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Chimeric Antigen Receptor T Cells for Sustained Remissions in Leukemia
Open accessAbstract
BACKGROUND: Relapsed acute lymphoblastic leukemia (ALL) is difficult to treat despite the availability of aggressive therapies. Chimeric antigen receptor-modified T cells targeting CD19 may overcome many limitations of conventional therapies and induce remission in patients with refractory disease. METHODS: We infused autologous T cells transduced with a CD19-directed chimeric antigen receptor (CTL019) lentiviral vector in patients with relapsed or refractory ALL at doses of 0.76×10(6) to 20.6×10(6) CTL019 cells per kilogram of body weight. Patients were monitored for a response, toxic effects, and the expansion and persistence of circulating CTL019 T cells. RESULTS: A total of 30 children and adults received CTL019. Complete remission was achieved in 27 patients (90%), including 2 patients with blinatumomab-refractory disease and 15 who had undergone stem-cell transplantation. CTL019 cells proliferated in vivo and were detectable in the blood, bone marrow, and cerebrospinal fluid of patients who had a response. Sustained remission was achieved with a 6-month event-free survival rate of 67% (95% confidence interval [CI], 51 to 88) and an overall survival rate of 78% (95% CI, 65 to 95). At 6 months, the probability that a patient would have persistence of CTL019 was 68% (95% CI, 50 to 92) and the probability that a patient would have relapse-free B-cell aplasia was 73% (95% CI, 57 to 94). All the patients had the cytokine-release syndrome. Severe cytokine-release syndrome, which developed in 27% of the patients, was associated with a higher disease burden before infusion and was effectively treated with the anti-interleukin-6 receptor antibody tocilizumab. CONCLUSIONS: Chimeric antigen receptor-modified T-cell therapy against CD19 was effective in treating relapsed and refractory ALL. CTL019 was associated with a high remission rate, even among patients for whom stem-cell transplantation had failed, and durable remissions up to 24 months were observed. (Funded by Novartis and others; CART19 ClinicalTrials.gov numbers, NCT01626495 and NCT01029366.).
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“however, as with TCRs, the adverse effects of CAR T-cell therapy appear to be mechanism based and not a result of using viral vectors [74].”
From Clinical use of lentiviral vectors (2018) · cites this paper as [74]
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“The anti-IL-6R antibodies tocilizumab and sarilumab are used to treat RA, Castleman’s disease and CAR-T-induced CRS (71–75, 352, 364) and have promise for treating the severe form of COVID-19 (365–367).”
From IL-6 in inflammation, autoimmunity and cancer (2021) · cites this paper as [364]
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“Clinical trials using CD19-targeted CAR T-cell therapy for B-cell acute lymphoblastic leukemia have demonstrated high efficacy, with durable complete response rates in >60% of patients with relapsed or refractory disease [74, 75].”
From Clinical use of lentiviral vectors (2018) · cites this paper as [74]
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“One important on-target side effect of CD19 CAR T-cell therapy is B-cell aplasia, which is associated with long-term CAR T-cell persistence [74].”
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“The anti-IL-6R antibody tocilizumab is effective at treating patients with CAR-T-induced cytokine release syndrome (CRS) (352, 364) and is being considered for treating ARDS in COVID-19 patients (365–368).”
From IL-6 in inflammation, autoimmunity and cancer (2021) · cites this paper as [364]
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“In patients who received tocilizumab, severe clinical manifestations rapidly improved 1–3 days after injection (Maude et al., 2014”
From Targeting Interleukin-6 Signaling in Clinic (2019) · cites this paper as Maude et al., 2014
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BackgroundAcute Kidney Injury after CAR-T Cell Therapy: Low Incidence and Rapid Recovery
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“However, different CAR constructs confer different rates and severity of CRS.”
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Siglec-6 is a novel target for CAR T-cell therapy in acute myeloid leukemia
Jetani, H., Navarro‐Bailón, A., Maucher, M., Frenz, S., Verbruggen, C., Yeguas, A., Vídriales, M., González, M., Saborido, J. R., Kraus, S., et al. (2021) · Blood · doi:10.1182/blood.2020009192 · Cited by 110
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CAR T Cell Therapy: A Versatile Living Drug
Marco, R. C. D., Monzó, H. J., & Ojala, P. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076300 · Cited by 120
“By the end of the two-year-long cohort, 19 patients were reported to still be in remission, most with no further therapy [31].”
BackgroundMethodCytokine-mediated CAR T therapy resistance in AML
Bhagwat, A. S., Torres, L., Shestova, O. E., Shestov, M., Mellors, P. W., Fisher, H. R., Farooki, S., Frost, B. F., Loken, M. R., Gaymon, A. L., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-03271-5 · Cited by 117
“Assays were performed as previously described 76 .”
