Best Practice & Research Clinical Haematology
Volume 21, Issue 3 , Pages 391-404 , September 2008

Peptide vaccines for myeloid leukaemias

  • Tao Dao, MD, PhD (Senior Research Scientist)
  • ,
  • David A. Scheinberg, MD, PhD (Chairman)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +1 646 888 2190; Fax: +1 646 422 0296.

References 

  1. Melief CJ, Kast WM. T-cell immunotherapy of tumours by adoptive transfer of cytotoxic T lymphocytes and by vaccination with minimal essential epitopes. Immunological Reviews. 1995;145:167–177
  2. Falkenburg JH, Smit WM, Willemze R. Cytotoxic T-lymphocyte (CTL) responses against acute or chronic myeloid leukemia. Immunological Reviews. 1997;157:223–230
  3. Antin JH. Graft-versus-leukemia: no longer an epiphenomenon. Blood. 1993;82:2273–2277
  4. Barrett J, Child R. Non-myeloablative stem cell transplants. British Journal of Haematology. 2000;111:6–17
  5. Kolb HJ, Schmid C, Barrett AJ, et al. Graft-versus-leukemia reactions in allogeneic chimera. Blood. 2004;103:767–776
  6. van Rhee F, Lin F, Cullis JO, et al. Relapse of chronic myeloid leukemia after allogeneic bone marrow transplant: the case for giving donor lymphocyte transfusion before the onset of hematological relapse. Blood. 1994;83:3377–3383
  7. Kolb HJ, Holler E. Adoptive immunotherapy with donor lymphocyte transfusions. Current Opinion in Oncology. 1997;9:139–145
  8. Falkenburg JH, van de Corput L, Marijt EW, et al. Minor histocompatibility antigens in human stem cell transplantation. Experimental Hematology. 2003;31:734–751
  9. Smit WM, Rijnbeek M, van Bergen CAM, et al. T cells recognizing leukemic CD34+progenitor cells mediate the anti-leukemic effect of donor lymphocyte infusions for relapsed chronic myeloid leukemia after allogeneic stem cell transplantation. Proceedings of the National Academy of Sciences of the United States of America. 1998;95:10152–10157
  10. Butt NM, Wang L, Abu-Eisha HM, et al. BCR-ABL-specific T cells can be detected in healthy donors and in chronic myeloid leukemia patients following allogeneic stem cell transplantation. Blood. 2004;103:3245
  11. Choudhury A, Gajewski JL, Liang JC, et al. Use of leukemic dendritic cells for the generation of anti-leukemic cellular cytotoxicity against Philadelphia chromosome-positive chronic myelogenous leukemia. Blood. 1997;89:1133–1142
  12. Pinilla-Ibarz J, Cathcart K, Scheinberg DA. CML vaccines as a paradigm of the specific immunotherapy of cancer. Blood Reviews. 2000;14:111–120
  13. 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
  14. Rusakiewicz S, Molldrem JJ. Immunotherapeutic peptide vaccination with leukemia-associated antigens. Current Opinion in Immunology. 2006;18:599–604
  15. Barrett AJ, Rezwani K. Translational mini-review series on vaccines: peptide vaccines for myeloid leukemias. Clinical and Experimental Immunology. 2007;148:189–198
  16. Rice J, Dunn S, Piper K, et al. DNA fusion vaccines induce epitope-specific cytotoxic CD8+ T cells against human leukemia-associated minor histocompatibility antigens. Cancer Research. 2006;66:5436
  17. Cheuk ATC, Guinn BA. Immunotherapy of acute myeloid leukemia: development of a whole cell vaccine. Frontiers in Bioscience. 2008;13:2022–2029
  18. Schmitt A, Hus I, Schmitt M. Dendritic cell vaccines for leukemia patients. Expert Review of Anticancer Therapy. 2007;7:275–283
  19. Bocchia M, Korontsvit T, Xu Q, et al. Specific human cellular immunity to bcr-abl oncogene-derived peptides. Blood. 1996;87:3587–3592
  20. 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
  21. Call KM, Glaser T, Ito CY, et al. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell. 1990;60:509–520
  22. Oka Y, Tsuboi A, Elisseeva OA, et al. WT1 peptide cancer vaccine for patients with hematopoietic malignancies and solid cancers. Science World Journal. 2007;7:649–665
  23. Chen J, Schmitt A, Bunjes D, et al. The receptor for hyaluronic acid-mediated motility induces specific CD8+ T cells response in healthy donors and patients with chronic myeloid leukemia after allogeneic stem cell transplantation. International Journal of Oncology. 2007;30:1119–1127
