Review
. 2021 Jan; 12(1):81.
doi: 10.1186/s13287-020-02128-1.

CAR T cells in solid tumors: challenges and opportunities

Faroogh Marofi 1 Roza Motavalli 2 Vladimir A Safonov 3 Lakshmi Thangavelu 4 Alexei Valerievich Yumashev 5 Markov Alexander 6 Navid Shomali 7 Max Stanley Chartrand 8 Yashwant Pathak 9 Mostafa Jarahian 10 Sepideh Izadi 7 Ali Hassanzadeh 7 Naghmeh Shirafkan 7 Safa Tahmasebi 7 Farhad Motavalli Khiavi 11 
Affiliations
  • PMID: 33494834
  •     134 References
  •     42 citations

Abstract

Background: CARs are simulated receptors containing an extracellular single-chain variable fragment (scFv), a transmembrane domain, as well as an intracellular region of immunoreceptor tyrosine-based activation motifs (ITAMs) in association with a co-stimulatory signal.

Main Body: Chimeric antigen receptor (CAR) T cells are genetically engineered T cells to express a receptor for the recognition of the particular surface marker that has given rise to advances in the treatment of blood disorders. The CAR T cells obtain supra-physiological properties and conduct as "living drugs" presenting both immediate and steady effects after expression in T cells surface. But, their efficacy in solid tumor treatment has not yet been supported. The pivotal challenges in the field of solid tumor CAR T cell therapy can be summarized in three major parts: recognition, trafficking, and surviving in the tumor. On the other hand, the immunosuppressive tumor microenvironment (TME) interferes with T cell activity in terms of differentiation and exhaustion, and as a result of the combined use of CARs and checkpoint blockade, as well as the suppression of other inhibitor factors in the microenvironment, very promising results were obtained from the reduction of T cell exhaustion.

Conclusion: Nowadays, identifying and defeating the mechanisms associated with CAR T cell dysfunction is crucial to establish CAR T cells that can proliferate and lyse tumor cells severely. In this review, we discuss the CAR signaling and efficacy T in solid tumors and evaluate the most significant barriers in this process and describe the most novel therapeutic methods aiming to the acquirement of the promising therapeutic outcome in non-hematologic malignancies.

Keywords: CAR T cells; Cell therapy; Chimeric antigen receptor; Solid tumors.

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Donald M O'Rourke, MacLean P Nasrallah, +18 authors, Marcela V Maus.
Sci Transl Med, 2017 Jul 21; 9(399). PMID: 28724573    Free PMC article.
Highly Cited.
HER2 overexpression correlates with survival after curative resection of pancreatic cancer.
Masahiro Komoto, Bunzo Nakata, +5 authors, Kosei Hirakawa.
Cancer Sci, 2009 May 13; 100(7). PMID: 19432892
High-Affinity GD2-Specific CAR T Cells Induce Fatal Encephalitis in a Preclinical Neuroblastoma Model.
Sarah A Richman, Selene Nunez-Cruz, +6 authors, Michael C Milone.
Cancer Immunol Res, 2017 Nov 29; 6(1). PMID: 29180536    Free PMC article.
Highly Cited.
CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients.
Barbara Savoldo, Carlos Almeida Ramos, +13 authors, Gianpietro Dotti.
J Clin Invest, 2011 May 05; 121(5). PMID: 21540550    Free PMC article.
Highly Cited.
Effective Targeting of TAG72+ Peritoneal Ovarian Tumors via Regional Delivery of CAR-Engineered T Cells.
John P Murad, Anna K Kozlowska, +8 authors, Saul J Priceman.
Front Immunol, 2018 Dec 05; 9. PMID: 30510550    Free PMC article.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Exclusion of T Cells From Pancreatic Carcinomas in Mice Is Regulated by Ly6C(low) F4/80(+) Extratumoral Macrophages.
Gregory L Beatty, Rafael Winograd, +8 authors, Robert H Vonderheide.
Gastroenterology, 2015 Apr 19; 149(1). PMID: 25888329    Free PMC article.
