : 827 835.
19. + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003 9 : 1144 1150.
20. Cohen JL, Trenado A, Vasey D, Klatzmann D, Salomon BL. CD4+CD25+ immunoregulatory T cells: New therapeutics for graft-versus-host disease. J Exp Med 2002 196 : 401 406.
21. Bluestone JA, Thomson AW, Shevach EM, Weiner HL. What does the future hold for cell-based tolerogenic therapy? Nat Rev Immunol 2007 7 : 650 654.
22. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25 +regulatory T cells. Nat Immunol 2003 4 : 330 336.
23. Allan SE, Alstad AN, Merindol N et al. Generation of potent and stable human CD4+ T regulatory cells by activation-independent expression of FOXP3. Mol Ther 2008 16 : 194 202.
24. Allan SE, Passerini L, Bacchetta R et al. The role of 2 FOXP3 isoforms in the generation of human CD4+ Tregs. J Clin Invest 2005 115 : 3276 3284.
25. Fu S, Zhang N, Yopp AC et al. TGF-beta induces Foxp3 + T-regulatory cells from CD4+ CD25- precursors. Am J Transplant 2004 4 : 1614 1627.
26. DiPaolo RJ, Brinster C, Davidson TS, Andersson J, Glass D, Shevach EM. Autoantigen-specific TGFbeta-induced Foxp3+ regulatory T cells prevent autoimmunity by inhibiting dendritic cells from activating autoreactive T cells. J Immunol 2007 179 : 4685 4693.
27. Schiopu A, Wood KJ. Regulatory T cells: Hypes and limitations. Curr Opin Organ Transplant 2008 13 : 333 338.
28. Williams MA, Trambley J, Ha J et al. Genetic characterization of strain differences in the ability to mediate CD40/CD28-independent rejection of skin allografts. J Immunol 2000 165 : 6849 6857.
29. - T cells by in vitro Foxp3 gene transfer, can induce transplantation tolerance. Transplantation 2005 79 : 1310 1316.
30. Zeiser R, Leveson-Gower DB, Zambricki EA et al. Differential impact of mammalian target of rapamycin inhibition on CD4+CD25+Foxp3+ regulatory T cells compared with conventional CD4 +T cells. Blood 2008 111 : 453 462.
31. Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005 105 : 4743 4748.
32. Thomson AW, Turnquist HR, Raimondi G. Immunoregulatory functions of mTOR inhibition. Nat Rev Immunol 2009 9 : 324 337.
33. Down JD, Ploemacher RE. Transient and permanent engraftment potential of murine hematopoietic stem cell subsets: Differential effects of host conditioning with gamma radiation and cytotoxic drugs. Exp Hematol 1993 21 : 913 921.
34. Chan WF, Razavy H, Luo B, Shapiro AM, Anderson CC. Development of either split tolerance or robust tolerance along with humoral tolerance to donor and third-party alloantigens in nonmyeloablative mixed chimeras. J Immunol 2008 180 : 5177 5186.
35. Lu L-F, Lind EF, Gondek DC et al. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 2006 442 : 997 1002.
36. Bigenzahn S, Blaha P, Koporc Z et al. The role of non-deletional tolerance mechanisms in a murine model of mixed chimerism with costimulation blockade. Am J Transplant 2005 5 : 1237 1247.
37. Graca L, Cobbold SP, Waldmann H. Identification of regulatory T cells in tolerated allografts. J Exp Med 2002 195 : 1641 1646.
38. Kurtz J, Wekerle T, Sykes M. Tolerance in mixed chimerism - A role for regulatory cells? Trends Immunol 2004 25 : 518 523.
39. Kurtz J, Shaffer J, Lie A, Anosova N, Benichou G, Sykes M. Mechanisms of early peripheral CD4 T-cell tolerance induction by anti-CD154 monoclonal antibody and allogeneic bone marrow transplantation: Evidence for anergy and deletion but not regulatory cells. Blood 2004 103 : 4336 4343.
40. Dyson PJ, Knight AM, Fairchild S, Simpson E, Tomonari K. Genes encoding ligands for deletion of Vb11 T cells cosegregate with mammary tumour virus genomes. Nature 1991 349 : 531 532.
41. Bill J, Kanagawa O, Woodland D, Palmer E. The MHC molecule I-E is necessary but not sufficient for the clonal deletion of VB11 bearing T cells. J Exp Med 1989 169 : 1405 1419.
42. Genovese MC, Becker JC, Schiff M et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005 353 : 1114 1123.
43. Vincenti F, Larsen C, Durrbach A et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med 2005 353 : 770 781.
44. Adams AB, Shirasugi N, Jones TR et al. Development of a chimeric anti-CD40 monoclonal antibody that synergizes with LEA29Y to prolong islet allograft survival. J Immunol 2005 174 : 542 550.
45. Gilson CR, Milas Z, Gangappa S et al. Anti-CD40 monoclonal antibody synergizes with CTLA4-Ig in promoting long-term graft survival in murine models of transplantation. J Immunol 2009 183 : 1625 1635.
46. Ford ML, Larsen CP. Translating costimulation blockade to the clinic: Lessons learned from three pathways. Immunol Rev 2009 229 : 294 306.
47. Karim M, Feng G, Wood KJ, Bushell AR. CD25+CD4+ regulatory T cells generated by exposure to a model protein antigen prevent allograft rejection: Antigen-specific reactivation in vivo is critical for bystander regulation. Blood 2005 105 : 4871 4877.
48. Bachar-Lustig E, Rachamin N, Li H-W, Lan F, Reisner Y. Megadose of T cell-depleted bone marrow overcomes MHC barriers in sublethally irradiated mice. Nat Med 1995 1 : 1268 1273.
49. Wekerle T, Nikolic B, Pearson DA, Swenson KG, Sykes M. Minimal conditioning required in a murine model of T cell depletion, thymic irradiation and high-dose bone marrow transplantation for the induction of mixed chimerism and tolerance. Transpl Int 2002 15 : 248 253.
50. Seung E, Mordes JP, Rossini AA, Greiner DL. Hematopoietic chimerism and central tolerance created by peripheral-tolerance induction without myeloablative conditioning. J Clin Invest 2003 112 : 795 808.