Ex vivo characterization of polyclonal memory CD8+ T-cell responses to PRAME-specific peptides in patients with acute lymphoblastic leukemia and acute and chronic myeloid leukemia

Blood

Volumn 113, Issue 10, 2009, Pages 2245-2255

  Rezvani, Katayoun ^a,b   Yong, Agnes S M ^b   Tawab, Abdul ^c   Jafarpour, Behnam ^b   Eniafe, Rhoda ^b   Mielke, Stephan ^b,d   Savani, Bipin N ^b,e   Keyvanfar, Keyvan ^b   Li, Yixin ^c   Kurlander, Roger ^c   Barrett, A John ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d Wurzburg Army Medical Center   (Germany)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; EPITOPE; GAMMA INTERFERON; HLA A ANTIGEN; MELANOMA ANTIGEN; PREFERENTIALLY EXPRESSED ANTIGEN OF MELANOMA; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANTIGEN DETECTION; ANTIGEN EXPRESSION; ARTICLE; CANCER PATIENT; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL LEVEL; CELLULAR IMMUNITY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DONOR; EX VIVO STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOGENICITY; MEMORY T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION;

EID: 64049107901     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-03-144071     Document Type: Article

References (58)

1. 1.Ikeda H, Lethe B, Lehmann F, et al. Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity. 1997;6: 199-208.
2. van Baren N, Chambost H, Ferrant A, et al. PRAME, a gene encoding an antigen recognized on a human melanoma by cytolytic T cells, is expressed in acute leukaemia cells. Br J Haematol. 1998;102:1376-1379.
3. van't Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415:530-536.
4. Boon K, Edwards JB, Siu IM, et al. Comparison of medulloblastoma and normal neural transcrip-tomes identifies a restricted set of activated genes. Oncogene. 2003;22:7687-7694.
5. Epping MT, Wang L, Edel MJ, et al. The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling. Cell. 2005;122: 835-847.
6. Kessler JH, Beekman NJ, Bres-Vloemans SA, et al. Efficient identification of novel HLA-A(*)0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasome-mediated digestion analysis. J Exp Med. 2001;193:73-88.
7. + T cells specific for PRAME: a target for T-cell therapy. Clin Cancer Res. 2006;12:3130-3136.
8. Quintarelli C, Dotti G, DeAngelisB, et al. CytotoxicT lymphocytes directed to the preferentially expressed antigen of melanoma (PRAME) target chronic myeloid leukemia. Blood. 2008;112:1876-1885.
9. Greiner J, Schmitt M, Li L, et al. Expression of tumor-associated antigens in acute myeloid leukemia: implications for specific immunotherapeu-tic approaches. Blood. 2006;108:4109-4117.
10. Li L, Giannopoulos K, Reinhardt P, et al. Immuno-therapy for patients with acute myeloid leukemia using autologous dendritic cells generated from leukemic blasts. Int J Oncol. 2006;28:855-861.
11. Grunebach F, Mirakaj V, Mirakaj V, et al. BCR-ABL is not an immunodominant antigen in chronic myelogenous leukemia. Cancer Res. 2006;66: 5892-5900.
12. Steinbach D, Viehmann S, Zintl F, Gruhn B. PRAME gene expression in childhood acute lym-phoblastic leukemia. Cancer Genet Cytogenet. 2002;138:89-91.
13. Matsushita M, Ikeda H, Kizaki M, et al. Quantitative monitoring of the PRAME gene for the detection of minimal residual disease in leukaemia. BrJ Haematol.2001;112:916-926.
14. Diamond DJ, York J, Sun JY, Wright CL, Forman SJ. Development of a candidate HLAA*0201 restricted peptide-based vaccine against human cytomegalovirus infection. Blood. 1997;90:1751-1767.
15. Parkhurst MR, Salgaller ML, Southwood S, et al. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-Az.ast;0201-binding residues. J Immunol. 1996;157:2539-2548.
16. Zaremba S, Barzaga E, Zhu M, et al. Identification of an enhancer agonist cytotoxic Tlympho-cyte peptide from human carcinoembryonic antigen. Cancer Res. 1997;57:4570-4577.
