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Published in: Immunologic Research 2-3/2014

01-05-2014 | IMMUNOLOGY AT STANFORD UNIVERSITY

Path to clinical transplantation tolerance and prevention of graft-versus-host disease

Author: Samuel Strober

Published in: Immunologic Research | Issue 2-3/2014

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Abstract

Although organ and bone marrow transplantations are life-saving procedures for patients with terminal diseases, the requirement for the lifelong use of immunosuppressive drugs to prevent organ graft rejection and the development of graft versus host disease (GVHD) remain important problems. Experimental approaches to solve these problems, first in preclinical models and then in clinical studies, developed at Stanford during the past 40 years are summarized in this article. The approaches use fractionated radiation of the lymphoid tissues, a procedure initially developed to treat Hodgkin’s disease, to alter the immune system such that tolerance to organ transplants can be achieved and GVHD can be prevented after the establishment of chimerism. In both instances, the desired goal was achieved when the balance of immune cells was changed to favor regulatory innate and adaptive immune cells that suppress the conventional immune cells that ordinarily promote inflammation and tissue injury.
Literature
1.
go back to reference Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells. Nature. 1953;172:603–6.CrossRefPubMed Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells. Nature. 1953;172:603–6.CrossRefPubMed
2.
go back to reference Hume DM, Egdahl RH. Progressive destruction of renal homografts isolated from the regional lymphatics of the host. Surgery. 1955;38:194–214.PubMed Hume DM, Egdahl RH. Progressive destruction of renal homografts isolated from the regional lymphatics of the host. Surgery. 1955;38:194–214.PubMed
3.
go back to reference Gowans JL. The fate of parental strain small lymphocytes in F1 hybrid rats. Ann N Y Acad Sci. 1962;99:432–55.CrossRefPubMed Gowans JL. The fate of parental strain small lymphocytes in F1 hybrid rats. Ann N Y Acad Sci. 1962;99:432–55.CrossRefPubMed
4.
go back to reference Gowans JL, Knight EJ. The route of re-circulation of lymphocytes in the rat. Proc R Soc Lond B Biol Sci. 1964;159:257–82.CrossRefPubMed Gowans JL, Knight EJ. The route of re-circulation of lymphocytes in the rat. Proc R Soc Lond B Biol Sci. 1964;159:257–82.CrossRefPubMed
5.
go back to reference Marchesi VT, Gowans JL. The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc R Soc Lond B Biol Sci. 1964;159:283–90.CrossRefPubMed Marchesi VT, Gowans JL. The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc R Soc Lond B Biol Sci. 1964;159:283–90.CrossRefPubMed
7.
go back to reference Zan-Bar I, Strober S, Vitetta ES. The relationship between surface immunoglobulin isotype and immune function of murine B lymphocytes. I. Surface immunoglobulin isotypes on primed B cells in the spleen. J Exp Med. 1977;145:1188–205.CrossRefPubMed Zan-Bar I, Strober S, Vitetta ES. The relationship between surface immunoglobulin isotype and immune function of murine B lymphocytes. I. Surface immunoglobulin isotypes on primed B cells in the spleen. J Exp Med. 1977;145:1188–205.CrossRefPubMed
9.
go back to reference Knapp MR, Jones PP, Black SJ, Vitetta ES, Slavin S, Strober S. Characterization of a spontaneous murine B cell leukemia (BCL1). I. Cell surface expression of IgM, IgD, Ia, and FcR. J Immunol. 1979;123:992–9.PubMed Knapp MR, Jones PP, Black SJ, Vitetta ES, Slavin S, Strober S. Characterization of a spontaneous murine B cell leukemia (BCL1). I. Cell surface expression of IgM, IgD, Ia, and FcR. J Immunol. 1979;123:992–9.PubMed
10.
go back to reference Strober S, Gronowicz ES, Knapp MR, Slavin S, Vitetta ES, Warnke RA, et al. Immunobiology of a spontaneous murine B cell leukemia (BCL1). Immunol Rev. 1979;48:169–95.CrossRefPubMed Strober S, Gronowicz ES, Knapp MR, Slavin S, Vitetta ES, Warnke RA, et al. Immunobiology of a spontaneous murine B cell leukemia (BCL1). Immunol Rev. 1979;48:169–95.CrossRefPubMed
11.
