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Transplantation Tolerance, Microchimerism, and the Two-Way Paradigm

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REFERENCES

  1. Cohn M. The wisdom of hindsight. Ann Rev Immunology 1994; 12: 1–62.

    Google Scholar 

  2. Billingham RE, Brent L, Medawar PB. “Actively acquired tolerance” of foreign cells. Nature 1953; 172: 603–606.

    PubMed  Google Scholar 

  3. Billingham R, Brent L, Medawar P. Quantitative studies on tissue transplantation immunity. III. Actively acquired tolerance. Phil Trans R Soc Lond (Biol) 1956; 239: 357–412.

    Google Scholar 

  4. Starzl TE, Demetris AJ. Transplantation milestones: Viewed with one-and two-way paradigms of tolerance. JAMA 1959; 46: 876–879.

    Google Scholar 

  5. Mannick JA, Lochte HL, Ashley CA, Thomas ED, Ferrebee JW. A functioning kidney homotransplant in the dog. Surgery 1959; 46: 821–828.

    Google Scholar 

  6. Hume DM, Jackson BT, Zukoski CF, Lee HM, Kauffman HM, Egdahl RH. The homotransplantation of kidneys and of fetal liver and spleen after total body irradiation. Ann Surg 1960; 152: 354–373.

    Google Scholar 

  7. Main JM, Prehn RT. Successful skin homografts after the administration of high dosage X radiation and homologous bone marrow. J Natl Cancer Inst 1995; 15: 1023–1029.

    Google Scholar 

  8. Trentin JJ. Mortality and skin transplantability in X-irradiated mice receiving isologous or heterologous bone marrow. Proc Soc Exper Biol Med 1956; 92: 688–693.

    Google Scholar 

  9. Billingham R, Brent L. A simple method for inducing tolerance of skin homografts in mice. Trans Bull 1957; 4: 67–71.

    Google Scholar 

  10. Simonsen M. The impact on the developing embryo and newborn animal of adult homologous cells. Acta Path Microbiol Scand 1957; 40: 480–500.

    Google Scholar 

  11. Billingham R, Brent L. Quantitative studies on transplantation immunity. IV. Induction of tolerance in newborn mice and studies on the phenomenon of runt disease. Phil Trans R Soc Lond (Biol) 1959; 242: 439–477.

    Google Scholar 

  12. Merrill JP, Murray JE, Harrison JH, Friedman EA, Dealy JB, Jr., Dammin GJ. Successful homotransplantation of the kidney between non-identical twins. New Engl J Med 1960; 262: 1251–1260.

    Google Scholar 

  13. Hamburger J, Vaysse J, Crosnier J, Auvert J, Lalanne CL, Hopper J, Jr. Renal homotransplantation in man after radiation of the recipient. Am J Med 1962; 32: 854–871.

    Google Scholar 

  14. Kuss R, Legrain M, Mathe G, Nedey R, Camey M. Homologous human kidney transplantation. Experience with six patients. Postgrad Med J 1962; 38: 528–531.

    Google Scholar 

  15. Murray JE, Merrill JP, Harrison JH, Wilson RE, Dammin GJ. Prolonged survival of human-kidney homografts by immunosuppressive drug therapy. New Engl J Med 1963; 268: 1315–1323.

    Google Scholar 

  16. Starzl TE, Marchioro TL, Waddell WR. The reversal of rejection in human renal homografts with subsequent development of homograft tolerance. Surg Gynecol Obstet 1963; 117: 385–395.

    Google Scholar 

  17. Hume DM, Magee JH, Kaufmann HM, Jr. Rittenbury MS, Prout GR. Renal homotransplantation in man in modified recipients. 1963; 158: 642–643.

    Google Scholar 

  18. Woodruff MFA, Robson JS, Nolan B, Lambie AT, Wilson TI, Clark JG. Homotransplantation of kidney in patients treated by preoperative local irradiation and postoperative in administration of an antimetabolite (Imuran). Lancet 1963; 2: 675–682.

    Google Scholar 

  19. Simonsen M. On the acquisition of tolerance by adult cells. Ann NY ACAD Science 1960; 87: 382–390.

    Google Scholar 

  20. Michie D, Woodruff MFA, Zeiss IM. An investigation of immunological tolerance based on chimera analysis. Immunology 1961; 4: 413–424.

    Google Scholar 

  21. Simonsen M. Graft versus host reactions. Their natural history, and applicability as tools of research. Progr Allergy 1962; 6: 349–467.

    Google Scholar 

  22. Schaffner KF. Theory change in immunology, Part I: Extended theories and scientific progress. Theor Med 1992; 13: 175–189.