Highly Cited.
Alpharetroviral vectors: from a cancer-causing agent to a useful tool for human gene therapy.
Julia D Suerth, Verena Labenski, Axel Schambach.
Viruses, 2014 Dec 10; 6(12). PMID: 25490763    Free PMC article.
Review.
Mesothelin is a target of chimeric antigen receptor T cells for treating gastric cancer.
Jiang Lv, Ruocong Zhao, +24 authors, Peng Li.
J Hematol Oncol, 2019 Feb 20; 12(1). PMID: 30777106    Free PMC article.
Expanding the Therapeutic Window for CAR T Cell Therapy in Solid Tumors: The Knowns and Unknowns of CAR T Cell Biology.
Keisuke Watanabe, Shunichiro Kuramitsu, Avery D Posey, Carl H June.
Front Immunol, 2018 Nov 13; 9. PMID: 30416506    Free PMC article.
Highly Cited. Review.
MUC1 expression in primary and metastatic pancreatic cancer cells for in vitro treatment by (213)Bi-C595 radioimmunoconjugate.
C F Qu, Y Li, +8 authors, B J Allen.
Br J Cancer, 2004 Dec 16; 91(12). PMID: 15599383    Free PMC article.
Correction: Identification of neoepitopes recognized by tumor-infiltrating lymphocytes (TILs) from patients with glioma.
Davide Valentini, Martin Rao, +8 authors, Markus Maeurer.
Oncotarget, 2019 Jan 08; 9(95). PMID: 30613370    Free PMC article.
Safety, tumor trafficking and immunogenicity of chimeric antigen receptor (CAR)-T cells specific for TAG-72 in colorectal cancer.
Kristen M Hege, Emily K Bergsland, +7 authors, Stephen A Sherwin.
J Immunother Cancer, 2017 Mar 28; 5. PMID: 28344808    Free PMC article.
Highly Cited.
Chimeric Antigen Receptor-Modified T Cells Redirected to EphA2 for the Immunotherapy of Non-Small Cell Lung Cancer.
Ning Li, Shaohui Liu, +7 authors, Qiong Zhao.
Transl Oncol, 2017 Nov 14; 11(1). PMID: 29132013    Free PMC article.
ROR1-CAR T cells are effective against lung and breast cancer in advanced microphysiologic 3D tumor models.
Lars Wallstabe, Claudia Göttlich, +8 authors, Michael Hudecek.
JCI Insight, 2019 Aug 16; 4(18). PMID: 31415244    Free PMC article.
Control of triple-negative breast cancer using ex vivo self-enriched, costimulated NKG2D CAR T cells.
Yali Han, Wei Xie, De-Gang Song, Daniel J Powell.
J Hematol Oncol, 2018 Jul 08; 11(1). PMID: 29980239    Free PMC article.
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.
Z Eshhar, T Waks, G Gross, D G Schindler.
Proc Natl Acad Sci U S A, 1993 Jan 15; 90(2). PMID: 8421711    Free PMC article.
Highly Cited.
The siRNA-mediated downregulation of PD-1 alone or simultaneously with CTLA-4 shows enhanced in vitro CAR-T-cell functionality for further clinical development towards the potential use in immunotherapy of melanoma.
Bianca Simon, Dennis C Harrer, +4 authors, Ugur Uslu.
Exp Dermatol, 2018 Apr 29; 27(7). PMID: 29704887
Clinical investigation of CAR T cells for solid tumors: Lessons learned and future directions.
Stephen J Bagley, Donald M O'Rourke.
Pharmacol Ther, 2019 Oct 20; 205. PMID: 31629009
Review.
4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies.
Syam Tammana, Xin Huang, +7 authors, Xianzheng Zhou.
Hum Gene Ther, 2009 Sep 02; 21(1). PMID: 19719389    Free PMC article.
Use of chimeric antigen receptor NK-92 cells to target mesothelin in ovarian cancer.
Bihui Cao, Manting Liu, +12 authors, Zhenfeng Zhang.