go back to reference Knapp MR, Liu CP, Newell N, Ward RB, Tucker PW, Strober S, et al. Simultaneous expression of immunoglobulin mu and delta heavy chains by a cloned B-cell lymphoma: a single copy of the VH gene is shared by two adjacent CH genes. Proc Natl Acad Sci U S A. 1982;79:2996–3000.PubMedCentralCrossRefPubMed Knapp MR, Liu CP, Newell N, Ward RB, Tucker PW, Strober S, et al. Simultaneous expression of immunoglobulin mu and delta heavy chains by a cloned B-cell lymphoma: a single copy of the VH gene is shared by two adjacent CH genes. Proc Natl Acad Sci U S A. 1982;79:2996–3000.PubMedCentralCrossRefPubMed
12.
go back to reference Kaplan HS. Hodgkin’s Disease. Harvard University Press, Cambridge, Mass. 1972:89–104, 279–316. Kaplan HS. Hodgkin’s Disease. Harvard University Press, Cambridge, Mass. 1972:89–104, 279–316.
13.
go back to reference Levy R, Kaplan HS. Impaired lymphocyte function in untreated Hodgkin’s disease. N Engl J Med. 1974;290:181–6.CrossRefPubMed Levy R, Kaplan HS. Impaired lymphocyte function in untreated Hodgkin’s disease. N Engl J Med. 1974;290:181–6.CrossRefPubMed
14.
go back to reference Fuks Z, Strober S, Bobrove AM, Sasazuki T, McMichael A, Kaplan HS. Long term effects of radiation of T and B lymphocytes in peripheral blood of patients with Hodgkin’s disease. J Clin Investig. 1976;58:803–14.PubMedCentralCrossRefPubMed Fuks Z, Strober S, Bobrove AM, Sasazuki T, McMichael A, Kaplan HS. Long term effects of radiation of T and B lymphocytes in peripheral blood of patients with Hodgkin’s disease. J Clin Investig. 1976;58:803–14.PubMedCentralCrossRefPubMed
15.
go back to reference Gottlieb MS, Schroff R, Schanker HM, Weisman JD, Fan PT, Wolf RA, et al. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N Engl J Med. 1981;305:1425–31.CrossRefPubMed Gottlieb MS, Schroff R, Schanker HM, Weisman JD, Fan PT, Wolf RA, et al. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N Engl J Med. 1981;305:1425–31.CrossRefPubMed
16.
go back to reference Slavin S, Strober S, Fuks Z, Kaplan HS. Long-term survival of skin allografts in mice treated with fractionated total lymphoid irradiation. Science. 1976;193:1252–4.CrossRefPubMed Slavin S, Strober S, Fuks Z, Kaplan HS. Long-term survival of skin allografts in mice treated with fractionated total lymphoid irradiation. Science. 1976;193:1252–4.CrossRefPubMed
17.
go back to reference Slavin S, Strober S, Fuks Z, Kaplan HS. Induction of specific tissue transplantation 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.CrossRefPubMed Slavin S, Strober S, Fuks Z, Kaplan HS. Induction of specific tissue transplantation 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.CrossRefPubMed
18.
go back to reference Slavin S, Reitz B, Bieber CP, Kaplan HS, Strober S. Transplantation tolerance in adult rats using total lymphoid irradiation: permanent survival of skin, heart, and marrow allografts. J Exp Med. 1978;147:700–7.CrossRefPubMed Slavin S, Reitz B, Bieber CP, Kaplan HS, Strober S. Transplantation tolerance in adult rats using total lymphoid irradiation: permanent survival of skin, heart, and marrow allografts. J Exp Med. 1978;147:700–7.CrossRefPubMed
19.
go back to reference Slavin S, Fuks Z, Kaplan HS, Strober S. Transplantation of allogeneic bone marrow without graft-versus-host disease using total lymphoid irradiation. J Exp Med. 1978;147:963–72.CrossRefPubMed Slavin S, Fuks Z, Kaplan HS, Strober S. Transplantation of allogeneic bone marrow without graft-versus-host disease using total lymphoid irradiation. J Exp Med. 1978;147:963–72.CrossRefPubMed
20.
