Allorestricted T lymphocytes with a high avidity T-cell receptor towards NY-ESO-1 have potent anti-tumor activity

International Journal of Cancer

Volumn 125, Issue 3, 2009, Pages 649-655

  Krönig, Holger ^a   Hofer, Kathrin ^a   Conrad, Heinke ^a,b   Guilaume, Philippe ^c   Müller, Julia ^a   Schiemann, Matthias ^d   Lennerz, Volker ^e   Cosma, Antonio ^b   Peschel, Christian ^a   Busch, Dirk H ^b,d   Romero, Pedro ^c   Bernhard, Helga ^a,b,f  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^f KLINIKUM DARMSTADT   (Germany)

Author keywords

Antigens peptides epitopes; Cytotoxic T cells; Human; Tumor immunity

Indexed keywords

EPITOPE; HLA A ANTIGEN; NY ESO 1 ANTIGEN; T LYMPHOCYTE RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE TRANSFER; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN CELL; LYMPHOCYTE SUBPOPULATION; MELANOMA; MOLECULAR RECOGNITION; MYELOMA; NONHUMAN; PRIORITY JOURNAL; SOLID TUMOR; T LYMPHOCYTE; TUMOR CELL LINE;

ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CYTOTOXICITY TESTS, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENES, T-CELL RECEPTOR; HLA-A ANTIGENS; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, CYTOTOXIC;

EID: 67650035114     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24414     Document Type: Article

References (43)

