Th2 and tc2 cells in the regulation of GVHD, GVL, and graft rejection: Considerations for the allogeneic transplantation therapy of leukemia and lymphoma

Leukemia and Lymphoma

Volumn 38, Issue 3-4, 2000, Pages 221-234

  Fowler, Daniel H ^a,b   Gress, Ronald E ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Allotransplantation; GVHD; GVL; Stem cell transplant; Tc1 and Tc2 cells; Th1 cells; Th2 cells; Therapy of leukemia and lymphoma

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; PERFORIN;

ALLOGENIC BONE MARROW TRANSPLANTATION; CYTOKINE RELEASE; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LEUKEMIA; LYMPHOMA; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 0034067656     PISSN: 10428194     EISSN: None     Source Type: Journal    
DOI: 10.3109/10428190009087014     Document Type: Review

References (84)

1. Singhal, S., Powles, R., Treleaven, J., Kulkarni, S., Horton, C., and Mehta, J. (1995). Long-term outcome of adult acute leukemia patients who are alive and well two years after allogeneic bone marrow transplantation from an HLA- identical sibling. Leukemia Lymphoma, 34(3-4):287-94.
2. Bensinger, W.I., Buckner, D., and Gahrton, G. (1997). Allogeneic stem cell transplantation for multiple myeloma. Hematology Oncology Clinics of North America, 11(1):147-57.
3. Pavletic, Z.S., Bishop, M.R., Bierman, P.J., and Armitage, J.O. (1996). Bone marrow transplantation in chronic lymphocytic leukemia and lymphomas. Biomedical Pharmacotherapy, 50(3-4):118-24.
4. Petersdorf, E., Anasetti, C., Servida, P., Martin, P., and Hansen, J. (1998). Effect of HLA matching on outcome of related and unrelated donor transplantation therapy for chronic myelogenous leukemia. Hematology Oncology Clinics of North America, 12(1):107-21.
5. Aversa, F., Terenzi, A., Carotti, A., Felicini, R., Jacucci, R., Zei, T., Latini, P., Aristei, C., Santucci, A., Martelli, M.P., Cunningham, I., Reisner, Y., and Martelli, M.F. (1999). Improved outcome with T-cell-depleted bone marrow transplantation for acute leukemia. Journal of Clinical Oncology, 17(5):1545-50.
6. Lamparelli, T., Van Lint, M.T., Gualandi, F., Occhini, D., Barbanti, M., Sacchi, N., Ficai, F., Ghinatti, C., Ferrara, G.B., Delfino, L., Pozzi, S., Morabito, A., Zikus, P., Vitale, V., Coruo, R., Frassoni, F., and Bacigalupo, A. (1997). Bone marrow transplantation for chronic myeloid leukemia (CML) from unrelated and sibling donors: single center experience. Bone Marrow Transplantation, 20(12): 1057-62.
7. Kolb, H.J., Mittermuller, J., Clemm, C., Holler, E., Ledderose, G., Brehm, G., Heim, M., and Wilmanns, W. (1990). Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood, 76:2462-2465.
8. Porter, D.L., Roth, M.S., Lee, S.J., McGarigle, C., Ferrara, J.L., and Antin, J.H. (1996). Adoptive immunotherapy with donor mononuclear cell infusions to treat relapse of acute leukemia or myelodysplasia after allogeneic bone marrow transplantation. Bone Marrow Transplantation, 18:975-980.
9. Porter, D.L., Roth, M.S., McGarigle, C., Ferrara, J.L., and Antin J.H. (1994). Induction of graft-versus-host disease as immunotherapy for relapsed chronic myeloid leukemia. New England Journal of Medicine, 330(2):100-6.
10. Mandigers, C.M., Meijerink, J.P., Raemaekers, J.M., Schattenberg, A.V., and Mensink, E.J. (1998). Graft-versus-lymphoma effect of donor leucocyte infusion shown by real-time quantitative PCR analysis of t(14;18) [letter]. Lancet, 352(9139):1522-3.