Self-citationThe Cellular Immunotherapy Revolution: Arming the Immune System for Precision Therapy
Paucek, R. D., Baltimore, D., & Li, G. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.02.002 · Cited by 104
Evolution to plasmablastic lymphoma evades CD19‐directed chimeric antigen receptor T cells
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Self-citationAvoidance of On-Target Off-Tumor Activation Using a Co-stimulation-Only Chimeric Antigen Receptor
Fisher, J. P. H., Abramowski, P., Don, N. D. W., Flutter, B. R., Capsomidis, A., Cheung, G. W.-K., Gustafsson, K. T., & Anderson, J. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.03.002 · Cited by 106
Cytokine release syndrome: Who is at risk and how to treat
Frey, N. V. (2017) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2017.09.002 · Cited by 106
Self-citationThe Pharmacology of T Cell Therapies
Milone, M. C., & Bhoj, V. G. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.01.010 · Cited by 103
Yap suppresses T-cell function and infiltration in the tumor microenvironment
Stampouloglou, E., Cheng, N., Federico, A. N., Slaby, E. M., Monti, S., Szeto, G. L., & Varelas, X. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000591 · Cited by 108
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Wang, T., Tang, Y., Cai, J., Wan, X., Hu, S., Lu, X., Xie, Z., Qiao, X., Jiang, H., Shao, J., et al. (2022) · Journal of Clinical Oncology · doi:10.1200/jco.22.01214 · Cited by 113
“censored): Transplant 78 (0) 77 (0) 71 (2) 54 (18) 35 (35) 25 (45) 15 (55) 10 (60) 1 (69) No transplant* 194 (0) 120 (72) 86 (98) 55 (124) 42 (136) 26 (151) 15 (162) 5 (172) 0 (177) 0 4 8 12 16 20 24 28 32 100”
BackgroundInfluentialLarson, S. M., Walthers, C. M., Ji, B., Ghafouri, S. N., Naparstek, J., Trent, J., Chen, J. M., Roshandell, M., Harris, C. M., Khericha, M., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0964 · Cited by 111
Kailayangiri, S., Altvater, B., Spurny, C., Jamitzky, S., Schelhaas, S., Jacobs, A. H., Wiek, C., Roellecke, K., Hanenberg, H., Hartmann, W., et al. (2017) · OncoImmunology · doi:10.1080/2162402x.2016.1250050 · Cited by 104
Challenges and opportunities of allogeneic donor-derived CAR T cells
Yang, Y., Jacoby, E., & Fry, T. J. (2015) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000181 · Cited by 101
Tanaka, M., Tashiro, H., Omer, B. A., Lapteva, N., Ando, J., Ngo, M. C., Mehta, B., Dotti, G., Kinchington, P. R., Leen, A. M., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-2138 · Cited by 104
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Pediatric Cancer Immunotherapy: Opportunities and Challenges
Wedekind, M. F., Denton, N. L., Chen, C., & Cripe, T. P. (2018) · Pediatric Drugs · doi:10.1007/s40272-018-0297-x · Cited by 113
Recombination of a dual-CAR-modified T lymphocyte to accurately eliminate pancreatic malignancy
Zhang, E., Yang, P., Gu, J., Wu, H., Chi, X., Liu, C., Wang, Y., Xue, J., Qi, W., Sun, Q., et al. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0646-9 · Cited by 109
Production of Lentiviral Vectors Using Suspension Cells Grown in Serum-free Media
Bauler, M. N., Roberts, J. K., Wu, C., Fan, B., Ferrara, F., Yip, B. H., Diao, S., Kim, Y., Moore, J., Zhou, S., et al. (2019) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2019.11.011 · Cited by 105
TCR Redirected T Cells for Cancer Treatment: Achievements, Hurdles, and Goals
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Hepatocellular carcinoma: signaling pathways, targeted therapy, and immunotherapy
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CARs: Synthetic Immunoreceptors for Cancer Therapy and Beyond
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Limitations and opportunities for immune checkpoint inhibitors in pediatric malignancies
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Toll-like receptor 2 costimulation potentiates the antitumor efficacy of CAR T Cells
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Towards Immunotherapy for Pediatric Brain Tumors
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Emerging Approaches for Regulation and Control of CAR T Cells: A Mini Review
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“Retrospective analyses from clinical trials indicate that inadequate clinical responses to CAR T cell therapy might also be associated with an insufficient expansion and persistence of functional CAR T cells in vivo [3, 12].”