1. Gnjatic S, Nishikawa H, Jungbluth AA, Güre AO, Ritter G, Jäger E, Knuth A, Chen A-T, Old LJ. NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 2006;95:1-30.
2. Jäger E, Chen Y-T, Drijfhout JW, Karbach J, Ringhoffer M, Jäger D, Arand M, Wada H, Noguchi Y, Stockert E, Knuth A, Old LJ. Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitope. J Exp Med 1998;187:265-70.
3. Jäger E, Nagata Y, Gnjatic S, Wada H, Stockert E, Karbach J, Dunbar PR, Lee SY, Jungblut A, Jäger D, Arand M, Ritter G, et al. Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral and cellular immune responses. Proc Natl Acad Sci USA 2000;97:4760-5.
4. Karbach J, Gnjatic S, Pauligk C, Bender A, Maeurer M, Schultze JL, Nadler K, Wahle C, Knuth A, Old LJ, Jäger E. Tumor-reactive CD8+ T-cell clones in patients after NY-ESO-1 peptide vaccination. Int J Cancer 2007;121:2042-8.
5. Gnjatic S, Atanackovic D, Jäger E, Matsuo M, Selvakumar A, Altorki NK, Maki RG, Dupont B, Ritter G, Chen Y, Knuth A, Old LJ. Survey of naturally occurring CD4+ T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses. Proc Natl Acad Sci USA 2003;100:8862-7.
6. Condomines M, Hose D, Raynaud P, Hundemer M, DeVos J, Baudard M, Moehler T, Pantesco V, Moos M, Schved J-F, Rossi J-F, Rème T, et al. Cancer/testis genes in multiple myeloma: expression patterns and prognosis value determined by microarray analysis. J Immunol 2007;178:3307-15.
7. van Rhee F, Szmania SM, Zhan F, Gupta SK, Pomtree M, Lin P, Batchu RB, Moreno A, Spagnoli G, Shaughnessy J, Tricot G. NYESO-1 is highly expressed in poor-prognosis multiple myeloma and induces spontaneous humoral and cellular immune responses. Blood 2005;105:3939-44.
8. Jäger E, Ringhoffer M, Karbach J, Arand M, Oesch F, Knuth A. Inverse relationship of melanocyte differentiation antigen expression in melanoma tissues and CD8+ cytotxic T-cell responses: evidence for immunoselection of antigen-loss variants in vivo. Int J Cancer 1996;16:470-6.
9. Yee C, Thompson JA, Roche P, Byrd DR, Lee PP, Piepkorn M, Kenyon K, Davis MM, Riddell SR, Greenberg PD. Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of T cell-mediated vitiligo. J Exp Med 2000;192:1637-43.
10. Baumgaertner P, Rufer N, Devevre E, Derre L, Rimoldi D, Geldhof C, Voelter V, Liènard D, Romero P, Speiser DE. Ex vivo detectable human CD8 T-cell responses to cancer-testis antigens. Cancer Res 2006;66:1912-6.
11. Gotter J, Brors B, Hergenhahn M, Kyewski B. Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J Exp Med 2004;199:155-66.
12. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, Greenberg PD. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci USA 2002;99:16168-73.
13. Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A, Sixbey J, Gresik MV, Carrum G, Hudson M, Dilloo D, Gee A, et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus Hodgkin's disease. J Exp Med 2004;200:1623-33.
14. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, Rogers LJ, Gracia GJ, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-57.
15. Mackensen A, Meidenbauer N, Vogl S, Laumer M, Berger J, Andreesen R. Phase I study of adoptive T-cell therapy using antigenspecific CD8+ T cells for the treatment of patients with metastatic melanoma. J Clin Oncol 2006;24:5060-8.
16. Schumacher TNM. T-cell-receptor gene therapy. Nat Rev Immunol 2002;2:512-9.
17. Clay TM, Custer MC, Sachs J, Hwu P, Rosenberg SA, Nishimura MI. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J Immunol 1999;163:507-13.
18. Morgan RA, Dudley ME, Yu YYL, Zheng Z, Robbins PE, Theoret MR, Wunderlich JR, Hughes MS, Restifo NP, Rosenberg SA. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J Immunol 2003;171:3287-95.
19. Engels B, Noessner E, Frankenberger B, Blankenstein T, Schendel DJ, Uckert W. Redirecting human T lymphocytes toward renal cell carcinoma specificity by retroviral transfer of T cell receptor genes. Hum Gene Ther 2005;16:799-810.
20. Xue S-A, Gao L, Hart D, Gillmore R, Qasim W, Thraser A, Apperley J, Engels B, Uckert W, Morris E, Stauss H. Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene transduced human T cells. Blood 2005;106:3062-7.
21. Sommermeyer D, Neudorfer J, Weinhold M, Engels B, Noessner E, Heemskerk MHM, Schendel DJ, Blankenstein T, Bernhard H, Uckert W. Designer T cells by T cell receptor replacement. Eur J Immunol 2006;36:3052-9.
22. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, Zheng Z, Nahvi A, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006;314:126-9.
