Cellular basis of long-term organ transplant acceptance: Pivotal role of intrathymic clonal deletion and thymic dependence of bone marrow microchimerism-associated tolerance

American Journal of Kidney Diseases

Volumn 31, Issue 2, 1998, Pages 197-212

  Remuzzi, Giuseppe ^a,b  

^a OSPEDALI RIUNITI   (Italy)

^b MARIO NEGRI INST PHARMACOL RES   (Italy)

Author keywords

Clonal deletion; Microchimerism; Mixed bone marrow chimeras; Thymus; Transplant tolerance

Indexed keywords

T LYMPHOCYTE RECEPTOR;

BONE MARROW TRANSPLANTATION; CHIMERA; GRAFT REJECTION; HUMAN; IMMUNOLOGICAL TOLERANCE; KIDNEY TRANSPLANTATION; LIVER TRANSPLANTATION; NONHUMAN; ORGAN TRANSPLANTATION; REVIEW; T LYMPHOCYTE; THYMUS;

EID: 0031908533     PISSN: 02726386     EISSN: None     Source Type: Journal    
DOI: 10.1053/ajkd.1998.v31.pm9469488     Document Type: Article

References (110)

1. Terasaki PI, Cecka JM, Cho Y: Overview, in Terasaki PI, Cecka JM (eds): Clinical Transplants 1990. Los Angeles, CA, UCLA Tissue Typing Laboratory, 1990, pp 585-601
2. Opelz G, Schwarz V, Engelmann A, Back D, Wilk M, Keppel E: Long-term impact of HLA matching on kidney graft survival in cyclosporine-treated recipients. Transplant Proc 23:373-375, 1991
3. Heck CF, Shumway SJ, Kaye MP: The registry of the International Society for Heart Transplantation: Sixth official-report - 1989. J Heart Transplant 8:271-274, 1989
4. Pearson TC, Madsen JC, Morris PJ, Wood KJ: The induction of transplantation tolerance using donor antigen and CD4 monoclonal antibody. Transplant Proc 22:1955-1956, 1990
5. Wood ML, Monaco AP, Gozzo JJ, Liegeois A: Use of homozygous allogeneic bone marrow for induction of tolerance with ALS. I. Dose and timing. Transplant Proc 3:676-679, 1971
6. Caridis DT, Liegeois A, Barrett I, Monaco AP: Enhanced survival of canine renal allografts of ALS-treated dogs given bone marrow. Transplant Proc 5:671-675, 1973
7. Fradelizi D, Mahouy G, De Riberolles C, Lecomte Y, Alhomme P, Douard MC, Chotin G, Martelli H, Daburon F, Vaiman M: Allograft tolerance in pigs after fractionated total lymphoid irradiation. II. Kidney graft after conventional total lymphoid irradiation and bone marrow cell grafting. Transplantation 31:365-368, 1981
8. Thomas JM, Carver FM, Burnett CM, Thomas FT: Enhanced allograft survival in rhesus monkeys treated with anti-human thymocyte globulin and donor lymphoid cells. Transplant Proc 13:599-602, 1981
9. Thomas JM, Carver FM, Foil MB, Hall WR, Adams C, Fahrenbruch GB, Thomas FT: Renal allograft tolerance induced with ATG and donor bone marrow in outbred rhesus monkeys. Transplantation 36:104-106, 1983
10. Reyes J, Zeevi A, Ramos H, Tzakis A, Todo S, Demetris AJ, Nour B, Nalesnik M, Trucco M, Abu-Elmagd K, Fung JJ, Starzl TE: Frequent achievement of a drug-free state after orthotopic liver transplantation. Transplant Proc 25:3315-3319, 1993
11. Starzl TE: Cell migration and chimerism - A unifying concept in transplantation - With particular reference to HLA matching and tolerance induction. Transplant Proc 25:8-12, 1993
12. Starzl TE, Demetris AJ, Murase N, Thomson AW, Trucco M, Ricordi C: Donor cell chimerism permitted by immunosuppressive drugs: A new view of organ transplantation. Immunol Today 14:326-332, 1993
13. Starzl TE, Demetris A, Murase N, Ildstad S, Ricordi C, Trucco M: Cell migration, chimerism, and graft acceptance. Lancet 339:1579-1582, 1992
14. Kashiwagi N, Porter KA, Penn I, Brettschneider L, Starzl TE: Studies of homograft sex and of gamma globulin phenotypes after orthotopic homotransplantation of the human liver. Surg Forum 20:374-376, 1969
