Specificity for the tumor-associated self-antigen WT1 drives the development of fully functional memory T cells in the absence of vaccination

Blood

Volumn 117, Issue 25, 2011, Pages 6813-6824

  Pospori, Constandina ^a   Xue, Shao An ^a   Holler, Angelika ^a   Voisine, Cecile ^a   Perro, Mario ^a   King, Judith ^a   Fallah Arani, Farnaz ^b   Flutter, Barry ^b   Chakraverty, Ronjon ^a   Stauss, Hans J ^a   Morris, Emma C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; HLA A1 ANTIGEN; T LYMPHOCYTE RECEPTOR; WT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN FUNCTION; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL POPULATION; FEMALE; GENE TRANSFER; HEMATOPOIETIC STEM CELL; HLA SYSTEM; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; THYMOCYTE; THYMUS; VACCINATION;

EID: 79959518670     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-304568     Document Type: Article

References (41)

1. Inoue K, Ogawa H, Sonoda Y, et al. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia. Blood. 1997;89(4):1405-1412. (Pubitemid 27080005)
2. Inoue K, Ogawa H, Yamagami T, et al. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels. Blood. 1996;88(6):2267-2278. (Pubitemid 26307931)
3. Inoue K, Sugiyama H, Ogawa H, et al. WT1 as a new prognostic factor and a new marker for the detection of minimal residual disease in acute leukemia. Blood. 1994;84(9):3071-3079. (Pubitemid 24328100)
4. Menssen HD, Renkl HJ, Rodeck U, et al. Presence of Wilms' tumor gene (wt1) transcripts and the WT1 nuclear protein in the majority of human acute leukemias. Leukemia. 1995;9(6):1060-1067.
5. Tamaki H, Ogawa H, Inoue K, et al. Increased expression of the Wilms tumor gene (WT1) at relapse in acute leukemia. Blood. 1996;88(11):4396-4398. (Pubitemid 26399190)
6. Cilloni D, Renneville A, Hermitte F, et al. Realtime 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;27(31):5195-5201.
7. 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 U S A. 2004;101(38):13885-13890. (Pubitemid 39298502)
8. Keilholz U, Letsch A, Busse A, et al. A clinical and immunologic phase 2 trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS. Blood. 2009;113(26):6541-6548.
9. Gillmore R, Xue SA, Holler A, et al. Detection of Wilms' tumor antigen-specific CTL in tumor-draining lymph nodes of patients with early breast cancer. Clin Cancer Res. 2006;12(1):34-42. (Pubitemid 43166173)
10. 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(8):236-242.
11. Rezvani K, Yong AS, Savani BN, et al. Graftversus- leukemia effects associated with detectable Wilms tumor-1 specific T lymphocytes after allogeneic stem-cell transplantation for acute lymphoblastic leukemia. Blood. 2007;110(6):1924-1932. (Pubitemid 47443906)
12. Chaise C, Buchan SL, Rice J, et al. DNA vaccination induces WT1-specific T-cell responses with potential clinical relevance. Blood. 2008;112(7):2956- 2964.
13. Murao A, Oka Y, Tsuboi A, et al. High frequencies of less differentiated and more proliferative WT1-specific CD8 T cells in bone marrow in tumor-bearing patients: an important role of bone marrow as a secondary lymphoid organ. Cancer Sci. 2010;101(4):848-854.
14. 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(24):8799-8807. (Pubitemid 43005931)
15. Tanaka-Harada Y, Kawakami M, Oka Y, et al. Biased usage of BV gene families of T-cell receptors of WT1 (Wilms' tumor gene)-specific CD8+ T cells in patients with myeloid malignancies. Cancer Sci. 2010;101(3):594-600.
16. Weber G, Karbach J, Kuci S, et al. WT1 peptide-specific T cells generated from peripheral blood of healthy donors: possible implications for adoptive immunotherapy after allogeneic stem cell transplantation. Leukemia. 2009;23(9):1634-1642.
17. Wolfl M, Kuball J, Ho WY, et al. 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;110(1):201-210. (Pubitemid 47026836)
18. Boyman O, Letourneau S, Krieg C, Sprent J. Homeostatic proliferation and survival of naive and memory T cells. Eur J Immunol. 2009;39(8):2088-2094.
