Engineered T cells: the promise and challenges of cancer immunotherapy

Fesnak, Andrew D.; June, Carl H.; Levine, Bruce L.

doi:10.1038/nrc.2016.97

Cited by 1,074CAR-T cell therapy researchImmunotherapy and Immune ResponsesT-cell and B-cell Immunology

Engineered T cells: the promise and challenges of cancer immunotherapy

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Fesnak, Andrew D., June, Carl H., Levine, Bruce L.·2016·Nature Reviews Cancer

DOI 10.1038/nrc.2016.97PMC PMC5543811

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Abstract

The immune system evolved to distinguish non-self from self to protect the organism. As cancer is derived from our own cells, immune responses to dysregulated cell growth present a unique challenge. This is compounded by mechanisms of immune evasion and immunosuppression that develop in the tumour microenvironment. The modern genetic toolbox enables the adoptive transfer of engineered T cells to create enhanced anticancer immune functions where natural cancer-specific immune responses have failed. Genetically engineered T cells, so-called 'living drugs', represent a new paradigm in anticancer therapy. Recent clinical trials using T cells engineered to express chimeric antigen receptors (CARs) or engineered T cell receptors (TCRs) have produced stunning results in patients with relapsed or refractory haematological malignancies. In this Review we describe some of the most recent and promising advances in engineered T cell therapy with a particular emphasis on what the next generation of T cell therapy is likely to entail.

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Genetically engineered immune cell therapies are effective for some cancer types but still cannot cure most tumors.
“Genetically engineered immune cell therapies have proven effective for treatment of some cancer types (Esensten et al., 2017; Fesnak et al., 2016; June and Sadelain, 2018; Sadelain et al., 2017), but they still cannot cure most tumors.”
From Pooled Knockin Targeting for Genome Engineering of Cellular Immunotherapies (2020) · cites this paper as Fesnak et al., 2016
CAR-T cells with the same antibody have been less successful and less reproducible for other B-cell tumours (such as chronic lymphoblastic leukaemia) and for other antibodies and solid tumours.
“CAR-T cells with the same antibody have been less successful and less reproducible for other B-cell tumours (such as chronic lymphoblastic leukaemia) and for other antibodies and solid tumours107.”
From How to design preclinical studies in nanomedicine and cell therapy to maximize the prospects of clinical translation (2018) · cites this paper as [107]

