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PMID: 20631300 Published · ppublish English Clinical Trial, Phase I Clinical Trial, Phase II Journal Article Research Support, Non-U.S. Gov't

Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination.

Van Tendeloo VF, Van de Velde A, Van Driessche A, Cools N, Anguille S, Ladell K, Gostick E, Vermeulen K, Pieters K, Nijs G, Stein B, Smits EL, Schroyens WA, Gadisseur AP, Vrelust I, Jorens PG, Goossens H, de Vries IJ, Price DA, Oji Y, Oka Y, Sugiyama H, Berneman ZN

Abstract

Active immunization using tumor antigen-loaded dendritic cells holds promise for the adjuvant treatment of cancer to eradicate or control residual disease, but so far, most dendritic cell trials have been performed in end-stage cancer patients with high tumor loads. Here, in a phase I/II trial, we investigated the effect of autologous dendritic cell vaccination in 10 patients with acute myeloid leukemia (AML). The Wilms' tumor 1 protein (WT1), a nearly universal tumor antigen, was chosen as an immunotherapeutic target because of its established role in leukemogenesis and superior immunogenic characteristics. Two patients in partial remission after chemotherapy were brought into complete remission after intradermal administration of full-length WT1 mRNA-electroporated dendritic cells. In these two patients and three other patients who were in complete remission, the AML-associated tumor marker returned to normal after dendritic cell vaccination, compatible with the induction of molecular remission. Clinical responses were correlated with vaccine-associated increases in WT1-specific CD8+ T cell frequencies, as detected by peptide/HLA-A*0201 tetramer staining, and elevated levels of activated natural killer cells postvaccination. Furthermore, vaccinated patients showed increased levels of WT1-specific IFN-gamma-producing CD8+ T cells and features of general immune activation. These data support the further development of vaccination with WT1 mRNA-loaded dendritic cells as a postremission treatment to prevent full relapse in AML patients.