go back to reference Woodley SL, Gurley KE, Hoffmann SL, Nicolls MR, Hagberg R, Clayberger C, et al. Induction of tolerance to heart allografts in rats using posttransplant total lymphoid irradiation and anti-T cell antibodies. Transplantation. 1993;56:1443–7.CrossRefPubMed Woodley SL, Gurley KE, Hoffmann SL, Nicolls MR, Hagberg R, Clayberger C, et al. Induction of tolerance to heart allografts in rats using posttransplant total lymphoid irradiation and anti-T cell antibodies. Transplantation. 1993;56:1443–7.CrossRefPubMed
21.
go back to reference Hayamizu K, Lan F, Huie P, Sibley RK, Strober S. Comparison of chimeric acid and non-chimeric tolerance using posttransplant total lymphoid irradiation: cytokine expression and chronic rejection. Transplantation. 1999;68:1036–44.CrossRefPubMed Hayamizu K, Lan F, Huie P, Sibley RK, Strober S. Comparison of chimeric acid and non-chimeric tolerance using posttransplant total lymphoid irradiation: cytokine expression and chronic rejection. Transplantation. 1999;68:1036–44.CrossRefPubMed
22.
go back to reference Higuchi M, Zeng D, Shizuru J, Gworek J, Dejbakhsh-Jones S, Taniguchi M, et al. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J Immunol. 2002;169:5564–70.CrossRefPubMed Higuchi M, Zeng D, Shizuru J, Gworek J, Dejbakhsh-Jones S, Taniguchi M, et al. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J Immunol. 2002;169:5564–70.CrossRefPubMed
23.
go back to reference Lan F, Hayamizu K, Strober S. Cyclosporine facilitates chimeric and inhibits nonchimeric tolerance after posttransplant total lymphoid irradiation. Transplantation. 2000;69:649–55.CrossRefPubMed Lan F, Hayamizu K, Strober S. Cyclosporine facilitates chimeric and inhibits nonchimeric tolerance after posttransplant total lymphoid irradiation. Transplantation. 2000;69:649–55.CrossRefPubMed
24.
go back to reference Liu YP, Li Z, Nador RG, Strober S. Simultaneous protection against allograft rejection and graft-versus-host disease after total lymphoid irradiation: role of natural killer T cells. Transplantation. 2008;85:607–14.CrossRefPubMed Liu YP, Li Z, Nador RG, Strober S. Simultaneous protection against allograft rejection and graft-versus-host disease after total lymphoid irradiation: role of natural killer T cells. Transplantation. 2008;85:607–14.CrossRefPubMed
25.
go back to reference Ildstad ST, Wren SM, Bluestone JA, Barbieri SA, Sachs DH. Characterization of mixed allogeneic chimeras. Immunocompetence, in vitro reactivity, and genetic specificity of tolerance. J Exp Med. 1985;162:231–44.CrossRefPubMed Ildstad ST, Wren SM, Bluestone JA, Barbieri SA, Sachs DH. Characterization of mixed allogeneic chimeras. Immunocompetence, in vitro reactivity, and genetic specificity of tolerance. J Exp Med. 1985;162:231–44.CrossRefPubMed
26.
go back to reference Sharabi Y, Sachs DH. Mixed chimerism and permanent specific transplantation tolerance induced by a nonlethal preparative regimen. J Exp Med. 1989;169:493–502.CrossRefPubMed Sharabi Y, Sachs DH. Mixed chimerism and permanent specific transplantation tolerance induced by a nonlethal preparative regimen. J Exp Med. 1989;169:493–502.CrossRefPubMed
27.
go back to reference Pillai AB, George TI, Dutt S, Teo P, Strober S. Host NKT cells can prevent graft-versus-host disease and permit graft antitumor activity after bone marrow transplantation. J Immunol. 2007;178:6242–51.CrossRefPubMed Pillai AB, George TI, Dutt S, Teo P, Strober S. Host NKT cells can prevent graft-versus-host disease and permit graft antitumor activity after bone marrow transplantation. J Immunol. 2007;178:6242–51.CrossRefPubMed
28.
