Chimaeric antigen receptor T-cell therapy for tumour immunotherapy

Bioscience Reports

Volumn 37, Issue 1, 2017, Pages

  Sha, Huan Huan ^a   Wang, Dan Dan ^b   Yan, Da Li ^a   Hu, Yong ^a   Yang, Su Jin ^b   Liu, Si Wen ^a   Feng, Ji Feng ^a  

^a JIANGSU CANCER HOSPITAL   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD123 ANTIGEN; CD137 LIGAND; CD19 ANTIGEN; CD20 ANTIGEN; CD27 ANTIGEN; CD28 ANTIGEN; CD30 ANTIGEN; CD33 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; GANGLIOSIDE GD2; GRANZYME; INTERLEUKIN 12; PERFORIN; PROSTATE SPECIFIC MEMBRANE ANTIGEN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR; VASCULOTROPIN RECEPTOR 2; WT1 PROTEIN; CD19-SPECIFIC CHIMERIC ANTIGEN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ANGIOGENESIS; ANTIGEN STRUCTURE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER PROGNOSIS; CELL GROWTH; CELL KILLING; CELL SURFACE; CELL SURVIVAL; CELL THERAPY; CYTOKINE STORM; CYTOTOXIC T LYMPHOCYTE; DNA MODIFICATION; FEVER; HEMATOLOGIC MALIGNANCY; HUMAN; HYPOTENSION; HYPOXIA; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; INTRACELLULAR SIGNALING; LYMPHOCYTE PROLIFERATION; NONHUMAN; PROTEIN EXPRESSION; RESPIRATORY DISTRESS; REVIEW; T CELL THERAPY; T LYMPHOCYTE ACTIVATION; ADOPTIVE TRANSFER; ANIMAL; CHEMISTRY; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PROCEDURES; PROTEIN CONFORMATION; T LYMPHOCYTE; TRANSPLANTATION; VASCULARIZATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; HUMANS; IMMUNOTHERAPY; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN CONFORMATION; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 85011536735     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20160332     Document Type: Review

References (95)

1. Couzin-Frankel, J. (2013) Cancer immunotherapy. Science 342, 1432-1433.
2. Ruella, M. and Kalos, M. (2014) Adoptive immunotherapy for cancer. Immunol. Rev. 257, 14-38.
3. Brentjens, R.J. and Curran, K.J. (2012) Novel cellular therapies for leukemia: CAR-modified T cells targeted to the CD19 antigen. Hematology/Am. Soc. of Hematol. Edu. Program 2012, 143-151.
4. Heiblig, M., Elhamri, M., Michallet, M. and Thomas, X. (2015) Adoptive immunotherapy for acute leukemia: new insights in chimeric antigen receptors. World J. Stem Cells 7, 1022-1038.
5. Firor, A.E., Jares, A. and Ma, Y. (2015) From humble beginnings to success in the clinic: chimeric antigen receptor-modified T-cells and implications for immunotherapy. Exp. Biol. Med. 240, 1087-1098.
6. Suryadevara, C.M., Gedeon, P.C., Sanchez-Perez, L., Verla, T., Alvarez-Breckenridge, C., Choi, B.D. et al. (2015) Are BiTEs the "missing link" in cancer therapy? Oncoimmunology 4, e1008339.
7. Stone, J.D., Aggen, D.H., Schietinger, A., Schreiber, H. and Kranz, D.M. (2012) A sensitivity scale for targeting T cells with chimeric antigen receptors (CARs) and bispecific T-cell engagers (BiTEs). Oncoimmunology 1, 863-873.
8. Maude, S.L., Frey, N., Shaw, P.A., Aplenc, R., Barrett, D.M., Bunin, N.J. et al. (2014) Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371, 1507-1517.
9. Kochenderfer, J.N., Dudley, M.E., Kassim, S.H., Somerville, R.P., Carpenter, R.O., Stetler-Stevenson, M. et al. (2015) 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. 33, 540-549.