  24. Pinilla-Ibarz J, Cathcart K, Korontsvit T, et al. Vaccination of patients with chronic myelogenous leukemia with bcr-abl oncogene breakpoint fusion peptides generate specific immune responses. Blood. 2000;95:1781–1787
  25. Cathcart K, Pinilla-Ibarz J, Korontsvit T, et al. A multivalent bcr-abl fusion peptide vaccination trial in patients with chronic myeloid leukemia. Blood. 2004;103:1037–1042
  26. Rojas JM, Knight K, Wang L, et al. Clinical evaluation of BCR-ABL peptide immunization in chronic myeloid leukemia: results of the EPIC study. Leukemia. 2007;21:2287–2295
  27. Bocchia M, Gentili S, Abruzzes E, et al. Effect of p210 multipeptide vaccine associated with imatinib or interferon in patients with chronic myeloid leukemia and persistent residual disease: a multi center observation trial. The Lancet. 2005;365:657–662
  28. Mailander V, Scheinbenbogen C, Thiel E, et al. Complete remission in a patient with recurrent myeloid leukemia induced by vaccination with WT1 peptide in the absence of hematological or renal toxicity. Leukemia. 2004;18:165–166
  29. Keilholz U, Letsch A, Asemissen A, et al. Clinical and immune responses of WT1-peptide vaccination in patients with acute myeloid leukemia. ASCO Annual Meeting Proceedings. Journal of Clinical Oncology. 2006;24:2511
  30. Oka Y, Tsuboi A, Taguchi T, et al. Induction of WT1 (Wilms' tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:13885–13890
  31. Kawakami M, Oka Y, Tsuboi A, et al. Clinical and immunologic responses to very low-dose vaccination with WT1 peptide (5 micrg/body) in a patient with chronic myelomonocytic leukemia. International Journal of Hematology. 2007;85:426–429
  32. Qazilbash MH, Wieder E, Rios R, et al. Vaccination with the PR1 leukemia-associated antigen can induce complete remission in patients with myeloid leukemia. Blood. 2004;104:[abstract 259]
  33. Schmitt M, Schmitt A, Rojewski MT, et al. RHAMM-R3 peptide vaccination in patients with acute myeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses. Blood. 2008;111:1357–1365
  34. Bocchia M, Wentworth PA, Southwood S, et al. Specific binding of leukemia oncogene fusion peptides to HLA class I molecules. Blood. 1995;85:2680–2684
  35. Greco G, Fruci D, Accapezzato D, et al. Two bcr-abl junction peptides bind HLA-A3 molecules and allo specific induction of human cytotoxic T lymphocytes. Leukemia. 1996;10:693–699
  36. Buzyn A, Ostankovitch M, Zerbia A, et al. Peptides derived from the whole sequences of BCR-ABL bind to several class I molecules allowing specific induction of human cytotoxic T lymphocytes. European Journal of Immunology. 1997;27:2066–2072
  37. Berke Z, Anderson MH, Pedersen M, et al. Peptides spanning the junctional region of both the abl/bcr and the bcr/abl fusion proteins bind common HLA class I molecules. Leukemia. 2000;14:419–426
  38. Posthuman EF, van Bergen CA, Kester MG, et al. Proteosomal degradation of BCR/ABL protein can generate an HLA-A*0301-restricted peptide, but high-avidity T cells recognizing this leukemia-specific antigen were not demonstrated. Haematologica. 2004;89:1062–1071
  39. Clark RE, Dodi A, 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
  40. Yontda P, Firat H, Garcia-Pons F, et al. Cytotoxic T cell response against chimeric p210 BCR-ABL protein in patients with chronic myelogenous leukemia. The Journal of Clinical Investigation. 1998;101:2290–2296
  41. Pinilla-Ibarz J, Korontsvit T, Zakhaleva V, et al. Synthetic peptide analogs derived from bcr/abl fusion protein and the induction of heteroclitic human T cell responses. Haematologica. 2005;90:1324–1332
  42. Fayolle C, Deriaud E, Leclerc C. In vivo induction of cytotoxic T cell response by a free synthetic peptide requires CD4+ T cell help. Journal of Immunology (Baltimore, Md.: 1950). 1991;147:4069–4073
  43. Shirai M, Pendleton CD, Ahlers J, et al. Helper-cytotoxic T lymphocyte (CTL) determinant linkage required for priming of anti-HIV CD8+ CTL in vivo with peptide vaccine constructs. Journal of Immunology (Baltimore, Md.: 1950). 1994;152:549–556
  44. Hiranuma K, Tamaki S, Nishimura Y, et al. Helper T cell determinant peptide contributes to induction of cellular immune responses by peptide vaccines against hepatitis C virus. The Journal of General Virology. 1999;80:187–193