go back to reference Lan F, Zeng D, Huie P, Higgins JP, Strober S. Allogeneic bone marrow cells that facilitate complete chimerism and eliminate tumor cells express both CD8 and T-cell antigen receptor-alpha beta. Blood. 2001;97:3458–65.CrossRefPubMed Lan F, Zeng D, Huie P, Higgins JP, Strober S. Allogeneic bone marrow cells that facilitate complete chimerism and eliminate tumor cells express both CD8 and T-cell antigen receptor-alpha beta. Blood. 2001;97:3458–65.CrossRefPubMed
29.
go back to reference Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S, et al. CD4 + CD25 + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9:1144–50.CrossRefPubMed Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S, et al. CD4 + CD25 + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9:1144–50.CrossRefPubMed
30.
go back to reference Slavin S, Strober S. Induction of allograft tolerance after total lymphoid irradiation (TLI): development of suppressor cells of the mixed leukocyte reaction (MLR). J Immunol. 1979;123:942–6.PubMed Slavin S, Strober S. Induction of allograft tolerance after total lymphoid irradiation (TLI): development of suppressor cells of the mixed leukocyte reaction (MLR). J Immunol. 1979;123:942–6.PubMed
31.
go back to reference King DP, Strober S, Kaplan HS. Suppression of the mixed leukocyte response and of graft-vs-host disease by spleen cells following total lymphoid irradiation (TLI). J Immunol. 1981;126:1140–5.PubMed King DP, Strober S, Kaplan HS. Suppression of the mixed leukocyte response and of graft-vs-host disease by spleen cells following total lymphoid irradiation (TLI). J Immunol. 1981;126:1140–5.PubMed
32.
go back to reference King DP, Strober S. Immunoregulatory changes induced by total lymphoid irradiation. II. Development of thymus-leukemia antigen-positive and -negative suppressor T cells that differ in their regulatory function. J Exp Med. 1981;154:13–23.CrossRefPubMed King DP, Strober S. Immunoregulatory changes induced by total lymphoid irradiation. II. Development of thymus-leukemia antigen-positive and -negative suppressor T cells that differ in their regulatory function. J Exp Med. 1981;154:13–23.CrossRefPubMed
33.
go back to reference Okada S, Strober S. Spleen cells from adult mice given total lymphoid irradiation or from newborn mice have similar regulatory effects in the mixed leukocyte reaction. I. Generation of antigen-specific suppressor cells in the mixed leukocyte reaction after the addition of spleen cells from adult mice given total lymphoid irradiation. J Exp Med. 1982;156:522–38.CrossRefPubMed Okada S, Strober S. Spleen cells from adult mice given total lymphoid irradiation or from newborn mice have similar regulatory effects in the mixed leukocyte reaction. I. Generation of antigen-specific suppressor cells in the mixed leukocyte reaction after the addition of spleen cells from adult mice given total lymphoid irradiation. J Exp Med. 1982;156:522–38.CrossRefPubMed
34.
go back to reference Bendelac A, Rivera MN, Park SH, Roark JH. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol. 1997;15:535–62.CrossRefPubMed Bendelac A, Rivera MN, Park SH, Roark JH. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol. 1997;15:535–62.CrossRefPubMed
35.
go back to reference Kronenberg M, Engel I. On the road: progress in finding the unique pathway of invariant NKT cell differentiation. Curr Opin Immunol. 2007;19:186–93.CrossRefPubMed Kronenberg M, Engel I. On the road: progress in finding the unique pathway of invariant NKT cell differentiation. Curr Opin Immunol. 2007;19:186–93.CrossRefPubMed
36.
go back to reference Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, et al. Foxp3 + CD25 + CD4 + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev. 2006;212:8–27.CrossRefPubMed Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, et al. Foxp3 + CD25 + CD4 + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev. 2006;212:8–27.CrossRefPubMed
37.
go back to reference Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol. 2003;3:199–210.CrossRefPubMed Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol. 2003;3:199–210.CrossRefPubMed
39.
go back to reference Garcia MR, Ledgerwood L, Yang Y, Xu J, Lal G, Burrell B, et al. Monocytic suppressive cells mediate cardiovascular transplantation tolerance in mice. J Clin Investig. 2010;120:2486–96.PubMedCentralCrossRefPubMed Garcia MR, Ledgerwood L, Yang Y, Xu J, Lal G, Burrell B, et al. Monocytic suppressive cells mediate cardiovascular transplantation tolerance in mice. J Clin Investig. 2010;120:2486–96.PubMedCentralCrossRefPubMed
40.