15. Porter KA: Pathology of the orthotopic homograft and heterograft, in Starzl TE (ed): Experience in Hepatic Transplantation. Philadelphia, PA, Saunders, 1969, pp 464-465
16. Starzl TE, Demetris AJ, Trucco M, Ramos H, Zeevi A, Rudert WA, Kocova M, Ricordi C, Ildstad S, Murase N: Systemic chimerism in human female recipients of male livers. Lancet 340:876-877, 1992
17. Sriwatanawongsa V, Davies HFFS, Brons IGM, Aspinal R, Thiru S, Jamieson NV, Calne RY: Continued presence of donor leukocytes in recipients of liver grafts. Transplant Proc 25:371-372, 1993
18. Schlitt HJ, Raddatz G, Steinhoff G: Passenger lymphocytes in human liver allografts and their potential role after transplantation. Transplantation 56:951-955, 1993
19. Collins RH, Anastani J, Terstappen LWMM, Nikaein A, Feng J, Fay JW, Klintmalm G, Stone MJ: Donor-derived long-term multilineage hematopoiesis in a liver-transplant recipient. N Engl J Med 328:762-765, 1993
20. Suberbielle C, Caillat-Zucman S, Legendre C, Bodemer C, Noel LH, Kreis H, Bach IF: Peripheral microchimerism in long-term cadaveric kidney allograft recipients. Lancet 343:1468-1469, 1994
21. Schlitt HJ, Hundrieser J, Hisanaga M, Uthoff K, Karck M, Wahlers T, Wonigelt D, Pichlmayer R: Dynamic patterns of donor-type microchimerism after heart transplantation. Lancet 343:1469-1471, 1994
22. Keenan RJ, Zeevi A, Banas R, Sommers E, Spichty K, Yousem S, Kocova M, Trucco M, Starzl TE, Griffith B: Micro-chimerism is associated with a lower incidence of chronic rejection after lung transplantation. J Heart Lung Transplant 13:A-9, 1994 (abstr)
23. Rolles K, Burroughs AK, Davidson BR, Karatapanis S, Prentice HG, Hamon MD: Donor-specific bone marrow infusion after orthotopic liver transplantation. Lancet 343: 263-264, 1994
24. Qian S, Demetris AJ, Murase N, Rao AS, Fung JJ, Starzl TE: Murine liver allograft transplantation: Tolerance and donor cell chimerism. Hepatology 19:916-924, 1994
25. Rudert WA, Kocova M, Rao AS, Trucco M: Fine quantitation by competitive PCR of circulating donor cells in post transplant chimeric recipients. Transplantation 58:964-965, 1994
26. Steinman RM: The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271-296, 1991
27. Austyn JM, Hankins DF, Larsen CP, Morris PJ, Rao AS, Roake JA: Isolation and characterization of dendritic cells from mouse heart and kidney. J Immunol 152:2401-2410, 1994
28. Lu L, Woo J, Rao AS, Li Y, Watkins SC, Qian S, Starzl TE, Demetris AJ, Thomson AW: Propagation of dendritic cell progenitors from normal mouse liver using granulocyte/macrophage stimulating factor and their maturational development in the presence of type I collagen. J Exp Med 179:1823-1834, 1994
29. Thomson AW, Lu L, Subbotin VM, Li Y, Qian S, Rao AS, Fung JJ, Starzl TE: In vitro propagation and homing of liver-derived dendritic cell progenitors to lymphoid tissues of allogeneic recipients: Implications for the establishment and maintenance of donor cell chimerism following liver transplantation. Transplant Proc 59:544-551, 1995
30. Rao AS, Thomson AW, Shapiro R, Starzl TE: Chimerism after whole organ transplantation: Its relationship to graft rejection and tolerance induction. Curr Opin Nephrol Hypertens 3:589-595, 1994
31. Calne RY, Sells RA, Pena JR, Davis DR, Millard PR, Herbertson NB, Binns RM, Davies DAL: Induction of immunological tolerance by porcine liver allografts. Nature 223:472-476, 1969
32. Starzl TE: Experience in Hepatic Transplantation. Philadelphia, PA, Saunders, 1969
33. Strange English pigs. Lancet 2:940-941, 1969 (editorial)
34. Hiesse C, Samuel D, Blanchet P, Larue J-R, Bensadoun H, Castaing D, Adam R, Charpentier B, Bismuth H: Results of combined kidney and liver transplantation in 22 patients: Renal rejection frequency and long-term allograft tolerance. XVI International Congress of the Transplant Society, Barcelona, Spain, August 25, 1996, p 142 (abstr)
