Biology of Blood and Marrow Transplantation
Volume 12, Issue 11 , Pages 1114-1124 , November 2006

Minor Histocompatibility Antigen DDX3Y Induces HLA-DQ5-Restricted T Cell Responses with Limited TCR-Vβ Usage Both In Vivo and In Vitro

  • David Laurin

      Affiliations

    • Cell Therapy Department, Etablissement Français du Sang Région Rhône-Alpes, Rhône, France
    • David Laurin and Eric Spierings contributed equally to this study.
    • ,
  • Eric Spierings

      Affiliations

    • Department of Immunohematology and Blood Transfusion and the Laboratory of Experimental Hematology
    • David Laurin and Eric Spierings contributed equally to this study.
    • ,
  • Lars T. van der Veken

      Affiliations

    • Department of Experimental Hematology, Leiden University Medical Center, Leiden, The Netherlands
    • ,
  • Abdelbasset Hamrouni

      Affiliations

    • INSERM U524, Lille, France
    • ,
  • J.H. Frederik Falkenburg

      Affiliations

    • Department of Experimental Hematology, Leiden University Medical Center, Leiden, The Netherlands
    • ,
  • Gerard Souillet

      Affiliations

    • Department of Hematology, Hôpital Debrousse, Lyon, France
    • ,
  • Corine Vermeulen

      Affiliations

    • Department of Immunohematology and Blood Transfusion and the Laboratory of Experimental Hematology
    • ,
  • Annie Farre

      Affiliations

    • Cell Therapy Department, Etablissement Français du Sang Région Rhône-Alpes, Rhône, France
    • ,
  • Claire Galambrun

      Affiliations

    • Department of Hematology, Hôpital Debrousse, Lyon, France
    • ,
  • Dominique Rigal

      Affiliations

    • Cell Therapy Department, Etablissement Français du Sang Région Rhône-Alpes, Rhône, France
    • ,
  • Yves Bertrand

      Affiliations

    • Department of Immunology, Hôpital Lyon-Sud, Lyon, France
    • ,
  • Els Goulmy

      Affiliations

    • Department of Immunohematology and Blood Transfusion and the Laboratory of Experimental Hematology
    • ,
  • Assia Eljaafari

      Affiliations

    • Cell Therapy Department, Etablissement Français du Sang Région Rhône-Alpes, Rhône, France
    • Immunology Unit, Hospices Civils de Lyon, BioMerieux Mixed Research Immunogenomics Unit, Lyon, France
    • Corresponding Author InformationCorrespondence and reprint requests: Assia Eljaafari, MD, PhD, Hospices Civils de Lyon, bioMerieux Mixed Research Immunology Unit, Hopital E. Herriot, Place d’Arsonval, 69437 Lyon Cedex 03, France.

Received 22 January 2006 ,Accepted 20 July 2006.