11. Ratanatharathorn, V., Uberti, J., Karanes, C., Abella, E., Lum, L.G., Momin, F., Cummings, G., and Sensenbrenner, L.L. (1994). Prospective comparative trial of autologous versus allogeneic bone marrow transplantation in patients with non-Hodgkin's lymphoma. Blood, 84:1050-1055.
12. Tricot, G., Vesole, D.H., Jagannath, S., Hilton, J., Munshi, N., and Barlogie, B. (1996). Graft-versus-myeloma effect: proof of principle. Blood, 87(3):1196-8.
13. Kolb, H.J. (1998). Donor leukocyte transfusions for treatment of leukemic relapse after bone marrow transplantation. EBMT Immunology and Chronic Leukemia Working Parties. Vox Sanguinis, 2:321-9.
14. Collins, R.H., Jr., Shpilberg, O., Drobyski, W.R., Porter, D.L., Giralt, S., Champlin, R., Goodman, S.A., Wolff, S.N., Hu, W., Verfaillie, C., List, A., Dalton, W., Ognoskie, N., Chetrit, A., Antin, J.H., and Nemunaitis, J. (1997). Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation [see comments]. Journal of Clinical Oncology, 15(2):433-44.
15. Poynton, C.H. (1988). T cell depletion in bone marrow transplantation. Bone Marrow Transplantation, 3:265-279.
16. Quinones, R.R., Gutierrez, R.H., Dinndorf, P.A., Gress, R.E., Ney, A.B., Taylor, B., Karandish, S., Carter, C.S., Luban, N.L., and Reaman, G.H. (1993). Extended-cycle elutriation to adjust T-cell content in HLA-disparate bone marrow transplantation. Blood, 82:307-317.
17. Champlin, R., Gajewski, J., Feig, S., Giorgi, J., Lyddane, N., Lee, K., Schmidt, I., Winston, D., Ho, W., and Reichert, T. (1989). Selective depletion of CD8 positive T-lymphocytes for prevention of graft-versus-host disease following allogeneic bone marrow transplantation. Transplant Proceedings, 21:2947-2948.
18. Bordignon, C., Bonini, C., Verzeletti, S., Nobili, N., Maggioni, D., Traversari, C., Giarazzi, R., Servida, P., Zappone, E., and Benazzi, E. (1995). Transfer of the HSV-tk gene into donor peripheral blood lymphocytes for in vivo modulation of donor anti-tumor immunity after allogeneic bone marrow transplantation. Human Gene Therapy, 6:813-819.
19. Mosmann, T.R., Cherwinski, H., Bond, M.W., Giedlin, M.A., and Coffman, R.L. (1986). Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology, 136:2348-2357.
20. Sad, S., and Mosmann, T.R. (1994). Single IL-2-Secreting Precursor CD4 T cell Can Develop into either Th1 or Th2 Cytokine Secretion Phenotype. Journal of Immunology, 153:3514-3522.
21. Sad, S., Marcotte, R., and Mosmann, T.R. (1995). Cytokine-induced differentiation of precursor mouse CD8+ T cells into cytotoxic CD8+ T cells secreting Th1 or Th2 cytokines. Immunity, 2:271-279.
22. Croft, M., Carter, L., Swain, S.L., and Dutton, R.W. (1994). Generation of polarized antigen-specific CD8 effector populations: reciprocal action of interleukin (IL)-4 and IL-12 in promoting type 2 versus type 1 cytokine profiles. Journal of Experimental Medicine, 180:1715-1728.
23. Powrie, F., Correa-Oliveira, R., Mauze, S., and Coffman, R.L. (1994). Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity. Journal of Experimental Medicine, 179:589-600.
24. Sher, A., Gazzinelli, R.T., Oswald, I.P., Clerici, M., Kullberg, M., Pearce, E.J., Berzofsky, J.A., Mosmann, T.R., James, S.L., Morse, H.C., and Shearer, G.M. (1992). Role of T-cell derived cytokines in the downregulation of immune responses in parasitic and retroviral infection. Immunology Reviews, 127:183-204.
25. Romagnani, S. (1994). Lymphokine production by human T cells in disease states. Annual Review of Immunology, 12:227-257.
