Development of a T cell receptor targeting an HLA-A*0201 restricted epitope from the cancer-testis antigen SSX2 for adoptive immunotherapy of cancer

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Abate Daga, Daniel ^a   Speiser, Daniel E ^b   Chinnasamy, Nachimuthu ^a   Zheng, Zhili ^a   Xu, Hui ^a   Feldman, Steven A ^a   Rosenberg, Steven A ^a   Morgan, Richard A ^a,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c BLUEBIRD BIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER TESTIS ANTIGEN; EPITOPE; GAMMA INTERFERON; HLA A 0201 ANTIGEN; HLA A ANTIGEN; RETROVIRUS VECTOR; SSX2 ANTIGEN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TETRAMER; UNCLASSIFIED DRUG; HLA A2 ANTIGEN; HLA-A*02:01 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; REPRESSOR PROTEIN; SYNOVIAL SARCOMA X BREAKPOINT PROTEINS; TUMOR ANTIGEN; TUMOR PROTEIN;

ANTIGEN EXPRESSION; ANTIGEN PURIFICATION; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INFILTRATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ENGINEERING; CLONING VECTOR; CODON; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; DRUG TARGETING; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; LYMPHOMA; MELANOMA; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PERIPHERAL LYMPHOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; SEROLOGY; SYNOVIAL SARCOMA; TUMOR CELL LINE; ADOPTIVE IMMUNOTHERAPY; GENETICS; IMMUNOLOGY; MALE; PROCEDURES; TESTIS;

ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; EPITOPES; HLA-A2 ANTIGEN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; MALE; NEOPLASM PROTEINS; RECEPTORS, ANTIGEN, T-CELL; REPRESSOR PROTEINS; TESTIS;

EID: 84899892697     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093321     Document Type: Article

References (51)