17. McCutcheon M, Wehner N, Wensky A, et al. A sensitive ELISPOT assay to detect low-frequency human T lymphocytes. J Immunol Methods. 1997;210:149-166.
18. Kurlander RJ, Tawab A, Fan Y, Carter CS, Read EJ. Afunctional comparison of mature human dendritic cells prepared in fluorinated ethylene-propylene bags or polystyrene flasks. Transfusion. 2006;46:1494-1504.
19. Beillard E, Pallisgaard N, van der Velden VH, et al. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR)-a Europe against cancer program. Leukemia. 2003;17:2474-2486.
20. Yong AS, Szydlo RM, Goldman JM, Apperley JF, Melo JV. Molecular profiling of CD34+ cells identifies low expression of CD7, along with high expression of proteinase 3 or elastase, as predictors of longer survival in patients with CML. Blood. 2006;107:205-212.
21. Segal NH, Blachere NE, Guevara-Patino JA, et al. Identification of cancer-testis genes expressed by melanoma and soft tissue sarcoma using bioinformatics. Cancer Immun. 2005;5:2.
22. Alexander MA, Damico CA, Wieties KM, Hansen TH, Connolly JM. Correlation between CD8 dependency and determinant density using peptide-induced, Ld-restricted cytotoxic T lymphocytes. J Exp Med. 1991;173:849-858.
23. Molldrem JJ, Lee PP, Kant S, et al. Chronic myelogenous leukemia shapes host immunity by selective deletion of high-avidity leukemia-specific T cells. J Clin Invest. 2003;111:639-647.
24. Betts MR, Brenchley JM, Price DA, et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for de-granulation. J Immunol Methods. 2003;281:65-78.
25. Appay V, Dunbar PR, Callan M, et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med.2002;8:379-385.
26. Rezvani K, Grube M, Brenchley JM, et al. Functional leukemia-associated antigen-specific memory CD8+ T cells exist in healthy individuals and in patients with chronic myelogenous leukemia before and after stem cell transplantation. Blood. 2003;102:2892-2900.
27. Rezvani K, Brenchley JM, Price DA, et al. 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;11:8799-8807.
28. Rezvani K, Price D, Brenchley J, et al. Transfer of PR1-specific T-cell clones from donor to recipient by stem cell transplantation and association with GvL activity. Cytotherapy. 2007;9:245-251.
29. Gannage M, Abel M, Michallet AS, et al. Ex vivo characterization of multiepitopic tumor-specific CD8 T cells in patients with chronic myeloid leukemia: implications for vaccine development and adoptive cellular immunotherapy. J Immunol. 2005;174:8210-8218.
30. Scheibenbogen C, Letsch A, Thiel E, et al. CD8 T-cell responses to Wilms tumor gene product WT1 and proteinase 3 in patients with acute my-eloid leukemia. Blood. 2002;100:2132-2137.
31. Flanagan KL, Lee EA, Gravenor MB, et al. Unique T cell effector functions elicited by Plasmodium falciparum epitopes in malaria-exposed Africans tested by three T cell assays. J Immunol. 2001;167:4729-4737.
32. Karlsson AC, Martin JN, Younger SR, et al. Comparison of the ELISPOT and cytokine flow cytom-etry assays for the enumeration of antigen-spe-cificT cells. J Immunol Methods. 2003;283:141-153.
33. Whiteside TL, Zhao Y, Tsukishiro T, et al. Enzyme-linked immunospot, cytokine flow cytom-etry, and tetramers in the detection of T-cell responses to a dendritic cell-based multipeptide vaccine in patients with melanoma. Clin Cancer Res. 2003;9:641-649.
34. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory Tcell subsets: function, generation, and maintenance. Annu Rev Immunol. 2004;22:745-763.
35. Godkin AJ, Thomas HC, Openshaw PJ. Evolution of epitope-specific memory CD4(+) T cells after clearance of hepatitis C virus. J Immunol. 2002; 169:2210-2214.
36. Steinbach D, Hermann J, Viehmann S, Zintl F, Gruhn B. Clinical implications of PRAME gene expression in childhood acute myeloid leukemia. Cancer Genet Cytogenet. 2002;133:118-123.
