Blood Reviews
Volume 17, Issue 3 , Pages 153-162 , September 2003

The graft versus leukemia response after allogeneic hematopoietic stem cell transplantation

  • Stanley R Riddell

      Affiliations

    • D3-100, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., Seattle, WA 98109, USA
    • Corresponding Author InformationCorrespondence to: Stanley R. Riddell MD, D3-100, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., Seattle, WA 98109, USA. Tel.: +1-206-667-5249; Fax: +1-206-667-7983
  • ,
  • Carolina Berger

      Affiliations

    • GSF-Haematologikum, Institute of Molecular Immunology, Room 401, Marchioninstr. 25, 81377 Munich, Germany
  • ,
  • Makoto Murata

      Affiliations

    • D3-100, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., Seattle, WA 98109, USA
  • ,
  • Sophia Randolph

      Affiliations

    • D3-100, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., Seattle, WA 98109, USA
  • ,
  • Edus H Warren

      Affiliations

    • D3-100, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., Seattle, WA 98109, USA

References 

  1. Appelbaum FR. The current status of hematopoietic cell transplantation. Annu. Rev. Med. 2002;28:28
  2. Weiden PL, Flournoy N, Thomas ED, et al.  Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. N. Engl. J. Med. 1979;300:1068–1073
  3. Weiden PL, Sullivan KM, Flournoy N, Storb R, Thomas ED. Antileukemic effect of chronic graft-versus-host disease: contribution to improved survival after allogeneic marrow transplantation. N. Engl. J. Med. 1981;304:1529–1533
  4. Horowitz MM, Gale RP, Sondel PM, et al.  Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75:555–562
  5. Kolb HJ, Mittermuller J, Clemm C, et al.  Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood. 1990;76:2462–2465
  6. Collins RH, Shpilberg O, Drobyski WR, et al.  Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J. Clin. Oncol. 1997;15:433–444
  7. Porter DL, Collins RH, Hardy C, et al.  Treatment of relapsed leukemia after unrelated donor marrow transplantation with unrelated donor leukocyte infusions. Blood. 2000;95:1214–1221
  8. Levine JE, Braun T, Penza SL, et al.  Prospective trial of chemotherapy and donor leukocyte infusions for relapse of advanced myeloid malignancies after allogeneic stem-cell transplantation. J. Clin. Oncol. 2002;20:405–412
  9. Champlin R, Khouri I, Shimoni A, et al.  Harnessing graft-versus-malignancy: non-myeloablative preparative regimens for allogeneic haematopoietic transplantation, an evolving strategy for adoptive immunotherapy. Br. J. Haematol. 2000;111:18–29
  10. McSweeney PA, Niederwieser D, Shizuru JA, et al.  Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus-tumor effects. Blood. 2001;97:3390–3400
  11. Khouri IF, Saliba RM, Giralt SA, et al.  Nonablative allogeneic hematopoietic transplantation as adoptive immunotherapy for indolent lymphoma: low incidence of toxicity, acute graft-versus-host disease, and treatment-related mortality. Blood. 2001;98:3595–3599
  12. Corradini P, Tarella C, Olivieri A, et al.  Reduced-intensity conditioning followed by allografting of hematopoietic cells can produce clinical and molecular remissions in patients with poor-risk hematologic malignancies. Blood. 2002;99:75–82
  13. Childs R, Chernoff A, Contentin N, et al.  Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation. N. Engl. J. Med. 2000;343:750–758
  14. Rini BI, Zimmerman T, Stadler WM, Gajewski TF, Vogelzang NJ. Allogeneic stem-cell transplantation of renal cell cancer after nonmyeloablative chemotherapy: feasibility, engraftment, and clinical results. J. Clin. Oncol. 2002;20:2017–2024