10. Prapa, M., Caldrer, S., Spano, C., Bestagno, M., Golinelli, G., Grisendi, G. et al. (2015) A novel anti-GD2/4-1BB chimeric antigen receptor triggers neuroblastoma cell killing. Oncotarget 6, 24884-24894.
11. Pule, M.A., Savoldo, B., Myers, G.D., Rossig, C., Russell, H.V., Dotti, G. et al. (2008) Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat. Med. 14, 1264-1270.
12. Louis, C.U., Savoldo, B., Dotti, G., Pule, M., Yvon, E., Myers, G.D. et al. (2011) Antitumor activity and long-Term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118, 6050-6056.
13. Miao, H., Choi, B.D., Suryadevara, C.M., Sanchez-Perez, L., Yang, S., De Leon, G. et al. (2014) EGFRvIII-specific chimeric antigen receptor T cells migrate to and kill tumor deposits infiltrating the brain parenchyma in an invasive xenograft model of glioblastoma. Plos One 9, e94281.
14. Choi, B.D., Suryadevara, C.M., Gedeon, P.C., Herndon II, J.E., Sanchez-Perez, L., Bigner, D.D. et al. (2014) Intracerebral delivery of a third generation EGFRvIII-specific chimeric antigen receptor is efficacious against human glioma. J. Clin. Neurosci. 21, 189-190.
15. Kim, M.G., Kim, D., Suh, S.K., Park, Z., Choi, M.J. and Oh, Y.K. (2016) Current status and regulatory perspective of chimeric antigen receptor-modified T cell therapeutics. Arch. Pharm. Res. 39, 437-452.
16. Pircher, M., Schirrmann, T. and Petrausch, U. (2015) T cell engineering. Prog. Tumor Res. 42, 110-135.
17. Gross, G., Waks, T. and Eshhar, Z. (1989) Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-Type specificity. Proc. Natl. Acad. Sci. U.S.A. 86, 10024-10028.
18. Savoldo, B., Ramos, C.A., Liu, E., Mims, M.P., Keating, M.J., Carrum, G. et al. (2011) CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J. Clin. Invest. 121, 1822-1826.
19. Kochenderfer, J.N., Dudley, M.E., Feldman, S.A., Wilson, W.H., Spaner, D.E., Maric, I. et al. (2012) 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.
20. Chmielewski, M. and Abken, H. (2015) TRUCKs: The fourth generation of CARs. Expert Opin. Biol. Ther. 15, 1145-1154.
21. Dai, H., Wang, Y., Lu, X. and Han, W. (2016) Chimeric antigen receptors modified T-Cells for cancer therapy. J. Natl. Cancer Inst. 108, 439.
22. Rafiq S, D.T., Brentjens, R.J., Scheinberg, D.A. and Liu, C. (2014) Engineered T cell receptor-mimic antibody, (TCRm) chimeric antigen receptor (CAR) T cells against the intracellular protein Wilms tumor-1 (WT1) for treatment of hematologic and solid cancers. Blood 124, 2155.
23. Chinnasamy, D., Yu, Z., Theoret, M.R., Zhao, Y., Shrimali, R.K., Morgan, R.A. et al. (2010) Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J. Clin. Invest. 120, 3953-3968.
24. Chinnasamy, D., Tran, E., Yu, Z., Morgan, R.A., Restifo, N.P. and Rosenberg, S.A. (2013) Simultaneous targeting of tumor antigens and the tumor vasculature using T lymphocyte transfer synergize to induce regression of established tumors in mice. Cancer Res. 73, 3371-3380.
25. Frigault, M.J. and Maus, M.V. (2016) Chimeric antigen receptor-modified T cells strike back. Int. Immunol. 28, 355-363.
26. Watanabe, K., Terakura, S., Martens, A.C., van Meerten, T., Uchiyama, S., Imai, M. et al. (2015) Target antigen density governs the efficacy of anti-CD20-CD28-CD3 zeta chimeric antigen receptor-modified effector CD8+ T cells. J. Immunol. 194, 911-920.