go back to reference Lan F, Zeng D, Higuchi M, Huie P, Higgins JP, Strober S. Predominance of NK1.1 + TCR alpha beta + or DX5 + TCR alpha beta + T cells in mice conditioned with fractionated lymphoid irradiation protects against graft-versus-host disease: “natural suppressor” cells. J Immunol. 2001;167:2087–96.CrossRefPubMed Lan F, Zeng D, Higuchi M, Huie P, Higgins JP, Strober S. Predominance of NK1.1 + TCR alpha beta + or DX5 + TCR alpha beta + T cells in mice conditioned with fractionated lymphoid irradiation protects against graft-versus-host disease: “natural suppressor” cells. J Immunol. 2001;167:2087–96.CrossRefPubMed
41.
go back to reference Higuchi M, Zeng D, Shizuru J, Gworek J, Dejbakhsh-Jones S, Taniguchi M, et al. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J Immunol. 2002;169:5564–70.CrossRefPubMed Higuchi M, Zeng D, Shizuru J, Gworek J, Dejbakhsh-Jones S, Taniguchi M, et al. Immune tolerance to combined organ and bone marrow transplants after fractionated lymphoid irradiation involves regulatory NK T cells and clonal deletion. J Immunol. 2002;169:5564–70.CrossRefPubMed
42.
go back to reference Lan F, Zeng D, Higuchi M, Higgins JP, Strober S. Host conditioning with total lymphoid irradiation and antithymocyte globulin prevents graft-versus-host disease: the role of CD1-reactive natural killer T cells. Biol Blood Marrow Transpl. 2003;9:355–63.CrossRef Lan F, Zeng D, Higuchi M, Higgins JP, Strober S. Host conditioning with total lymphoid irradiation and antithymocyte globulin prevents graft-versus-host disease: the role of CD1-reactive natural killer T cells. Biol Blood Marrow Transpl. 2003;9:355–63.CrossRef
43.
go back to reference Nador RG, Hongo D, Baker J, Yao Z, Strober S. The changed balance of regulatory and naive T cells promotes tolerance after TLI and anti-T-cell antibody conditioning. Am J Transpl. 2010;10:262–72.CrossRef Nador RG, Hongo D, Baker J, Yao Z, Strober S. The changed balance of regulatory and naive T cells promotes tolerance after TLI and anti-T-cell antibody conditioning. Am J Transpl. 2010;10:262–72.CrossRef
44.
go back to reference Hongo D, Tang X, Dutt S, Nador RG, Strober S. Interactions between NKT cells and Tregs are required for tolerance to combined bone marrow and organ transplants. Blood. 2012;119:1581–9.PubMedCentralCrossRefPubMed Hongo D, Tang X, Dutt S, Nador RG, Strober S. Interactions between NKT cells and Tregs are required for tolerance to combined bone marrow and organ transplants. Blood. 2012;119:1581–9.PubMedCentralCrossRefPubMed
45.
go back to reference Pillai AB, George TI, Dutt S, Strober S. Host natural killer T cells induce an interleukin-4-dependent expansion of donor CD4 + CD25 + Foxp3 + T regulatory cells that protects against graft-versus-host disease. Blood. 2009;113:4458–67.PubMedCentralCrossRefPubMed Pillai AB, George TI, Dutt S, Strober S. Host natural killer T cells induce an interleukin-4-dependent expansion of donor CD4 + CD25 + Foxp3 + T regulatory cells that protects against graft-versus-host disease. Blood. 2009;113:4458–67.PubMedCentralCrossRefPubMed
46.
go back to reference Hongo D, Tang, X, Baker, J., Strober, S. Requirement for interactions of natural killer T Cells and myeloid derived Suppressor cells for transplantation tolerance. Am J Transpl (submitted). 2014. Hongo D, Tang, X, Baker, J., Strober, S. Requirement for interactions of natural killer T Cells and myeloid derived Suppressor cells for transplantation tolerance. Am J Transpl (submitted). 2014.
