Reassessing target antigens for adoptive T-cell therapy

Nature Biotechnology

Volumn 31, Issue 11, 2013, Pages 999-1008

  Hinrichs, Christian S ^a   Restifo, Nicholas P ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN RECEPTORS; CLINICAL EXPERIENCE; CLINICAL RESPONSE; CROSS-REACTIVITY; IMMUNOTHERAPEUTIC; MALIGNANT CELLS; MALIGNANT TISSUES; TARGET SELECTION;

EPITOPES; HISTOLOGY; ONCOLOGY; TUMORS;

T-CELLS;

EPITOPE; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; AUTOIMMUNITY; B LYMPHOCYTE; CROSS REACTION; CYTOKINE PRODUCTION; HUMAN; MELANOCYTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGENS; AUTOIMMUNE DISEASES; CELL- AND TISSUE-BASED THERAPY; CROSS REACTIONS; DRUG DELIVERY SYSTEMS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MODELS, IMMUNOLOGICAL; NEOPLASMS; T-LYMPHOCYTES;

EID: 84887474711     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2725     Document Type: Review

References (108)

1. Cheever, M.A. et al. The prioritization of cancer antigens: a National Cancer Institute pilot project for the acceleration of translational research. Clin. Cancer Res. 15, 5323-5337 (2009).
2. Rosenberg, S.A., Yang, J.C. & Restifo, N.P. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10, 909-915 (2004).
3. Rosenberg, S.A. et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17, 4550-4557 (2011).
4. Robbins, P.F. 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. 29, 917-924 (2011).
5. Kochenderfer, J.N. 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 119, 2709-2720 (2012).
6. Heslop, H.E. et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115, 925-935 (2010).
7. Paulos, C.M. et al. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J. Clin. Invest. 117, 2197-2204 (2007).
8. Antony, P.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. 174, 2591-2601 (2005).
9. Gattinoni, L. et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J. Exp. Med. 202, 907-912 (2005).
10. Johnson, L.A. et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114, 535-546 (2009).
11. Parkhurst, M.R. et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19, 620-626 (2011).
12. Morgan, R.A. et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J. Immunother. 36, 133-151 (2013).
13. Morgan, R.A. 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. 18, 843-851 (2010).
14. Linette, G.P. et al. Cardiovascular toxicity and titin cross-reactivity of affinity enhanced T cells in myeloma and melanoma. Blood 122, 863-871 (2013).
15. Cameron, B.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. 5, 197ra103 (2013).
16. Palmer, D.C. et al. Vaccine-stimulated, adoptively transferred CD8+ T cells traffic indiscriminately and ubiquitously while mediating specific tumor destruction. J. Immunol. 173, 7209-7216 (2004).
17. Palmer, D.C. et al. Effective tumor treatment targeting a melanoma/melanocyte-associated antigen triggers severe ocular autoimmunity. Proc. Natl. Acad. Sci. USA 105, 8061-8066 (2008).
18. Overwijk, W.W. et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 198, 569-580 (2003).
19. Leibovich, B.C. et al. Carbonic anhydrase IX is not an independent predictor of outcome for patients with clear cell renal cell carcinoma. J. Clin. Oncol. 25, 4757-4764 (2007).
20. Brouwers, A.H., Mulders, P.F.A. & Oyen, W.J.G. Carbonic anhydrase IX expression in clear cell renal cell carcinoma and normal tissues: experiences from (radio) immunotherapy. J. Clin. Oncol. 26, 3808-3809, author reply 3811-3812 (2008).
21. Ivanov, S. et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 158, 905-919 (2001).
22. Brouwers, A.H. et al. Lack of efficacy of two consecutive treatments of radioimmunotherapy with 131I-cG250 in patients with metastasized clear cell renal cell carcinoma. J. Clin. Oncol. 23, 6540-6548 (2005).
23. Lamers, C.H.J. et al. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J. Clin. Oncol. 24, e20-e22 (2006).
24. Lamers, C.H. et al. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol. Ther. 21, 904-912 (2013).