27. Till, B.G., Jensen, M.C., Wang, J., Qian, X., Gopal, A.K., Maloney, D.G. et al. (2012) CD20-specific adoptive immunotherapy for lymphoma using a chimeric antigen receptor with both CD28 and 4-1BB domains: pilot clinical trial results. Blood 119, 3940-3950.
28. Savoldo, B., Rooney, C.M., Di Stasi, A., Abken, H., Hombach, A., Foster, A.E. et al. (2007) Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 110, 2620-2630.
29. Di Stasi, A., De Angelis, B., Rooney, C.M., Zhang, L., Mahendravada, A., Foster, A.E. et al. (2009) T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and antitumor activity in a Hodgkin tumor model. Blood 113, 6392-6402.
30. Hombach, A.A., Gorgens, A., Chmielewski, M., Murke, F., Kimpel, J., Giebel, B. et al. (2016) Superior therapeutic index in lymphoma therapy: CD30 CD34 hematopoietic stem cells resist a chimeric antigen receptor (CAR) T cell attack. Mol. Ther. 24, 1432-1434.
31. Ramos, C.A., Heslop, H.E. and Brenner, M.K. (2016) CAR-T cell therapy for lymphoma. Annu. Rev. Med. 67, 165-183.
32. Walter, R.B. (2014) The role of CD33 as therapeutic target in acute myeloid leukemia. Expert Opin. Ther. Targets 18, 715-718.
33. O'Hear, C., Heiber, J.F., Schubert, I., Fey, G. and Geiger, T.L. (2015) Anti-CD33 chimeric antigen receptor targeting of acute myeloid leukemia. Haematologica 100, 336-344.
34. Mardiros, A., Forman, S.J. and Budde, L.E. (2015) T cells expressing CD123 chimeric antigen receptors for treatment of acute myeloid leukemia. Curr. Opin. Hematol. 22, 484-488.
35. Mardiros, A., Dos Santos, C., McDonald, T., Brown, C.E., Wang, X., Budde, L.E. et al. (2013) T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia. Blood 122, 3138-3148.
36. Gill, S., Tasian, S.K., Ruella, M., Shestova, O., Li, Y., Porter, D.L. et al. (2014) Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 123, 2343-2354.
37. Santoro, S.P., Kim, S., Motz, G.T., Alatzoglou, D., Li, C., Irving, M. et al. (2015) T cells bearing a chimeric antigen receptor against prostate-specific membrane antigen mediate vascular disruption and result in tumor regression. Cancer Immunol. Res. 3, 68-84.
38. Zuccolotto, G., Fracasso, G., Merlo, A., Montagner, I.M., Rondina, M., Bobisse, S. et al. (2014) PSMA-specific CAR-engineered T cells eradicate disseminated prostate cancer in preclinical models. PLoS ONE 9, e109427.
39. Ma, Q., Gomes, E.M., Lo, A.S. and Junghans, R.P. (2014) Advanced generation anti-prostate specific membrane antigen designer T cells for prostate cancer immunotherapy. Prostate 74, 286-296.
40. Ruella, M. and Levine, B.L. (2016) Smart CARS: optimized development of a chimeric antigen receptor (CAR) T cell targeting epidermal growth factor receptor variant III (EGFRvIII) for glioblastoma. Ann. Transl. Med. 4, 13.
41. Suzuki, M. and Cheung, N.K. (2015) Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin. Ther. Targets 19, 349-362.
42. Chinnasamy, D., Yu, Z., Kerkar, S.P., Zhang, L., Morgan, R.A., Restifo, N.P. et al. (2012) Local delivery of interleukin-12 using T cells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin. Cancer Res. 18, 1672-1683.
43. Jiang, H., Zhang, W., Shang, P., Zhang, H., Fu, W., Ye, F. et al. (2014) Transfection of chimeric anti-CD138 gene enhances natural killer cell activation and killing of multiple myeloma cells. Mol. Oncol. 8, 297-310.
44. Blat, D., Zigmond, E., Alteber, Z., Waks, T. and Eshhar, Z. (2014) Suppression of murine colitis and its associated cancer by carcinoembryonic antigen-specific regulatory T cells. Mol. Ther. 22, 1018-1028.
