Priming of PRAME- and WT1-specific CD8+ T cells in healthy donors but not in AML patients in complete remission: Implications for immunotherapy

OncoImmunology

Volumn 2, Issue 4, 2013, Pages

  van den Ancker, Willemijn ^a   Ruben, Jurjen M ^a   Westers, Theresia M ^a   Wulandari, Dewi ^a   Bontkes, Hetty J ^a   Hooijberg, Erik ^a   Stam, Anita G M ^a   Santegoets, Saskia J A M ^a   Ossenkoppele, Gert J ^a   de Gruijl, Tanja ^a   Van de Loosdrecht, Arjan ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Acute myeloid leukemia; Dendritic cell based vaccination; Immunotherapy; PRAME; T cell priming; WT1

Indexed keywords

ANTINEOPLASTIC AGENT; ARGINYLMETHIONYLPHENYLALANYLPROLYLASPARAGINYLALANYLPROLYLTYROSYLLEUCINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; HLA A2 ANTIGEN; PREFERENTIALLY EXPRESSED ANTIGEN OF MELANOMA; TETRAMER; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VALYLLEUCYLASPARTYLGLYCYLLEUCYLASPARTYLVALYLLEUCYLLEUCINE; WT1 PROTEIN;

ACTIVE IMMUNIZATION; ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL PRIMING; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG CYTOTOXICITY; DRUG TARGETING; HUMAN; HUMAN CELL; INTERFERON PRODUCTION; LEUKEMIA REMISSION; PROCEDURES CONCERNING CELLS;

EID: 84886945123     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.23971     Document Type: Article

References (33)