26. Ferrara, J.L., Abhyankar, S., and Gilliland, D.G. (1993). Cytokine storm of graft-versus-host disease: a critical effector role for interleukin-1. Transplant Proceedings, 25:1216-1217.
27. Schwarer, A.P., Jiang, Y.Z., Brookes, P.A., Barrett, A.J., Batchelor, J.R., Goldman, J.M., and Lechler, R.I. (1994). Frequency of anti-recipient alloreactive helper T-cell precursors in donor blood and graft-versus-host disease after HLA-identical sibling bone-marrow transplantation. Lancet, 341:203-205.
28. Ramsdell, F., Seaman, M.S., Miller, R.E., Picha, K.S., Kennedy, M.K., and Lynch. D.H. (1994). Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. International Immunology, 6:1545-1553.
29. Baker, M.B., Riley, R.L., Podack, E.R., and Levy, R.B. (1997). Graft-versus-host-disease-associated lymphoid hypoplasia and B cell dysfunction is dependent upon donor T cell-mediated Fas-ligand function, but not perform function. Proceedings of the National Academy of Sciences, U S A, 94(4): 1366-71.
30. Braun, M.Y., Lowin, B., French, L., Acha-Orbea, H., and Tschopp, J. (1996). Cytotoxic T cells deficient in both functional fas ligand and perform show residual cytolytic activity yet lose their capacity to induce lethal acute graft-versus-host disease. Journal of Experimental Medicine, 183:657-661.
31. Das, H., Imoto, S., Murayama, T., Kajimoto, K., Sugimoto, T., Isobe, T., Nakagawa, T., Nishimura, R., and Kuizumi, T. (1999). Levels of soluble FasL and FasL gene expression during the development of graft-versus-host disease in DLT-treated patients. British Journal of Haematology, 104(4):795-800.
32. Kanda, Y., Tanaka, Y. Shirakawa, K., Yatomi, T., Nakamura, N., Kami, M., Saito, T. Izutsu, K., Asai, T., Yuji, K., Ogawa, S., Honda, H., Mitani, K., Chiba, S., Yazaki, Y., and Hirai, H. (1998). Increased soluble Fas-ligand in sera of bone marrow transplant recipients with acute graft-versus-host disease. Bone Marrow Transplantation, 22(8):751-4.
33. Sher, A., Fiorentino, D., Caspar, P., Pearce, E., and Mosmann, T. (1991). Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. Journal of Immunology, 147:2713-2716.
34. Oswald, I.P., Wynn, T.A., Sher, A., and James, S.L. (1992). Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proceedings of the National Academy of Sciences, U.S.A., 89:8676-8680.
35. Bogdan, C., and Nathan, C. (1993). Modulation of macrophage function by transforming growth factor beta, interleukin-4, and interleukin-10. Annals of the N.Y. Academy of Sciences, 685:713-739.
36. Korngold, R. (1992). Lethal graft-versus-host disease in mice directed to multiple minor histocompatibility antigens: features of CD8+ and CD4+ T cell responses. Bone Marrow Transplantation, 9:355-364.
37. Carter, L.L., and Dutton, R.W. (1995). Relative perforin- and Fas-mediated lysis in T1 and T2 CD8 effector populations. Journal of Immunology, 155:1028-1031.
38. Lin, T., Brunner, T., Tietz, B., Madsen, J., Bonfoco, E., Reaves, M., Huflejt, M., and Green, D.R. (1998). Fas ligand-mediated killing by intestinal intraepithelial lymphocytes. Participation in intestinal graft-versus-host disease. Journal of Clinical Investigation, 101(3):570-7.
39. Graubert, T.A., DiPersio, J.F., Russell, J.H., and Ley, T.J. (1997). Perforin/granzyme-dependent and independent mechanisms are both important for the development of graft-versus-host disease after murine bone marrow transplantation. Journal of Clinical Investigation, 100(4):904-11.
40. Nestel, F.P., Price, K.S., Seemayer, T.A., and Lapp, W.S. (1992). Macrophage priming and lipopolysaccharide-triggered release of tumor necrosis factor alpha during graft-versus-host disease. Journal of Experimental Medicine, 175:405-413.