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Regression of Experimental Medulloblastoma following Transfer of HER2-Specific T Cells
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Ovarian cancer stem cells express ROR1, which can be targeted for anti–cancer-stem-cell therapy
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Combining a CD20 Chimeric Antigen Receptor and an Inducible Caspase 9 Suicide Switch to Improve the Efficacy and Safety of T Cell Adoptive Immunotherapy for Lymphoma
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T Lymphocytes Expressing a CD16 Signaling Receptor Exert Antibody-Dependent Cancer Cell Killing
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Interleukin-13 receptor alpha chain: a novel tumor-associated transmembrane protein in primary explants of human malignant gliomas.
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Targeting of folate receptor β on acute myeloid leukemia blasts with chimeric antigen receptor–expressing T cells
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Targeting the Intracellular WT1 Oncogene Product with a Therapeutic Human Antibody
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Mesothelin Overexpression Is a Marker of Tumor Aggressiveness and Is Associated with Reduced Recurrence-Free and Overall Survival in Early-Stage Lung Adenocarcinoma
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Ror1, a cell surface receptor tyrosine kinase is expressed in chronic lymphocytic leukemia and may serve as a putative target for therapy
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Promoter trapping reveals significant differences in integration site selection between MLV and HIV vectors in primary hematopoietic cells
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Safety of Targeting ROR1 in Primates with Chimeric Antigen Receptor–Modified T Cells
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Reversal of tumor immune inhibition using a chimeric cytokine receptor.
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Redirection of Genetically Engineered CAR-T Cells Using Bifunctional Small Molecules
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Crosstalk between ROR1 and the Pre-B Cell Receptor Promotes Survival of t(1;19) Acute Lymphoblastic Leukemia
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Manufacture of Clinical-Grade CD19-Specific T Cells Stably Expressing Chimeric Antigen Receptor Using Sleeping Beauty System and Artificial Antigen Presenting Cells
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Tolerance and efficacy of autologous or donor-derived T cells expressing CD19 chimeric antigen receptors in adult B-ALL with extramedullary leukemia
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T cells redirected against CD70 for the immunotherapy of CD70-positive malignancies
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Patient-derived glioblastoma stem cells are killed by CD133-specific CAR T cells but induce the T cell aging marker CD57
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IL-12-secreting CD19-targeted cord blood-derived T cells for the immunotherapy of B-cell acute lymphoblastic leukemia
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piggyBac Transposon/Transposase System to Generate CD19-Specific T Cells for the Treatment of B-Lineage Malignancies
Manuri, P. R., Wilson, M. H., Maiti, S. N., Mi, T., Singh, H., Olivares, S., Dawson, M. J., Huls, H. M., Lee, D. A., Rao, P. H., et al. (2009) · Human Gene Therapy · doi:10.1089/hum.2009.114 · Cited by 141 · see citing works
Immunotherapy of Metastatic Melanoma Using Genetically Engineered GD2-Specific T cells
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Durable Remissions in Children with Relapsed/Refractory ALL Treated with T Cells Engineered with a CD19-Targeted Chimeric Antigen Receptor (CTL019)
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Blockade of PD-1 immunosuppression boosts CAR T-cell therapy
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Expression of Interleukin-13 Receptor α2 in Glioblastoma Multiforme: Implications for Targeted Therapies
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Ror1 Is a Pseudokinase That Is Crucial for Met-Driven Tumorigenesis
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CAR T cells transform to trucks: chimeric antigen receptor–redirected T cells engineered to deliver inducible IL-12 modulate the tumour stroma to combat cancer
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Trends in long-term survival of patients with chronic lymphocytic leukemia from the 1980s to the early 21st century
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PiggyBac-mediated Cancer Immunotherapy Using EBV-specific Cytotoxic T-cells Expressing HER2-specific Chimeric Antigen Receptor
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Large-Scale Production of CD4+ T Cells from HIV-1-Infected Donors After CD3/CD28 Costimulation*
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EGFRvIII-Specific Chimeric Antigen Receptor T Cells Migrate to and Kill Tumor Deposits Infiltrating the Brain Parenchyma in an Invasive Xenograft Model of Glioblastoma
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Trafficking of CAR-Engineered Human T Cells Following Regional or Systemic Adoptive Transfer in SCID Beige Mice
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Vaccine-Stimulated, Adoptively Transferred CD8+ T Cells Traffic Indiscriminately and Ubiquitously while Mediating Specific Tumor Destruction
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IGF1R- and ROR1-Specific CAR T Cells as a Potential Therapy for High Risk Sarcomas
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Infusing CD19-Directed T Cells to Augment Disease Control in Patients Undergoing Autologous Hematopoietic Stem-Cell Transplantation for Advanced B-Lymphoid Malignancies
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Graft-versus-tumor response in patients with multiple myeloma is associated with antibody response to BCMA, a plasma-cell membrane receptor
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First Clinical Application of Talen Engineered Universal CAR19 T Cells in B-ALL
