Chimeric antigen receptor-modified T cells strike back

International Immunology

Volumn 28, Issue 7, 2016, Pages 355-363

  Frigault, Matthew J ^a   Maus, Marcela V ^a  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

Cellular immunotherapy; Chimeric antigen receptor; Clinical immunology; Gene therapy; T cell therapy

Indexed keywords

CD19 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; IBRUTINIB; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TISAGENLECLEUCEL T; TOCILIZUMAB; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; APLASIA; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE APLASIA; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CARDIOTOXICITY; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; CELL TRANSFER; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); CYTOKINE PRODUCTION; CYTOKINE RELEASE SYNDROME; GENE TRANSFER; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INTRACELLULAR SIGNALING; LARGE CELL LYMPHOMA; LEUKAPHERESIS; LUNG TOXICITY; LYMPHOCYTE DIFFERENTIATION; MULTICENTER STUDY (TOPIC); NEUROTOXICITY; NONHODGKIN LYMPHOMA; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SOLID TUMOR; STRUCTURE ACTIVITY RELATION; SURVIVAL RATE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT; ADOPTIVE IMMUNOTHERAPY; ANIMAL; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; NEOPLASM; PROCEDURES; TRANSPLANTATION; TUMOR ESCAPE;

ANIMALS; ANTIGENS, NEOPLASM; GENETIC ENGINEERING; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TREATMENT OUTCOME; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 84977119407     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxw018     Document Type: Article

References (70)