    Google Scholar 

  23. Schaffner KF. Theory change in immunology, Part II: The clonal selection theory. Theor Med 1992; 13: 191–216.

    Google Scholar 

  24. Nossal GJV: Cellular mechanisms of immunologic tolerance. Ann Rev Immunol 1983; 1: 33–62.

    Google Scholar 

  25. Tauber AI: The Immune Self: Theory or Metaphor? Cambridge University Press 1994.

  26. Burnet FM. The new approach to immunology. N Engl J Med 1961; 264: 24–34.

    Google Scholar 

  27. Bach F, Hirschhorn K. Lymphocyte interaction: A potential histocompatibility test in vitro. Science 1964; 143: 813–814.

    Google Scholar 

  28. Bain B, Vas MR, Lowenstein L. The development of large immature mononuclear cells in mixed leukocyte cultures. Blood 1964; 23: 108–116.

    Google Scholar 

  29. Mathe G, Amiel JL, Schwarzenberg L, Cattan A, Schneider M. Haematopoietic chimera in man after allogenic (homologous) bone marrow transplantation. Brit Med J 1963; 2: 1633–1635.

    Google Scholar 

  30. Gatti RA, Meuwissen HJ, Allen HD, Hong R, Good RA. Immunological reconstitution of sex-linked lymphopenic immunological deficiency. Lancet 1968; 2: 1366–1369.

    Google Scholar 

  31. Bach FH, Albertini RJ, Joo P, Anderson JL, Bortin MM. Bone-marrow transplantation in a patient with the Wiskott-Aldrich syndrome. Lancet 1968; 2: 1364–1366.

    Google Scholar 

  32. Thomas ED. Allogeneic marrow grafting: A story of man and dog. In: History of Transplantation: Thirty-Five Recollections (Terasaki PI, ed) UCLA Tissue Typing Laboratory, Los Angeles, CA, 1991, pp. 379–393.

    Google Scholar 

  33. van Bekkum DW. Bone marrow transplantation: A story of stem cells. In: Terasaki PI, ed. History of Transplanation: Thirty-Five Recollections. UCLA Tissue Typing Laboratory, Los Angeles, CA, 1991, pp. 395–434.

    Google Scholar 

  34. Harrison DE. Competitive repopulation in unirradiated normal recipients. Blood 1993; 81: 2473–2474.

    Google Scholar 

  35. Mariani T, Martinez C, Smith JM, Good RA. Induction of immunological tolerance to male skin isografts in female mice subsequent to neonatal period. Proc Soc Exp Biol Med 1959; 101: 596–599.

    Google Scholar 

  36. Brent L, Gowland G. Induction of tolerance of skin homografts in immunologically competent mice. Nature 1962; 196: 1298–1301.

    Google Scholar 

  37. Stewart FM, Crittenden RB, Lowry PA, Pearson-White S, Quesenberry PJ. Longterm engraftment of normal and post-5-fluorouracil murine marrow into normal nonmyeloablated mice. Blood 1993; 81: 2566–2571.

    Google Scholar 

  38. Starzl TE, Demetris AJ, Murase N, Ildstad S, Ricordi C, Trucco M. Cell migration, chimerism, and graft acceptance. Lancet 1992; 339: 1579–1582.

    PubMed  Google Scholar 

  39. 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 1992; 340: 876–877.

    PubMed  Google Scholar 

  40. Starzl TE, Demetris AJ, Trucco M, Murase N, Ricordi C, Ildstad S, Ramos H, Todo S, Tzakis A, Fung JJ, Nalesnik M, Rudert WA, Kocova M. Cell migration and chimerism after whole organ transplantation: The basis of graft acceptance. Hepatology 1993; 17: 1127–1152.

    PubMed  Google Scholar 

  41. Starzl TE, Demetris AJ, Trucco M, Zeevi A, Ramos H, Terasaki P, Rudert WA, Kocova M, Ricordi C, Ildstad S, Murase N. Chimerism and donor specific nonreactivity 27 to 29 years after kidney allotransplantation. Transplantation 1993; 55: 1272–1277.

    PubMed  Google Scholar 

  42. Starzl TE, Demetris AJ, Trucco M, Ricordi S, Ildstad S, Terasaki P, Murase N, Kendall RS, Kocova M, Rudert WA, Zeevi A, Van Thiel D. Chimerism after liver transplantation for type IV glycogen storage disease and Type I Gaucher's disease. New Engl J Med 1993; 328: 745–749.

    PubMed  Google Scholar 

  43. Demetris AJ, Murase N, Rao AS, Starzl TE. The role of passenger leukocytes in rejection and “tolerance” after solid organ transplantation: a potential explanation of a paradox. In: JL Touraine, ed. Rejection and Tolerance, Volume 25. Dordrecht Kluwer Academic Publishers 1994: 325–392.