  15. Farag SS, Fehniger TA, Ruggeri L, Velardi A, Caligiuri MA. Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood. 2002;100:1935–1947
  16. Molldrem JJ, Komanduri K, Wieder E. Overexpressed differentiation antigens as targets of graft-versus-leukemia reactions. Curr. Opin. Hematol. 2002;9:503–508
  17. Moretta A, Bottino C, Vitale M, et al.  Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 2001;19:197–223
  18. Storkus WJ, Alexander J, Payne JA, Dawson JR, Cresswell P. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc. Natl. Acad. Sci. USA. 1989;86:2361–2364
  19. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 2001;1:41–49
  20. Miller JS. Biology of natural killer cells in cancer and infection. Cancer Invest. 2002;20:405–419
  21. Ruggeri L, Capanni M, Urbani E, et al.  Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295:2097–2100
  22. Zijlstra M, Auchincloss H, Loring JM, Chase CM, Russell PS, Jaenisch R. Skin graft rejection by β 2-microglobulin-deficient mice. J. Exp. Med. 1992;175:885–893
  23. Yu YY, Kumar V, Bennett M. Murine natural killer cells and marrow graft rejection. Annu. Rev. Immunol. 1992;10:189–213
  24. Ruggeri L, Capanni M, Casucci M, et al.  Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94:333–339
  25. Bocchia M, Korontsvit T, Xu Q, et al.  Specific human cellular immunity to bcr-abl oncogene-derived peptides. Blood. 1996;87:3587–3592
  26. Clark RE, Dodi IA, Hill SC, et al.  Direct evidence that leukemic cells present HLA-associated immunogenic peptides derived from the BCR-ABL b3a2 fusion protein. Blood. 2001;98:2887–2893
  27. Pinilla-Ibarz J, Cathcart K, Korontsvit T, et al.  Vaccination of patients with chronic myelogenous leukemia with bcr-abl oncogene breakpoint fusion peptides generates specific immune responses. Blood. 2000;95:1781–1787
  28. Molldrem JJ, Clave E, Jiang YZ, et al.  Cytotoxic T lymphocytes specific for a nonpolymorphic proteinase 3 peptide preferentially inhibit chronic myeloid leukemia colony-forming units. Blood. 1997;90:2529–2534
  29. Molldrem J, Dermime S, Parker K, et al.  Targeted T-cell therapy for human leukemia: cytotoxic T lymphocytes specific for a peptide derived from proteinase 3 preferentially lyse human myeloid leukemia cells. Blood. 1996;88:2450–2457
  30. Ohminami H, Yasukawa M, Fujita S. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood. 2000;95:286–293
  31. Bellantuono I, Gao L, Parry S, et al.  Two distinct HLA-A0201-presented epitopes of the Wilms tumor antigen 1 can function as targets for leukemia-reactive CTL. Blood. 2002;100:3835–3837
  32. Andersen MH, Pedersen LO, Capeller B, Brocker EB, Becker JC, thor Straten P. Spontaneous cytotoxic T-cell responses against survivin-derived MHC class I-restricted T-cell epitopes in situ as well as ex vivo in cancer patients. Cancer Res. 2001;61:5964–5968
  33. Golub TR. Genomic approaches to the pathogenesis of hematologic malignancy. Curr. Opin. Hematol. 2001;8:252–261
  34. Molldrem JJ, Lee PP, Wang C, et al.  Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat. Med. 2000;6:1018–1023
  35. Molldrem JJ, Kant S, Sijie L, et al.  Peptide vaccination with PRI elicits active T cell immunity that induces cytogenetic remission in acute myelogenous leukemia. Blood. 2002;100:8a
  36. Gao L, Bellantuono I, Elsasser A, et al.  Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood. 2000;95:2198–2203
  37. Harty JT, Tvinnereim AR, White DW. CD8+ T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 2000;18:275–308
  38. Ferrara JL. Cellular and cytokine effectors of acute graft versus host disease. Int. J. Hematol. 2002;76:195–198
  39. Ringden O, Labopin M, Gorin NC, et al.  Is there a graft-versus-leukaemia effect in the absence of graft-versus-host disease in patients undergoing bone marrow transplantation for acute leukaemia. Br. J. Haematol. 2000;111:1130–1137