35. Rasmussen A, Davies HFFS, Jamieson NV, Calne R: Combined transplantation of liver and kidney from the same donor protects the kidney from rejection and improves kidney graft survival. 6th Congress of the European Society of Organ Transplantation, Rodos, Greece, October 25, 1993 (abstr)
36. Margreiter R, Kronberger R, Koller J: Can a liver graft from the same donor protect a kidney from rejection? Transplant Proc 20:522-523, 1988 (suppl 1)
37. Gonwa TA, Nery JR, Husberg BS: Simultaneous liver and renal transplantation in man. Transplantation 46:690-693, 1988
38. Najarian JS, Ferguson RM, Sutherland DER, Slavin S, Kim T, Kersey T, Simmons RL: Fractionated total lymphoid irradiation as preparative immunosuppressive in high risk renal transplantation. Ann Surg 196:442-452, 1982
39. Kahn DR, Hong R, Greenberg AJ, Gilbert EF, Darumos GC, Dufek JH: Total lymphoid irradiation and bone marrow in human heart transplantation. Ann Thorac Surg 38:169-171, 1984
40. Ricordi C, Tzakis AG, Zeevi A, Rybka WB, Demetris AJ, Fontes P, Nalesnik MA, Trucco M, Ukah FO, Ball EO, Mullen EE, Marino IR, Fung JJ, Starzl TE: Reversal of graft-versus-host disease with infusion of autologous bone marrow. Cell Transplant 3:187-192, 1994
41. Monaco AP, Wood ML: Studies on heterologous antilymphocyte serum in mice: VII. Optimal cellular antigen for induction of immunologic tolerance with ALS. Transplant Proc 2:489-493, 1970
42. Barber WH, Mankin JA, Laskow DA, Deierhoi MH, Julian BA, Curtis JJ, Diethelm AG: Long-term results of a controlled prospective study with transfusion of donor-specific bone marrow in 57 cadaveric renal allograft recipients. Transplantation 51:70-75, 1991
43. Fontes P, Rao AS, Demetris AJ, Zeevi A, Trucco M, Caroll P, Rybka WB, Ricordi C, Dodson F, Shapiro R, Tzakis AG, Todo S, Abu-Elmagd K, Jordan M, Fung JJ, Starzl TE: Augmentation with bone marrow of donor leukocyte migration for kidney, liver, heart, and pancreas islet transplantation. Lancet 344:151-155, 1994
44. Rao AS, Fontes P, Zeevi A, Trucco M, Dodson FS, Rybka WB, Shapiro R, Jordan M, Pham SM, Rilo HL, Seskey T, Todo S, Scantlebury V, Vivas C, Demetris AJ, Fung JJ, Starzl TE: Augmentation of chimerism in whole organ recipients by simultaneous infusion of donor bone marrow cells. Transplant Proc 27:210-212, 1995
45. Ueda M, Hundriesser J, Hisanaga M: Development of microchimerism in pediatric patients after living-related liver transplantation. Clin Transplant 1997 (in press)
46. Elwood ET, Larsen CP, Maurer DH, Routenberg KL, Neylan JF, Whelchel JD: Microchimerism and rejection in clinical transplantation. Lancet 349:1358-1360, 1997
47. Ishida H, Kawai T, Tanabe K: Status of microchimerism in recipients 15 years after living related renal kidney transplantation. Transplantation 62:126-128, 1996
48. Hisanaga M, Hundrieser J, Boker K: Development, stability, and clinical correlations of allogeneic microchimerism after solid organ transplantation. Transplantation 61:4-46, 1996
49. Ricordi C, Karatzas T, Nery J, Webb M, Selvaggi G, Fernandez L, Khan FA, Ruiz P, Schiff E, Olson L, Fernandez H, Bean J, Esquenazi V, Miller J, Tzakis AG: High-dose donor bone marrow infusions to enhance allograft survival. The effect of timing. Transplantation 63:7-11, 1997
50. Strominger JL: Developmental biology of T cell receptors. Science 244:943-950, 1989
51. Weiss A: Structure and function of the T cell antigen receptor. J Clin Invest 86:1015-1022, 1990
