The growing world of CAR T cell trials: a systematic review

Cancer Immunology, Immunotherapy

Volumn 65, Issue 12, 2016, Pages 1433-1450

  Holzinger, Astrid ^a,b   Barden, Markus ^a,b   Abken, Hinrich ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Adoptive cell therapy; CAR; Chimeric antigen receptor; Clinical trial; T cell

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; CANCER IMMUNOTHERAPY; CANCER REGRESSION; EX VIVO STUDY; GENE TRANSFER; HEMATOLOGIC MALIGNANCY; HUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; T LYMPHOCYTE; ADOPTIVE IMMUNOTHERAPY; IMMUNOLOGY; PROCEDURES;

HUMANS; IMMUNOTHERAPY, ADOPTIVE; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84986275877     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1895-5     Document Type: Review

References (46)

1. Eshhar Z (2008) The T-body approach: redirecting T cells with antibody specificity. Handb Exp Pharmacol 181:329–342. doi:10.1007/978-3-540-73259-4_14
2. Finney HM, Lawson AD, Bebbington CR, Weir AN (1998) Chimeric receptors providing both primary and costimulatory signaling in T cells from a single gene product. J Immunol 161:2791–2797
3. Hombach A, Wieczarkowiecz A, Marquardt T et al (2001) Tumor-specific T cell activation by recombinant immunoreceptors: CD3 zeta signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3 zeta signaling receptor molecule. J Immunol 167:6123–6131
4. Chmielewski M, Kopecky C, Hombach AA, Abken H (2011) IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res 71:5697–5706
5. Maude SL, Frey N, Shaw PA et al (2014) Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 371:1507–1517. doi:10.1056/NEJMoa1407222
6. Singh N, Frey NV, Grupp SA, Maude SL (2016) CAR T Cell Therapy in Acute Lymphoblastic Leukemia and Potential for Chronic Lymphocytic Leukemia. Curr Treat Options Oncol 17:28. doi:10.1007/s11864-016-0406-4
7. Savoldo B, Ramos CA, Liu E et al (2011) CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Investig 121:1822–1826. doi:10.1172/JCI46110
8. Cruz CRY, Micklethwaite KP, 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 122:2965–2973. doi:10.1182/blood-2013-06-506741
9. Xu X-J, Zhao H-Z, Tang Y-M (2013) Efficacy and safety of adoptive immunotherapy using anti-CD19 chimeric antigen receptor transduced T-cells: a systematic review of phase I clinical trials. Leuk Lymphoma 54:255–260. doi:10.3109/10428194.2012.715350
10. Zhang T, Cao L, Xie J et al (2015) Efficiency of CD19 chimeric antigen receptor-modified T cells for treatment of B cell malignancies in phase I clinical trials: a meta-analysis. Oncotarget 6:33961–33971. doi:10.18632/oncotarget.5582
11. Kalos M, Levine BL, Porter DL et al (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. doi:10.1126/scitranslmed.3002842
12. Porter DL, Levine BL, Kalos M et al (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365:725–733. doi:10.1056/NEJMoa1103849
13. Porter DL, Hwang W-T, Frey NV et al (2015) Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med 7:303ra139. doi:10.1126/scitranslmed.aac5415
14. Brentjens RJ, Rivière I, Park JH 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. doi:10.1182/blood-2011-04-348540
15. Kochenderfer JN, Dudley ME, Feldman SA 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. doi:10.1182/blood-2011-10-384388
16. Davila ML, Bouhassira DCG, Park JH et al (2014) Chimeric antigen receptors for the adoptive T cell therapy of hematologic malignancies. Int J Hematol 99:361–371. doi:10.1007/s12185-013-1479-5
17. Lee DW, Kochenderfer JN, 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 385:517–528. doi:10.1016/S0140-6736(14)61403-3
18. Morgan RA, Yang JC, Kitano M et al (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. doi:10.1038/mt.2010.24
19. Ahmed N, Brawley VS, Hegde M et al (2015) Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol 33:1688–1696. doi:10.1200/JCO.2014.58.0225
20. Gross G, Eshhar Z (2016) Therapeutic potential of T cell chimeric antigen receptors (CARs) in cancer treatment: counteracting off-tumor toxicities for safe CAR T cell therapy. Annu Rev Pharmacol Toxicol 56:59–83. doi:10.1146/annurev-pharmtox-010814-124844
21. Fedorov VD, Themeli M, Sadelain M (2013) PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci Transl Med 5:215ra172. doi:10.1126/scitranslmed.3006597
22. Kloss CC, Condomines M, Cartellieri M et al (2012) Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol 31:71–75. doi:10.1038/nbt.2459