  45. Schoenberger SP, Toes RE, van der Voort EI, et al. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature. 1998;393:480–483
  46. Alexander J, Fikes J, Hoffman S, et al. The optimization of helper T lymphocyte (HTL) function in vaccine development. Immunologic Research. 1998;18:79–92
  47. Scheinbenbogen C, Schadendorf D, Bechrakis NE, et al. Effects of granulocyte-macrophage colony-stimulating factor and foreign helper protein as immunologic adjuvants on the T-cell response to vaccination with tyrosinase peptides. International Journal of Cancer. 2003;104:188–194
  48. Zeng G, Li Y, El-Gamil M, et al. Generation of NY-ESO-1-specific CD4+ and CD8+ T cells by a single peptide with dual MHC class I and II specificities: a new strategy for vaccine design. Cancer Research. 2002;62:3630–3635
  49. Chen W, Peace DJ, Rovira DK, et al. T-cell immunity to the joining region of p210 BCR-ABL protein. Proceedings of the National Academy of Sciences of the United States of America. 1992;89:1468–1472
  50. Matte CC, Cormier J, Anderson BE, et al. Graft-versus-leukemia in retrovirally induced murine CML model: mechanisms of T-cell killing. Blood. 2004;103:4353–4361
  51. Yasukawa M, Ohminami H, Kolima K, et al. HLA class II-restricted antigen presentation of endogenous bcr-abl fusion protein by chronic myelogenous leukemia-derived dendritic cells to CD4 (+) T lymphocytes. Blood. 2001;98:1498–1505
  52. Bosch GJ, Joosten AM, Kessler JH, et al. Recognition of BCR-ABL positive leukemic blasts by human CD4+ T cells elicited by priming in vitro immunization with a BCR-ABL breakpoint peptide. Blood. 1996;88:3522–3527
  53. Bosch GJ, Kessler JH, Joosten AM, et al. A BCR-ABL oncoprotein p210 b2a2 fusion region sequence is recognized by HLA-DR2a restricted cytotoxic T lymphocytes and presented by HLA-DR matched cells transfected with an Iib2a2 construct. Blood. 1999;94:1038–1045
  54. Maslak PJ, Dao T, Gomez M, et al. A pilot vaccination trial of synthetic analog peptides derived from BCR-ABL breakpoints in CML patients with minimal disease. Leukemia, Feb 7, 2008 [Epub].
  55. Jorgenson HG, Allan EK, Graham SM, et al. Lonafarnib reduces the resistance of primitive quiescent CML cells to imatinib mesylate in vitro. Leukemia. 2005;9:1184–1191
  56. Copland M, Jorgensen HG, Holyoake TL. Evolving molecular therapy for chronic myeloid leukemia – are we on target?. Hematology. 2005;10:349–359
  57. Keilholz U, Menssen HD, Craiger A, et al. Wilms' tumor gene 1 (WT1) in human neoplasia. Leukemia. 2005;19:1318–1323
  58. Miwa H, Beran M, Sauders GF. Expression of Wilms' tumor gene (WT1) in human leukemias. Leukemia. 1992;6:405–409
  59. Gaiger A, Carter L, Greinix H, et al. WT1-specific serum antibodies in patients with leukemia. Clinical Cancer Research. 2001;7(Suppl. 3):761s–765s
  60. Rosenfield C, Cheever MA, Gaiger A. WT1 in acute leukemia, chronic myelogenous leukemia and myelodysplastic syndrom: therapeutic potential of WT1 targetted therapies. Leukemia. 2003;17:1301–1312
  61. Hutchings Y, Osada T, Woo CY, et al. Immunotherapeutic targeting of Wilms' tumor protein. Current Opinion in Molecular Therapeutics. 2007;9:62–69
  62. Oka Y, Udaka K, Tsuboi A, et al. Cancer immunotherapy targeting Wilms tumor gene WT1 product. Journal of immunology (Baltimore, Md.: 1950). 2000;164:1873–1880
  63. Kobayashi H, Nagato T, Aoki N, et al. Defining MHC class II T helper epitopes from WT1 antigen. Cancer Immunology Immunotherapy. 2006;55:850–860
  64. Knights AJ, Zaniou A, Rees RC, et al. Prediction of an HLA-DR-binding peptide derived from Wilms' tumor 1 protein and demonstration of in vitro immunogenicity of WT1 (124-138)-pulsed dendritic cells generated according to an optimal protocol. Cancer Immunology Immunotherapy. 2002;51:271–281
  65. Fujiki F, Oka Y, Tsuboi A, et al. Identification and characterization of a WT1 (Wilms tumor gene) protein-derived HLA-DRB1*0405-restricted 16-mer helper peptide that promotes the induction and activation of WT1-specific cytotoxic T lymphocytes. Journal of Immunotherapy. 2007;30:282–293