52. Finkel TH, Kubo RT, Cambier JC: T-cell development and transmembrane signaling: Changing biological responses through an unchanging receptor. Immunol Today 12:79-85, 1991
53. Arden B, Klotz J, Siu G, Hood L: Diversity and structure of genes of the alpha family of mouse T-cell antigen receptor. Nature 316:783-787, 1985
54. Boyd RL, Hugo P: Towards an integrated view of thymopoiesis. Immunol Today 12:71-85, 1991
55. Ramsdell F, Fowlkes BJ: Clonal deletion versus clonal anergy: The role of the thymus inducing self tolerance. Science 248:1342-1348, 1990
56. Davis MM: T cell receptor gene diversity and selection. Annu Rev Biochem 59:475-491, 1990
57. Owen RD: Immunogenetic consequences of vascular anastomoses between bovine twins. Science 102:400-401, 1945
58. Billingham RE, Brent L, Medawar PB: Actively acquired tolerance to foreign cells. Nature 172:603-608, 1953
59. Morrissey PJ, Bradley D, Sharrow SO, Singer A: T cell tolerance to non-H-2 encoded stimulatory alloantigens is modulated intrathymically but not prethymically. J Exp Med 158:365-377, 1983
60. Ridge JP, Fuchs EJ, Matzinger P: Neonatal tolerance revisited: Turning on newborn T cells with dendritic cells. Science 271:1723-1726, 1996
61. Turka LA: Normal immune responses, in Neilson EG, Couser WG (eds): Immunologic Renal Diseases. Philadelphia, PA, Lippincott-Raven, 1997, pp 65-94
62. Strober S, Slavin S, Gottlieb M, Zen-Bar I, King DP, Hopper RT, Fuks Z, Grumet FC, Kaplan HS: Allograft tolerance after total lymphoid irradiation (TLI). Immunol Rev 46:84-112, 1979
63. Brent L, Hanser JA, Kilshaw PJ: Unresponsiveness to skin allograft induced by tissue extracts and antilymphocytic serum. Transplant Proc 3:684-687, 1971
64. Isakovic K, Smith SB, Waksman BH: Role of the thymus in tolerance. I. Tolerance to bovine gamma globulin in thymectomized irradiated rats grafted with thymus from tolerant donors. J Exp Med 122:1103-1108, 1965
65. Staples PJ, Gery I, Waksman BH: Role of the thymus in tolerance. III. Tolerance to bovine gamma globulin after direct injection of antigen into the shielded thymus of irradiated rats. J Exp Med 123:127-139, 1966
66. Shimonkevitz RP, Bevan MJ: Split tolerance induced by the intrathymic adoptive transfer of thymocyte stem cells. J Exp Med 168:143-156, 1988
67. Posselt AM, Barker CF, Tomaszewski JE, Markmann JF, Choti MA, Naji A: Induction of donor-specific unresponsiveness by intrathymic islet transplantation. Science 249: 1293-1295, 1990
68. Mayo GL, Possel AM, Campos L, Noorchashm N, Barker CF, Naji A: Intrathymic transplantation promotes survival of islet xenografts (rat→mouse). Transplant Proc 26:758, 1994
69. Zeng Y, Bluestone JA, Ildstad ST, Torres MA, Montag AG, Thistlethwaite RJ Jr: Long-term functional xenograft tolerance after intrathymic islet transplantation (Lewis rat→B6 mouse). Transplant Proc 25:438-439, 1993
70. Remuzzi G, Rossini M, Imberti O, Perico N: Kidney graft survival in rats without immunosuppressants after intrathymic glomerular transplantation. Lancet 337:750-752, 1991
71. Perico N, Barbui C, Remuzzi G: Studies of privileged sites and organ transplantation. Exp Nephrol 1:120-127, 1993
72. Remuzzi G, Perico N, Carpenter CB, Sayegh MH: The thymic way to transplantation tolerance. J Am Soc Nephrol 5:1639-1646, 1995
73. Naji A: Induction of tolerance by intrathymic inoculation of alloantigen. Curr Opin Immunol 8:704-709, 1996
74. Ohzato H, Monaco AP: Induction of specific unresponsiveness (tolerance) to skin allografts by intrathymic donor-specific splenocyte injection in antilymphocyte serum-treated mice. Transplantation 54:1090-1095, 1992