47.
go back to reference Ferrara JL, Levy R, Chao NJ. Pathophysiologic mechanisms of acute graft-vs.-host disease. Biol Blood Marrow Transpl. 1999;5:347–56.CrossRef Ferrara JL, Levy R, Chao NJ. Pathophysiologic mechanisms of acute graft-vs.-host disease. Biol Blood Marrow Transpl. 1999;5:347–56.CrossRef
48.
go back to reference Palathumpat V, Dejbakhsh-Jones S, Holm B, Strober S. Different subsets of T cells in the adult mouse bone marrow and spleen induce or suppress acute graft-versus-host disease. J Immunol. 1992;149:808–17.PubMed Palathumpat V, Dejbakhsh-Jones S, Holm B, Strober S. Different subsets of T cells in the adult mouse bone marrow and spleen induce or suppress acute graft-versus-host disease. J Immunol. 1992;149:808–17.PubMed
49.
go back to reference Palathumpat V, Holm B, Dejbakhsh-Jones S, Strober S. Treatment of BCL1 leukemia by transplantation of low density fractions of allogeneic bone marrow and spleen cells. J Immunol. 1992;148:3319–26.PubMed Palathumpat V, Holm B, Dejbakhsh-Jones S, Strober S. Treatment of BCL1 leukemia by transplantation of low density fractions of allogeneic bone marrow and spleen cells. J Immunol. 1992;148:3319–26.PubMed
50.
go back to reference Zeng D, Lewis D, Dejbakhsh-Jones S, Lan F, Garcia-Ojeda M, Sibley R, et al. Bone marrow NK1.1(−) and NK1.1(+) T cells reciprocally regulate acute graft versus host disease. J Exp Med. 1999;189:1073–81.PubMedCentralCrossRefPubMed Zeng D, Lewis D, Dejbakhsh-Jones S, Lan F, Garcia-Ojeda M, Sibley R, et al. Bone marrow NK1.1(−) and NK1.1(+) T cells reciprocally regulate acute graft versus host disease. J Exp Med. 1999;189:1073–81.PubMedCentralCrossRefPubMed
51.
go back to reference Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med. 2002;196:389–99.PubMedCentralCrossRefPubMed Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med. 2002;196:389–99.PubMedCentralCrossRefPubMed
52.
go back to reference Chaidos A, Patterson S, Szydlo R, Chaudhry MS, Dazzi F, Kanfer E, et al. Graft invariant natural killer T-cell dose predicts risk of acute graft-versus-host disease in allogeneic hematopoietic stem cell transplantation. Blood. 2012;119:5030–6.CrossRefPubMed Chaidos A, Patterson S, Szydlo R, Chaudhry MS, Dazzi F, Kanfer E, et al. Graft invariant natural killer T-cell dose predicts risk of acute graft-versus-host disease in allogeneic hematopoietic stem cell transplantation. Blood. 2012;119:5030–6.CrossRefPubMed
53.
go back to reference Rubio MT, Moreira-Teixeira L, Bachy E, Bouillie M, Milpied P, Coman T, et al. Early posttransplantation donor-derived invariant natural killer T-cell recovery predicts the occurrence of acute graft-versus-host disease and overall survival. Blood. 2012;120:2144–54.CrossRefPubMed Rubio MT, Moreira-Teixeira L, Bachy E, Bouillie M, Milpied P, Coman T, et al. Early posttransplantation donor-derived invariant natural killer T-cell recovery predicts the occurrence of acute graft-versus-host disease and overall survival. Blood. 2012;120:2144–54.CrossRefPubMed
54.
go back to reference Lowsky R, Takahashi T, Liu YP, Dejbakhsh-Jones S, Grumet FC, Shizuru JA, et al. Protective conditioning for acute graft-versus-host disease. N Engl J Med. 2005;353:1321–31.CrossRefPubMed Lowsky R, Takahashi T, Liu YP, Dejbakhsh-Jones S, Grumet FC, Shizuru JA, et al. Protective conditioning for acute graft-versus-host disease. N Engl J Med. 2005;353:1321–31.CrossRefPubMed
55.