  66. Guo Y, Niiya H, Azuma T, et al. Direct recognition and lysis of leukemia cells by WT1-specific CD4+ T lymphocytes in an HLA class II-restricted manner. Blood. 2005;106:1415–1418
  67. May RJ, Dao T, Pinilla-Ibarz J, et al. Peptide epitopes from the Wilms tumor 1 oncoprotein stimulate CD4+ and CD8+ T cells that recognize and kill human malignant mesothelioma tumor cells. Clinical Cancer Research. 2007;13:4547–4555
  68. Oka Y, Tsuboi A, Murakami M, et al. Wilms tume gene peptide-based immunotherapy for patients with overt leukemia from myelodysplastic syndrome (MDS) or MDS with myelofibrosis. International Journal of Hematology. 2003;78:56–61
  69. Tsuboi A, Oka Y, Nakajima H, et al. Long-term follow-up of three patients with acute myeloid leukemia with minimal residual disease who were treated with WT1 vaccination. In: Third international conference on WT1 in human malignancies, Berlin Sept 20-21, 2007.
  70. 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
  71. Li Z, Oka Y, Tsuboi A, et al. WT1(235), a ninemer peptide derived from Wilms tumor gene product, is a candidate peptide for the vaccination of HLA-A0201-positive patients with hematopoietic malignancies. International Journal of Hematology. 2005;82:458–459
  72. Rezwani K, Young ASM, Mielke S, et al. Leukemia-associated antigen specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies. Blood. 2008;111:236–242
  73. Pinilla-Ibarz J, Mary RJ, Korontsvit T, et al. Improved human T-cell responses against synthetic HLA-A0201 analog peptides derived from the WT1 oncoprotein. Leukemia. 2006;20:2025–2033
  74. Krug LM, Maslak P, Dao T, et al Clinical development of a heteroclitic WT-1 peptide vaccine in patients with hematologic and thoracic malignancies. In: Third international conference on WT1 in human malignancies, Berlin Sept. 20-21, 2007.
  75. Asemissen AM, Keilholz U, Tenzer S, et al. Identification of a highly immunogenic HLA-A*01-binding T cell epitope of WT1. Clinical Cancer Research. 2006;12:7476–7482
  76. Barrett J, Rezvani K. Neutrophil granule proteins as targets of leukemia-specific immune responses. Current Opinion in Hematology. 2006;13:15–20
  77. Zhang P, Nelson E, Radomska HS, et al. Induction of granulocytic differentiation by 2 pathways. Blood. 2002;99:4406–4412
  78. Molldrem J, Clave E, Jiang YZ, et al. Cytotoxic lymphocytes specific for a nonpolymorphic proteinase 3 peptide preferentially inhibit chronic myeloid leukemia colony-forming units. Blood. 1997;90:2529–2534
  79. Molldrem JJ, Lee PP, Wang C, et al. A PR1 human leukocyte antigen-A2 tetramer can be used to isolate low-frequency cytotoxic T lymphocytes from healthy donors that selectively lyse chronic myelogenous leukemia. Cancer Research. 1999;59:2675–2681
  80. Molldrem JJ, Lee PP, Kant S, et al. Chronic myelogenous leukemia shapes host immunity by selective deletion of high-avidity leukemia-specific T cells. The Journal of Clinical Investigation. 2003;111:639–674
  81. Molldrem JJ, Lee PP, Wang C, et al. Evidence that specific T lymphocytes may participate in elimination of chronic myelogenous leukemia. Natural Medicines. 2000;6:1018–1023
  82. Greiner J, Li L, Ringhoffer M, et al. Identification and characterization of epitopes of the receptor for hyaluronic acid-mediated motility (RHAMM/CD168) recognized by CD8+ T cells of HLA-A2-positive patients with acute myeloid leukemia. Blood. 2005;106:938–945
  83. Chong G, Morse MA. Combining cancer vaccines with chemotherapy. Expert Opinion. 2005;6:2813–2820
  84. Livingston PO, Cunningham-Rundless S, Marfleet G, et al. Inhibition of suppressor-cell activity by cyclophosphamide in patients with malignant melanoma. Journal of Biological Response Modifiers. 1987;6:392–403
  85. Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. Journal of Clinical Oncology. 2005;23:2346–2357
  86. Liu G, Akasaki Y, Khong HT, et al. Cytotoxic T cell targeting of TRP-2 sensitizes human malignant glioma to chemotherapy. Oncogene. 2005;24:5226–5234

PII: S1521-6926(08)00051-0

doi: 10.1016/j.beha.2008.05.001

Best Practice & Research Clinical Haematology
Volume 21, Issue 3 , Pages 391-404 , September 2008