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The Inside Out of Lentiviral Vectors
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CD28z CARs and Armored CARs
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Affinity maturation of T-cell receptor-like antibodies for Wilms tumor 1 peptide greatly enhances therapeutic potential
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Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy
Sharma, P., Hu-Lieskovan, S., Wargo, J. A., & Ribas, A. (2017) · Cell · doi:10.1016/j.cell.2017.01.017 · Cited by 5,588 · see citing works
Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges
Fukumura, D., Kloepper, J., Amoozgar, Z., Duda, D. G., & Jain, R. K. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2018.29 · Cited by 2,027 · see citing works
Recent Strategies to Develop Innovative Photosensitizers for Enhanced Photodynamic Therapy
Pham, T. C., Nguyen, V.-N., Choi, Y., Lee, S., & Yoon, J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00381 · Cited by 1,813 · see citing works
Ionizable Lipid Nanoparticle-Mediated mRNA Delivery for Human CAR T Cell Engineering
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Self-citation
Bacterial outer membrane vesicles suppress tumor by interferon-γ-mediated antitumor response
Kim, O. Y., Park, H. T., Dinh, N. T. H., Choi, S. J., Lee, J., Kim, J. H., Lee, S.-W., & Gho, Y. S. (2017) · Nature Communications · doi:10.1038/s41467-017-00729-8 · Cited by 616 · see citing works
Systematic Immunotherapy Target Discovery Using Genome-Scale In Vivo CRISPR Screens in CD8 T Cells
Dong, M. B., Wang, G., Chow, R. D., Ye, L., Zhu, L., Dai, X., Park, J. J., Kim, H. R., Errami, Y., Guzman, C. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.07.044 · Cited by 330 · see citing works
Biomineralized Bacterial Outer Membrane Vesicles Potentiate Safe and Efficient Tumor Microenvironment Reprogramming for Anticancer Therapy
Qing, S., Lyu, C., Zhu, L., Pan, C., Wang, S., Li, F., Wang, J., Yue, H., Gao, X., Jia, R., et al. (2020) · Advanced Materials · doi:10.1002/adma.202002085 · Cited by 309 · see citing works
Glioblastoma-targeted CD4+ CAR T cells mediate superior antitumor activity
Wang, D., Aguilar, B., Starr, R., Alizadeh, D., Brito, A., Sarkissian, A., Ostberg, J. R., Forman, S. J., & Brown, C. E. (2018) · JCI Insight · doi:10.1172/jci.insight.99048 · Cited by 233 · see citing works
Pooled Knockin Targeting for Genome Engineering of Cellular Immunotherapies
Roth, T. L., Li, P. J., Blaeschke, F., Nies, J. F., Apathy, R., Mowery, C., Yu, R., Nguyen, M. L. T., Lee, Y., Truong, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.039 · Cited by 186 · see citing works
How to design preclinical studies in nanomedicine and cell therapy to maximize the prospects of clinical translation
Ioannidis, J. P. A., Kim, B. Y. S., & Trounson, A. (2018) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0314-y · Cited by 175 · see citing works
The effects of monocytes on tumor cell extravasation in a 3D vascularized microfluidic model
Boussommier-Calleja, A., Atiyas, Y., Haase, K., Headley, M., Lewis, C., & Kamm, R. D. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.03.005 · Cited by 158 · see citing works
Vaccine efficacy against primary and metastatic cancer with in vitro-generated CD103 <sup>+</sup> conventional dendritic cells
Zhou, Y., Slone, N., Chrisikos, T. T., Kyrysyuk, O., Babcock, R. L., Medik, Y. B., Li, H. S., Kleinerman, E. S., & Watowich, S. S. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2019-000474 · Cited by 112 · see citing works
Engineering chimeric antigen receptor-T cells for cancer treatment
Ye, B., Stary, C. M., Li, X., Gao, Q., Kang, C., & Xiong, X. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0814-0 · Cited by 95 · see citing works
Diacylglycerol kinases in T cell tolerance and effector function
Chen, S. S., Hu, Z., & Zhong, X.-P. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00130 · Cited by 44 · see citing works
Biological Basis for Novel Mesothelioma Therapies
Obacz, J., Yung, H., Shamseddin, M., Linnane, E., Liu, X., Azad, A. A., Rassl, D. M., Fairen-Jimenez, D., Rintoul, R. C., Nikolić, M. Z., et al. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01462-2 · Cited by 31 · see citing works
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Authors: Fesnak, A. D., June, C. H., & Levine, B. L.
Affiliations: University of Pennsylvania (US)
Corresponding author: Fesnak, Andrew D.
Levine, Bruce L.
ORCID: Fesnak, Andrew D.
June, Carl H.
Levine, Bruce L.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2016-08-23
Volume: 16
Issue: 9
Pages: 566-581
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc.2016.97
PMC: PMC5543811
OpenAlex: W2515679023
Cited by: 1,074
References: 252
Citations by year: 2026: 55 · 2025: 76 · 2024: 73 · 2023: 71 · 2022: 91 · 2021: 144 · 2020: 134 · 2019: 127 · 2018: 161 · 2017: 122 · 2016: 13 · 2015: 1 · 2014: 1
FWCI: 14.18
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Parker Foundation
Leukemia and Lymphoma Society
National Institutes of Health
National Heart, Lung, and Blood Institute (T32HL007775)
National Cancer Institute (R01CA165206, R01CA120409, P30CA016520)
Topics: Health Sciences › Medicine › Oncology › CAR-T cell therapy research
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: engineered T cells, adoptive cell transfer, cancer immunotherapy, chimeric antigen receptor, engineered T cell receptors, B-cell malignancies, hematologic malignancies, solid tumors, tumor immune evasion, tumor microenvironment, immune tolerance
MeSH terms: Gene Editing, Antigens, Neoplasm, Clinical Trials as Topic, Forecasting, Genetic Engineering, HLA Antigens, Humans, Neoplasms, Receptors, Antigen, T-Cell, Recombinant Fusion Proteins, Syndrome, T-Lymphocyte Subsets, Cytokines, Immunotherapy, Adoptive, Antigen Presentation, Gene Transfer Techniques, Models, Immunological, Antigens, CD19, Tumor Escape, Hematologic Neoplasms, T-Cell Antigen Receptor Specificity, Tumor Microenvironment, Costimulatory and Inhibitory T-Cell Receptors

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