37. Steinbach D, Schramm A, Eggert A, et al. Identification of a set of seven genes for the monitoring of minimal residual disease in pediatric acute my-eloid leukemia. Clin Cancer Res. 2006;12:2434-2441.
38. Tajeddine N, Millard I, Gailly P, Gala JL. Real-time RT-PCR quantification of PRAME gene expression for monitoring minimal residual disease in acute myeloblastic leukaemia. Clin Chem Lab Med. 2006;44:548-555.
39. van Baren N, Chambost H, Ferrant A, et al. PRAME, a gene encoding an antigen recognized on a human melanoma by cytolytic T cells, is expressed in acute leukaemia cells. Br J Haematol. 1998;102:1376-1379.
40. Kaufman DL, Clare-Salzler M, Tian J, et al. Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes. Nature. 1993;366:69-72.
41. Tisch R, Yang XD, Singer SM, et al. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature. 1993;366:72-75.
42. Brossart P, Wirths S, Stuhler G, et al. Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood. 2000;96:3102-3108.
43. Rezvani K, Yong AS, Savani BN, et al. Graft-versus-leukemia effects associated with detectable Wilms tumor-1 specific T lymphocytes following allogeneic stem cell transplantation for acute lymphoblastic leukemia (ALL). Blood. 2007; 110:1924-1932.
44. Molldrem JJ, Lee PP, Wang C, et al. Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat Med. 2000;6:1018-1023.
45. Yong AS, Rezvani K, Savani BN, et al. High PR3 or ELA2 expression by CD34+ cells in advanced-phase chronic myeloid leukemia is associated with improved outcome following allogeneic stem cell transplantation and may improve PR1 pep-tide-driven graft-versus-leukemia effects. Blood. 2007;110:770-775.
46. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443:350-354.
47. Penna A, Pilli M, Zerbini A, et al. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology. 2007;45:588-601.
48. Lee PP, Yee C, Savage PA, et al. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat Med. 1999;5:677-685.
49. Schmitt M, Li L, Giannopoulos K, et al. Chronic myeloid leukemia cells express tumor-associated antigens eliciting specific CD8+ T-cell responses and are lacking costimulatory molecules. Exp He-matol. 2006;34:1709-1719.
50. Grube M, Moritz S, Obermann EC, et al. CD8+ T cells reactive to survivin antigen in patients with multiple myeloma. Clin Cancer Res. 2007;13: 1053-1060.
51. Goodyear OC, Pratt G, McLarnon A, CookM, Piper K, Moss P. Differential pattern of CD4+ and CD8+ Tcell immunity to MAGE-A1/A2/A3 in patients with monoclonal gammopathy of undetermined significance (MGUS) and multiple myeloma. Blood. 2008;112:3362-3372.
52. Goodyear O, Piper K, Khan N, et al. CD8+ T cells specific for cancer germline gene antigens are found in many patients with multiple myeloma, and their frequency correlates with disease burden. Blood. 2005;106:4217-4224.
53. Mailander V, Scheibenbogen C, Thiel E, et al. Complete remission in a patient with recurrent acute myeloid leukemia induced by vaccination with WT1 peptide in the absence of hematologi-cal or renal toxicity. Leukemia. 2004;18:165-166.
54. 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. Proc Natl Acad Sci USA. 2004;101:13885-13890.
55. Qazilbash MH, Wieder E, Rios R, et al. Vaccination with the PR1 leukemia-associated antigen can induce complete remission in patients with myeloid leukemia. ASH Annual Meeting Abstracts. 2004;104:259.
56. Rezvani K, Yong AS, 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.
57. Yong AS, Keyvanfar K, Eniafe R, et al. Hemato-poietic stem cells and progenitors of chronic my-eloid leukemia express leukemia-associated antigens: implications for the graft-versus-leuke-mia effect and peptide vaccine-based immuno-therapy. Leukemia. 2008;22:1721-1727.
58. Radich JP, Dai H, Mao M, et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci U S A. 2006;103:2794-2799.