Donor-lymphocyte infusion induces transplantation tolerance by activating systemic and graft-infiltrating double-negative regulatory T cells

Blood

Volumn 100, Issue 9, 2002, Pages 3408-3414

  Young, Kevin J ^a   Yang, Liming ^a   James Phillips, M ^a   Zhang, Li ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b CCRW 2 809   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN;

ANIMAL CELL; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; GRAFT REJECTION; HISTOLOGY; IMMUNOLOGICAL TOLERANCE; LEUKOCYTE MIGRATION; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN ALLOGRAFT; SKIN GRAFT; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

EID: 0036839481     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-01-0235     Document Type: Article

References (65)

1. Van Twuyver E, Kast WM, Mooijaart RJD, Melief CJM, de Waal LP. Induction of transplantation tolerance by intravenous injection of allogeneic lymphocytes across an H-2 class-Ii mismatch. Different mechanisms operate in tolerization across an H-2 class-I versus H-2 class-II disparity. Eur J Immunol. 1990;20:441-444.
2. Soulillou JP, Blandin F, Gunther E, Lemoine V. Genetics of the blood transfusion effect on heart allografts in rats. Transplantation. 1984;38:63-67.
3. Soulillou JP. Donor-specific transfusion-induced tolerance: Mechanisms revisited. Transplant Proc. 1998;30:2438-2440.
4. Quigley RL, Wood KJ, Morris PJ. Transfusion induces blood donor-specific suppressor cells. J Immunol. 1989;142:463-470.
5. Saitovitch D, Bushell A, Mabbs DW, Morris PJ, Wood KJ. Kinetics of induction of transplantation tolerance with a nondepleting anti-CD4 monoclonal antibody and donor-specific transfusion before transplantation. Transplantation. 1996;61:1642-1647.
6. Wong W, Morris PJ, Wood KJ. Syngeneic bone marrow expressing a single donor class I MHC molecule permits acceptance of a fully allogeneic cardiac allograft. Transplantation. 1996;62:1462-1468.
7. Der Zwan AV, Besseling AC, de Waal LP, Boog CJP. Specific tolerance induction and transplantation: A single-day protocol. Blood. 1997;89:2596-2601.
8. Brennan DC, Flye MW. Donor-specific transfusion and donor bone marrow infusion in renal transplantation tolerance: A review of efficacy and mechanisms. Am J Kidney Dis. 1995;26:701-715.
9. Flye MW, Burton K, Mohanakumar T, et al. Donor-specific transfusions have long-term beneficial effects for human renal allografts. Transplantation. 1995;60:1395-1401.
10. Sollinger HW, Kalayoglu M, Belzer FO. Use of the donor specific transfusion protocol in living-unrelated donor-recipient combinations. Ann Surg. 1986;202:315-321.
11. Inoue S, Aikawa M, Dobashi Y, et al. Donor-specific transfusion for kidney transplantation in the cyclosporine era. Transplant Proc. 1996;28:1220-1221.
12. Lagaaij EL, Henneman IPH, Ruigrok M, et al. Effect of one HLA-DR antigen-matched and completely HLA-DR-mismatched blood transfusion on survival of heart and kidney allografts. N Engl J Med. 1989;321:701-705.
13. Anderson CB, Brennan D, Keller C, et al. Beneficial effects of donor-specific transplantation on long-term renal allograft function. Transplant Proc. 1995;271:991-994.
14. Salvatierra O Jr, Melzer JJ, Vincenti F, et al. Donor-specific blood transfusions versus cyclosporine - The DST story. Transplant Proc. 1987;19:160-166.
15. Noris M, Azzollini N, Mister M, et al. Peripheral donor leukocytes prolong survival of rat renal allografts. Kidney Int. 1999;56:1101-1112.
16. Sykes M. Mixed chimerism and transplant tolerance. Immunity. 2001;14:417-424.
17. Van Twuyver E, Mooijaart RJD, ten Berge JM, et al. Pretransplantation blood transfusion revisited. N Engl J Med. 1991;325:1210-1213.