Biochem Biophys Res Commun, 2020 Jan 26; 524(1). PMID: 31980173
Targeting and suppression of HER3-positive breast cancer by T lymphocytes expressing a heregulin chimeric antigen receptor.
Bai-Le Zuo, Bo Yan, +4 authors, Lin-Tao Jia.
Cancer Immunol Immunother, 2017 Nov 12; 67(3). PMID: 29127433
Modification of cytokine-induced killer cells with folate receptor alpha (FRα)-specific chimeric antigen receptors enhances their antitumor immunity toward FRα-positive ovarian cancers.
Shuguang Zuo, Yuqing Wen, +4 authors, Kanda Fu.
Mol Immunol, 2017 Apr 01; 85. PMID: 28360017
Phase I Trial of Anti-PSMA Designer CAR-T Cells in Prostate Cancer: Possible Role for Interacting Interleukin 2-T Cell Pharmacodynamics as a Determinant of Clinical Response.
Richard P Junghans, Qiangzhong Ma, +8 authors, Stephen I Cohen.
Prostate, 2016 Jun 22; 76(14). PMID: 27324746
The basic principles of chimeric antigen receptor design.
Michel Sadelain, Renier Brentjens, Isabelle Rivière.
Cancer Discov, 2013 Apr 04; 3(4). PMID: 23550147    Free PMC article.
Highly Cited. Review.
Bispecific T-Cell Redirection versus Chimeric Antigen Receptor (CAR)-T Cells as Approaches to Kill Cancer Cells.
William R Strohl, Michael Naso.
Antibodies (Basel), 2019 Sep 24; 8(3). PMID: 31544847    Free PMC article.
Review.
Successful eradication of established peritoneal ovarian tumors in SCID-Beige mice following adoptive transfer of T cells genetically targeted to the MUC16 antigen.
Alena A Chekmasova, Thapi D Rao, +4 authors, Renier J Brentjens.
Clin Cancer Res, 2010 Jul 16; 16(14). PMID: 20628030    Free PMC article.
Chimeric antigen receptor T cell (CAR-T) immunotherapy for solid tumors: lessons learned and strategies for moving forward.
Jian Li, Wenwen Li, +3 authors, Qi Zhao.
J Hematol Oncol, 2018 Feb 13; 11(1). PMID: 29433552    Free PMC article.
Highly Cited. Review.
Killing Mechanisms of Chimeric Antigen Receptor (CAR) T Cells.
Mohamed-Reda Benmebarek, Clara Helke Karches, +3 authors, Sebastian Kobold.
Int J Mol Sci, 2019 Mar 17; 20(6). PMID: 30875739    Free PMC article.
Highly Cited. Review.
Antitumor activity of NKG2D CAR-T cells against human colorectal cancer cells in vitro and in vivo.
Xinna Deng, Fei Gao, +7 authors, Jianhui Cai.
Am J Cancer Res, 2019 Jun 21; 9(5). PMID: 31218103    Free PMC article.
Micromolar affinity CAR T cells to ICAM-1 achieves rapid tumor elimination while avoiding systemic toxicity.
Spencer Park, Enda Shevlin, +5 authors, Moonsoo M Jin.
Sci Rep, 2017 Nov 01; 7(1). PMID: 29085043    Free PMC article.
Carbonic anhydrase IX as an imaging and therapeutic target for tumors and metastases.
Narges K Tafreshi, Mark C Lloyd, +2 authors, David L Morse.
Subcell Biochem, 2013 Oct 23; 75. PMID: 24146382    Free PMC article.
Review.
Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity.
Stefani Spranger, Riyue Bao, Thomas F Gajewski.
Nature, 2015 May 15; 523(7559). PMID: 25970248
Highly Cited.
Any closer to successful therapy of multiple myeloma? CAR-T cell is a good reason for optimism.
Faroogh Marofi, Safa Tahmasebi, +10 authors, Farhad Motavalli Khiavi.
Stem Cell Res Ther, 2021 Mar 31; 12(1). PMID: 33781320    Free PMC article.
Review.
Polysaccharide-based nanomedicines for cancer immunotherapy: A review.