1. van den Ancker W, van Luijn MM, Westers TM, Bontkes HJ, Ruben JM, de Gruijl TD, et al. Recent advances in antigen-loaded dendritic cell-based strategies for treatment of minimal residual disease in acute myeloid leukemia. Immunotherapy 2010; 2:69-83; PMID:20635890; http://dx.doi.org/10.2217/imt.09.85
2. Kessler JH, Beekman NJ, Bres-Vloemans SA, Verdijk P, van Veelen PA, Kloosterman-Joosten AM, et al. Efficient identification of novel HLA-A 0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasomemediated digestion analysis. J Exp Med 2001; 193:73-88; PMID:11136822; http://dx.doi.org/10.1084/jem.193.1.73
3. Van Tendeloo VF, Van de Velde AL, Van Driessche A, Cools N, Anguille S, Ladell K, et al. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci U S A 2010; 107:13824-9; PMID:20631300; http://dx.doi.org/10.1073/pnas.1008051107
4. Greiner J, Schmitt M, Li L, Giannopoulos K, Bosch K, Schmitt A, et al. Expression of tumor-associated antigens in acute myeloid leukemia: Implications for specific immunotherapeutic approaches. Blood 2006; 108:4109-17; PMID:16931630; http://dx.doi.org/10.1182/blood-2006-01-023127
5. Oehler VG, Guthrie KA, Cummings CL, Sabo K, Wood BL, Gooley T, et al. The preferentially expressed antigen in melanoma (PRAME) inhibits myeloid differentiation in normal hematopoietic and leukemic progenitor cells. Blood 2009; 114:3299-308; PMID:19625708; http://dx.doi.org/10.1182/blood-2008-07-170282
6. Greiner J, Bullinger L, Guinn BA, Döhner H, Schmitt M. Leukemia-associated antigens are critical for the proliferation of acute myeloid leukemia cells. Clin Cancer Res 2008; 14:7161-6; PMID:19010831; http://dx.doi.org/10.1158/1078-0432.CCR-08-1102
7. Kerst G, Bergold N, Viebahn S, Gieseke F, Kalinova M, Trka J, et al. WT1 protein expression in slowly proliferating myeloid leukemic cell lines is scarce throughout the cell cycle with a minimum in G0/G1 phase. Leuk Res 2008; 32:1393-9; PMID:18457871; http://dx.doi.org/10.1016/j.leukres.2008.03.006
8. Bellantuono I, Gao L, Parry S, Marley S, Dazzi F, Apperley J, et al. Two distinct HLA-A0201-presented epitopes of the Wilms tumor antigen 1 can function as targets for leukemia-reactive CTL. Blood 2002; 100:3835-7; PMID:12411326; http://dx.doi.org/10.1182/blood.V100.10.3835
9. Candoni A, Tiribelli M, Toffoletti E, Cilloni D, Chiarvesio A, Michelutti A, et al. Quantitative assessment of WT1 gene expression after allogeneic stem cell transplantation is a useful tool for monitoring minimal residual disease in acute myeloid leukemia. Eur J Haematol 2009; 82:61-8; PMID:18801058; http://dx.doi.org/10.1111/j.1600-0609.2008.01158.x
10. Matsushita M, Ikeda H, Kizaki M, Okamoto S, Ogasawara M, Ikeda Y, et al. Quantitative monitoring of the PRAME gene for the detection of minimal residual disease in leukaemia. Br J Haematol 2001; 112:916-26; PMID:11298586; http://dx.doi.org/10.1046/j.1365-2141.2001.02670.x
11. Østergaard M, Olesen LH, Hasle H, Kjeldsen E, Hokland P. WT1 gene expression: an excellent tool for monitoring minimal residual disease in 70% of acute myeloid leukaemia patients - results from a single-centre study. Br J Haematol 2004; 125:590-600; PMID:15147374; http://dx.doi.org/10.1111/j.1365-2141.2004.04952.x
12. Yong AS, Keyvanfar K, Eniafe R, Savani BN, Rezvani K, Sloand EM, et al. Hematopoietic stem cells and progenitors of chronic myeloid leukemia express leukemiaassociated antigens: implications for the graft-versusleukemia effect and peptide vaccine-based immunotherapy. Leukemia 2008; 22:1721-7; PMID:18548092; http://dx.doi.org/10.1038/leu.2008.161
13. Gao L, Bellantuono I, Elsässer A, Marley SB, Gordon MY, Goldman JM, et al. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood 2000; 95:2198-203; PMID:10733485
14. Greiner J, Döhner H, Schmitt M. Cancer vaccines for patients with acute myeloid leukemia--definition of leukemia-associated antigens and current clinical protocols targeting these antigens. Haematologica 2006; 91:1653-61; PMID:17145602
15. Griffioen M, Kessler JH, Borghi M, van Soest RA, van der Minne CE, Nouta J, et al. Detection and functional analysis of CD8+ T cells specific for PRAME: a target for T-cell therapy. Clin Cancer Res 2006; 12:3130-6; PMID:16707612; http://dx.doi.org/10.1158/1078-0432.CCR-05-2578
16. Rosenfeld C, Cheever MA, Gaiger A. WT1 in acute leukemia, chronic myelogenous leukemia and myelodysplastic syndrome: therapeutic potential of WT1 targeted therapies. Leukemia 2003; 17:1301-12; PMID:12835718; http://dx.doi.org/10.1038/sj.leu.2402988