  44. Iwaki Y, Starzl TE, Yagihashi A, Taniwaki S, Abu-Elmagd K, Tzakis A, Fung J, Todo S. Replacement of donor lymphoid tissue in human small bowel transplants under FK 506 immunosuppression. Lancet 1991; 337: 818–819.

    Google Scholar 

  45. Murase N, Starzl TE, Ye Q, Tsamandas A, Thomson AW, Rao AS, Demetris AJ. Multilineage hematopoietic reconstitution of supralethally irradiated rats by syngeneic whole organ transplantation: with particular reference to the liver. Transplantation 1996; 61: 1–3.

    Google Scholar 

  46. Taniguchi H, Toyoshima T, Fukao K, Nakauchi H Presence of hematopoietic stem cells in the adult liver. Nature Medicine 1996; 2: 198–203.

    Google Scholar 

  47. 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 1969; 20: 374–376.

    Google Scholar 

  48. Porter KA. Pathology of the orthotopic homograft and heterograft. In: Starzl TE, ed. Experience In Hepatic Transplantation. Philadelphia, PA: WB Saunders Company, 1969; 446–465.

    Google Scholar 

  49. Murase N, Demetris AJ, Matsuzaki T, Yagihasi A, Todo S, Fung J, Starzl TE. Long survival in rats after multivisceral versus isolated small bowel allotransplantation under FK 506. Surgery 1991; 110: 87–98.

    Google Scholar 

  50. Starzl TE, Todo S, Tzakis A, Alessiani M, Casavilla A, Abu-Elmagd K, Fung JJ. The many faces of multivisceral transplantation. Surg Gynecol Obstet 1991; 172: 335–344.

    Google Scholar 

  51. Starzl TE, Demetris AJ, Murase N, Trucco M, Thomson AW, Rao AS. The lost chord: Microchimerism. Immunol Today 1996; 17: 577–584; 588.

    Google Scholar 

  52. Starzl TE, Zinkernagel RM. Antigen localization and migration in immunity and tolerance. New Eng J Med, in press.

  53. Steinmuller D. Immunization with skin isografts taken from tolerant mice. Science 1967; 158: 127–129.

    Google Scholar 

  54. Elkins WL, Guttmann RD. Pathogenesis of a local graft versus host reaction: Immunogenicity of circulating host leukocytes. Science 1968; 159: 1250, 1251.

    Google Scholar 

  55. Hart DNJ, Winearls CG, Fabre JW. Graft adaptation: studies on possible mechanisms in long-term surviving rat renal allografts. Transplantation 1980; 30: 73–80.

    Google Scholar 

  56. Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor-strain dendritic cells. J Exp Med 1982; 155: 31.

    Google Scholar 

  57. Talmage DW, Dart G, Radovich J, Lafferty KJ. Activation of transplant immunity: effect of donor leukocytes on thyroid allograft rejection. Science 1976; 191: 385–387.

    Google Scholar 

  58. Lafferty KJ, Prowse SJ, Simenovic CJ. Immunobiology of tissue transplantation: a return to the passenger leukocyte concept. Ann Rev Immunol 1983; 1: 143–173.

    Google Scholar 

  59. Przepiorka D, Thomas ED, Durham DM, Fisher L. Use of a probe to repeat sequence of the Y chromosome for detection of host cells in peripheral blood of bone marrow transplant recipients. Am J Clin Pathol 1991; 95: 201–206.

    Google Scholar 

  60. Wessman M, Popp S, Ruutu T, Volin L, Cremer T, Knuutila S. Detection of residual host cells after bone marrow transplantation using non-isotopic in situ hyubridization and karyotype analysis. Bone Marrow Transplant 1993; 11: 279–284.

    Google Scholar 

  61. Schwartz R, Andre-Schwartz J. Neoplastic sequelae of allogenic disease. I. Theoretical considerations and experimental design. Ann NY Acad Sci 1966; 129: 804–821.

    Google Scholar 

  62. Penn I, Hammond W, Brettschneider L, Starzl TE. Malignant lymphomas in transplantation patients. Transplant Proc 1969; 1: 106–112.

    PubMed  Google Scholar 

  63. Starzl TE, Penn I, Putnam CW, Groth CG, Halgrimson CG. Iatrogenic alterations of immunologic surveillance in man and their influence on malignancy. Transplant Rev 1971; 7: 112–145.

    Google Scholar 

  64. Nalesnik MA, Rao AS, Furukawa H, Pham S, Zeevi A, Fung JJ, Klein G, Gritsch A, Elder E, Whiteside TL, Starzl TE. Autologous lymphokine-activated killer (LAK) cell therapy of EBV+ and EBV- lymphoproliferative disorders arising in organ transplant recipients. Transplantation 1997; 63: 1200–1205.