45. Morgan, R.A., Yang, J.C., Kitano, M., Dudley, M.E., Laurencot, C.M. and Rosenberg, S.A. (2010) 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.
46. Caruso, H.G., Hurton, L.V., Najjar, A., Rushworth, D., Ang, S., Olivares, S. et al. (2015) Tuning sensitivity of CAR to EGFR density limits recognition of normal tissue while maintaining potent antitumor activity. Cancer Res. 75, 3505-3518.
47. Kloss, C.C., Condomines, M., Cartellieri, M., Bachmann, M. and Sadelain, M. (2013) Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat. Biotechnol. 31, 71-75.
48. Fedorov, V.D., Themeli, M. and Sadelain, M. (2013) PD-1-And CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-Target immunotherapy responses. Sci. Transl. Med. 5, 215ra172.
49. Johnson, L.A., Scholler, J., Ohkuri, T., Kosaka, A., Patel, P.R., McGettigan, S.E. et al. (2015) Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma. Sci. Transl. Med. 7, 275ra22.
50. Hudecek, M., Lupo-Stanghellini, M.T., Kosasih, P.L., Sommermeyer, D., Jensen, M.C., Rader, C. et al. (2013) Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin. Cancer Res. 19, 3153-3164.
51. Geldres, C., Savoldo, B. and Dotti, G. (2016) Chimeric antigen receptor-redirected T cells return to the bench. Semin. Immunol. 28, 3-9.
52. Maude, S.L., Barrett, D., Teachey, D.T. and Grupp, S.A. (2014) Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J. 20, 119-122.
53. Davila, M.L., Riviere, I., Wang, X., Bartido, S., Park, J., Curran, K. et al. (2014) Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci. Transl. Med. 6, 224ra25.
54. Grupp, S.A., Kalos, M., Barrett, D., Aplenc, R., Porter, D.L., Rheingold, S.R. et al. (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 368, 1509-1518.
55. Di Stasi, A., Tey, S.K., Dotti, G., Fujita, Y., Kennedy-Nasser, A., Martinez, C. et al. (2011) Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365, 1673-1683.
56. Ciceri, F., Bonini, C., Stanghellini, M.T., Bondanza, A., Traversari, C., Salomoni, M. et al. (2009) Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): A non-randomised phase I-II study. Lancet Oncol. 10, 489-500.
57. Wang, W. and Wang, Y. (2012) Equipping CAR-modified T cells with a brake to prevent chronic adverse effects. Curr. Gene Ther. 12, 493-495.
58. Kenderian, S.S., Ruella, M., Shestova, O., Klichinsky, M., Aikawa, V., Morrissette, J.J. et al. (2015) CD33-specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia 29, 1637-1647.
59. Sun, N., Liang, J., Abil, Z. and Zhao, H. (2012) Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease. Mol. Biosyst. 8, 1255-1263.
60. Yang, H., Wang, H., Shivalila, C.S., Cheng, A.W., Shi, L. and Jaenisch, R. (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379.
61. Sadelain, M., Papapetrou, E.P. and Bushman, F.D. (2011) Safe harbours for the integration of new DNA in the human genome. Nat. Rev. Cancer 12, 51-58.
62. Chhabra, A. (2011) TCR-engineered, customized, antitumor T cells for cancer immunotherapy: Advantages and limitations. Scientific World J. 11, 121-129.
63. Ninomiya, S., Narala, N., Huye, L., Yagyu, S., Savoldo, B., Dotti, G. et al. (2015) Tumor indoleamine 2, 3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs. Blood 125, 3905-3916.
64. Jensen, M.C., Popplewell, L., Cooper, L.J., DiGiusto, D., Kalos, M., Ostberg, J.R. et al. (2010) Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol. Blood Marrow Transplant. 16, 1245-1256.