17. Rezvani K, Yong AS, Savani BN, Mielke S, Keyvanfar K, Gostick E, et al. Graft-versus-leukemia effects associated with detectable Wilms tumor-1 specific T lymphocytes after allogeneic stem-cell transplantation for acute lymphoblastic leukemia. Blood 2007; 110:1924-32; PMID:17505014; http://dx.doi.org/10.1182/blood-2007-03-076844
18. Scheibenbogen C, Letsch A, Thiel E, Schmittel A, Mailaender V, Baerwolf S, et al. CD8 T-cell responses to Wilms tumor gene product WT1 and proteinase 3 in patients with acute myeloid leukemia. Blood 2002; 100:2132-7; PMID:12200377; http://dx.doi.org/10.1182/blood-2002-01-0163
19. Hooijberg E, Ruizendaal JJ, Snijders PJ, Kueter EW, Walboomers JM, Spits H. Immortalization of human CD8+ T cell clones by ectopic expression of telomerase reverse transcriptase. J Immunol 2000; 165:4239-45; PMID:11035057
20. Greiner J, Ringhoffer M, Taniguchi M, Li L, Schmitt A, Shiku H, et al. mRNA expression of leukemia-associated antigens in patients with acute myeloid leukemia for the development of specific immunotherapies. Int J Cancer 2004; 108:704-11; PMID:14696097; http://dx.doi.org/10.1002/ijc.11623
21. Ho WY, Nguyen HN, Wolfl M, Kuball J, Greenberg PD. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naïve repertoire. J Immunol Methods 2006; 310:40-52; PMID:16469329; http://dx.doi.org/10.1016/j.jim.2005.11.023
22. Rasaiyaah J, Noursadeghi M, Kellam P, Chain B. Transcriptional and functional defects of dendritic cells derived from the MUTZ-3 leukaemia line. Immunology 2009; 127:429-41; PMID:19538250; http://dx.doi.org/10.1111/j.1365-2567.2008.03018.x
23. Santegoets SJ, Schreurs MW, Masterson AJ, Liu YP, Goletz S, Baumeister H, et al. In vitro priming of tumor-specific cytotoxic T lymphocytes using allogeneic dendritic cells derived from the human MUTZ-3 cell line. Cancer Immunol Immunother 2006; 55:1480-90; PMID:16468034; http://dx.doi.org/10.1007/s00262-006-0142-x
24. Quintarelli C, Dotti G, De Angelis B, Hoyos V, Mims M, Luciano L, et al. Cytotoxic T lymphocytes directed to the preferentially expressed antigen of melanoma (PRAME) target chronic myeloid leukemia. Blood 2008; 112:1876-85; PMID:18591381; http://dx.doi.org/10.1182/blood-2008-04-15004525.
25. Quintarelli C, Dotti G, Hasan ST, De Angelis B, Hoyos V, Errichiello S, et al. High-avidity cytotoxic T lymphocytes specific for a new PRAME-derived peptide can target leukemic and leukemic-precursor cells. Blood 2011; 117:3353-62; PMID:21278353; http://dx.doi.org/10.1182/blood-2010-08-300376
26. Szczepanski MJ, Szajnik M, Czystowska M, Mandapathil M, Strauss L, Welsh A, et al. Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Clin Cancer Res 2009; 15:3325-32; PMID:19417016; http://dx.doi.org/10.1158/1078-0432.CCR-08-3010
27. Ohnishi K, Yamanishi H, Naito K, Utsumi M, Yokomaku S, Hirabayashi N, et al. Reconstitution of peripheral blood lymphocyte subsets in the long-term disease-free survivors of patients with acute myeloblastic leukemia. Leukemia 1998; 12:52-8; PMID:9436920; http://dx.doi.org/10.1038/sj.leu.2400891
28. Rutella S. Granulocyte colony-stimulating factor for the induction of T-cell tolerance. Transplantation 2007; 84(Suppl):S26-30; PMID:17632408; http://dx.doi.org/10.1097/01.tp.0000269611.66517.bf
29. Amir AL, van der Steen DM, van Loenen MM, Hagedoorn RS, de Boer R, Kester MD, et al. PRAMEspecific Allo-HLA-restricted T cells with potent antitumor reactivity useful for therapeutic T-cell receptor gene transfer. Clin Cancer Res 2011; 17:5615-25; PMID:21771875; http://dx.doi.org/10.1158/1078-0432.CCR-11-1066
30. Gutierrez-Cosío S, de la Rica L, Ballestar E, Santamaría C, Sánchez-Abarca LI, Caballero-Velazquez T, et al. Epigenetic regulation of PRAME in acute myeloid leukemia is different compared to CD34+ cells from healthy donors: effect of 5-AZA treatment. Leuk Res 2012; 36:895-9; PMID:22503131; http://dx.doi.org/10.1016/j.leukres.2012.02.030
31. Yan M, Himoudi N, Basu BP, Wallace R, Poon E, Adams S, et al. Increased PRAME antigen-specific killing of malignant cell lines by low avidity CTL clones, following treatment with 5-Aza-2'-Deoxycytidine. Cancer Immunol Immunother 2011; 60:1243-55; PMID:21553146; http://dx.doi.org/10.1007/s00262-011-1024-4
32. Santegoets SJ, Masterson AJ, van der Sluis PC, Lougheed SM, Fluitsma DM, van Den Eertwegh AJ, et al. A CD34(+) human cell line model of myeloid dendritic cell differentiation: evidence for a CD14(+) CD11b(+) Langerhans cell precursor. J Leukoc Biol 2006; 80:1337-44; PMID:16959899; http://dx.doi.org/10.1189/jlb.0206111
33. Westers TM, Houtenbos I, Schuurhuis GJ, Ossenkoppele GJ, van de Loosdrecht AA. Quantification of T-cell-mediated apoptosis in heterogeneous leukemia populations using four-color multiparameter flow cytometry. Cytometry A 2005; 66:71-7; PMID:15895438; http://dx.doi.org/10.1002/cyto.a.20146