41. Hill, G.R., Crawford, J.M., Cooke, K.R., Brinson, Y.S., Pan, L., and Ferrara, J.L. (1997). Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood, 90(8):3204-13.
42. Estaquier, J., and Ameisen, J.C. (1997). A role for T-helper type-1 and type-2 cytokines in the regulation of human monocyte apoptosis. Blood, 90(4):1618-25.
43. Nishimura, T., and Ohta, A. (1999). A critical role for antigen-specific Th1 cells in acute liver injury in mice. Journal of Immunology, 162(11):6503-9.
44. Champlin, R., Ho, W., Gajewski, J., Feig, S., Burnison, M., Holley, G., Greenberg, P, Lee, K., Schmid, I., and Giorgi, J. (1990). Selective depletion of CD8+ T lymphocytes for prevention of graft- versus-host disease after allogeneic hone marrow transplantation. Blood, 76(2):418-23.
45. Fowler, D.H., Kurasawa, K., Husebekk, A., Cohen, P.A., and Gress, R.E. (1994). Cells of Th2 cytokine phenotype prevent LPS-induced lethality during murine graft-versus-host reaction. Regulation of cytokines and CD8+ lymphoid engraftment. Journal of Immunology, 152:1004-1013.
46. nded. New York: Marcel Decker, Inc.
47. Krenger, W., Snyder, K.M., Byon, J.C., Falzarano, G., and Ferrara, J.L. (1995). Polarized type 2 alloreactive CD4+ and CD8+ donor T cells fail to induce experimental acute graft-versus-host disease. Journal of Immunology, 155:585-593.
48. Krenger, W., Cooke, K.R., Crawford, J.M., Sonis, S.T., Simmons, R., Pan, L., Demonte, J., Jr., Kavandikar, M., and Ferrara, J.L. (1996). Transplantation of polarized type 2 donor T cells reduces mortality caused by experimental graft-versus-host disease. Transplantation, 62:1278-1285.
49. Krenger, W., Snyder, K., Smith, S., and Ferrara, J.L. (1994). Effects of exogenous interleukin-10 in a murine model of graft-versus-host disease to minor histocompatibility antigens. Transplantation, 58:1251-1257.
50. Blazar, B.R., Taylor, P.A., Smith, S., and Vallera, D.A. (1995). Interleukin-10 administration decreases survival in murine recipients of major histocompatibility complex disparate donor bone marrow grafts. Blood, 85(3):842-51.
51. Blazar, B.R., Taylor, P.A., Panoskaltsis-Mortari, A., Narula, S.K., Smith, S.R., Roncarolo, M.G., and Vallera, D.A. (1998). Interleukin-10 dose-dependent regulation of CD4+ and CD8+ T cell- mediated graft-versus-host disease. Transplantation, 66(9):1220-9.
52. Baker, K.S., Roncarolo, M.G., Peters, C., Bigler, M., DeFor, T., and Blazar, B.R. (1999). High spontaneous IL-10 production in unrelated bone marrow transplant recipients is associated with fewer transplant-related complications and early deaths. Bone Marrow Transplantation, 23(11):1123-9.
53. Fowler, D.H., Kurasawa, K., Smith, R., Eckhaus, M.A., and Gress, R.E. (1994). Donor CD4-enriched Cells of Th2 Cytokine Phenotype Regulate Graft-versus-Host Disease Without Impairing Allogeneic Engraftment in Sublethally Irradiated Mice. Blood, 84(9):3540-3549.
54. Martin, P.J., Akatsuka, Y., Hahne, M., and Sale, G. (1998). Involvement of donor T-cell cytotoxic effector mechanisms in preventing allogeneic marrow graft rejection. Blood, 92(6):2177-81.
55. Halverson, D., Schwartz, G., Carter, C., Gress, R.E., and Fowler, D.H. (1997). In Vitro Generation of Allospecific Human CD8+ T Cells of Tc1 and Tc2 Phenotype. Blood, 90, (5):2089-2096.
56. Qin, S., Cobbold, S.P., Pope, H., Elliott, J., Kioussis, D., Davies, J., and Waldmann, H. (1993). Infectious transplantation tolerance. Science, 259:974-977.