1. Rosenberg SA (2012) Raising the Bar: The Curative Potential of Human Cancer Immunotherapy. Science Translational Medicine 4.
2. Restifo NP, Dudley ME, Rosenberg SA (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nature Reviews Immunology 12: 269- 281.
3. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129. (Pubitemid 44547756)
4. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, et al. (2008) Adoptive Cell Therapy for Patients With Metastatic Melanoma: Evaluation of Intensive Myeloablative Chemoradiation Preparative Regimens. Journal of Clinical Oncology 26: 5233-5239.
5. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, et al. (2011) Durable Complete Responses in Heavily Pretreated Patients with Metastatic Melanoma Using T-Cell Transfer Immunotherapy. Clinical Cancer Research 17: 4550-4557.
6. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, et al. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114: 535-546.
7. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DAN, et al. (2011) T Cells Targeting Carcinoembryonic Antigen Can Mediate Regression of Metastatic Colorectal Cancer but Induce Severe Transient Colitis. Molecular Therapy 19: 620-626.
8. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, et al. (2012) B-cell depletion and remissions of malignancy along with cytokineassociated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptortransduced T cells. Blood 119: 2709-2720.
9. Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, et al. (2013) Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nature Medicine 19: 747-+.
10. Dubovsky JA, McNeel DG (2007) Inducible expression of a prostate cancer-testis antigen, SSX-2, following treatment with a DNA methylation inhibitor. Prostate 67: 1781-1790. (Pubitemid 350228730)
11. Hofmann O, Caballero OL, Stevenson BJ, Chen YT, Cohen T, et al. (2008) Genome-wide analysis of cancer/testis gene expression. Proceedings of the National Academy of Sciences of the United States of America 105: 20422- 20427.
12. Suri A (2006) Cancer testis antigens - their importance in immunotherapy and in the early detection of cancer. Expert Opinion on Biological Therapy 6: 379-389.
13. Simpson AJG, Caballero OL, Jungbluth A, Chen YT, Old LJ (2005) Cancer/ testis antigens, gametogenesis and cancer. Nature Reviews Cancer 5: 615-625.
14. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, et al. (2011) Tumor Regression in Patients With Metastatic Synovial Cell Sarcoma and Melanoma Using Genetically Engineered Lymphocytes Reactive With NY-ESO-1. Journal of Clinical Oncology 29: 917-924.
15. Clark J, Rocques PJ, Crew AJ, Gill S, Shipley J, et al. (1994) Identification of Novel Genes, Syt and Ssx, Involved in the T(X18)(P11.2q11.2) Translocation Found in Human Synovial Sarcoma. Nature Genetics 7: 502-508. (Pubitemid 24308337)
16. Crew AJ, Clark J, Fisher C, Gill S, Grimer R, et al. (1995) Fusion of Syt to 2 Genes, Ssx1 and Ssx2, Encoding Proteins with Homology to the Kruppel- Associated Box in Human Synovial Sarcoma (Vol 14, Pg 2333, 1995). Embo Journal 14: 5456-5456.
17. Tureci O, Sahin U, Schobert I, Koslowski M, Schmitt H, et al. (1996) The SSX- 2 gene, which is involved in the t(X;18) translocation of synovial sarcomas, codes for the human tumor antigen HOM-MEL-40. Cancer Research 56: 4766-4772. (Pubitemid 26338082)
18. Ayyoub M, Rimoldi D, Guillaume P, Romero P, Cerottini JC, et al. (2003) Tumor-reactive, SSX-2-specific CD8 (+) T cells are selectively expanded during immune responses to antigen-expressing tumors in melanoma patients. Cancer Research 63: 5601-5606. (Pubitemid 37139884)
19. Robbins PF, Li YF, El-Gamil M, Zhao YB, Wargo JA, et al. (2008) Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. Journal of Immunology 180: 6116-6131.
20. Parkhurst MR, Joo J, Riley JP, Yu ZY, Li Y, et al. (2009) Characterization of Genetically Modified T-Cell Receptors that Recognize the CEA:691-699 Peptide in the Context of HLA-A2.1 on Human Colorectal Cancer Cells. Clinical Cancer Research 15: 169-180.
21. Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, et al. (2008) NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res 36: W509-512.
22. Wargo JA, Robbins PF, Li Y, Zhao YB, El-Gamil M, et al. (2009) Recognition of NY-ESO-1+tumor cells by engineered lymphocytes is enhanced by improved vector design and epigenetic modulation of tumor antigen expression. Cancer Immunology Immunotherapy 58: 383-394.
23. Cohen CJ, Zhao Y, Zheng Z, Rosenberg SA, Morgan RA (2006) 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 66: 8878-8886. (Pubitemid 44449206)
24. Hughes MS, Yu YYL, Dudley ME, Zheng ZL, Robbins PF, et al. (2005) Transfer of a TCR gene derived from a patient with a marked antitumor response conveys highly active T-cell effector functions. Human Gene Therapy 16: 457-472. (Pubitemid 40647143)
25. Zhao YB, Zheng ZL, Robbins PF, Khong HT, Rosenberg SA, et al. (2005) Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tunior cell lines. Journal of Immunology 174: 4415-4423. (Pubitemid 40396025)
26. Onodera M, Yachie A, Nelson DM, Welchlin H, Morgan RA, et al. (1997) A simple and reliable method for screening retroviral producer clones without selectable markers. Human Gene Therapy 8: 1189-1194. (Pubitemid 27394127)