25. Hammarström, S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9, 67-81 (1999).
26. Uhlen, M. et al. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250 (2010).
27. McCall, M.N., Uppal, K., Jaffee, H.A., Zilliox, M.J. & Irizarry, R.A. The Gene Expression Barcode: leveraging public data repositories to begin cataloging the human and murine transcriptomes. Nucleic Acids Res. 39, D1011-D1015 (2011).
28. Gulley, J.L. et al. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin. Cancer Res. 14, 3060-3069 (2008).
29. Marshall, J.L. et al. Phase I study of sequential vaccinations with fowlpox-CEA(6D)-TRICOM alone and sequentially with vaccinia-CEA(6D)-TRICOM, with and without granulocyte-macrophage colony-stimulating factor, in patients with carcinoembryonic antigen-expressing carcinomas. J. Clin. Oncol. 23, 720-731 (2005).
30. Ullenhag, G.J. et al. Durable carcinoembryonic antigen (CEA)-specific humoral and cellular immune responses in colorectal carcinoma patients vaccinated with recombinant CEA and granulocyte/macrophage colony-stimulating factor. Clin. Cancer Res. 10, 3273-3281 (2004).
31. Bos, R. et al. Balancing between antitumor efficacy and autoimmune pathology in T-cell-mediated targeting of carcinoembryonic antigen. Cancer Res. 68, 8446-8455 (2008).
32. Natali, P.G. et al. Expression of the p185 encoded by HER2 oncogene in normal and transformed human tissues. Int. J. Cancer 45, 457-461 (1990).
33. Kawashima, I. et al. The multi-epitope approach for immunotherapy for cancer: identification of several CTL epitopes from various tumor-associated antigens expressed on solid epithelial tumors. Hum. Immunol. 59, 1-14 (1998).
34. Jones, K.L. & Buzdar, A.U. Evolving novel anti-HER2 strategies. Lancet Oncol. 10, 1179-1187 (2009).
35. Atanackovic, D. et al. Booster vaccination of cancer patients with MAGE-A3 protein reveals long-term immunological memory or tolerance depending on priming. Proc. Natl. Acad. Sci. USA 105, 1650-1655 (2008).
36. van Baren, N. et al. Tumoral and immunologic response after vaccination of melanoma patients with an ALVAC virus encoding MAGE antigens recognized by T cells. J. Clin. Oncol. 23, 9008-9021 (2005).
37. Chinnasamy, N. 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. 186, 685-696 (2011).
38. Uckun, F.M. et al. Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins. Blood 71, 13-29 (1988).
39. Kochenderfer, J.N. 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 116, 4099-4102 (2010).
40. Grupp, S.A. et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 368, 1509-1518 (2013).
41. Porter, D.L., Levine, B.L., Kalos, M., Bagg, A. & June, C.H. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733 (2011).
42. Kalos, M. et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3, 95ra73 (2011).
43. Brentjens, R.J. et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 5, 177ra38 (2013).
44. Brentjens, R.J. et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 118, 4817-4828 (2011).
45. Anderson, L.D. et al. Identification of MAGE-C1 (CT-7) epitopes for T-cell therapy of multiple myeloma. Cancer Immunol. Immunother. 60, 985-997 (2011).
46. Maus, M.V. & June, C.H. Zoom zoom: racing CARs for multiple myeloma. Clin. Cancer Res. 19, 1917-1919 (2013).
47. Carpenter, R.O. et al. B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma. Clin. Cancer Res. 19, 2048 (2013).
48. Hinrichs, C.S., Palmer, D.C., Rosenberg, S.A. & Restifo, N.P. Glucocorticoids do not inhibit antitumor activity of activated CD8+ T cells. J. Immunother. 28, 517-524 (2005).
49. Di Stasi, A. et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365, 1673-1683 (2011).
50. Kloss, C.C., Condomines, M., Cartellieri, M., Bachmann, M. & Sadelain, M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat. Biotechnol. 31, 71-75 (2013).
51. Hanada, K. & Restifo, N.P. Double or nothing on cancer immunotherapy. Nat. Biotechnol. 31, 33-34 (2013).
52. Hinrichs, C.S. et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc. Natl. Acad. Sci. USA 106, 17469-17474 (2009).