1. Burnet, F. M. 1967. Immunological aspects of malignant disease. Lancet 1:1171.
2. 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. USA 86:10024.
3. Irving, B. A. and Weiss, A. 1991. The cytoplasmic domain of the T cell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways. Cell 64:891.
4. Letourneur, F. and Klausner, R. D. 1991. T-cell and basophil activation through the cytoplasmic tail of T-cell-receptor zeta family proteins. Proc. Natl Acad. Sci. USA 88:8905.
5. Romeo, C. and Seed, B. 1991. Cellular immunity to HIV activated by CD4 fused to T cell or Fc receptor polypeptides. Cell 64:1037.
6. Deeks, S. G., Wagner, B., Anton, P. A. et al. 2002. A phase II randomized study of HIV-specific T-cell gene therapy in subjects with undetectable plasma viremia on combination antiretroviral therapy. Mol. Ther. 5:788.
7. Mitsuyasu, R. T., Anton, P. A., Deeks, S. G. et al. 2000. Prolonged survival and tissue trafficking following adoptive transfer of CD4zeta gene-modified autologous CD4(+) and CD8(+) T cells in human immunodeficiency virus-infected subjects. Blood 96:785.
8. Scholler, J., Brady, T. L., Binder-Scholl, G. et al. 2012. Decadelong safety and function of retroviral-modified chimeric antigen receptor T cells. Sci. Transl. Med. 4:132ra53.
9. Huston, J. S., Levinson, D., Mudgett-Hunter, M. et al. 1988. Protein engineering of antibody binding sites: recovery of specific activity in an anti-digoxin single-chain Fv analogue produced in Escherichia coli. Proc. Natl Acad. Sci. USA 85:5879.
10. Maus, M. V., Haas, A. R., Beatty, G. L. et al. 2013. T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol. Res. 1:26.
11. Guest, R. D., Hawkins, R. E., Kirillova, N. et al. 2005. The role of extracellular spacer regions in the optimal design of chimeric immune receptors: evaluation of four different scFvs and antigens. J. Immunother. 28:203.
12. James, S. E., Greenberg, P. D., Jensen, M. C. et al. 2008. Antigen sensitivity of CD22-specific chimeric TCR is modulated by target epitope distance from the cell membrane. J. Immunol. 180:7028.
13. Frigault, M. J., Lee, J., Basil, M. C. et al. 2015. Identification of chimeric antigen receptors that mediate constitutive or inducible proliferation of T cells. Cancer Immunol. Res. 3:356.
14. Hombach, A., Hombach, A. A. and Abken, H. 2010. Adoptive immunotherapy with genetically engineered T cells: modification of the IgG1 Fc 'spacer' domain in the extracellular moiety of chimeric antigen receptors avoids 'off-target' activation and unintended initiation of an innate immune response. Gene Ther. 17:1206.
15. Jonnalagadda, M., Mardiros, A., Urak, R. et al. 2015. Chimeric antigen receptors with mutated IgG4 Fc spacer avoid fc receptor binding and improve T cell persistence and antitumor efficacy. Mol. Ther. 23:757.
16. Eshhar, Z., Waks, T., Gross, G. and Schindler, D. G. 1993. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc. Natl Acad. Sci. USA 90:720.
17. Brocker, T. 2000. Chimeric Fv-zeta or Fv-epsilon receptors are not sufficient to induce activation or cytokine production in peripheral T cells. Blood 96:1999.
18. Brocker, T. and Karjalainen, K. 1995. Signals through T cell receptor- zeta chain alone are insufficient to prime resting T lymphocytes. J. Exp. Med. 181:1653.
19. Maher, J., Brentjens, R. J., Gunset, G., Rivière, I. and Sadelain, M. 2002. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta /CD28 receptor. Nat. Biotechnol. 20:70.
20. Guedan, S., Chen, X., Madar, A. et al. 2014. ICOS-based chimeric antigen receptors program bipolar TH17/TH1 cells. Blood 124:1070.
21. Loskog, A., Giandomenico, V., Rossig, C., Pule, M., Dotti, G. and Brenner, M. K. 2006. Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia 20:1819.
22. Milone, M. C., Fish, J. D., Carpenito, C. et al. 2009. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17:1453.
23. Carpenito, C., Milone, M. C., Hassan, R. et al. 2009. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc. Natl Acad. Sci. USA 106:3360.
24. Wang, J., Jensen, M., Lin, Y. et al. 2007. Optimizing adoptive polyclonal T cell immunotherapy of lymphomas, using a chimeric T cell receptor possessing CD28 and CD137 costimulatory domains. Hum. Gene Ther. 18:712.
25. Gill, S. and June, C. H. 2015. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol. Rev. 263:68.
26. Flynn, J. K. and Gorry, P. R. 2014. Stem memory T cells (TSCM)- their role in cancer and HIV immunotherapies. Clin. Transl. Immunol. 3:e20.
27. Barrett, D. M., Singh, N., Porter, D. L., Grupp, S. A. and June, C. H. 2014. Chimeric antigen receptor therapy for cancer. Annu. Rev. Med. 65:333.
28. Paulos, C. M., Carpenito, C., Plesa, G. et al. 2010. The inducible costimulator (ICOS) is critical for the development of human T(H)17 cells. Sci. Transl. Med. 2:55ra78.
29. Maus, M. V., Grupp, S. A., Porter, D. L. and June, C. H. 2014. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 123:2625.
30. Singh, H., Moyes, J. S., Huls, M. H. and Cooper, L. J. 2015. Manufacture of T cells using the Sleeping Beauty system to enforce expression of a CD19-specific chimeric antigen receptor. Cancer Gene Ther. 22:95.
31. Depoil, D., Fleire, S., Treanor, B. L. et al. 2008. CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat. Immunol. 9:63.
32. Scheuermann, R. H. and Racila, E. 1995. CD19 antigen in leukemia and lymphoma diagnosis and immunotherapy. Leuk. Lymphoma 18:385.
33. Porter, D. L., Hwang, W. T., Frey, N. V. et al. 2015. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci. Transl. Med. 7:303ra139.