Yujun Zeng, Yufan Xiang, +6 authors, Kui Luo.
Bioact Mater, 2021 Apr 06; 6(10). PMID: 33817416    Free PMC article.
Review.
Chimeric Antigen Receptor Design and Efficacy in Ovarian Cancer Treatment.
Katarzyna M Terlikowska, Bożena Dobrzycka, Sławomir J Terlikowski.
Int J Mol Sci, 2021 Apr 04; 22(7). PMID: 33800608    Free PMC article.
Review.
The Future of Cancer Diagnosis, Treatment and Surveillance: A Systemic Review on Immunotherapy and Immuno-PET Radiotracers.
Virginia Liberini, Riccardo Laudicella, +5 authors, Désirée Deandreis.
Molecules, 2021 May 01; 26(8). PMID: 33920423    Free PMC article.
Systematic Review.
Tissue-Resident and Recruited Macrophages in Primary Tumor and Metastatic Microenvironments: Potential Targets in Cancer Therapy.
Tiziana Cotechini, Aline Atallah, Arielle Grossman.
Cells, 2021 May 01; 10(4). PMID: 33924237    Free PMC article.
Review.
CAR-engineered NK cells; a promising therapeutic option for treatment of hematological malignancies.
Faroogh Marofi, Marwan Mahmood Saleh, +13 authors, Farhad Motavalli Khiavi.
Stem Cell Res Ther, 2021 Jul 04; 12(1). PMID: 34215336    Free PMC article.
Review.
The Evolution of Cancer Immunotherapy.
Meshaal Khan, Ajay V Maker, Shikha Jain.
Vaccines (Basel), 2021 Jul 03; 9(6). PMID: 34200997    Free PMC article.
Review.
CAR-T Cell Therapy: Mechanism, Management, and Mitigation of Inflammatory Toxicities.
Joseph W Fischer, Nirjal Bhattarai.
Front Immunol, 2021 Jul 06; 12. PMID: 34220853    Free PMC article.
Review.
A deep insight into CRISPR/Cas9 application in CAR-T cell-based tumor immunotherapies.
Ehsan Razeghian, Mahyuddin K M Nasution, +12 authors, Farhad Motavalli Khiavi.
Stem Cell Res Ther, 2021 Jul 30; 12(1). PMID: 34321099    Free PMC article.
Review.
Novel CAR T therapy is a ray of hope in the treatment of seriously ill AML patients.
Faroogh Marofi, Heshu Sulaiman Rahman, +13 authors, Mostafa Jarahian.
Stem Cell Res Ther, 2021 Aug 21; 12(1). PMID: 34412685    Free PMC article.
Review.
Linking Immunity with Genomics in Sarcomas: Is Genomic Complexity an Immunogenic Trigger?
Siddh van Oost, Debora M Meijer, +2 authors, Noel F C C de Miranda.
Biomedicines, 2021 Aug 28; 9(8). PMID: 34440251    Free PMC article.
Review.
Recent advances in antibody-based immunotherapy strategies for COVID-19.
Abdolreza Esmaeilzadeh, Samaneh Rostami, +2 authors, Majid Ahmadi.
J Cell Biochem, 2021 Jun 24; 122(10). PMID: 34160093    Free PMC article.
Review.
Cytolytic Activity of CAR T Cells and Maintenance of Their CD4+ Subset Is Critical for Optimal Antitumor Activity in Preclinical Solid Tumor Models.
Marianna Csaplár, János Szöllősi, +2 authors, Árpád Szöőr.
Cancers (Basel), 2021 Sep 11; 13(17). PMID: 34503109    Free PMC article.
Mesenchymal Stem/Stromal Cells as a Vehicle for Cytokine Delivery: An Emerging Approach for Tumor Immunotherapy.
Ehsan Razeghian, Ria Margiana, +6 authors, Mostafa Jarahian.
Front Med (Lausanne), 2021 Sep 14; 8. PMID: 34513882    Free PMC article.
Review.
Oncolytic viruses for triple negative breast cancer and beyond.