53. Hinrichs, C.S. et al. Type 17 CD8+ T cells display enhanced antitumor immunity. Blood 114, 596-599 (2009).
54. Hinrichs, C.S. et al. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood 117, 808-814 (2011).
55. Kerkar, S.P. et al. IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. J. Clin. Invest. 121, 4746-4757 (2011).
56. Muranski, P. et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 35, 972-985 (2011).
57. Gattinoni, L. et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 17, 1290-1297 (2011).
58. Zhong, S. et al. T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy. Proc. Natl. Acad. Sci. USA 110, 6973-6978 (2013).
59. Theoret, M.R. et al. Relationship of p53 overexpression on cancers and recognition by Anti-p53 T cell receptor-transduced T cells. Hum. Gene Ther. 19, 1219-1231 (2008).
60. Wu, C. et al. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130 (2009).
61. Grubb, G.R., Yun, K., Williams, B.R., Eccles, M.R. & Reeve, A.E. Expression of WT1 protein in fetal kidneys and Wilms tumors. Lab. Investig. 71, 472-479 (1994).
62. Mundlos, S. et al. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119, 1329-1341 (1993).
63. Ramani, P. & Cowell, J.K. The expression pattern of Wilms' tumour gene (WT1) product in normal tissues and paediatric renal tumours. J. Pathol. 179, 162-168 (1996).
64. Inoue, K. et al. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia. Blood 89, 1405-1412 (1997).
65. Chapuis, A.G. et al. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci. Transl. Med. 5, 174ra27 (2013).
66. Seregni, E. et al. Structure, function and gene expression of epithelial mucins. Tumori 83, 625-632 (1997).
67. Cao, Y. et al. Mucins (MUC1 and MUC3) of gastrointestinal and breast epithelia reveal different and heterogeneous tumor-associated aberrations in glycosylation. J. Histochem. Cytochem. 45, 1547-1557 (1997).
68. Ayyoub, M. et al. Proteasome-assisted identification of a SSX-2-derived epitope recognized by tumor-reactive CTL infiltrating metastatic melanoma. J. Immunol. 168, 1717-1722 (2002).
69. Zhao, Y. et al. Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J. Immunol. 174, 4415-4423 (2005).
70. Ottaviani, S., Zhang, Y., Boon, T. & van der Bruggen, P.A. MAGE-1 antigenic peptide recognized by human cytolytic T lymphocytes on HLA-A2 tumor cells. Cancer Immunol. Immunother. 54, 1214-1220 (2005).
71. Haso, W. et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood 121, 1165-1174 (2013).
72. Hersey, P., Jamal, O., Henderson, C., Zardawi, I. & D'Alessandro, G. Expression of the gangliosides GM3, GD3 and GD2 in tissue sections of normal skin, naevi, primary and metastatic melanoma. Int. J. Cancer 41, 336-343 (1988).
73. Alvarez-Rueda, N. et al. A monoclonal antibody to O-acetyl-GD2 ganglioside and not to GD2 shows potent anti-tumor activity without peripheral nervous system cross-reactivity. PLoS ONE 6, e25220 (2011).
74. Mennel, H.D. et al. Expression of GD2-epitopes in human intracranial tumors and normal brain. Exp. Toxicol. Pathol. 44, 317-324 (1992).
75. Louis, C.U. et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118, 6050-6056 (2011).
76. Wolfgang, C.D., Essand, M., Vincent, J.J., Lee, B. & Pastan, I. TARP: a nuclear protein expressed in prostate and breast cancer cells derived from an alternate reading frame of the T cell receptor gamma chain locus. Proc. Natl. Acad. Sci. USA 97, 9437-9442 (2000).
77. Hillerdal, V., Nilsson, B., Carlsson, B., Eriksson, F. & Essand, M. T cells engineered with a T cell receptor against the prostate antigen TARP specifically kill HLA-A2+ prostate and breast cancer cells. Proc. Natl. Acad. Sci. USA 109, 15877-15881 (2012).
78. Kris, M.G.N.R. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. J. Am. Med. Assoc. 290, 2149-2158 (2003).
79. Savage, D.G. & Antman, K.H. Imatinib mesylate-a new oral targeted therapy. N. Engl. J. Med. 346, 683-693 (2002).
80. Kwak, E.L. et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N. Engl. J. Med. 363, 1693-1703 (2010).
