Biology of Blood and Marrow Transplantation
Volume 13, Issue 2 , Pages 151-163 , February 2007

Promiscuity of the AlloHLA-A2 Restricted T Cell Repertoire Hampers the Generation of Minor Histocompatibility Antigen-specific Cytotoxic T Cells across HLA Barriers

  • Liesbeth E.M. Oosten

      Affiliations

    • Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands
    • Corresponding Author InformationCorrespondence and reprint requests: Liesbeth E. M. Oosten, MD, Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, E3-Q, Albinusdreef 2, 2333 ZA Leiden, The Netherlands
  • ,
  • Els Blokland

      Affiliations

    • Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands
  • ,
  • Michel G.D. Kester

      Affiliations

    • Department of Hematology, Leiden University Medical Center, Leiden, The Netherlands
  • ,
  • J.H. Frederik Falkenburg

      Affiliations

    • Department of Hematology, Leiden University Medical Center, Leiden, The Netherlands
  • ,
  • Astrid G.S. van Halteren

      Affiliations

    • Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands
  • ,
  • Els Goulmy

      Affiliations

    • Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands

Received 29 August 2006 ,Accepted 20 October 2006.

References 

  1. Armitage JO. Bone marrow transplantation. N Engl J Med. 1994;330:827–838
  2. Anasetti C, Amos D, Beatty PG, et al. Effect of HLA compatibility on engraftment of bone marrow transplants in patients with leukemia or lymphoma. N Engl J Med. 1989;320:197–204
  3. Ottinger H, Grosse-Wilde M, Schmitz A, Grosse-Wilde H. Immunogenetic marrow donor search for 1012 patients: a retrospective analysis of strategies, outcome and costs. Bone Marrow Transplant. 1994;14(suppl 4):S34–S38
  4. Aversa F, Tabilio A, Velardi A, et al. Treatment of high-risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Engl J Med. 1998;339:1186–1193
  5. Sykes M, Preffer F, McAfee S, et al. Mixed lymphohaemopoietic chimerism and graft-versus-lymphoma effects after non-myeloablative therapy and HLA-mismatched bone-marrow transplantation. Lancet. 1999;353:1755–1759
  6. Champlin RE, Passweg JR, Zhang MJ, et al. T-cell depletion of bone marrow transplants for leukemia from donors other than HLA-identical siblings: advantage of T-cell antibodies with narrow specificities. Blood. 2000;95:3996–4003
  7. Ash RC, Horowitz MM, Gale RP, et al. Bone marrow transplantation from related donors other than HLA-identical siblings: effect of T cell depletion. Bone Marrow Transplant. 1991;7:443–452
  8. Horowitz MM, Gale RP, Sondel PM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75:555–562
  9. Champlin R. T-cell depletion for allogeneic bone marrow transplantation: impact on graft-versus-host disease, engraftment, and graft-versus-leukemia. J Hematother. 1993;2:27–42
  10. Kolb HJ, Holler E. Adoptive immunotherapy with donor lymphocyte transfusions. Curr Opin Oncol. 1997;9:139–145
  11. Lewalle P, Delforge A, Aoun M, et al. Growth factors and DLI in adult haploidentical transplant: a three-step pilot study towards patient and disease status adjusted management. Blood Cells Mol Dis. 2004;33:256–260
  12. 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
  13. Mutis T, Blokland E, Kester M, Schrama E, Goulmy E. Generation of minor histocompatibility antigen HA-1-specific cytotoxic T cells restricted by nonself HLA molecules: a potential strategy to treat relapsed leukemia after HLA-mismatched stem cell transplantation. Blood. 2002;100:547–552
  14. Savage P, Gao L, Vento K, et al. Use of B cell-bound HLA-A2 class I monomers to generate high-avidity, allo-restricted CTLs against the leukemia-associated protein Wilms tumor antigen. Blood. 2004;103:4613–4615
