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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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Going non-viral: the Sleeping Beauty transposon system breaks on through to the clinical side
Hudecek, M., Izsvák, Z., Johnen, S., Renner, M., Thumann, G., & Ivics, Z. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1304354 · Cited by 99
Chimeric Antigen Receptors: A Cell and Gene Therapy Perspective
Rivière, I., & Sadelain, M. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.03.034 · Cited by 96
Novel immunotherapies for adult patients with B-lineage acute lymphoblastic leukemia
Wei, G., Wang, J., Huang, H., & Zhao, Y. (2017) · Journal of Hematology & Oncology · doi:10.1186/s13045-017-0516-x · Cited by 93
CD20-CD19 Bispecific CAR T Cells for the Treatment of B-Cell Malignancies
Martyniszyn, A., Krahl, A.-C., Andre, M. C., Hombach, A. A., & Abken, H. (2017) · Human Gene Therapy · doi:10.1089/hum.2017.126 · Cited by 98
CAR-T cell therapy: a potential new strategy against prostate cancer
Schepisi, G., Cursano, M. C., Casadei, C., Menna, C., Altavilla, A., Lolli, C., Cerchione, C., Paganelli, G., Santini, D., Tonini, G., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0741-7 · Cited by 97
A Bump in the Road: How the Hostile AML Microenvironment Affects CAR T Cell Therapy
Epperly, R., Gottschalk, S. M., & Velasquez, M. P. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00262 · Cited by 98
Immunotherapy for advanced hepatocellular carcinoma, where are we?
Li, Z., Ding, J., Li, H., Wang, Z., & Wu, J. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188441 · Cited by 95
Ruxolitinib mitigates steroid‐refractory CRS during CAR T therapy
Pan, J., Deng, B., Ling, Z., Song, W., Xu, J., Duan, J., Wang, Z., Chang, A. H., Feng, X., & Tan, Y. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16176 · Cited by 95
Impact of T cell characteristics on CAR-T cell therapy in hematological malignancies
Tao, Z., Chyra, Z., Kotulová, J., Celichowski, P., Mihályová, J., Charvátová, S., & Hájek, R. (2024) · Blood Cancer Journal · doi:10.1038/s41408-024-01193-6 · Cited by 101
“CAR-T cell therapy has been most successful in pediatric and young adult B-ALL patients, with a high CR rate of 90%; this is in contrast to MM patients, whose median age is over 70 and whose reported CR rate ranges from 33 to 73% [1, 13, 14].”
Current modalities in cancer immunotherapy: Immunomodulatory antibodies, CARs and vaccines
Lohmueller, J. J., & Finn, O. J. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.03.008 · Cited by 96
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The Emergence of Universal Immune Receptor T Cell Therapy for Cancer
Minutolo, N. G., Hollander, E. E., & Powell, D. J. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00176 · Cited by 98
“T cell expansion and persistence may be another issue with UIR T cells, as these two factors are key correlatives for predicting durable clinical remission (10, 24, 108, 109).”
BackgroundDeterminants of response and resistance to CAR T cell therapy
Lesch, S., Benmebarek, M.-R., Cadilha, B. L., Stoiber, S., Subklewe, M. S., Endres, S., & Kobold, S. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.11.004 · Cited by 96
Lingering effects of chemotherapy on mature T cells impair proliferation
Das, R. K., O’Connor, R. S., Grupp, S. A., & Barrett, D. M. (2020) · Blood Advances · doi:10.1182/bloodadvances.2020001797 · Cited by 97
Self-citationEngineering better chimeric antigen receptor T cells
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Immune-based therapies for childhood cancer
Mackall, C. L., Merchant, M. S., & Fry, T. J. (2014) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2014.177 · Cited by 93
Review: Current clinical applications of chimeric antigen receptor (CAR) modified T cells
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Chimeric antigen receptors for adoptive T cell therapy in acute myeloid leukemia
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Hypogammaglobulinemia due to CAR T‐cell therapy
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Diagnosis and management of pulmonary toxicity associated with cancer immunotherapy
Rashdan, S., Minna, J. D., & Gerber, D. E. (2018) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(18)30172-3 · Cited by 93
A highly soluble Sleeping Beauty transposase improves control of gene insertion
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A BAFF ligand-based CAR-T cell targeting three receptors and multiple B cell cancers
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The next wave of cellular immunotherapies in pancreatic cancer
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“These therapies have been very successful in treatment of hematological malignancies, with one study reporting up to 90% of individuals achieving remission.(31,32) So far, no CAR T cell therapy is approved for solid tumors.”
Background4-1BB immunotherapy: advances and hurdles
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“Although CAR T cells containing either of these costimulatory domains exhibit comparable antitumor ef fi cacy in patients with B-cell malignancies, preclinical models have shown substantial biological distinctions between CD28 and 4-1BB 39,40 .”
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Cancer immunology and canine malignant melanoma: A comparative review
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Posttransplant chimeric antigen receptor therapy
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Advances on chimeric antigen receptor-modified T-cell therapy for oncotherapy
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“06× 107 cells/kg 27 CR, 3 NR, 2 Relapse CRS, neurologic toxic effects, delayed encephalopathy, seizures [44]”
Preclinical evaluation of CD8+ anti-BCMA mRNA CAR T cells for treatment of multiple myeloma
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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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