81. Flaherty, K.T. et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363, 809-819 (2010).
82. Warren, R.L. & Holt, R.A. A census of predicted mutational epitopes suitable for immunologic cancer control. Hum. Immunol. 71, 245-254 (2010).
83. American Cancer Society. Cancer Facts & Figures 2013 http://www.cancer.org/acs/groups/content/@epidemiologysurveilance/documents/ document/acspc-036845.pdf (ACA, 2013).
84. Forbes, S.A. et al. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res. 38, D652-D657 (2010).
85. Robbins, P.F. et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 19, 747-752 (2013).
86. Restifo, N.P., Dudley, M.E. & Rosenberg, S.A. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12, 269-281 (2012).
87. Kenter, G.G. et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361, 1838-1847 (2009).
88. Riemer, A.B. et al. A conserved E7-derived cytotoxic T lymphocyte epitope expressed on human papillomavirus 16-transformed HLA-A2+ epithelial cancers. J. Biol. Chem. 285, 29608-29622 (2010).
89. Evans, M. et al. Antigen processing defects in cervical carcinomas limit the presentation of a CTL epitope from human papillomavirus 16 E6. J. Immunol. 167, 5420-5428 (2001).
90. Anonymous. Do no harm. Nat. Biotechnol. 31, 365 (2013).
91. Hofmann, O. et al. Genome-wide analysis of cancer/testis gene expression. Proc. Natl. Acad. Sci. USA 105, 20422-20427 (2008).
92. Silver, D.A., Pellicer, I., Fair, W.R., Heston, W.D. & Cordon-Cardo, C. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin. Cancer Res. 3, 81-85 (1997).
93. Zhang, S. et al. Selection of tumor antigens as targets for immune attack using immunohistochemistry: I. Focus on gangliosides. Int. J. Cancer 73, 42-49 (1997).
94. Yuki, N., Yamada, M., Tagawa, Y., Takahashi, H. & Handa, S. Pathogenesis of the neurotoxicity caused by anti-GD2 antibody therapy. J. Neurol. Sci. 149, 127-130 (1997).
95. Sturrock, A.B. et al. Structure, chromosomal assignment, and expression of the gene for proteinase-3. The Wegener's granulomatosis autoantigen. J. Biol. Chem. 267, 21193-21199 (1992).
96. Abattyani, Z., Xerri, L., Hassoun, J., Bonerandi, J.J. & Grob, J.J. Tyrosinase gene expression in human tissues. Pigment Cell Res. 6, 400-405 (1993).
97. Fukuda, S. & Pelus, L.M. Survivin, a cancer target with an emerging role in normal adult tissues. Mol. Cancer Ther. 5, 1087-1098 (2006).
98. Elgamal, A.A. et al. Detection of prostate specific antigen in pancreas and salivary glands: a potential impact on prostate cancer overestimation. J. Urol. 156, 464-468 (1996).
99. Ishikawa, T. et al. Expression of alpha-fetoprotein and prostate-specific antigen genes in several tissues and detection of mRNAs in normal circulating blood by reverse transcriptase-polymerase chain reaction. Jpn. J. Clin. Oncol. 28, 723-728 (1998).
100. Hiyama, E., Hiyama, K., Yokoyama, T. & Shay, J.W. Immunohistochemical detection of telomerase (hTERT) protein in human cancer tissues and a subset of cells in normal tissues. Neoplasia 3, 17-26 (2001).
101. Hiyama, K. et al. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J. Immunol. 155, 3711-3715 (1995).
102. Hiyama, E. et al. Telomerase activity in human intestine. Int. J. Oncol. 9, 453-458 (1996).
103. Shay, J.W. & Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer 33, 787-791 (1997).
104. Taylor, R.S. et al. Detection of telomerase activity in malignant and nonmalignant skin conditions. J. Invest. Dermatol. 106, 759-765 (1996).
105. Hirai, H., Maru, Y., Hagiwara, K., Nishida, J. & Takaku, F. A novel putative tyrosine kinase receptor encoded by the eph gene. Science 238, 1717-1720 (1987).
106. Sewell, A.K. Why must T cells be cross-reactive? Nat. Rev. Immunol. 12, 669-677 (2012).
107. Oldstone, M.B.A. Molecular mimicry and immune-mediated diseases. FASEB J. 12, 1255-1265 (1998).
108. Irvine, D.J., Purbhoo, M.A., Krogsgaard, M. & Davis, M.M. Direct observation of ligand recognition by T cells. Nature 419, 845-849 (2002).