Isolation and characterization of an HLA-DPB1∗04:01-restricted MAGE-A3 T-cell receptor for cancer immunotherapy

Journal of Immunotherapy

Volumn 39, Issue 5, 2016, Pages 191-201

  Yao, Xin ^a,b   Lu, Yong Chen ^a   Parker, Linda L ^a   Li, Yong F ^a   El Gamil, Mona ^a   Black, Mary A ^a   Xu, Hui ^a   Feldman, Steven A ^a   Van Der Bruggen, Pierre ^c,d   Rosenberg, Steven A ^a   Robbins, Paul F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Cellular Biomedicine Group Inc   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d DE DUVE INSTITUTE   (Belgium)

Author keywords

Cancer immunotherapy; Cancer germline antigens; Tumor immunology

Indexed keywords

GAMMA INTERFERON; HLA DPB1 ANTIGEN; MELANOMA ANTIGEN 3; MELANOMA ANTIGEN A3; MELANOMA ANTIGEN A6; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG; CANCER VACCINE; CD4 ANTIGEN; HLA DP ANTIGEN; HLA-DPB1*04:01 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MAGEA3 PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR PROTEIN;

ADOPTIVE TRANSFER; AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PATIENT; CAUCASIAN; CD4+ T LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; FEASIBILITY STUDY; GENE PRODUCT; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TUMOR IMMUNOLOGY; TUMOR REGRESSION; ADOPTIVE IMMUNOTHERAPY; ANTIGEN PRESENTATION; CELL SEPARATION; CROSS REACTION; GENE THERAPY; GENETICS; HELPER CELL; IMMUNOLOGY; METABOLISM; PROCEDURES; TRANSPLANTATION; VACCINATION;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CANCER VACCINES; CD4 ANTIGENS; CELL SEPARATION; CLONE CELLS; CROSS REACTIONS; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENETIC THERAPY; HLA-DP BETA-CHAINS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MELANOMA; NEOPLASM PROTEINS; RECEPTORS, ANTIGEN, T-CELL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; VACCINATION;

EID: 84971223739     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0000000000000123     Document Type: Article

References (59)