75. Dono K, Wood ML, Ohzato H, Otsu I, Gottschalk R, Maki T, Monaco AP: Marked prolongation of rat skin xenografts induced by intrathymic injection of xenogeneic splenocytes and a short course of rapamycin in antilymphocyte serum-treated mice. Transplantation 59:929-932, 1995
76. Sayegh MH, Perico N, Imberti O, Hancock WW, Carpenter CB, Remuzzi G: Thymic recognition of class II major histocompatibility complex allopeptides induces donor-specific unresponsiveness to renal allografts. Transplantation 56:461-465, 1993
77. Sayegh MH, Perico N, Gallon L, Imberti O, Hancock WW, Remuzzi G, Carpenter CB: Mechanism of acquired thymic unresponsiveness to renal allografts. Transplantation 58:125-132, 1994
78. Shirwan H, Mhoyan A, Leamer M, Wang C, Makowka L, Cramer DV: The role of donor class I peptides in the induction of allograft tolerance. XVI International Congress of the Transplant Society, Barcelona, Spain, August 25, 1996, p 47 (abstr)
79. Chowdhury NC, Murphy B, Sayegh MH, Jin M-X, Roy D, Hardy MA, Oluwole SF: Acquired systemic tolerance to rat cardiac allografts induced by intrathymic inoculation of systemic polymorphic MHC class I allopeptides. 15th American Society for Transplant Physicians Meeting, Dallas, TX, May 26-30, 1996, p 140 (abstr)
80. Knechtle SJ, Wang J, Jiao S, Geissler EK, Sumimoto R, Wolff J: Induction of specific tolerance by intrathymic injection of recipient muscle cells transfected with donor class I major histocompatibility complex. Transplantation 57:990-996, 1994
81. Perico N, Rossini M, Imberti O, Remuzzi G: Thymus-mediated immune tolerance to renal allograft is donor but not tissue specific. J Am Soc Nephrol 2:1063-1071, 1991
82. Odorico JS, Barker CF, Markmann JF, Posselt AM, Naji A: Prolonged survival of rat cardiac allografts after intrathymic inoculation of donor thymocytes. Transplant Proc 25:295-296, 1993
83. Campos L, Alfrey EA, Posselt AM, Odorico JM, Barker CF, Naji A: Prolonged survival of rat orthotopic liver allograft after intrathymic inoculation of donor-strain cells. Transplantation 55:866-870, 1993
84. Goss JA, Nakafusa Y, Flye MW: Intrathymic injection of donor alloantigens induces donor-specific vascularized allograft tolerance without immunosuppression. Ann Surg 216:409-416, 1992
85. Nakafusa Y, Goss JA, Flye MW: Prevention by thymectomy of tolerance induced by intrathymic injection of donor splenocytes. Surgery 114:183-190, 1993
86. Odorico JS, O'Conner T, Campos L, Barker CF, Posselt AM, Naji A: Examination of the mechanisms responsible for tolerance induction after intrathymic inoculation of allogeneic bone marrow. Ann Surg 218:525-531, 1993
87. Oluwole SF, Jin M-X, Chowdhury NC, Ohajekwe OA: Effectiveness of intrathymic inoculation of soluble antigens in the induction of specific unresponsiveness to rat islet allografts without transient recipient immunosuppression. Transplantation 58:1077-1081, 1994
88. Odorico J, Barker CF, Posselt AM, Naji A: Induction of donor-specific tolerance to rat cardiac allografts by intrathymic inoculation of bone marrow. Surgery 112:370-377, 1992
89. Posselt AM, Odorico JS, Barker CF, Naji A: Promotion of pancreatic islet allograft survival by intrathymic transplantation of bone marrow. Diabetes 41:1148-1152, 1992
90. Kappler J, Roehm N, Marrack P: T cell tolerance by clonal elimination in the thymus. Cell 49:273-280, 1987
91. Qin S, Cobbold S, Benjamin R, Waldmann H: Induction of classical transplantation tolerance in the adult. J Exp Med 169:779-794, 1989
92. Miller RG: An immunological suppressor cell inactivating T-lymphocyte precursor cells recognizing it. Nature 287:544-546, 1980
93. Markmann JF, Odorico JS, Bassiri IT, Desai N, Kim JI, Barker CF: Deletion of donor reactive T lymphocytes in adult mice after intrathymic inoculation with lymphoid cells. Transplantation 55:871-877, 1993