27. Wargo JA, Robbins PF, Li Y, Zhao Y, El-Gamil M, et al. (2009) 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 58: 383-394.
28. Yang S, Cohen CJ, Peng PD, Zhao Y, Cassard L, et al. (2008) Development of optimal bicistronic lentiviral vectors facilitates high-level TCR gene expression and robust tumor cell recognition. Gene Ther 15: 1411-1423.
29. Garcia CB, Shaffer CM, Eid JE (2012) Genome-wide recruitment to Polycombmodified chromatin and activity regulation of the synovial sarcoma oncogene SYT-SSX2. BMC Genomics 13: 189.
30. Przybyl J, Jurkowska M, Rutkowski P, Debiec-Rychter M, Siedlecki JA (2012) Downstream and intermediate interactions of synovial sarcoma-associated fusion oncoproteins and their implication for targeted therapy. Sarcoma 2012: 249219.
31. Shiraishi T, Terada N, Zeng Y, Suyama T, Luo J, et al. (2011) Cancer/Testis antigens as potential predictors of biochemical recurrence of prostate cancer following radical prostatectomy. Journal of Translational Medicine 9.
32. Smith HA, Cronk RJ, Lang JM, McNeel DG (2011) Expression and Immunotherapeutic Targeting of the SSX Family of Cancer-Testis Antigens in Prostate Cancer. Cancer Research 71: 6785-6795.
33. Atanackovic D, Arfsten J, Cao YR, Gnjatic S, Schnieders F, et al. (2007) Cancertestis antigens are commonly expressed in multiple myeloma and induce systemic immunity following allogeneic stem cell transplantation. Blood 109: 1103-1112. (Pubitemid 46220657)
34. Taylor BJ, Reiman T, Pittman JA, Keats JJ, de Bruijn DRH, et al. (2005) SSX cancer testis antigens are expressed in most multiple myeloma patients - Coexpression of SSX1, 2, 4, and 5 correlates with adverse prognosis and high frequencies of SSX-positive PCs. Journal of Immunotherapy 28: 564-575.
35. dos Santos NR, Torensma R, de Vries TJ, Schreurs MW, de Bruijn DR, et al. (2000) Heterogeneous expression of the SSX cancer/testis antigens in human melanoma lesions and cell lines. Cancer Res 60: 1654-1662.
36. Taylor BJ, Reiman T, Pittman JA, Keats JJ, de Bruijn DR, et al. (2005) SSX cancer testis antigens are expressed in most multiple myeloma patients: coexpression of SSX1, 2, 4, and 5 correlates with adverse prognosis and high frequencies of SSX-positive PCs. J Immunother 28: 564-575. (Pubitemid 41533090)
37. Atanackovic D, Luetkens T, Hildebrandt Y, Arfsten J, Bartels K, et al. (2009) Longitudinal analysis and prognostic effect of cancer-testis antigen expression in multiple myeloma. Clin Cancer Res 15: 1343-1352.
38. Hoffman-Censits J, Fu M (2013) Chemotherapy and targeted therapies: are we making progress in castrate-resistant prostate cancer? Semin Oncol 40: 361-374.
39. Kharfan-Dabaja MA, Hamadani M, Reljic T, Nishihori T, Bensinger W, et al. (2013) Comparative efficacy of tandem autologous versus autologous followed by allogeneic hematopoietic cell transplantation in patients with newly diagnosed multiple myeloma: a systematic review and meta-analysis of randomized controlled trials. J Hematol Oncol 6: 2.
40. Gure AO, Wei IJ, Old LJ, Chen YT (2002) The SSX gene family: Characterization of 9 complete genes. International Journal of Cancer 101: 448-453.
41. Ayyoub M, Stevanovic S, Sahin U, Guillaume P, Servis C, et al. (2002) Proteasome-assisted identification of a SSX-2-derived epitope recognized by tumor-reactive CTL infiltrating metastatic melanoma. Journal of Immunology 168: 1717-1722. (Pubitemid 34135769)
42. Bricard G, Bouzourene H, Martinet O, Rimoldi D, Halkic N, et al. (2005) Naturally acquired MAGE-A10- and SSX-2-specific CD8+ T cell responses in patients with hepatocellular carcinoma. J Immunol 174: 1709-1716.
43. Perez-Diez A, Joncker NT, Choi K, Chan WF, Anderson CC, et al. (2007) CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346- 5354.
44. Corthay A, Skovseth DK, Lundin KU, Rosjo E, Omholt H, et al. (2005) Primary antitumor immune response mediated by CD4+ T cells. Immunity 22: 371-383. (Pubitemid 40387478)
45. Chinnasamy N, Wargo JA, Yu Z, Rao M, Frankel TL, et al. (2011) 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. Journal of Immunology 186: 685-696.
46. Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, et al. (2013) Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 36: 133-151.
47. Ochi T, Fujiwara H, Okamoto S, An J, Nagai K, et al. (2011) Novel adoptive Tcell immunotherapy using a WT1-specific TCR vector encoding silencers for endogenous TCRs shows marked antileukemia reactivity and safety. Blood 118: 1495-1503.
48. Provasi E, Genovese P, Lombardo A, Magnani Z, Liu PQ, et al. (2012) Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat Med 18: 807-815.
49. Davis JL, Theoret MR, Zheng ZL, Lamers CHJ, Rosenberg SA, et al. (2010) Development of Human Anti-Murine T-Cell Receptor Antibodies in Both Responding and Nonresponding Patients Enrolled in TCR Gene Therapy Trials. Clinical Cancer Research 16: 5852-5861.
50. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, et al. (2013) Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122: 863-871.
51. Guo ZS, Hong JA, Irvine KR, Chen GA, Spiess PJ, et al. (2006) De novo induction of a cancer/testis antigen by 5-aza-2'-deoxycytidine augments adoptive immunotherapy in a murine tumor model. Cancer Res 66: 1105-1113. (Pubitemid 43165979)