  40. Faber LM, van der Hoeven J, Goulmy E, et al.  Recognition of clonogenic leukemic cells, remission bone marrow and HLA-identical donor bone marrow by CD8+ or CD4+ minor histocompatibility antigen-specific cytotoxic T lymphocytes. J. Clin. Invest. 1995;96:877–883
  41. Warren EH, Greenberg PD, Riddell SR. Cytotoxic T-lymphocyte-defined human minor histocompatibility antigens with a restricted tissue distribution. Blood. 1998;91:2197–2207
  42. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997;3:730–737
  43. Lapidot T, Sirard C, Vormoor J, et al.  A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–648
  44. Bonnet D, Warren EH, Greenberg PD, Dick JE, Riddell SR. CD8(+) minor histocompatibility antigen-specific cytotoxic T lymphocyte clones eliminate human acute myeloid leukemia stem cells. Proc. Natl. Acad. Sci. USA. 1999;96:8639–8644
  45. Warren EH, Gavin M, Greenberg PD, Riddell SR. Minor histocompatibility antigens as targets for T-cell therapy after bone marrow transplantation. Curr. Opin. Hematol. 1998;5:429–433
  46. Walter EA, Greenberg PD, Gilbert MJ, et al.  Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 1995;333:1038–1044
  47. Schreiber H, Wu TH, Nachman J, Kast WM. Immunodominance and tumor escape. Semin. Cancer Biol. 2002;12:25–31
  48. Riker A, Cormier J, Panelli M, et al.  Immune selection after antigen-specific immunotherapy of melanoma. Surgery. 1999;126:112–120
  49. Hunt DF, Henderson RA, Shabanowitz J, et al.  Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science. 1992;255:1261–1263
  50. Van Pel A, van der Bruggen P, Coulie PG, et al.  Genes coding for tumor antigens recognized by cytolytic T lymphocytes. Immunol. Rev. 1995;145:229–250
  51. Warren EH, Otterud BE, Linterman RW, et al.  Feasibility of using genetic linkage analysis to identify the genes encoding T cell-defined minor histocompatibility antigens. Tissue Antigens. 2002;59:293–303
  52. Gratwohl A, Hermans J, Niederwieser D, van Biezen A, van Houwelingen HC, Apperley J. Female donors influence transplant-related mortality and relapse incidence in male recipients of sibling blood and marrow transplants. Hematol. J. 2001;2:363–370
  53. Meadows L, Wang W, den Haan JM, et al.  The HLA-A*0201-restricted H-Y antigen contains a posttranslationally modified cysteine that significantly affects T cell recognition. Immunity. 1997;6:273–281
  54. Wang W, Meadows LR, den Haan JM, et al.  Human H-Y: a male-specific histocompatibility antigen derived from the SMCY protein. Science. 1995;269:1588–1590
  55. Pierce RA, Field ED, den Haan JM, et al.  Cutting edge: the HLA-A*0101-restricted HY minor histocompatibility antigen originates from DFFRY and contains a cysteinylated cysteine residue as identified by a novel mass spectrometric technique. J. Immunol. 1999;163:6360–6364
  56. Dickinson AM, Wang XN, Sviland L, et al.  In situ dissection of the graft-versus-host activities of cytotoxic T cells specific for minor histocompatibility antigens. Nat. Med. 2002;8:410–414
  57. Mutis T, Gillespie G, Schrama E, Falkenburg JH, Moss P, Goulmy E. Tetrameric HLA class I-minor histocompatibility antigen peptide complexes demonstrate minor histocompatibility antigen-specific cytotoxic T lymphocytes in patients with graft-versus-host disease. Nat. Med. 1999;5:839–842
  58. Warren EH, Gavin MA, Simpson E, et al.  The human UTY gene encodes a novel HLA-B8-restricted H-Y antigen. J. Immunol. 2000;164:2807–2814
  59. Lahn BT, Page DC. Functional coherence of the human Y chromosome. Science. 1997;278:675–680