19. Haluszczak C, Akue AD, Hamilton SE, et al. The antigen-specific CD8+ T cell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion. J Exp Med. 2009;206(2):435-448.
20. Huang T, Wei B, Velazquez P, Borneman J, Braun J. Commensal microbiota alter the abundance and TCR responsiveness of splenic naive CD4+ T lymphocytes. Clin Immunol. 2005;117(3):221-230. (Pubitemid 43005208)
21. Gao L, Bellantuono I, Elsasser A, et al. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood. 2000;95(7):2198-2203. (Pubitemid 30167714)
22. Stauss HJ. Immunotherapy with CTLs restricted by nonself MHC. Immunol Today. 1999;20(4):180-183.
23. Xue SA, Gao L, Hart D, et al. Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene-transduced human T cells. Blood. 2005;106(9):3062-3067. (Pubitemid 41565901)
24. Xue SA, Gao L, Thomas S, et al. Development of a Wilms' tumor antigen-specific T-cell receptor for clinical trials: engineered patient's T cells can eliminate autologous leukemia blasts in NOD/SCID mice. Haematologica. 2010;95(1):126-134.
25. Hart DP, Xue SA, Thomas S, et al. Retroviral transfer of a dominant TCR prevents surface expression of a large proportion of the endogenous TCR repertoire in human T cells. Gene Ther. 2008;15(8):625-631.
26. Kingsman SM, Mitrophanous K, Olsen JC. Potential oncogene activity of the woodchuck hepatitis post-transcriptional regulatory element (WPRE). Gene Ther. 2005;12(1):3-4. (Pubitemid 40090038)
27. Holst J, Szymczak-Workman AL, Vignali KM, Burton AR, Workman CJ, Vignali DA. Generation of T-cell receptor retrogenic mice. Nat Protoc. 2006;1(1):406-417.
28. Yang L, Baltimore D. Long-term in vivo provision of antigen-specific T cell immunity by programming hematopoietic stem cells. Proc Natl Acad Sci U S A. 2005;102(12):4518-4523. (Pubitemid 40397144)
29. Cohen CJ, Zhao Y, Zheng Z, Rosenberg SA, Morgan RA. Enhanced antitumor activity of murine-human hybrid T-cell receptor (TCR) in human lymphocytes is associated with improved pairing and TCR/CD3 stability. Cancer Res. 2006;66(17):8878-8886. (Pubitemid 44449206)
30. Kuball J, Dossett ML, Wolfl M, et al. Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood. 2007;109(6):2331-2338. (Pubitemid 46425872)
31. Oka Y, Udaka K, Tsuboi A, et al. Cancer immunotherapy targeting Wilms' tumor gene WT1 product. J Immunol. 2000;164(4):1873-1880. (Pubitemid 30108741)
32. Kent J, Coriat AM, Sharpe PT, Hastie ND, van Heyningen V. The evolution of WT1 sequence and expression pattern in the vertebrates. Oncogene. 1995;11(9):1781-1792.
33. Schonrich G, Kalinke U, Momburg F, et al. Downregulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction. Cell. 1991;65(2):293-304. (Pubitemid 121006059)
34. Murali-Krishna K, Lau LL, Sambhara S, Lemonnier F, Altman J, Ahmed R. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science. 1999;286(5443):1377-1381.
35. Becker TC, Coley SM, Wherry EJ, Ahmed R. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J Immunol. 2005;174(3):1269-1273.
36. Leitao C, Freitas AA, Garcia S. The role of TCR specificity and clonal competition during reconstruction of the peripheral T cell pool. J Immunol. 2009;182(9):5232-5239.
37. Hohenstein P, Hastie ND. The many facets of the Wilms' tumor gene, WT1. Hum Mol Genet. 2006;15(2):R196-R201. (Pubitemid 44446794)
38. Cho BK, Rao VP, Ge Q, Eisen HN, Chen J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med. 2000;192(4):549-556. (Pubitemid 30666255)
39. Goldrath AW, Bogatzki LY, Bevan MJ. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med. 2000;192(4):557-564. (Pubitemid 30666256)
40. Min B, McHugh R, Sempowski GD, Mackall C, Foucras G, Paul WE. Neonates support lymphopenia-induced proliferation. Immunity. 2003;18(1):131-140. (Pubitemid 36120694)
41. Martinez-Estrada OM, Lettice LA, Essafi A, et al. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet. 2010;42(1):89-93.