34. Kalos, M., Levine, B. L., Porter, D. L., Katz, S., Grupp, S. A., Bagg, A. and June, C. H. 2011. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3:95ra73.
35. 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.
36. Brentjens, R. J., Riviere, I., Park, J. H. 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.
37. Kochenderfer, J. N., Dudley, M. E., Feldman, S. A. et al. 2012. B-cell depletion and remissions of malignancy along with cytokineassociated toxicity in a clinical trial of anti-CD19 chimeric-antigenreceptor- transduced T cells. Blood 119:2709.
38. Kochenderfer, J. N., Dudley, M. E., Carpenter, R. O. et al. 2013. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 122:4129.
39. Kochenderfer, J. N., Dudley, M. E., Kassim, S. H. 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.
40. Cruz, C. R., Micklethwaite, K. P., Savoldo, B. 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.
41. Davila, M. L., Riviere, I., Wang, X. 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.
42. Brentjens, R. J., Davila, M. L., Riviere, I. et al. 2013. CD19- targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 5:177ra38.
43. Maude, S. L., Frey, N., Shaw, P. A. et al. 2014. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371:1507.
44. Grupp, S. A., Kalos, M., Barrett, D. et al. 2013. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 368:1509.
45. Lee, D. W., Kochenderfer, J. N., Stetler-Stevenson, M. 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.
46. Jaffe, E. S. 2009. The 2008 WHO classification of lymphomas: implications for clinical practice and translational research. Hematology Am. Soc. Hematol. Educ. Program 1:523.
47. Nabhan, C. and Rosen, S. T. 2014. Chronic lymphocytic leukemia: a clinical review. JAMA 312:2265.
48. Schuster, S. J., Svoboda, J., Nasta, S. D. et al. 2015. Sustained remissions following chimeric antigen receptor modified T cells directed against CD19 (CTL019) in patients with relapsed or refractory CD19+ lymphomas. Blood 126:183.
49. Turtle, C. J., Berger, C., Sommermeyer, D. et al. 2015. Anti-CD19 chimeric antigen receptor-modified t cell therapy for b cell nonhodgkin lymphoma and chronic lymphocytic leukemia: fludarabine and cyclophosphamide lymphodepletion improves in vivo expansion and persistence of CAR-T cells and clinical outcomes. Blood 126:184.
50. Al Ustwani, O., Gupta, N., Bakhribah, H., Griffiths, E., Wang, E. and Wetzler, M. 2016. Clinical updates in adult acute lymphoblastic leukemia. Crit. Rev. Oncol. Hematol. 99:189.
51. Pulte, D., Gondos, A. and Brenner, H. 2009. Improvement in survival in younger patients with acute lymphoblastic leukemia from the 1980s to the early 21st century. Blood 113:1408.
52. Fielding, A. K., Richards, S. M., Chopra, R. et al. 2007. Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood 109:944.
53. Park, J. H., Riviere, I., Wang, X. et al. 2015. Implications of minimal residual disease negative complete remission (MRD-CR) and allogeneic stem cell transplant on safety and clinical outcome of CD19-Targeted 19-28z CAR modified T cells in adult patients with relapsed, refractory B-cell ALL. Blood 126:682.
54. Maude, S. L., Barrett, D. M., Ambrose, D. E. et al. 2015. Efficacy and safety of humanized chimeric antigen receptor (CAR)- modified T cells targeting CD19 in children with relapsed/refractory ALL. Blood 126:683.
55. Lee, D. W., Stetler-Stevenson, M., Yuan, C. M. et al. 2015. Safety and response of incorporating CD19 Chimeric antigen receptor T cell therapy in typical salvage regimens for children and young adults with acute lymphoblastic leukemia. Blood 126:684.
56. Sotillo, E., Barrett, D. M., Black, K. L. et al. 2015. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov. 5:1282.
57. Gardner, R., Wu, D., Cherian, S. et al. 2016. Acquisition of a CD19 negative myeloid phenotype allows immune escape of MLLrearranged B-ALL from CD19 CAR-T cell therapy. Blood.
58. Sadelain, M. 2015. CAR therapy: the CD19 paradigm. J. Clin. Invest. 125:3392.
59. 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.
60. Teachey, D. T., Rheingold, S. R., Maude, S. L. et al. 2013. Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood 121:5154.
61. Maude, S. L., Teachey, D. T., Porter, D. L. and Grupp, S. A. 2015. CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Blood 125:4017.
62. Tang, Y. M. and Xu, X. J. 2011. Advances in hemophagocytic lymphohistiocytosis: pathogenesis, early diagnosis/differential diagnosis, and treatment. Sci. World J. 11:697.
63. 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.
64. Fraietta, J. A., Beckwith, K. A., Patel, P. R. et al. 2016. Ibrutinib enhances chimeric antigen receptor T-cell engraftment and efficacy in leukemia. Blood 127:1117.
65. 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.
66. Ikeda, H., Akahori, Y., Yoneyama, M. et al. 2015. Immunotherapy with chimeric antigen receptor targeting intracellular WT1 gene product complexed with HLA-a*24:02 molecule. Blood 126:4292.
67. Hoyos, V., Savoldo, B., Quintarelli, C. et al. 2010. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 24:1160.
68. Tasian, S. K., Kenderian, S. S., Shen, F. et al. 2015. Efficient termination of CD123-redirected chimeric antigen receptor T cells for acute myeloid leukemia to mitigate toxicity. Blood 126:565.
69. Wu, C. Y., Roybal, K. T., Puchner, E. M., Onuffer, J. and Lim, W. A. 2015. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science 350:aab4077.
70. Di Stasi, A., De Angelis, B., Rooney, C. M. 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.