Shengye Jin, Qin Wang, +2 authors, Shouping Xu.
Biomark Res, 2021 Sep 27; 9(1). PMID: 34563270    Free PMC article.
Review.
A Novel Treatment for Ewing's Sarcoma: Chimeric Antigen Receptor-T Cell Therapy.
Zili Lin, Ziyi Wu, Wei Luo.
Front Immunol, 2021 Sep 28; 12. PMID: 34566963    Free PMC article.
Review.
Heterogeneity in Pancreatic Cancer Fibroblasts-TGFβ as a Master Regulator?
Dale M Watt, Jennifer P Morton.
Cancers (Basel), 2021 Oct 14; 13(19). PMID: 34638468    Free PMC article.
Review.
Improving CAR T-Cell Persistence.
Violena Pietrobon, Lauren Anne Todd, +3 authors, Francesco Marincola.
Int J Mol Sci, 2021 Oct 14; 22(19). PMID: 34639168    Free PMC article.
Review.
Implications of Antigen Selection on T Cell-Based Immunotherapy.
Faye A Camp, Jill E Slansky.
Pharmaceuticals (Basel), 2021 Oct 24; 14(10). PMID: 34681217    Free PMC article.
Review.
Tandem CAR-T cells targeting FOLR1 and MSLN enhance the antitumor effects in ovarian cancer.
Zhen Liang, Jiao Dong, +11 authors, Zhi-Qing Liang.
Int J Biol Sci, 2021 Nov 23; 17(15). PMID: 34803504    Free PMC article.
Facing CAR T Cell Challenges on the Deadliest Paediatric Brain Tumours.
Cristina Ferreras, Lucía Fernández, +5 authors, Antonio Pérez-Martínez.
Cells, 2021 Nov 28; 10(11). PMID: 34831165    Free PMC article.
Review.
T Cell Engaging Immunotherapies, Highlighting Chimeric Antigen Receptor (CAR) T Cell Therapy.
Elien De Bousser, Nico Callewaert, Nele Festjens.
Cancers (Basel), 2021 Dec 11; 13(23). PMID: 34885176    Free PMC article.
Review.
Myeloid Immune Cells CARrying a New Weapon Against Cancer.
Rodrigo Nalio Ramos, Samuel Campanelli Freitas Couto, +5 authors, Vanderson Rocha.
Front Cell Dev Biol, 2022 Jan 04; 9. PMID: 34977027    Free PMC article.
Review.
An engineered oncolytic vaccinia virus encoding a single-chain variable fragment against TIGIT induces effective antitumor immunity and synergizes with PD-1 or LAG-3 blockade.
Shuguang Zuo, Min Wei, +7 authors, Jiwu Wei.
J Immunother Cancer, 2021 Dec 25; 9(12). PMID: 34949694    Free PMC article.
Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor (CAR) for tumor immunotherapy; recent progress.
Hendrik Setia Budi, Firdaus Nuri Ahmad, +6 authors, Faroogh Marofi.
Stem Cell Res Ther, 2022 Jan 31; 13(1). PMID: 35093187    Free PMC article.
Review.
Delivery of CD47 blocker SIRPα-Fc by CAR-T cells enhances antitumor efficacy.
Huanpeng Chen, Yuying Yang, +6 authors, Zhaofeng Huang.
J Immunother Cancer, 2022 Feb 04; 10(2). PMID: 35110357    Free PMC article.
Current Immunotherapeutic Approaches for Malignant Gliomas.
Myung-Hoon Han, Choong Hyun Kim.
Brain Tumor Res Treat, 2022 Feb 05; 10(1). PMID: 35118842    Free PMC article.
Review.
Nanoparticles for generating antigen-specific T cells for immunotherapy.
Savannah E Est-Witte, Natalie K Livingston, +2 authors, Jonathan P Schneck.
Semin Immunol, 2021 Dec 20; 56. PMID: 34922816    Free PMC article.
Review.
Clinically relevant T cell expansion media activate distinct metabolic programs uncoupled from cellular function.