MeSH Terms
Antigens, Neoplasm/immunology CD8-Positive T-Lymphocytes/immunology,metabolism Cancer Vaccines/immunology Dendritic Cells/immunology Humans Interferon-gamma/biosynthesis,immunology Leukemia, Myeloid, Acute/immunology,therapy RNA, Messenger/genetics Remission Induction Vaccination WT1 Proteins/genetics,immunology
Chemicals
Antigens, Neoplasm Cancer Vaccines RNA, Messenger WT1 Proteins Interferon-gamma
Authors & Affiliations
23 authors, click to expand affiliations / ORCID
Van Tendeloo Viggo F
University of Antwerp, Faculty of Medicine, Vaccine and Infectious Disease Institute (Vaxinfectio) and Center for Cell Therapy and Regenerative Medicine, Antwerp University Hospital, Antwerp B-2650, Belgium. [email protected]
Van de Velde Ann
Van Driessche Ann
Cools Nathalie
Anguille Sébastien
Ladell Kristin
Gostick Emma
Vermeulen Katrien
Pieters Katrien
Nijs Griet
Stein Barbara
Smits Evelien L
Schroyens Wilfried A
Gadisseur Alain P
Vrelust Inge
Jorens Philippe G
Goossens Herman
de Vries I Jolanda
Price David A
Oji Yusuke
Oka Yoshihiro
Sugiyama Haruo
Berneman Zwi N
References (58)
58 references, click to expand
  1. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels.
    Blood. 1996 Sep 15;88(6):2267-78 PMID: 8822948
  2. Real-time quantitative polymerase chain reaction detection of minimal residual disease by standardized WT1 assay to enhance risk stratification in acute myeloid leukemia: a European LeukemiaNet study.
    J Clin Oncol. 2009 Nov 1;27(31):5195-201 PMID: 19752335
  3. A tumor suppressor and oncogene: the WT1 story.
    Leukemia. 2007 May;21(5):868-76 PMID: 17361230
  4. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia.
    Blood. 1997 Feb 15;89(4):1405-12 PMID: 9028964
  5. High avidity myeloid leukemia-associated antigen-specific CD8+ T cells preferentially reside in the bone marrow.
    Blood. 2009 Mar 5;113(10):2238-44 PMID: 18997173
  6. T-cell responses of vaccinated cancer patients.
    Curr Opin Immunol. 2003 Apr;15(2):131-7 PMID: 12633661
  7. NK cell activation by dendritic cell vaccine: a mechanism of action for clinical activity.
    Cancer Immunol Immunother. 2006 Sep;55(9):1122-31 PMID: 16273350
  8. Dendritic cell vaccination and immune monitoring.
    Cancer Immunol Immunother. 2008 Oct;57(10):1559-68 PMID: 18618110
  9. T cell responses in melanoma patients after vaccination with tumor-mRNA transfected dendritic cells.
    Cancer Immunol Immunother. 2007 May;56(5):659-75 PMID: 16947019
  10. WT1 peptide vaccine for the treatment of cancer.
    Curr Opin Immunol. 2008 Apr;20(2):211-20 PMID: 18502632
  11. Induction of WT1 (Wilms' tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression.
    Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13885-90 PMID: 15365188
  12. Acute myeloid leukemia.
    N Engl J Med. 1999 Sep 30;341(14):1051-62 PMID: 10502596
  13. High WT1 expression after induction therapy predicts high risk of relapse and death in pediatric acute myeloid leukemia.
    J Clin Oncol. 2006 Apr 1;24(10):1507-15 PMID: 16575000
  14. Antigen-specific cellular immunotherapy of leukemia.
    Leukemia. 2005 Nov;19(11):1863-71 PMID: 16121214
  15. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1.
    Blood. 2000 Apr 1;95(7):2198-203 PMID: 10733485
  16. WT1 IgG antibody for early detection of nonsmall cell lung cancer and as its prognostic factor.
    Int J Cancer. 2009 Jul 15;125(2):381-7 PMID: 19384943
  17. Phase I/II study of vaccination with dendritic-like leukaemia cells for the immunotherapy of acute myeloid leukaemia.
    Br J Haematol. 2006 Apr;133(2):152-7 PMID: 16611305
  18. Cancer immunotherapy by dendritic cells.
    Immunity. 2008 Sep 19;29(3):372-83 PMID: 18799145
  19. A clinical and immunologic phase 2 trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS.
    Blood. 2009 Jun 25;113(26):6541-8 PMID: 19389880
  20. Cancer immunotherapy: moving beyond current vaccines.
    Nat Med. 2004 Sep;10(9):909-15 PMID: 15340416
  21. Idiotype vaccines for lymphoma: proof-of-principles and clinical trial failures.
    Nat Rev Cancer. 2009 Sep;9(9):675-81 PMID: 19701243
  22. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells.
    Blood. 2001 Jul 1;98(1):49-56 PMID: 11418462
  23. Clinical considerations in developing dendritic cell vaccine based immunotherapy protocols in cancer.
    Curr Mol Med. 2009 Aug;9(6):725-31 PMID: 19689299
  24. AML1-ETO rapidly induces acute myeloblastic leukemia in cooperation with the Wilms tumor gene, WT1.
    Blood. 2006 Apr 15;107(8):3303-12 PMID: 16380455
  25. Prognostic significance of quantitative analysis of WT1 gene transcripts by competitive reverse transcription polymerase chain reaction in acute leukaemia.
    Br J Haematol. 2003 Oct;123(1):49-59 PMID: 14510942
  26. The usefulness of monitoring WT1 gene transcripts for the prediction and management of relapse following allogeneic stem cell transplantation in acute type leukemia.
    Blood. 2003 Mar 1;101(5):1698-704 PMID: 12406915
  27. Unconventional cytokine profiles and development of T cell memory in long-term survivors after cancer vaccination.
    Cancer Immunol Immunother. 2009 Oct;58(10):1609-26 PMID: 19221745
  28. WT1 as a new prognostic factor and a new marker for the detection of minimal residual disease in acute leukemia.
    Blood. 1994 Nov 1;84(9):3071-9 PMID: 7949179
  29. Early prediction of treatment outcome in acute myeloid leukemia by measurement of WT1 transcript levels in peripheral blood samples collected after chemotherapy.