MethodModel‐Based Cellular Kinetic Analysis of Chimeric Antigen Receptor‐T Cells in Humans
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“Patients with substantial tumor burden frequently suffered from high cytokine release syndromes in several trials, suggesting rapid and significant CAR-T expansions in these patients.(17,26,27) However, based on the data utilized within our analysis, in patients with MM and CLL, pretreatment tumor burdens were not sta…”
ResultCAR-T Cell Therapy: From the Shop to Cancer Therapy
Uscanga‐Palomeque, A. C., Chávez-Escamilla, A. K., Alvizo-Báez, C. A., Saavedra-Alonso, S., Terrazas-Armendáriz, L. D., Támez-Guerra, R., Rodrı́guez-Padilla, C., & Alcocer-González, J. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115688 · Cited by 116
“For example, targeting CD19 can lead to B-cell dysplasia, as CD19 is highly expressed not only on malignant B cells but also on benign and most normal B cells [75,76].”
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Preservation of cell-based immunotherapies for clinical trials
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State of the art in CAR T cell therapy for CD19+ B cell malignancies
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“Initial attempts to manage CRS with high-dose steroids and TNF-α blockade failed, leading to the first successful use of tocilizumab in refractory CRS (13, 18).”
BackgroundRapidly Switchable Universal CAR-T Cells for Treatment of CD123-Positive Leukemia
Loff, S., Dietrich, J., Meyer, J.-E., Riewaldt, J., Spehr, J., Bonin, M. V., Gründer, C., Swayampakula, M., Franke, K., Feldmann, A., et al. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.04.009 · Cited by 104
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Sallman, D. A., Kerre, T. C. C., Havelange, V., Poiré, X., Lewalle, P., Wang, E. S., Brayer, J. B., Davila, M. L., Moors, I., Machiels, J., et al. (2023) · The Lancet Haematology · doi:10.1016/s2352-3026(22)00378-7 · Cited by 102
Two cases of severe pulmonary toxicity from highly active mesothelin-directed CAR T cells
Haas, A. R., Golden, R. J., Litzky, L. A., Engels, B., Zhao, L., Xu, F., Taraszka, J. A., Ramones, M., Granda, B. W., Chang, W., et al. (2023) · Molecular Therapy · doi:10.1016/j.ymthe.2023.06.006 · Cited by 103
Self-citationIncorporation of a hinge domain improves the expansion of chimeric antigen receptor T cells
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Adoptive T cell therapy: An overview of obstacles and opportunities
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Metadata
- Authors
- Maude, S. L., Frey, N., Shaw, P. A., Aplenc, R., Barrett, D. M., Bunin, N. J., Chew, A., Gonzalez, V. E., Zheng, Z., Lacey, S. F., Mahnke, Y. D., Melenhorst, J. J., Rheingold, S. R., Shen, A., Teachey, D. T., Levine, B. L., June, C. H., Porter, D. L., & Grupp, S. A.
- Affiliations
- Children's Hospital of Philadelphia (US)
- Abramson Cancer Center (US)
- University of Pennsylvania (US)
- ORCID
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2014-10-16
- Volume
- 371
- Issue
- 16
- Pages
- 1507-1517
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC4267531
- OpenAlex
- W2118796952
- Cited by
- 5,413
- References
- 30
- Citations by year
- 2026: 228 · 2025: 318 · 2024: 378 · 2023: 505 · 2022: 495 · 2021: 558 · 2020: 665 · 2019: 538 · 2018: 501 · 2017: 541 · 2016: 385 · 2015: 261 · 2014: 24
- FWCI
- 195.01
- Type
- journal article
- Language
- en
- Update notices
- correction (2016-03-10)
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Children's Hospital of Philadelphia
- St. Jude Children's Research Hospital
- School of Medicine, Indiana University
- National Cancer Institute (P30CA147859, R01CA165206, R01CA102646, R01CA116660, T32CA009615, P30CA016520)
- National Institute of Allergy and Infectious Diseases (P30AI045008)
- Topics
- Health Sciences › Medicine › Oncology › CAR-T cell therapy research
- Health Sciences › Medicine › Hematology › Acute Lymphoblastic Leukemia research
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- chimeric antigen receptor T cells, CD19, acute lymphoblastic leukemia, relapsed/refractory leukemia, CAR T-cell therapy, tisagenlecleucel, lentiviral vectors, complete remission, cytokine release syndrome, tocilizumab, B-cell aplasia, stem cell transplantation, event-free survival, sustained remission, pediatric and adult patients
- MeSH terms
- Adolescent, Adult, Child, Child, Preschool, Chimera, Female, Genetic Engineering, Genetic Vectors, Humans, Immunotherapy, Male, Middle Aged, Receptors, Antigen, T-Cell, Recurrence, Remission Induction, T-Lymphocytes, Genetic Therapy, Survival Rate, Lentivirus, Cytokines, Antigens, CD19, Precursor Cell Lymphoblastic Leukemia-Lymphoma, Young Adult, Antibodies, Monoclonal, Humanized
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