23. Sadovnikova E, Jopling LA, Soo KS, Stauss HJ. Generation of human tumor-reactive cytotoxic T cells against peptides presented by nonself HLA class I molecules. Eur J Immunol 1998;28:193-200.
24. Münz C, Obst R, Osen W, Stevanovic' S, Rammensee H-G. Alloreactivity as a source of high avidity peptide-specific human CTL. J Immunol 1999;162:25-34.
25. de Witte MA, Coccoris M, Wolkers MC, vandenBoom MD, Mesman EM, Song J-Y, van der Valk M, Haanen JBAG, Schumacher TNM. Targeting self-antigens through allogeneic TCR gene transfer. Blood 2006;108:870-7.
26. Busch DH, Philip IM, Vijh S, Pamer EG. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity 1998;8:353-62.
27. Pittet MJ, Rubio-Godoy V, Bioley G, Guillaume P, Bastard P, Speiser D, Luescher I, Cerottini J-C, Romero P, Zippelius A. Alpha3 domain mutants of peptide/MHC class I multimers allow the selective isolation of high avidity tumor-reactive CD8 T cells. J Immunol 2003;171:1844-9.
28. Neudorfer J, Schmidt B, Huster KM, Anderl F, Schiemann M, Holzapfel G, Schmidt T, Germeroth L, Wagner H, Peschel C, Busch DH, Bernhard H. Reversible HLA multimers (Streptamers) for the isolation of human cytotoxic T lymphocytes functionally active against tumor- and virus-derived antigens. J Immunol Methods 2007;320:119-31.
29. Wei S, Charmley P, Robinson MA, Concannon P. The extent of the human germline T-cell receptor V beta gene segment repertoire. Immunogenetics 1994;40:27-36.
30. Pittet MJ, Zippelius A, Speiser DE, Assenmacher M, Guilaume P, Valmori D, Liénard D, Lejeune F, Cerottini J-C, Romero P. Ex vivo IFN-g secretion by circulating CD8 lymphocytes: implications of a novel approach for T cell monitoring in infectious and malignant diseases. J Immunol 2001;166:7634-40.
31. Jonuleit H, Kuhn U, Müller G, Steinbrink K, Paragnik L, Schmitt E, Knop J, Enk AH. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997;27:3135-42.
32. Fleischer K, Schmidt B, Kastenmüller W, Busch DH, Drexler I, Sutter G, Heike M, Peschel C, Bernhard H. Melanoma-reactive class Irestricted cytotoxic T cell clones are stimulated by dendritic cells loaded with synthetic peptides, but fail to respond to dendritic cells pulsed with melanoma-derived heat shock proteins in vitro. J Immunol 2004;172:162-9.
33. Felix NJ, Donermeyer DL, Horvath S, Walters JJ, Gross ML, Suri A, Allen PM. Alloreactive T cells respond specifically to multiple distinct peptide-MHC complexes. Nat Immunol 2007;8:388-97.
34. Schuster IG, Busch DH, Eppinger E, Kremmer E, Milosevic S, Hennard C, Kuttler C, Ellwart JW, Frankenberger B, Nöβner E, Salat C, Bogner C, et al. Allorestricted T cells with specificity for the FMNL1-derived peptide PP2 have potent antitumor activity against hematological and other malignancies. Blood 2007;110:2931-9.
35. Jäger E, Gnjatic S, Nagata Y, Stockert E, Jäger D, Karbach J, Neumann A, Rieckenberg J, Chen YT, Ritter G, Hoffman E, Arand M, et al. Induction of primary NY-ESO-1 immunity: CD81 T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers. Proc Natl Acad Sci USA 2000;97:12198-203.
36. Bernhard H, Neudorfer J, Gebhard K, Conrad H, Hermann C, Nährig J, Fend F, Weber W, Busch DH, Peschel C. Adoptive transfer of autologous HER2-specific cytotoxic T lymphocytes for HER2-overexpressing breast cancer. Cancer Immunol Immunother 2008;57:271-80.
37. Stanislawski T, Voss R-H, Lotz C, Sadovnikova E, Willemsen RA, Kuball J, Ruppert T, Bolhuis RLH, Melief CJ, Huber C, Stauss HJ, Theobald M. Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat Immunol 2001;2:962-70.
38. Conrad H, Gebhard K, Krönig H, Neudorfer J, Busch DH, Peschel C, Bernhard H. Cytotoxic T lymphocytes directed against HER2 specifi-cally cross-react with HER3 and HER4. J Immunol 2008;180:8135-45.
39. Jäger E, Karbach J, Gnjatic S, Jäger D, Maeurer M, Atmaca A, Arand M, Skipper J, Stockert E, Chen A, Old LJ, Knuth A. Identification of a naturally processed NY-ESO-1 peptide recognized by CD8+ T cells in the context of HLA-B51. Cancer Immun 2002;2:12.
40. Cohn M. Degeneracy, mimicry and crossreactivity in immune recognition. Mol Immunol 2005;42:651-5.
41. Colf LA, Bankovich AJ, Hanick NA, Bowerman NA, Jones LL, Kranz DM, Garcia KC. How a single T cell receptor recognizes both self and foreign MHC. Cell 2007;129:135-46.
42. Zhao Y, Zeng Z, Robbins PF, Khong HT, Rosenberg SA, Morgan RA. Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J Immunol 2005;174:4415-23.
43. Zhao Y, Bennett AD, Zheng Z, Wang QJ, Robbins PF, Yu LYL, Li Y, Molloy PE, Dunn SM, Jakobsen BK, Rosenberg SA, Morgan RA. High-affinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. J Immunol 2007;179:5845-54.