  15. Dutoit V, Guillaume P, Romero P, Cerottini JC, Valmori D. Functional analysis of HLA-A*0201/Melan-A peptide multimer+ CD8+ T cells isolated from an HLA-A* 0201- donor: exploring tumor antigen allorestricted recognition. Cancer Immun. 2002;2:7
  16. Sadovnikova E, Parovichnikova EN, Savchenko VG, Zabotina T, Stauss HJ. The CD68 protein as a potential target for leukaemia-reactive CTL. Leukemia. 2002;16:2019–2026
  17. Moris A, Teichgraber V, Gauthier L, Buhring HJ, Rammensee H-G. Cutting edge: characterization of allorestricted and peptide-selective alloreactive T cells using HLA-tetramer selection. J Immunol. 2001;166:4818–4821
  18. Amrolia PJ, Reid SD, Gao L, et al. Allorestricted cytotoxic T cells specific for human CD45 show potent antileukemic activity. Blood. 2003;101:1007–1014
  19. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245–252
  20. Mutis T, Verdijk R, Schrama E, Esendam B, Brand A, Goulmy E. Feasibility of immunotherapy of relapsed leukemia with ex vivo-generated cytotoxic T lymphocytes specific for hematopoietic system-restricted minor histocompatibility antigens. Blood. 1999;93:2336–2341
  21. Goulmy E. Human minor histocompatibility antigens. Curr Opin Immunol. 1996;8:75–81
  22. de Bueger M, Bakker A, Van Rood JJ, van der Woude F, Goulmy E. Tissue distribution of human minor histocompatibility antigens (Ubiquitous versus restricted tissue distribution indicates heterogeneity among human cytotoxic T lymphocyte-defined non-MHC antigens). J Immunol. 1992;149:1788–1794
  23. van der Harst D, Goulmy E, Falkenburg JHF, et al. Recognition of minor histocompatibility antigens on lymphocytic and myeloid leukemic cells by cytotoxic T-cell clones. Blood. 1994;83:1060–1066
  24. Falkenburg JHF, Goselink HM, van der Harst D, et al. Growth inhibition of clonogenic leukemic precursor cells by minor histocompatibility antigen-specific cytotoxic T lymphocytes. J Exp Med. 1991;174:27–33
  25. Marijt WA, Heemskerk MH, Kloosterboer FM, et al. Hematopoiesis-restricted minor histocompatibility antigens HA-1- or HA-2-specific T cells can induce complete remissions of relapsed leukemia. Proc Natl Acad Sci USA. 2003;100:2742–2747
  26. Hambach L, Nijmeijer BA, Aghai Z, et al. Human cytotoxic T lymphocytes specific for a single minor histocompatibility antigen HA-1 are effective against human lymphoblastic leukaemia in NOD/scid mice. Leukemia. 2006;20:371–374
  27. 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
  28. 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
  29. 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
  30. Wills MR, Carmichael AJ, Mynard K, et al. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol. 1996;70:7569–7579
  31. Mutis T, Gillespie G, Schrama E, Falkenburg JHF, 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
  32. Gillespie G, Mutis T, Schrama E, et al. HLA class I-minor histocompatibility antigen tetramers select cytotoxic T cells with high avidity to the natural ligand. Hematol J. 2000;1:403–410
  33. de Bueger M, Verreck F, Blokland E, et al. Isolation of an HLA-A2.1 extracted human minor histocompatibility peptide. Eur J Immunol. 1993;23:614–618
  34. Oosten LEM, Blokland E, van Halteren AGS, et al. Artificial antigen-presenting constructs efficiently stimulate minor histocompatibility antigen-specific cytotoxic T lymphocytes. Blood. 2004;104:224–226
  35. Mommaas B, Kamp J, Drijfhout JW, et al. Identification of a novel HLA-B60-restricted T cell epitope of the minor histocompatibility antigen HA-1 locus. J Immunol. 2002;169:3131–3136