65. Schultze, J.L. and Nadler, L.M. (1999) T cell mediated immunotherapy for B cell lymphoma. J. Mol. Med. 77, 322-33.
66. Kershaw, M.H., Westwood, J.A., Parker, L.L., Wang, G., Eshhar, Z., Mavroukakis, S.A. et al. (2006) A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin. Cancer Res. 12, 6106-6115.
67. Lamers, C.H., Sleijfer, S., van Steenbergen, S., van Elzakker, P., van Krimpen, B., Groot, C. et al. (2013) 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.
68. Mirzaei, H.R., Mirzaei, H., Lee, S.Y., Hadjati, J. and Till, B.G. (2016) Prospects for chimeric antigen receptor (CAR) gammadelta T cells: A potential game changer for adoptive T cell cancer immunotherapy. Cancer Lett. 380, 413-423.
69. Rischer, M., Pscherer, S., Duwe, S., Vormoor, J., Jurgens, H. and Rossig, C. (2004) Human gammadelta T cells as mediators of chimaeric-receptor redirected anti-Tumour immunity. Br. J. Haematol. 126, 583-592.
70. Deniger, D.C., Switzer, K., Mi, T., Maiti, S., Hurton, L., Singh, H. et al. (2013) Bispecific T-cells expressing polyclonal repertoire of endogenous gammadelta T-cell receptors and introduced CD19-specific chimeric antigen receptor. Mol. Ther. 21, 638-647.
71. Curran, K.J., Seinstra, B.A., Nikhamin, Y., Yeh, R., Usachenko, Y., van Leeuwen, D.G. et al. (2015) Enhancing antitumor efficacy of chimeric antigen receptor T cells through constitutive CD40L expression. Mol. Ther. 23, 769-778.
72. Teachey, D.T., Lacey, S.F., Shaw, P.A., Melenhorst, J.J., Maude, S.L., Frey, N. et al. (2016) Identification of predictive biomarkers for cytokine release syndrome after chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Cancer Discov. 6, 664-697.
73. Chen, X., Han, J., Chu, J., Zhang, L., Zhang, J., Chen, C. et al. (2016) A combinational therapy of EGFR-CAR NK cells and oncolytic herpes simplex virus 1 for breast cancer brain metastases. Oncotarget 7, 27764-27767.
74. Tettamanti, S., Marin, V., Pizzitola, I., Magnani, C.F., Giordano Attianese, G.M., Cribioli, E. et al. (2013) Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br. J. Haematol. 161, 389-401.
75. Brentjens, R.J., Riviere, I., Park, J.H., Davila, M.L., Wang, X., Stefanski, J. et al. (2011) 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.
76. Porter, D.L., Levine, B.L., Kalos, M., Bagg, A. and June, C.H. (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733.
77. Cruz, C.R., Micklethwaite, K.P., Savoldo, B., Ramos, C.A., Lam, S., Ku, S. et al. (2013) Infusion of donor-derived CD19-redirected virus-specific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: A phase 1 study. Blood 122, 2965-2973.
78. Kochenderfer, J.N., Dudley, M.E., Carpenter, R.O., Kassim, S.H., Rose, J.J., Telford, W.G. et al. (2013) Donor-derived CD19-Targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 122, 4129-4139.
79. Lee, D.W., Kochenderfer, J.N., Stetler-Stevenson, M., Cui, Y.K., Delbrook, C., Feldman, S.A. et al. (2015) T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: A phase 1 dose-escalation trial. Lancet 385, 517-528.
80. Dai, H., Zhang, W., Li, X., Han, Q., Guo, Y., Zhang, Y. et al. (2015) Tolerance and efficacy of autologous or donor-derived T cells expressing CD19 chimeric antigen receptors in adult B-ALL with extramedullary leukemia. Oncoimmunology 4, e1027469.
81. Porter, D.L., Hwang, W.T., Frey, N.V., Lacey, S.F., Shaw, P.A., Loren, A.W. et al. (2015) Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci. Transl. Med. 7, 303ra139.
82. Garfall, A.L., Maus, M.V., Hwang, W.T., Lacey, S.F., Mahnke, Y.D., Melenhorst, J.J. et al. (2015) Chimeric antigen receptor T cells against CD19 for multiple myeloma. N. Engl. J. Med. 373, 1040-1047.