94. Hancock WW, Khoury SJ, Carpenter CB, Sayegh MH: Differential effects of oral versus intrathymic administration of polymorphic major histocompatibility complex class II peptides on mononuclear and endothelial cell activation and cytokine expression during a delayed-type hypersensitivity response. Am J Pathol 44:1149-1158, 1994
95. Fluck NC, Jones ND, Mellor AL, Wood KJ: Thymic events following intrathymic injections of alloantigens elucidated using TCR transgenic mice. XVI International Congress of the Transplant Society, Barcelona, Spain, August 25, 1996, p118 (abstr)
96. Gao E, Lo D, Sprent J: Strong T cell tolerance in parent-Fl bone marrow chimeras prepared with supralethal radiation. Evidence for clonal deletion and anergy. J Exp Med 171:1101-1121, 1990
97. Watt PC, Mullen Y, Nomura Y: Successful engraftment of autologous and allogeneic islets into the porcine thymus. J Surg Res 56:367-371, 1994
98. Knechtle SJ, Neville DM Jr, Thomas J, Hanaway M, Watkins D, Geissler E, Wang J: Thymic tolerance in primates: Preliminary results. American Society of Transplant Physicians Meeting, Chicago, IL, 1995, p 103 (abstr)
99. Remuzzi G, Ferrazzi P, Bontempelli M, Senni M, Glauber M, Ruggenenti P, Perico N: Preliminary results of intrathymic injection of donor cells to prevent acute rejection in human heart transplantation. J Am Soc Nephrol 6:1291-1294, 1995
100. Tomita Y, Khan A, Sykes M: Role of intrathymic clonal deletion and peripheral anergy in transplantation tolerance induced by bone marrow transplantation in mice conditioned with a nonmyeloablative regimen. J Immunol 153:1087-1098, 1994
101. Kawai T, Cosimi B, Colvin RB, Powelson J, Eason J, Kozlowski T, Sykes M, Monroy R, Tanaka M, Sachs DH: Mixed allogeneic chimerism and renal allograft tolerance in cynomolgus monkeys. Transplantation 59:256-262, 1995
102. Kahn A, Tomita Y, Sykes M: Thymic dependence of loss of tolerance in mixed allogeneic bone marrow chimeras after depletion of donor antigen. Peripheral mechanisms do not contribute to maintenance of tolerance. Transplantation 62:380-387, 1996
103. Sharabi Y, Sachs DH: Mixed chimerism and permanent specific transplantation tolerance induced by a nonlethal preparative regimen. J Exp Med 169:493-502, 1989
104. Starzl TE, Demetris AJ, Murase N, Trucco M, Thomson AW, Rao AS: The lost chord: Microchimerism and allograft survival. Immunol Today 17:577-584, 1996
105. Oluwole SF, Chowdhury NC, Fawwaz RA: Induction of donor specific unresponsiveness to rat cardiac allografts by intrathymic UV-B-irradiated donor spleen cells. Transplantation 55:1389-1395, 1993
106. Matsuura T, Hara Y, Imanishi M, Kurita T: Organspecific unresponsiveness induced by intrathymic injection of donor bone marrow cells and a short course of immunosuppression in the rat heart transplantation model. Transplant Immunol 1:277-281, 1993
107. Goss JA, Nakafusa Y, Yu S, Flye MW: Intrathymic injection of donor alloantigens induces specific tolerance to cardiac allografts. Transplantation 56:166-173, 1993
108. Chowdhury NC, Fawwaz RA, Oluwole SF: Induction of donor specific tolerance to rat cardiac and small bowel allografts by intrathymic inoculation of donor T cells. J Surg Res 54:368-374, 1993
109. Goss JA, Nakafusa Y, Finke EH, Flye MW, Lacy PE: Induction of tolerance to islet xenografts in a concordant rat-to-mouse model. Diabetes 43:16-23, 1994
110. Oluwole SF, Chowdhury NC, Jin MX: The relative contribution of intrathymic inoculation of donor leukocyte subpopulations in the induction of specific tolerance. Cell Immunol 153:163-170, 1994