23. Beatty GL, Haas AR, Maus MV et al (2014) Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-tumor activity in solid malignancies. Cancer Immunol Res 2:112–120. doi:10.1158/2326-6066.CIR-13-0170
24. Brentjens R, Yeh R, Bernal Y et al (2010) Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: case report of an unforeseen adverse event in a phase I clinical trial. Mol Ther 18:666–668. doi:10.1038/mt.2010.31
25. Grupp SA, Kalos M, Barrett D et al (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368:1509–1518. doi:10.1056/NEJMoa1215134
26. Chen F, Teachey DT, Pequignot E et al (2016) Measuring IL-6 and sIL-6R in serum from patients treated with tocilizumab and/or siltuximab following CAR T cell therapy. J Immunol Methods 434:1–8. doi:10.1016/j.jim.2016.03.005
27. Davila ML, 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. doi:10.1126/scitranslmed.3008226
28. Maude SL, Barrett D, Teachey DT, Grupp SA (2014) Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J 20:119–122. doi:10.1097/PPO.0000000000000035
29. Teachey DT, Lacey SF, Shaw PA et al (2016) Identification of predictive biomarkers for cytokine release syndrome after chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Cancer Discov 6:664–679. doi:10.1158/2159-8290.CD-16-0040
30. Katz SC, Burga RA, McCormack E et al (2015) Phase I hepatic immunotherapy for metastases study of intra-arterial chimeric antigen receptor-modified t-cell therapy for CEA + Liver Metastases. Clin Cancer Res 21:3149–3159. doi:10.1158/1078-0432.CCR-14-1421
31. Xu Y, Zhang M, Ramos CA et al (2014) Closely related T-memory stem cells correlate with in vivo expansion of CAR.CD19-T cells and are preserved by IL-7 and IL-15. Blood 123:3750–3759. doi:10.1182/blood-2014-01-552174
32. Abken H (2015) Adoptive therapy with CAR redirected T cells: the challenges in targeting solid tumors. Immunotherapy 7:535–544. doi:10.2217/imt.15.15
33. Kobold S, Grassmann S, Chaloupka M et al (2015) Impact of a new fusion receptor on PD-1-mediated immunosuppression in adoptive T cell therapy. J Natl Cancer Inst. doi:10.1093/jnci/djv146
34. Kawalekar OU, O’Connor RS, Fraietta JA et al (2016) Distinct signaling of coreceptors regulates specific metabolism pathways and impacts memory development in CAR T cells. Immunity 44:380–390. doi:10.1016/j.immuni.2016.01.021
35. Kochenderfer JN, Wilson WH, Janik JE et al (2010) 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. doi:10.1182/blood-2010-04-281931
36. Kochenderfer JN, Dudley ME, Kassim SH 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. doi:10.1200/JCO.2014.56.2025
37. Kochenderfer JN, Dudley ME, Carpenter RO et al (2013) Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 122:4129–4139. doi:10.1182/blood-2013-08-519413
38. Brentjens RJ, Davila ML, 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. doi:10.1126/scitranslmed.3005930
39. Garfall AL, Maus MV, Hwang W-T et al (2015) Chimeric antigen receptor T cells against CD19 for multiple myeloma. N Engl J Med 373:1040–1047. doi:10.1056/NEJMoa1504542
40. Till BG, Jensen MC, Wang J 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. doi:10.1182/blood-2011-10-387969
41. Wang Q, Wang Y, Lv H et al (2015) Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol Ther 23:184–191. doi:10.1038/mt.2014.164
42. Ritchie DS, Neeson PJ, Khot A et al (2013) Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther 21:2122–2129. doi:10.1038/mt.2013.154
43. van Schalkwyk MCI, Papa SE, Jeannon J-P et al (2013) Design of a phase I clinical trial to evaluate intratumoral delivery of ErbB-targeted chimeric antigen receptor T-cells in locally advanced or recurrent head and neck cancer. Hum Gene Ther Clin Dev 24:134–142. doi:10.1089/humc.2013.144
44. Morgan RA, Johnson LA, Davis JL et al (2012) Recognition of glioma stem cells by genetically modified T cells targeting EGFRvIII and development of adoptive cell therapy for glioma. Hum Gene Ther 23:1043–1053. doi:10.1089/hum.2012.041
45. Maus MV, Haas AR, Beatty GL et al (2013) T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol Res 1:26–31. doi:10.1158/2326-6066.CIR-13-0006
46. You F, Jiang L, Zhang B et al (2016) Phase 1 clinical trial demonstrated that MUC1 positive metastatic seminal vesicle cancer can be effectively eradicated by modified Anti-MUC1 chimeric antigen receptor transduced T cells. Sci China Life Sci. 59:386–397. doi:10.1007/s11427-016-5024-7