83. Till, B.G., Jensen, M.C., Wang, J., Chen, E.Y., Wood, B.L., Greisman, H.A. et al. (2008) Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 112, 2261-2271.
84. Wang, Y., Zhang, W.Y., Han, Q.W., Liu, Y., Dai, H.R., Guo, Y.L. et al. (2014) Effective response and delayed toxicities of refractory advanced diffuse large B-cell lymphoma treated by CD20-directed chimeric antigen receptor-modified T cells. Clin. Immunol. 155, 160-175.
85. Kobayashi, E., Kishi, H., Ozawa, T., Hamana, H., Nakagawa, H., Jin, A. et al. (2014) A chimeric antigen receptor for TRAIL-receptor 1 induces apoptosis in various types of tumor cells. Biochem. Biophys. Res. Commun. 453, 798-803.
86. Inaguma, Y., Akahori, Y., Murayama, Y., Shiraishi, K., Tsuzuki-Iba, S., Endoh, A. et al. (2014) Construction and molecular characterization of a T-cell receptor-like antibody and CAR-T cells specific for minor histocompatibility antigen HA-1H. Gene Ther. 21, 575-584.
87. Schuberth, P.C., Jakka, G., Jensen, S.M., Wadle, A., Gautschi, F., Haley, D. et al. (2013) Effector memory and central memory NY-ESO-1-specific re-directed T cells for treatment of multiple myeloma. Gene Ther. 20, 386-395.
88. Mata, M., Vera, J.F., Gerken, C., Rooney, C.M., Miller, T., Pfent, C. et al. (2014) Toward immunotherapy with redirected T cells in a large animal model: ex vivo activation, expansion, and genetic modification of canine T cells. J. Immunother. 37, 407-415.
89. Hu, W.X., Chen, H.P., Yu, K., Shen, L.X., Wang, C.Y., Su, S.Z. et al. (2012) Gene therapy of malignant solid tumors by targeting erbB2 receptors and by activating T cells. Cancer Biother. Radiopharm. 7, 711-718.
90. Geldres, C., Savoldo, B., Hoyos, V., Caruana, I., Zhang, M., Yvon, E. et al. (2014) T lymphocytes redirected against the chondroitin sulfate proteoglycan-4 control the growth of multiple solid tumors both in vitro and in vivo. Clin. Cancer Res. 20, 962-971.
91. Chow, K.K., Naik, S., Kakarla, S., Brawley, V.S., Shaffer, D.R., Yi, Z. et al. (2013) T cells redirected to EphA2 for the immunotherapy of glioblastoma. Mol. Ther. 21, 629-637.
92. Lanitis, E., Poussin, M., Hagemann, I.S., Coukos, G., Sandaltzopoulos, R., Scholler, N. et al. (2012) Redirected antitumor activity of primary human lymphocytes transduced with a fully human anti-mesothelin chimeric receptor. Mol. Ther. 20, 633-643.
93. Huang, G., Yu, L., Cooper, L.J., Hollomon, M., Huls, H. and Kleinerman, E.S. (2012) Genetically modified T cells targeting interleukin-11 receptor alpha-chain kill human osteosarcoma cells and induce the regression of established osteosarcoma lung metastases. Cancer Res. 72, 271-281.
94. Krebs, S., Chow, K.K., Yi, Z., Rodriguez-Cruz, T., Hegde, M., Gerken, C. et al. (2014) T cells redirected to interleukin-13Ralpha2 with interleukin-13 Mutein -chimeric antigen receptors have anti-glioma activity but also recognize interleukin-13Ralpha1. Cytotherapy 16, 1121-1131.
95. Kong, S., Sengupta, S., Tyler, B., Bais, A.J., Ma, Q., Doucette, S. et al. (2012) Suppression of human glioma xenografts with second-generation IL13R-specific chimeric antigen receptor-modified T cells. Clin. Cancer Res. 18, 5949-5960.