  60. den Haan JM, Meadows LM, Wang W, et al.  The minor histocompatibility antigen HA-1: a diallelic gene with a single amino acid polymorphism. Science. 1998;279:1054–1057
  61. den Haan JM, Sherman NE, Blokland E, et al.  Identification of a graft versus host disease-associated human minor histocompatibility antigen. Science. 1995;268:1476–1480
  62. Pierce RA, Field ED, Mutis T, et al.  The HA-2 minor histocompatibility antigen is derived from a diallelic gene encoding a novel human class I myosin protein. J. Immunol. 2001;167:3223–3230
  63. Murata M, Emi N, Hirabayashi N, et al.  No significant association between HA-1 incompatibility and incidence of acute graft-versus-host disease after HLA-identical sibling bone marrow transplantation in Japanese patients. Int. J. Hematol. 2000;72:371–375
  64. Goulmy E, Schipper R, Pool J, et al.  Mismatches of minor histocompatibility antigens between HLA-identical donors and recipients and the development of graft-versus-host disease after bone marrow transplantation. N. Engl. J. Med. 1996;334:281–285
  65. Tseng LH, Lin MT, Hansen JA, et al.  Correlation between disparity for the minor histocompatibility antigen HA-1 and the development of acute graft-versus-host disease after allogeneic marrow transplantation. Blood. 1999;94:2911–2914
  66. Lin MT, Gooley T, Hansen JA, et al.  Absence of statistically significant correlation between disparity for the minor histocompatibility antigen-HA-1 and outcome after allogeneic hematopoietic cell transplantation. Blood. 2001;98:3172–3173
  67. Brickner AG, Warren EH, Caldwell JA, et al.  The immunogenicity of a new human minor histocompatibility antigen results from differential antigen processing. J. Exp. Med. 2001;193:195–206
  68. Dolstra H, Fredrix H, Maas F, et al.  A human minor histocompatibility antigen specific for B cell acute lymphoblastic leukemia. J. Exp. Med. 1999;189:301–308
  69. Bonini C, Ferrari G, Verzeletti S, et al.  HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science. 1997;276:1719–1724
  70. Riddell SR, Elliott M, Lewinsohn DA, et al.  T-cell mediated rejection of gene-modified HIV-specific cytotoxic T lymphocytes in HIV-infected patients. Nat. Med. 1996;2:216–223
  71. Thomis DC, Marktel S, Bonini C, et al.  A Fas-based suicide switch in human T cells for the treatment of graft-versus-host disease. Blood. 2001;97:1249–1257
  72. Berger C, Blau CA, Clackson T, Riddell SR, Heimfeld S. CD28 costimulation and immunoaffinity-based selection efficiently generate primary gene-modified T cells for adoptive immunotherapy. Blood. 2003;101:476–484
  73. Rooney CM, Aguilar LK, Huls MH, Brenner MK, Heslop HE. Adoptive immunotherapy of EBV-associated malignancies with EBV-specific cytotoxic T-cell lines. Curr. Top Microbiol. Immunol. 2001;258:221–229
  74. Yee C, Thompson JA, Byrd D, et al.  Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl. Acad. Sci. USA. 2002;99:16168–16173
  75. Fontaine P, Roy-Proulx G, Knafo L, Baron C, Roy DC, Perreault C. Adoptive transfer of minor histocompatibility antigen-specific T lymphocytes eradicates leukemia cells without causing graft-versus-host disease. Nat. Med. 2001;7:789–794
  76. Lee PP, Yee C, Savage PA, et al.  Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 1999;5:677–685
  77. Vogt MH, Goulmy E, Kloosterboer FM, Blokland E, de Paus RA, Willemze R, et al. UTY gene codes for an HLA-B60-restricted human male-specific minor histocompatibility antigen involved in stem cell graft rejection: characterization of the critical polymorphic amino acid residues for T-cell recognition. Blood. 2000;96(Nov 1):3126–3132

PII: S0268-960X(03)00007-9

doi: 10.1016/S0268-960X(03)00007-9

Blood Reviews
Volume 17, Issue 3 , Pages 153-162 , September 2003