57. Fowler, D.H., Breglio, J., Nagel, G., and Gress, R.E. (1996). Allospecific CD4+, Th1/Th2 and CD8+, Tc1/Tc2 Populations in Murine GVL: Type I cells generate GVL, Type II cells abrogate GVL. Biology of Blood and Marrow Transplantation, 2:118-125.
58. Hill, L.L., Ouhtit, A., Loughlin, S.M., Kripke, M.L., Ananthaswamy, H.N., and Owen-Schauh, L.B. (1999). Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science, 285(5429):898-900.
59. van den Broek, M.E., Kagi, D., Ossendorp, F., Toes, R., Vamvakas, S., Lutz, W.K., Melief, C.J., Zinkernagel, R.M., and Hengartner, H. (1996). Decreased tumor surveillance in perforin-deficient mice. Journal of Experimental Medicine, 184(5):1781-90.
60. Earth, R.J., Jr., Mule, J.J., Spiess, P.J., and Rosenberg, S.A. (1991). Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. Journal of Experimental Medicine, 173:647-658.
61. Ding, L., Linsley, P.S., Huang, L.Y., Germain, R.N., and Shevach EM. (1993). IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. Journal of Immunology, 151:1224-1234.
62. Oswald, I.P., Gazzinelli, R.T., Sher, A., and James, S.L. (1992). IL-10 synergizes with IL-4 and transforming growth factor-beta to inhibit macrophage cytotoxic activity. Journal of Immunology, 148:3578-3582.
63. Fowler, D.H., Breglio, J., Nagel, G., Eckhaus, M., and Gress, R.E. (1996). Allospecific CD8+ Tc1 and Tc2 Populations in GVL and GVHD. Journal of Immunology, 157:4811-4821.
64. Tsukada, N., Kobata, T., Aizawa, Y., Yagita, H., and Okumura, K. (1999). Graft-versus-leukemia effect and graft-versus-host disease can be differentiated by cytotoxic mechanisms in a murine model of allogeneic bone marrow transplantation. Blood, 93(8):2738-47.
65. Hill, G.R., Cooke, K.R., Teshima, T., Crawford, J.M., Keith, J.C., Jr., Brinson, Y.S., Bungard, D., and Ferrara, J.L. (1998). Interleukin-11 promotes T cell polarization and prevents acute graft- versus-host disease after allogeneic bone marrow transplantation. Journal of Clinical Investigation, 102(1):115-23.
66. Teshima, T., Hill, G.R., Pan, L., Brinson, Y.S., van den Brink, M.R., Cooke, K.R., and Ferrara, J.L. (1999). IL-11 separates graft-versus-leukemia effects from graft-versus-host disease after bone marrow transplantation. Journal of Clinical Investigation, 104(3):317-25.
67. Bacigalupo, A., Soracco, M., Vassallo, F., Abate, M., Van Lint, M.T., Gualandi, F., Lamparelli, T., Occhini, D., Mordini, N., Bregante, S., Figari, O., Benvenuto, F., Sessarego, M., Fugazza, G., Carlier, P., Valbonesi, M., Aker, M., Kapelushnik, J., Pugatsch, T., Naparstek, E., Ben-Neria, S., Yehuda, O., Amar, A., Nagler, A., Slavin, S., and Or, R. (1997). Donor lymphocyte infusions (DLI) in patients with chronic myeloid leukemia following allogeneic bone marrow transplantation. Bone Marrow Transplantation, 19(9):927-32.
68. Garicochea, B., van Rhee, F., Spencer, A., Chase, A., Lin, F., Cross, N.C., and Goldmann, J.M. (1994). Aplasia after donor lymphocyte infusion (DLI) for CML in relapse after sex-mismatched BMT: recovery of donor-type haemopoiesis predicted by non-isotopic in situ hybridization (ISH). British Journal of Haematology, 88(2):400-2.
69. Gupta, P., Niehans, G.A., LeRoy, S.C., Gupta, K., Morrison, V.A., Schultz, C., Knapp, D.J., and Kratzke, R.A. (1999). Fas ligand expression in the bone marrow in myelodysplastic syndromes correlates with FAB subtype and anemia, and predicts survival. Leukemia, 13(1):44-70.