    Haematologica. 2008 Jun;93(6):921-4 PMID: 18443273
  30. Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene-transduced human T cells.
    Blood. 2005 Nov 1;106(9):3062-7 PMID: 16020516
  31. Leukemia-associated antigens are critical for the proliferation of acute myeloid leukemia cells.
    Clin Cancer Res. 2008 Nov 15;14(22):7161-6 PMID: 19010831
  32. Immunotherapy using autologous monocyte-derived dendritic cells pulsed with leukemic cell lysates for acute myeloid leukemia relapse after autologous peripheral blood stem cell transplantation.
    J Clin Apher. 2004;19(2):66-70 PMID: 15274198
  33. Treatment of older adults with acute myeloid leukemia: state of the art and current perspectives.
    Haematologica. 2008 Dec;93(12):1769-72 PMID: 19050066
  34. Quantitative assessment of WT1 expression by real time quantitative PCR may be a useful tool for monitoring minimal residual disease in acute leukemia patients.
    Leukemia. 2002 Oct;16(10):2115-21 PMID: 12357365
  35. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research.
    Clin Cancer Res. 2009 Sep 1;15(17):5323-37 PMID: 19723653
  36. Presence of Wilms' tumor gene (wt1) transcripts and the WT1 nuclear protein in the majority of human acute leukemias.
    Leukemia. 1995 Jun;9(6):1060-7 PMID: 7596170
  37. Immunotherapy for patients with acute myeloid leukemia using autologous dendritic cells generated from leukemic blasts.
    Int J Oncol. 2006 Apr;28(4):855-61 PMID: 16525634
  38. Acute myeloid leukaemia.
    Lancet. 2006 Nov 25;368(9550):1894-907 PMID: 17126723
  39. Immunotherapeutic peptide vaccination with leukemia-associated antigens.
    Curr Opin Immunol. 2006 Oct;18(5):599-604 PMID: 16870418
  40. RHAMM-R3 peptide vaccination in patients with acute myeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses.
    Blood. 2008 Feb 1;111(3):1357-65 PMID: 17978170
  41. Clinical-grade manufacturing of autologous mature mRNA-electroporated dendritic cells and safety testing in acute myeloid leukemia patients in a phase I dose-escalation clinical trial.
    Cytotherapy. 2009;11(5):653-68 PMID: 19530029
  42. Role of natural killer cell function in dendritic cell-based vaccines.
    Expert Rev Vaccines. 2006 Feb;5(1):55-65 PMID: 16451108
  43. Revised recommendations of the International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, and Reporting Standards for Therapeutic Trials in Acute Myeloid Leukemia.
    J Clin Oncol. 2003 Dec 15;21(24):4642-9 PMID: 14673054
  44. Real-time quantitative PCR detection of WT1 gene expression in children with AML: prognostic significance, correlation with disease status and residual disease detection by flow cytometry.
    Leukemia. 2002 Jul;16(7):1381-9 PMID: 12094264
  45. Progress in the treatment of acute myeloid leukemia.
    Cancer. 2007 Nov 1;110(9):1900-10 PMID: 17786921
  46. CD8 T-cell responses to Wilms tumor gene product WT1 and proteinase 3 in patients with acute myeloid leukemia.
    Blood. 2002 Sep 15;100(6):2132-7 PMID: 12200377
  47. T-cell responses directed against multiple HLA-A*0201-restricted epitopes derived from Wilms' tumor 1 protein in patients with leukemia and healthy donors: identification, quantification, and characterization.
    Clin Cancer Res. 2005 Dec 15;11(24 Pt 1):8799-807 PMID: 16361568
  48. Cancer vaccines for patients with acute myeloid leukemia--definition of leukemia-associated antigens and current clinical protocols targeting these antigens.
    Haematologica. 2006 Dec;91(12):1653-61 PMID: 17145602
  49. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules.
    J Immunol. 2004 Jun 1;172(11):6649-57 PMID: 15153480
  50. Human cytotoxic T lymphocytes specific for Wilms' tumor antigen-1 inhibit engraftment of leukemia-initiating stem cells in non-obese diabetic-severe combined immunodeficient recipients.
    Transplantation. 2003 May 15;75(9):1429-36 PMID: 12792492
  51. Growth inhibition of human leukemic cells by WT1 (Wilms tumor gene) antisense oligodeoxynucleotides: implications for the involvement of WT1 in leukemogenesis.
    Blood. 1996 Apr 1;87(7):2878-84 PMID: 8639907
  52. Post-remission treatment of acute myelogenous leukemia.
    N Engl J Med. 1995 Jan 26;332(4):260-2 PMID: 7808494
  53. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities.
    Blood. 2007 Jul 1;110(1):201-10 PMID: 17371945
  54. Leukemia-associated antigen-specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies.
    Blood. 2008 Jan 1;111(1):236-42 PMID: 17875804
  55. WT1 mRNA level in peripheral blood is a sensitive biomarker for monitoring minimal residual disease in acute myeloid leukemia.
    Tohoku J Exp Med. 2009 Oct;219(2):169-76 PMID: 19776535
  56. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells.
    Nat Med. 1996 Jan;2(1):52-8 PMID: 8564842
  57. Dendritic cell-based cancer gene therapy.
    Hum Gene Ther. 2009 Oct;20(10):1106-18 PMID: 19656053
  58. The Wilms' tumor gene WT1-GFP knock-in mouse reveals the dynamic regulation of WT1 expression in normal and leukemic hematopoiesis.
    Leukemia. 2007 Aug;21(8):1783-91 PMID: 17525726
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-08-03
Epub
2010-00-14
Pages
13824-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2922237
Subset
IM
Grants
Medical Research Council · G0501963 · United Kingdom
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