  36. Verdijk RM, Kloosterman A, Pool J, et al. Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: implications for stem cell transplantation and immunotherapy. Blood. 2004;103:1961–1964
  37. van Els CA, D’Amaro J, Pool J, et al. Immunogenetics of human minor histocompatibility antigens: their polymorphism and immunodominance. Immunogenetics. 1992;35:161–165
  38. Burrows SR, Khanna R, Silins SL, Moss DJ. The influence of antiviral T-cell responses on the alloreactive repertoire. Immunol Today. 1999;20:203–207
  39. Wucherpfennig KW. T cell receptor crossreactivity as a general property of T cell recognition. Mol Immunol. 2004;40:1009–1017
  40. Maverakis E, van den Elzen P, Sercarz EE. Self-reactive T cells and degeneracy of T cell recognition: evolving concepts—from sequence homology to shape mimicry and TCR flexibility. J Autoimmun. 2001;16:201–209
  41. Wilson DB, Wilson DH, Schroder K, et al. Specificity and degeneracy of T cells. Mol Immunol. 2004;40:1047–1055
  42. Heemskerk MH, de Paus RA, Lurvink EG, et al. Dual HLA class I and class II restricted recognition of alloreactive T lymphocytes mediated by a single T cell receptor complex. Proc Natl Acad Sci USA. 2001;98:6806–6811
  43. Matzinger P, Bevan MJ. Hypothesis: why do so many lymphocytes respond to major histocompatibility antigens?. Cell Immunol. 1977;29:1–5
  44. Lindahl KF, Wilson DB. Histocompatibility antigen-activated cytotoxic T lymphocytes (II. Estimates of the frequency and specificity of precursors). J Exp Med. 1977;145:508–522
  45. Rotzschke O, Falk K, Faath S, Rammensee H-G. On the nature of peptides involved in T cell alloreactivity. J Exp Med. 1991;174:1059–1071
  46. Chattopadhyay S, Theobald M, Biggs J, Sherman LA. Conformational differences in major histocompatibility complex-peptide complexes can result in alloreactivity. J Exp Med. 1994;179:213–219
  47. Elliott TJ, Eisen HN. Cytotoxic T lymphocytes recognize a reconstituted class I histocompatibility antigen (HLA-A2) as an allogeneic target molecule. Proc Natl Acad Sci USA. 1990;87:5213–5217
  48. Smith PA, Brunmark A, Jackson MR, Potter TA. Peptide-independent recognition by alloreactive cytotoxic T lymphocytes (CTL). J Exp Med. 1997;185:1023–1033
  49. Alexander-Miller MA, Burke K, Koszinowski UH, Hansen TH, Connolly JM. Alloreactive cytotoxic T lymphocytes generated in the presence of viral-derived peptides show exquisite peptide and MHC specificity. J Immunol. 1993;151:1–10
  50. Tallquist MD, Yun TJ, Pease LR. A single T cell receptor recognizes structurally distinct MHC/peptide complexes with high specificity. J Exp Med. 1996;184:1017–1026
  51. Obst R, Munz C, Stevanovic S, Rammensee H-G. Allo- and self-restricted cytotoxic T lymphocytes against a peptide library: evidence for a functionally diverse allorestricted T cell repertoire. Eur J Immunol. 1998;28:2432–2443
  52. Sadovnikova E, Stauss HJ. Peptide-specific cytotoxic T lymphocytes restricted by nonself major histocompatibility complex class I molecules: reagents for tumor immunotherapy. Proc Natl Acad Sci USA. 1996;93:13114–13118
  53. Wang W, Man S, Gulden PH, Hunt DF, Engelhard VH. Class I-restricted alloreactive cytotoxic T lymphocytes recognize a complex array of specific MHC-associated peptides. J Immunol. 1998;160:1091–1097
  54. Altman JD, Moss PA, Goulder PJ, et al. Phenotypic analysis of antigen-specific T lymphocytes. Science. 1996;274:94–96
  55. Ogg GS, Jin X, Bonhoeffer S, et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science. 1998;279:2103–2106

PII: S1083-8791(06)00732-4

doi: 10.1016/j.bbmt.2006.10.025

Biology of Blood and Marrow Transplantation
Volume 13, Issue 2 , Pages 151-163 , February 2007