References 

  1. 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
  2. Simpson E, Scott D, James E, et al. Minor H antigens: genes and peptides. Eur J Immunogenet. 2001;28:505–513
  3. Wallny HJ, Rammensee HG. Identification of classical minor histocompatibility antigen as cell-derived peptide. Nature. 1990;343:275–278
  4. Goulmy E. Human minor histocompatibility antigens: new concepts for marrow transplantation and adoptive immunotherapy. Immunol Rev. 1997;157:125–140
  5. Schreuder GM, Pool J, Blokland E, et al. A genetic analysis of human minor histocompatibility antigens demonstrates Mendelian segregation independent of HLA. Immunogenetics. 1993;38:98–105
  6. 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
  7. 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
  8. Lahn BT, Page DC. Functional coherence of the human Y chromosome. Science. 1997;278:675–680
  9. 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
  10. 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
  11. Vogt MH, de Paus RA, Voogt PJ, Willemze R, Falkenburg JH. DFFRY codes for a new human male-specific minor transplantation antigen involved in bone marrow graft rejection. Blood. 2000;95:1100–1105
  12. Vogt MH, Goulmy E, Kloosterboer FM, 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;96:3126–3132
  13. Spierings E, Vermeulen CJ, Vogt MH, et al. Identification of HLA class II-restricted H-Y-specific T-helper epitope evoking CD4+ T-helper cells in H-Y-mismatched transplantation. Lancet. 2003;362:610–615
  14. Torikai H, Akatsuka Y, Miyazaki M, et al. A Novel HLA-A*3303-restricted minor histocompatibility antigen encoded by an unconventional open reading frame of human TMSB4Y gene. J Immunol. 2004;173:7046–7054
  15. Zorn E, Miklos DB, Floyd BH, et al. Minor histocompatibility antigen DBY elicits a coordinated B and T cell response after allogeneic stem cell transplantation. J Exp Med. 2004;199:1133–1142
  16. Ivanov R, Aarts T, Hol S, et al. Identification of a 40S ribosomal protein S4-derived H-Y epitope able to elicit a lymphoblast-specific cytotoxic T lymphocyte response. Clin Cancer Res. 2005;11:1694–1703
  17. Spierings E, Wieles B, Goulmy E. Minor histocompatibility antigens—big in tumour therapy. Trends Immunol. 2004;25:56–60
  18. Rufer N, Wolpert E, Helg C, et al. HA-1 and the SMCY-derived peptide FIDSYICQV (H-Y) are immunodominant minor histocompatibility antigens after bone marrow transplantation. Transplantation. 1998;66:910–916
  19. Kloosterboer FM, van Luxemburg-Heijs SA, van Soest RA, et al. Direct cloning of leukemia-reactive T cells from patients treated with donor lymphocyte infusion shows a relative dominance of hematopoiesis-restricted minor histocompatibility antigen HA-1 and HA-2 specific T cells. Leukemia. 2004;18:798–808
  20. Goulmy E, Pool J, van den Elsen PJ. Interindividual conservation of T-cell receptor beta chain variable regions by minor histocompatibility antigen-specific HLA-A*0201-restricted cytotoxic T-cell clones. Blood. 1995;85:2478–2481
  21. Verdijk RM, Mutis T, Wilke M, Pool J, Schrama E, Brand A, et al. Exclusive TCRVbeta chain usage of ex vivo generated minor Histocompatibility antigen HA-1 specific cytotoxic T cells: implications for monitoring of immunotherapy of leukemia by TCRBV spectratyping. Hematol J. 2002;3:271–275
  22. van Els CA, Bakker A, Zwinderman AH, Zwaan FE, van Rood JJ, Goulmy E. Effector mechanisms in graft-versus-host disease in response to minor histocompatibility antigens (II. Evidence of a possible involvement of proliferative T cells). Transplantation. 1990;50:67–71
  23. Guerder S, Matzinger P. A fail-safe mechanism for maintaining self-tolerance. J Exp Med. 1992;176:553–564
  24. Ridge JP, Di Rosa F, Matzinger P. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature. 1998;393:474–478
  25. Zelenika D, Adams E, Mellor A, Simpson E. Rejection of H-Y disparate skin grafts by monospecific CD4+ Th1 and Th2 cells: no requirement for CD8+ T cells or B cells. J Immunol. 1998;161:1868–1874
  26. Miklos DB, Kim HT, Zorn E, et al. Antibody response to DBY minor histocompatibility antigen is induced after allogeneic stem cell transplantation and in healthy female donors. Blood. 2004;103:353–359
  27. Miklos DB, Kim HT, Miller KH, et al. Antibody responses to H-Y minor histocompatibility antigens correlate with chronic graft-versus-host disease and disease remission. Blood. 2005;105:2973–2978
  28. Eljaafari A, Farre A, Duperrier K, et al. Generation of helper and cytotoxic CD4+T cell clones specific for the minor histocompatibility antigen H-Y, after in vitro priming of human T cells by HLA-identical monocyte-derived dendritic cells. Transplantation. 2001;71:1449–1455
  29. Faber LM, van Luxemburg-Heijs SA, Veenhof WF, Willemze R, Falkenburg JH. Generation of CD4+ cytotoxic T-lymphocyte clones from a patient with severe graft-versus-host disease after allogeneic bone marrow transplantation: implications for graft-versus-leukemia reactivity. Blood. 1995;86:2821–2828
  30. Vogt MH, van den Muijsenberg JW, Goulmy E, et al. The DBY gene codes for an HLA-DQ5-restricted human male-specific minor histocompatibility antigen involved in graft-versus-host disease. Blood. 2002;99:3027–3032
  31. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994;179:1109–1118
  32. Romani N, Gruner S, Brang D, et al. Proliferating dendritic cell progenitors in human blood. J Exp Med. 1994;180:83–93
  33. Duperrier K, Eljaafari A, Dezutter-Dambuyant C, et al. Distinct subsets of dendritic cells resembling dermal DCs can be generated in vitro from monocytes, in the presence of different serum supplements. J Immunol Methods. 2000;238:119–131
  34. Hishii M, Andrews D, Boyle LA, et al. In vivo accumulation of the same anti-melanoma T cell clone in two different metastatic sites. Proc Natl Acad Sci U S A. 1997;94:1378–1383
  35. van der Veken LT, Hoogeboom M, de Paus RA, Willemze R, Falkenburg JH, Heemskerk MH. HLA class II restricted T-cell receptor gene transfer generates CD4(+) T cells with helper activity as well as cytotoxic capacity. Gene Ther. 2005;12:1686–1695
  36. Moonka D, Loh EY. A consensus primer to amplify both alpha and beta chains of the human T cell receptor. J Immunol Methods. 1994;169:41–51
  37. 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
  38. Verdijk RM, Mutis T, Esendam B, et al. Polyriboinosinic polyribocytidylic acid (poly(I:C)) induces stable maturation of functionally active human dendritic cells. J Immunol. 1999;163:57–61
  39. Berger MA, Korngold R. Immunodominant CD4+ T cell receptor Vbeta repertoires involved in graft-versus-host disease responses to minor histocompatibility antigens. J Immunol. 1997;159:77–85
  40. Heemskerk MH, Hoogeboom M, de Paus RA, Kester MG, et al. Redirection of antileukemic reactivity of peripheral T lymphocytes using gene transfer of minor histocompatibility antigen HA-2-specific T-cell receptor complexes expressing a conserved alpha joining region. Blood. 2003;102:3530–3540
  41. Bodmer JG, Marsh SG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, et al. Nomenclature for factors of the HLA System. In: Charron  editors. Genetic Diversity of HLA, functional and medical implications (Sevres Paris EDK). Vol II:1997;p. S505–S532Proceedings of the Twelfth International Histocompatibility Workshop
  42. Flowers ME, Pepe MS, Longton G, et al. Previous donor pregnancy as a risk factor for acute graft-versus-host disease in patients with aplastic anaemia treated by allogeneic marrow transplantation. Br J Haematol. 1990;74:492–496
  43. Kollman C, Howe CW, Anasetti C, et al. Donor characteristics as risk factors in recipients after transplantation of bone marrow from unrelated donors: the effect of donor age. Blood. 2001;98:2043–2051
  44. James E, Chai JG, Dewchand H, Macchiarulo E, Dazzi F, Simpson E. Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans. Blood. 2003;102:388–393
  45. 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

PII: S1083-8791(06)00498-8

doi: 10.1016/j.bbmt.2006.07.012

Biology of Blood and Marrow Transplantation
Volume 12, Issue 11 , Pages 1114-1124 , November 2006

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