go back to reference Kohrt HE, Turnbull BB, Heydari K, Shizuru JA, Laport GG, Miklos DB, et al. TLI and ATG conditioning with low risk of graft-versus-host disease retains antitumor reactions after allogeneic hematopoietic cell transplantation from related and unrelated donors. Blood. 2009;114:1099–109.PubMedCentralCrossRefPubMed Kohrt HE, Turnbull BB, Heydari K, Shizuru JA, Laport GG, Miklos DB, et al. TLI and ATG conditioning with low risk of graft-versus-host disease retains antitumor reactions after allogeneic hematopoietic cell transplantation from related and unrelated donors. Blood. 2009;114:1099–109.PubMedCentralCrossRefPubMed
56.
go back to reference Messina G, Giaccone L, Festuccia M, Irrera G, Scortechini I, Sorasio R, et al. Multicenter experience using total lymphoid irradiation and antithymocyte globulin as conditioning for allografting in hematological malignancies. Biol Blood Marrow Transpl. 2012;18:1600–7.CrossRef Messina G, Giaccone L, Festuccia M, Irrera G, Scortechini I, Sorasio R, et al. Multicenter experience using total lymphoid irradiation and antithymocyte globulin as conditioning for allografting in hematological malignancies. Biol Blood Marrow Transpl. 2012;18:1600–7.CrossRef
57.
go back to reference Cecka JM. The UNOS scientific renal transplant registry–ten years of kidney transplants. Clin Transpl. 1997;57:1–14. Cecka JM. The UNOS scientific renal transplant registry–ten years of kidney transplants. Clin Transpl. 1997;57:1–14.
58.
go back to reference Field EH, Strober S. Tolerance, mixed chimerism and protection against GVHD after TLI. Philos Trans R Soc Lond B Biol Sci. 2001;356:1–10.CrossRef Field EH, Strober S. Tolerance, mixed chimerism and protection against GVHD after TLI. Philos Trans R Soc Lond B Biol Sci. 2001;356:1–10.CrossRef
59.
go back to reference Strober S, Spitzer TR, Lowsky R, Sykes M. Translational studies in hematopoietic cell transplantation: treatment of hematologic malignancies as a stepping stone to tolerance induction. Semin Immunol. 2011;23:273–81.PubMedCentralCrossRefPubMed Strober S, Spitzer TR, Lowsky R, Sykes M. Translational studies in hematopoietic cell transplantation: treatment of hematologic malignancies as a stepping stone to tolerance induction. Semin Immunol. 2011;23:273–81.PubMedCentralCrossRefPubMed
60.
go back to reference Hunt SA, Strober S, Hoppe RT, Stinson EB. Total lymphoid irradiation for treatment of intractable cardiac allograft rejection. J Heart Lung Transpl. 1991;10:211–6. Hunt SA, Strober S, Hoppe RT, Stinson EB. Total lymphoid irradiation for treatment of intractable cardiac allograft rejection. J Heart Lung Transpl. 1991;10:211–6.
61.
go back to reference Tallaj JA, Pamboukian SV, George JF, Brown RN, Pajaro OE, Bourge RC, et al. Total lymphoid irradiation in heart transplantation: long-term efficacy and survival–an 18-year experience. Transplantation. 2011;92:1159–64.CrossRefPubMed Tallaj JA, Pamboukian SV, George JF, Brown RN, Pajaro OE, Bourge RC, et al. Total lymphoid irradiation in heart transplantation: long-term efficacy and survival–an 18-year experience. Transplantation. 2011;92:1159–64.CrossRefPubMed
62.
go back to reference Strober S, Modry DL, Hoppe RT, Pennock JL, Bieber CP, Holm BI, et al. Induction of specific unresponsiveness to heart allografts in mongrel dogs treated with total lymphoid irradiation and antithymocyte globulin. J Immunol. 1984;132:1013–8.PubMed Strober S, Modry DL, Hoppe RT, Pennock JL, Bieber CP, Holm BI, et al. Induction of specific unresponsiveness to heart allografts in mongrel dogs treated with total lymphoid irradiation and antithymocyte globulin. J Immunol. 1984;132:1013–8.PubMed
63.