70. Nishimura, M., Uchida, S., Mitsunaga, S., Yahagi, Y., Nakajima, K., Tadokoro, K., and Juji, T. (1997). Characterization of T-cell clones derived from peripheral blood lymphocytes of a patient with transfusion-associated graft-versus-host disease: Fas-mediated killing by CD4+ and CD8+ cytotoxic T-cell clones and tumor necrosis factor beta production by CD4+ T-cell clones. Blood, 89(4):1440-5.
71. Blazar, B.R., Taylor, P.A., Boyer, M.W., Panoskaltsis-Mortari, A., Allison, J.P., and Vallera, D.A. (1997). CD28/B7 interactions are required for sustaining the graft-versus-leukemia effect of delayed post-bone marrow transplantation splenocyte infusion in murine recipients of myeloid or lymphoid leukemia cells. Journal of Immunology, 159:3460-3473.
72. Williams JF, Petrus MJ, Wright JA, Husebekk A, Fellowes V, Read EJ, Gress, R.E., and Fowler, D.H. (1999). Fas-mediated lysis of chronic lymphocytic leukaemia cells: role of type I versus type II cytokines and autologous FasL-expressing T cells. British Journal of Haematology, 107.
73. Martin, P.J. (1993). Donor CD8 cells prevent allogeneic marrow graft rejection in mice: potential implications for marrow transplantation in humans. Journal of Experimental Medicine, 178:703-712.
74. Fink, P.J., Shimonkevitz, R.P., and Bevan, M.J. (1988). Veto cells. Annuual RevImmunol. 6:115-137.
75. Hiruma, K., Nakamura, H., Henkart, P.A., and Gress, R.E. (1992). Clonal deletion of postthymic T cells: veto cells kill precursor cytotoxic T lymphocytes. Journal of Experimental Medicine, 175:863-868.
76. George, J.F., and Thomas, J.M. (1999). The molecular mechanisms of veto mediated regulation of alloresponsiveness. Journal of Molecular Medicine, 77(7):519-26.
77. Nakamura, H., and Gress, R.E. (1990). Interleukin 2 enhancement of veto suppressor cell function in T-cell-depleted bone marrow in vitro and in vivo. Transplantation, 49:931-937.
78. Martin, P.J. (1996). Prevention of allogeneic marrow graft rejection by donor T cells that do not recognize recipient alloantigens: potential role of a veto mechanism. Blood. 88:962-969.
79. Bachar-Lustig, E., Li, H.W., Marcus, H., and Reisner, Y. (1998). Tolerance induction by megadose stem cell transplants: synergism between SCA-1+ Lin- cells and nonalloreactive Tcells. Transplant Proceedings, 30(8):4007-8.
80. Fowler, D., Whitfield, B., Livingston, M., Chrobak, P., and Gress, R.E. (1998). Non-host reactive donor CD8+ T cells of Tc2 phenotype potently inhibit marrow graft rejection. Blood, 91(11):4045-4050.
81. Mavroudis, D.A., Dermime, S., Molldrem, J., Jiang, Y.Z., Raptis, A., van Rhee, F., Hensel, N., Fellowes, V., Eliopoulos, G., and Barrett, A.J. (1998). Specific depletion of alloreactive T cells in HLA-identical siblings: a method for separating graft-versus-host and graft-versus-leukaemia reactions. British Journal of Haematology, 101(3):565-70.
82. Guinan, E.C., Boussiotis, V.A., Neuberg, D., Brennan, L.L., Hirano, N., Nadler, L.M., and Gribben, J.G. (1999). Transplantation of anergic histoincompatible bone marrow allografts. New England Journal of Medicine, 340(22): 1704-14.
83. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, and Roncarolo, M.G. (1997). A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature, 389(6652):737-42.
84. Sallusto, F., Lanzavecchia, A., and Mackay, CR. (1998). Chemokines and chemokine receptors in T-cell priming and Th1/Th2- mediated responses. Immunology Today, 19(12):568-74.