1. Rosenberg SA, Restifo NP. Adoptive cell transfer as personalized immunotherapy for human cancer. Science. 2015;348: 62-68.
2. Robbins PF, Kassim SH, Tran TL, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reac-tive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015;21:1019-1027.
3. Robbins PF, Morgan RA, Feldman SA, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol. 2011;29:917-924.
4. Rapoport AP, Stadtmauer EA, Binder-Scholl GK, et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat Med. 2015;21:914-921.
5. Kochenderfer JN, Wilson WH, Janik JE, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116:4099-4102.
6. Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365:725-733.
7. Kalos M, Levine BL, Porter DL, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3:95ra73.
8. Kochenderfer JN, Dudley ME, Feldman SA, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2012;119: 2709-2720.
9. Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5:177ra38.
10. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371:1507-1517.
11. Davila ML, Riviere I, Wang X, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014;6:224ra25.
12. Kochenderfer JN, Dudley ME, Kassim SH, et al. Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor. J Clin Oncol. 2015;33:540-549.
13. Lee DW, Kochenderfer JN, Stetler-Stevenson M, et al. T cells expressing CD19 chimeric antigen receptors for acute lympho-blastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet. 2015;385:517-528.
14. Johnson LA, Morgan RA, Dudley ME, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 2009;114:535-546.
15. Morgan RA, Yang JC, Kitano M, et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther. 2010;18:843-851.
16. Parkhurst MR, Yang JC, Langan RC, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther. 2011;19:620-626.
17. Morgan RA, Chinnasamy N, Abate-Daga D, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother. 2013;36:133-151.
18. Linette GP, Stadtmauer EA, Maus MV, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood. 2013;122:863-871.
19. Simpson AJ, Caballero OL, Jungbluth A, et al. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer. 2005;5:615-625.
20. Coulie PG, Van den Eynde BJ, van der Bruggen P, et al. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer. 2014;14:135-146.
21. van der Bruggen P, Traversari C, Chomez P, et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991;254:1643-1647.
22. Chomez P, De Backer O, Bertrand M, et al. An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res. 2001;61:5544-5551.
23. Rosenberg SA. Cell transfer immunotherapy for metastatic solid cancer-what clinicians need to know. Nat Rev Clin Oncol. 2011;8:577-585.
24. Roeder C, Schuler-Thurner B, Berchtold S, et al. MAGE-A3 is a frequent tumor antigen of metastasized melanoma. Arch Dermatol Res. 2005;296:314-319.
25. Tajima K, Obata Y, Tamaki H, et al. Expression of cancer/testis (CT) antigens in lung cancer. Lung Cancer. 2003;42:23-33.
26. Filho PA, Lopez-Albaitero A, Xi L, et al. Quantitative expression and immunogenicity of MAGE-3 and-6 in upper aerodigestive tract cancer. Int J Cancer. 2009;125: 1912-1920.
27. Kim J, Reber HA, Hines OJ, et al. The clinical significance of MAGEA3 expression in pancreatic cancer. Int J Cancer. 2006;118:2269-2275.
28. Luo G, Huang S, Xie X, et al. Expression of cancer-testis genes in human hepatocellular carcinomas. Cancer Immun. 2002; 2:11.
29. Han MH, Eom HS, Park WS, et al. Detection of circulating lymphoma cells in patients with non-Hodgkin lymphoma using MAGE-A3 gene expression in peripheral blood. Leuk Res. 2010;34:1127-1131.
30. Jungbluth AA, Ely S, DiLiberto M, et al. The cancer-testis antigens CT7 (MAGE-C1) and MAGE-A3/6 are commonly expressed in multiple myeloma and correlate with plasma-cell proliferation. Blood. 2005;106:167-174.
31. Gure AO, Chua R, Williamson B, et al. Cancer-testis genes are coordinately expressed and are markers of poor outcome in non-small cell lung cancer. Clin Cancer Res. 2005;11: 8055-8062.
32. Dhodapkar MV, Osman K, Teruya-Feldstein J, et al. Expression of cancer/testis (CT) antigens MAGE-A1, MAGE-A3, MAGE-A4, CT-7, and NY-ESO-1 in malignant gammopathies is heterogeneous and correlates with site, stage and risk status of disease. Cancer Immun. 2003;3:9.
33. Park TS, Groh EM, Patel K, et al. Expression of MAGE-A and NY-ESO-1 in primary and metastatic cancers. J Immun-other. 2016;39:1-7.
34. Cameron BJ, Gerry AB, Dukes J, et al. Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med. 2013;5:197ra103.
35. Francois V, Ottaviani S, Renkvist N, et al. The CD4(+) T-cell response of melanoma patients to a MAGE-A3 peptide vaccine involves potential regulatory T cells. Cancer Res. 2009;69: 4335-4345.
36. Morgan RA, Dudley ME, Wunderlich JR, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 2006;314:126-129.
37. Wargo JA, Robbins PF, Li Y, et al. Recognition of NY-ESO-1+ tumor cells by engineered lymphocytes is enhanced by improved vector design and epigenetic modulation of tumor antigen expression. Cancer Immunol Immunother. 2009;58: 383-394.
38. Cohen CJ, Zhao Y, Zheng Z, et al. 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;66:8878-8886.
39. Schultz ES, Lethe B, Cambiaso CL, et al. A MAGE-A3 peptide presented by HLA-DP4 is recognized on tumor cells by CD4+ cytolytic T lymphocytes. Cancer Res. 2000;60: 6272-6275.
40. Bendle GM, Linnemann C, Hooijkaas AI, et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med. 2010;16:565-570. 1p following 570.
41. Liu W, Cheng S, Asa SL, et al. The melanoma-associated antigen A3 mediates fibronectin-controlled cancer progression and metastasis. Cancer Res. 2008;68:8104-8112.
42. Yang B, O'Herrin SM, Wu J, et al. MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res. 2007;67:9954-9962.
43. Marcar L, Maclaine NJ, Hupp TR, et al. Mage-A cancer/testis antigens inhibit p53 function by blocking its interaction with chromatin. Cancer Res. 2010;70:10362-10370.
44. Monte M, Simonatto M, Peche LY, et al. MAGE-A tumor antigens target p53 transactivation function through histone deacetylase recruitment and confer resistance to chemother-apeutic agents. Proc Natl Acad Sci USA. 2006;103: 11160-11165.
45. Lu YC, Yao X, Li YF, et al. Mutated PPP1R3B is recognized by T cells used to treat a melanoma patient who experienced a durable complete tumor regression. J Immunol. 2013;190:6034-6042.
46. Chinnasamy N, Wargo JA, Yu Z, et al. A TCR targeting the HLA-A∗0201-restricted epitope of MAGE-A3 recognizes multiple epitopes of the MAGE-A antigen superfamily in several types of cancer. J Immunol. 2011;186:685-696.
47. Ossendorp F, Mengede E, Camps M, et al. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med. 1998;187:693-702.
48. Antony PA, Piccirillo CA, Akpinarli A, et al. CD8 + T cell immunity against a tumor/self-antigen is augmented by CD4 + T helper cells and hindered by naturally occurring T regulatory cells. J Immunol. 2005;174:2591-2601.
49. Muranski P, Boni A, Antony PA, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood. 2008;112:362-373.
50. Hirschhorn-Cymerman D, Budhu S, Kitano S, et al. Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. J Exp Med. 2012;209:2113-2126.
51. Quezada SA, Simpson TR, Peggs KS, et al. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med. 2010;207:637-650.
52. Xie Y, Akpinarli A, Maris C, et al. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J Exp Med. 2010;207:651-667.
53. Hunder NN, Wallen H, Cao J, et al. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med. 2008;358:2698-2703.
54. Tran E, Turcotte S, Gros A, et al. Cancer immunotherapy based on mutation-specific CD4 + T cells in a patient with epithelial cancer. Science. 2014;344:641-645.
55. Chaux P, Vantomme V, Stroobant V, et al. Identification of MAGE-3 epitopes presented by HLA-DR molecules to CD4(+) T lymphocytes. J Exp Med. 1999;189:767-778.
56. Manici S, Sturniolo T, Imro MA, et al. Melanoma cells present a MAGE-3 epitope to CD4(+) cytotoxic T cells in association with histocompatibility leukocyte antigen DR11. J Exp Med. 1999;189:871-876.
57. Kobayashi H, Song Y, Hoon DS, et al. Tumor-reactive T helper lymphocytes recognize a promiscuous MAGE-A3 epitope presented by various major histocompatibility complex class II alleles. Cancer Res. 2001;61:4773-4778.
58. Consogno G, Manici S, Facchinetti V, et al. Identification of immunodominant regions among promiscuous HLA-DR-restricted CD4 + T-cell epitopes on the tumor antigen MAGE-3. Blood. 2003;101:1038-1044.
59. Gonzalez-Galarza FF, Takeshita LY, Santos EJ, et al. Allele frequency net 2015 update: new features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Res. 2015;43(database issue):D784-D788.