go back to reference Levin B, Hoppe RT, Collins G, Miller E, Waer M, Bieber C, et al. Treatment of cadaveric renal transplant recipients with total lymphoid irradiation, antithymocyte globulin, and low-dose prednisone. Lancet. 1985;2:1321–5.CrossRefPubMed Levin B, Hoppe RT, Collins G, Miller E, Waer M, Bieber C, et al. Treatment of cadaveric renal transplant recipients with total lymphoid irradiation, antithymocyte globulin, and low-dose prednisone. Lancet. 1985;2:1321–5.CrossRefPubMed
64.
go back to reference Saper V, Chow D, Engleman ED, Hoppe RT, Levin B, Collins G, et al. Clinical and immunological studies of cadaveric renal transplant recipients given total-lymphoid irradiation and maintained on low-dose prednisone. Transplantation. 1988;45:540–6.CrossRefPubMed Saper V, Chow D, Engleman ED, Hoppe RT, Levin B, Collins G, et al. Clinical and immunological studies of cadaveric renal transplant recipients given total-lymphoid irradiation and maintained on low-dose prednisone. Transplantation. 1988;45:540–6.CrossRefPubMed
65.
go back to reference Chow D, Saper V, Strober S. Renal transplant patients treated with total lymphoid irradiation show specific unresponsiveness to donor antigens the mixed leukocyte reaction (MLR). J Immunol. 1987;138:3746–50.PubMed Chow D, Saper V, Strober S. Renal transplant patients treated with total lymphoid irradiation show specific unresponsiveness to donor antigens the mixed leukocyte reaction (MLR). J Immunol. 1987;138:3746–50.PubMed
66.
go back to reference Strober S, Dhillon M, Schubert M, Holm B, Engleman E, Benike C, et al. Acquired immune tolerance to cadaveric renal allografts. A study of three patients treated with total lymphoid irradiation. N Engl J Med. 1989;321:28–33.CrossRefPubMed Strober S, Dhillon M, Schubert M, Holm B, Engleman E, Benike C, et al. Acquired immune tolerance to cadaveric renal allografts. A study of three patients treated with total lymphoid irradiation. N Engl J Med. 1989;321:28–33.CrossRefPubMed
67.
go back to reference Strober S, Benike C, Krishnaswamy S, Engleman EG, Grumet FC. Clinical transplantation tolerance twelve years after prospective withdrawal of immunosuppressive drugs: studies of chimerism and anti-donor reactivity. Transplantation. 2000;69:1549–54.CrossRefPubMed Strober S, Benike C, Krishnaswamy S, Engleman EG, Grumet FC. Clinical transplantation tolerance twelve years after prospective withdrawal of immunosuppressive drugs: studies of chimerism and anti-donor reactivity. Transplantation. 2000;69:1549–54.CrossRefPubMed
68.
go back to reference Millan MT, Shizuru JA, Hoffmann P, Dejbakhsh-Jones S, Scandling JD, Grumet FC, et al. Mixed chimerism and immunosuppressive drug withdrawal after HLA-mismatched kidney and hematopoietic progenitor transplantation. Transplantation. 2002;73:1386–91.CrossRefPubMed Millan MT, Shizuru JA, Hoffmann P, Dejbakhsh-Jones S, Scandling JD, Grumet FC, et al. Mixed chimerism and immunosuppressive drug withdrawal after HLA-mismatched kidney and hematopoietic progenitor transplantation. Transplantation. 2002;73:1386–91.CrossRefPubMed
69.
go back to reference Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Millan MT, Shizuru JA, et al. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J Med. 2008;358:362–8.CrossRefPubMed Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Millan MT, Shizuru JA, et al. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J Med. 2008;358:362–8.CrossRefPubMed
70.
go back to reference Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Sarwal M, Millan MT, et al. Tolerance and withdrawal of immunosuppressive drugs in patients given kidney and hematopoietic cell transplants. Am J Transpl. 2012;12:1133–45.CrossRef Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Sarwal M, Millan MT, et al. Tolerance and withdrawal of immunosuppressive drugs in patients given kidney and hematopoietic cell transplants. Am J Transpl. 2012;12:1133–45.CrossRef
Metadata
Title
Path to clinical transplantation tolerance and prevention of graft-versus-host disease
Author
Samuel Strober
Publication date
01-05-2014
Publisher
Springer US
Published in
Immunologic Research / Issue 2-3/2014
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-014-8502-7

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