18. De Waal LP, van Twuyver E. Blood transfusion and allograft survival: Is mixed chimerism the solution for tolerance induction in clinical transplanration? Crit Rev Immunol. 1991;10:417-425.
19. Cohen DJ, Lee HM, Mohanakumar T. Mechanisms of CML hyporesponsiveness in long-term renal allograft recipients. Hum Immunol. 1985;14:279-286.
20. Herzog WR, Zanker B, Irschick E, et al. Selective reduction of donor-specific cytotoxic T lymphocyte precursors in patients with a well-functioning kidney allograft. Transplantation. 1987;43:384-389.
21. Lantz O, Alard P, Ben Aribia MH, et al. Persistence of donor-specific IL-2-secreting cells and cytotoxic T lymphocyte precursors in human kidney transplant recipients evidenced by limiting dilution analysis. J Immunol. 1990;144:3748-3755.
22. Terasaki PI. The beneficial transfusion effect on kidney graft survival attributed to clonal deletion. Transplantation. 1984;37:119-125.
23. + T cells and prolonged graft survival in a CTLA4-dependent manner. J Immunol. 2000;164:512-521.
24. Dallman MJ, Shiho O, Page TH, Wood KJ, Morris PJ. Peripheral tolerance to alloantigen results from altered regulation of the interleukin 2 pathway. J Exp Med. 1991;173:79-87.
25. Okada Y, Zuo XJ, Marchevsky AM, et al. Pretransplant donor-specific transfusions induce allograft rejection and IL-2 gene expression in the WKY→F344 functional tolerance model of rat lung transplantation. Transpl Immunol. 1998;6:137-146.
26. Josien R, Pannetier C, Douillard P, et al. Graft-infiltrating T helper cells, CD45RC phenotype, and Th1/Th2-related cytokines in donor-specific transfusion-induced tolerance in adult rats. Transplantation. 1995;60:1131-1139.
27. Iwakoshi NN, Markees TG, Turgeon N, et al. Skin allograft maintenance in a new synchimeric model system of tolerance. J Immunol. 2001;167:6623-6630.
28. - T cell clone in the induction of allograft tolerance by donor-specific blood transfusion. J Immunol. 2000;165:96-101.
29. Roelen DL, Bushell AR, Niimi M, et al. Immuno-regulation by CD4 T cells in the induction of specific immunological unresponsiveness to alloantigens in vivo: Evidence for a reduction in the frequency of alloantigen-specific cytotoxic T cells in vitro. Hum Immunol. 1998;59:529-539.
30. Douillard P, Pannetier C, Josien R, et al. Donor-specific blood transfusion-induced tolerance in adult rats with a dominant TCR-Vβ rearrangement in heart allografts. J Immunol. 1996;157:1250-1260.
31. Yang L, Du TB, Khan Q, Zhang L. Mechanisms of long-term donor-specific allograft survival induced by pretransplant infusion of lymphocytes. Blood. 1998;91:324-330.
32. Zhang ZX, Yang L, Young KJ, DuTemple B, Zhang L. Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat Med. 2000;6:782-789.
33. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T cell clones induced by oral tolerance: Suppression of autoimmune encephalomyelitis. Science. 1994;265:1237-1240.
34. Shevach EM. Regulatory T cells in autoimmunity. Annu Rev Immunol. 2000;18:423-449.
35. Sakaguchi S. Regulatory T cells: Key controllers of immunologic self-tolerance. Cell. 2000;101:455-458.
36. Chatenoud L, Salomon B, Bluestone JA. Suppressor T cells - They're back and critical for regulation of autoimmunity! Immunol Rev. 2001;182:149-163.
37. Roncarolo MG, Levings MK. The role of different subsets of T regulatory cells in controlling autoimmunity. Curr Opin Immunol. 2000;12:676-683.
38. + T cells in autoimmune diabetes. Nat Immunol. 2001;2:1117-1125.
39. + T cells restricted by the MHC class lb molecule, Qa-1. Annu Rev Immunol. 2000;18:185-216.
40. Hayday AC. γδ Cells: A right time and a right place for a conserved third way of protection. Annu Rev Immunol. 2000;18:975-1026.
41. - T-cell deficiency and IDDM in NOD/Lt mice. Diabetes. 1997;46:572-582.
42. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997;389:737-742.
43. Chai J-G, Bartok I, Chandler P, et al. Anergic T cells act as suppressor cells in vitro and in vivo. Eur J Immunol. 1999;29:686-692.
44. Lancaster F, Chui YL, Batchelor JR. Anti-idiotypic T cells suppress rejection of renal allografts in rats. Nature. 1985;315:336-337.
45. -T-cell subsets in determining transplantation rejection or tolerance. Immunol Rev. 2001;182:164-179.
46. Yang L, DuTemple B, Gorczynski RM, Levy G, Zhang L. Evidence for epitope spreading and active suppression in skin graft tolerance after donor-specific transfusion. Transplantation. 1999;67:1404-1410.
47. Zhang ZX, Stanford WL, Zhang L. Ly-6A is critical for the function of double negative regulatory T cells. Eur J Immunol. 2002;32:1584-1592.
48. + T cell as immune regulatory cell. J Mol Med. 2001;79:419-427.
49. Ford M, Young KJ, Ohashi PS, Zhang L. Immune regulatory function of Ipr double negative T cells in vitro and in vivo. J Exp Med. 2002;196:261-267.
50. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int. 1999;55:713-723.
51. Sha WC, Nelson CA, Newberry RD, et al. Selective expression of an antigen receptor on CD8-bearing T lymphocytes in transgenic mice. Nature. 1988;335:271-274.
52. Zhang L, Miller RG. The correlation of prolonged survival of maternal skin grafts with the presence of naturally transferred maternal T cells. Transplantation. 1993;56:918-921.
53. Bugeon L, Cuturi MC, Hallet MM, et al. Peripheral tolerance of an allograft in adult rats - Characterization by low interleukin-2 and interferon-γ mRNA levels and by strong accumulation of major histocompatibility complex transcripts in the graft. Transplantation. 1992;54:219-225.
54. Dallman MJ, Wood KJ, Morris PJ. Specific cytotoxic T cells are found in the nonrejected kidneys of blood-transfused rats. J Exp Med. 1987;165:566-571.
55. + regulatory cells. J Immunol. 2001;167:107-113.
56. Armstrong HE, Bolton EM, McMillan I, Spencer SC, Bradley JA. Prolonged survival of actively enhanced rat renal allografts despite accelerated cellular infiltration and rapid induction of both class I and class II MHC antigens. J Exp Med. 1987;164:891-907.
57. + T cells, Th2-like effector cells, in prolonging hepatic allografts in rats pretreated with a donor-specific blood transfusion. Hepatology. 1997;25:1008-1013.
58. Matzinger P. The JAM test. A simple assay for DNA fragmentation and cell death. J Immunol Methods. 1991;145:185-192.
59. George JF, Sweeney SD, Kirklin JK, et al. An essential role for Fas ligand in transplantation tolerance induced by donor bone marrow. Nat Med. 1998;4:333-335.
60. Thomas JM, Carver FM, Cuuningham PR, Olson LC, Thomas FT. Kidney allograft tolerance in primates without chronic immunosuppression - The role of veto cells. Transplantation. 1991;51:198-207.
61. Mason DW, Morris PJ. Inhibition of the accumulation, in rat kidney allografts, of specific - But not nonspecific - Cytotoxic cells by cyclosporine. Transplantation. 1984;37:46-51.
62. Bradley JA, Mason DW, Morris PJ. Evidence that rat renal allografts are rejected by cytotoxic T cells and not by nonspecific effectors. Transplantation. 1985;39:169-175.
63. Rush DN, Henry SF, Jeffery JR, Schroeder TJ, Gough J. Histological findings in early routine biopsies of stable renal allograft recipients. Transplantation. 1994;57:208-211.
64. Tourneur L, Malassagne B, Batteux F, et al. Transgenic expression of CD95 ligand on thyroid follicular cells confers immune privilege upon thyroid allografts. J Immunol. 2001;167:1338-1346.
65. Minagawa R, Okano S, Tomita Y, et al. Role of Fas-Fas ligand interaction in donor-specific transfusion-induced tolerance to H-Y antigen. Transplant Proc. 2001;33:283.