    PubMed  Google Scholar 

  65. Morecki S, Leshem B, Eid A, Slavin S. Alloantigen persistence in induction and maintenance of transplantation tolerance. J Exp Med 1987; 165: 1468–1480.

    Google Scholar 

  66. Demetris AJ, Murase N, Fujisaki S, Fung JJ, Rao AS, Starzl TE. Hematolymphoid cell trafficking, microchimerism, and GVHD reactions after liver, bone marrow, and heart transplantation. Transplantation Proc 1993; 25: 3337–3344.

    Google Scholar 

  67. Murase N, Starzl TE, Tanabe M, Fujisaki S, Miyazawa H, Ye Q, Delaney CP, Fung JJ, Demetris AJ. Variable chimerism, graft versus host disease, and tolerance after different kinds of cell and whole organ transplantation from Lewis to Brown-Norway rats. Transplantation 1995; 60: 158–171.

    Google Scholar 

  68. Murase N, Demetris AJ. Tsamandas Ac, Ye Q, Starzl TE. Heterogenous distribution of Chimerism produced by rat organ and bone marrow allotransplantation. Transplantation 1996; 61: 1126–1131.

    Google Scholar 

  69. Lu L, Rudert WA, Qian S, McCaslin D, Fu F, Rao AS, Trucco M, Fung JJ, Starzl TE, Thomson AW. Growth of donor-derived dendritic cells from the bone marrow of murine liver allograft recipients in response to granulocyte/macrophage colony-stimulating factor. J Exp Med 1995; 182: 379–387.

    Google Scholar 

  70. Thomson AW, Lu L, Wan Y, Qian S, Larsen CP, Starzl TE. Identification of donor-derived dendritic cell progenitors in bone marrow of spontaneously tolerant liver allograft recipients. Transplantation 1995; 60: 1555–1559.

    Google Scholar 

  71. Bushell A, Pearson TC, Morris PJ, Wood KJ. Donor recipient microchimerism is not required for tolerance induction following recipient pretreatment with donor-specific transfusion and anti-CD4 antibody. Transplantation 1995; 59: 1367–1371, 1996; 61: 169–170.

    Google Scholar 

  72. Wood K, Sachs DH. Chimerism and transplantation tolerance: cause and effect. Immunol Today. In Press December, 1996.

  73. Martinez C, Shapiro F, Good RA. Essential duration of parabiosis and development of tolerance to skin homografts in mice. Proc Soc Exp Biol Med 1960; 104: 256–259.

    Google Scholar 

  74. Slavin S, Strober S, Fuks Z, Kaplan HS. Induction of a specific tissue transplantation tolerance using fractionated total lymphoid irradiation tolerance using fractionated total lymphoid irradiation in adult mice: Long term survival of allogeneic bone marrow and skin grafts. J Exp Med 1977; 146: 34–48.

    PubMed  Google Scholar 

  75. Ildstad ST, Sachs DH. Reconstitution with syngeneic plusallogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature 1984; 307: 168–170.

    Google Scholar 

  76. Thomas J, Carver M, Cunningham P, Park K, Gonder J, Thomas F. Promotion of incompatible allograft acceptance in rhesus monkeys given posttransplant antithymocyte globulin and donor bone marrow. I. In vivo parameters and immunohistologic evidence suggesting microchimerism. Transplantation 1987; 43: 332–338.

    Google Scholar 

  77. Owen RD. Immunogenetic consequences of vascular anastomoses between bovine twins. Science 1945; 102: 400–401.

    Google Scholar 

  78. 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 1993; 14: 326–332.

    Google Scholar 

  79. Coutinho A. Beyond clonal selection and network. Immunol Rev 1989; 110: 63–87.

    Google Scholar 

  80. Cohen IR. The cognitive paradigm and the immunological homunclus. Immunol Today 1992; 13: 490–494.

    Google Scholar 

  81. Waldmann H, Cobbold SP, Benjamin R, Qin S. A theorectical framework for self-tolerance as its relevance to therapy of autoimmune diseases. J Autoimmun 1988; 1: 623–629.

    Google Scholar 

  82. Matzinger P. Tolerance, danger, and the extended family. Ann Rev Immunol 1994; 12: 991–1045.

    Google Scholar 

  83. Sterzl J, Silverstein AM. Development aspects of immunity. Adv Immunol 1967; 6: 337–459.

    PubMed  Google Scholar 

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  1. The Pittsburgh Transplantation Institute, Departments of Surgery and Pathology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, 15213, USA

    Thomas E. Starzl & Anthony J. Demetris

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Starzl, T.E., Demetris, A.J. Transplantation Tolerance, Microchimerism, and the Two-Way Paradigm. Theor Med Bioeth 19, 441–455 (1998). https://doi.org/10.1023/A:1009924907775

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