Sarah MacPherson, Sarah Keyes, +11 authors, Julian J Lum.
Mol Ther Methods Clin Dev, 2022 Mar 15; 24. PMID: 35284590    Free PMC article.
Effect of CRISPR/Cas9-Edited PD-1/PD-L1 on Tumor Immunity and Immunotherapy.
Yanxin Xu, Chen Chen, +2 authors, Zhenqiang Sun.
Front Immunol, 2022 Mar 19; 13. PMID: 35300341    Free PMC article.
Review.
Improving CAR-T immunotherapy: Overcoming the challenges of T cell exhaustion.
Diana Gumber, Leo D Wang.
EBioMedicine, 2022 Mar 19; 77. PMID: 35301179    Free PMC article.
Review.
Using the Power of Junctional Adhesion Molecules Combined with the Target of CAR-T to Inhibit Cancer Proliferation, Metastasis and Eradicate Tumors.
Christopher Mendoza, Dario Mizrachi.
Biomedicines, 2022 Feb 26; 10(2). PMID: 35203590    Free PMC article.
CAR race to cancer immunotherapy: from CAR T, CAR NK to CAR macrophage therapy.
Kevin Pan, Hizra Farrukh, +3 authors, Zheng Zhu.
J Exp Clin Cancer Res, 2022 Apr 02; 41(1). PMID: 35361234    Free PMC article.
Review.
Taking Lessons from CAR-T Cells and Going Beyond: Tailoring Design and Signaling for CAR-NK Cells in Cancer Therapy.
Katharina Eva Ruppel, Stephan Fricke, Ulrike Köhl, Dominik Schmiedel.
Front Immunol, 2022 Apr 05; 13. PMID: 35371071    Free PMC article.
Review.
Tumor Microenvironment of Hepatocellular Carcinoma: Challenges and Opportunities for New Treatment Options.
Zuzanna Sas, Ewa Cendrowicz, Isabel Weinhäuser, Tomasz P Rygiel.
Int J Mol Sci, 2022 Apr 13; 23(7). PMID: 35409139    Free PMC article.
Review.
Transcriptional determinants of cancer immunotherapy response and resistance.
Romi Gupta, Amitkumar Mehta, Narendra Wajapeyee.
Trends Cancer, 2022 Feb 08; 8(5). PMID: 35125331    Free PMC article.
Review.
CAR-T Cells/-NK Cells in Cancer Immunotherapy and the Potential of MSC to Enhance Its Efficacy: A Review.
Ler Yie Chan, Sylvia Annabel Dass, +3 authors, Fazlina Nordin.
Biomedicines, 2022 Apr 24; 10(4). PMID: 35453554    Free PMC article.
Review.
CAR-T Cells for the Treatment of Lung Cancer.
Luisa Chocarro, Hugo Arasanz, +13 authors, David Escors.
Life (Basel), 2022 Apr 24; 12(4). PMID: 35455052    Free PMC article.
Review.
Targeting CD10 on B-Cell Leukemia Using the Universal CAR T-Cell Platform (UniCAR).
Nicola Mitwasi, Claudia Arndt, +8 authors, Anja Feldmann.
Int J Mol Sci, 2022 May 15; 23(9). PMID: 35563312    Free PMC article.
Chimeric anti-GPC3 sFv-CD3ε receptor-modified T cells with IL7 co-expression for the treatment of solid tumors.
Yansha Sun, Yiwei Dong, +6 authors, Zonghai Li.
Mol Ther Oncolytics, 2022 May 17; 25. PMID: 35572194    Free PMC article.
Engineering the next generation of cell-based therapeutics.
Caleb J Bashor, Isaac B Hilton, +2 authors, Omid Veiseh.
Nat Rev Drug Discov, 2022 Jun 01;. PMID: 35637318
Review.
Exploring chitosan-shelled nanobubbles to improve HER2 + immunotherapy via dendritic cell targeting.
Monica Argenziano, Sergio Occhipinti, +5 authors, Roberta Cavalli.
Drug Deliv Transl Res, 2022 Jun 08;. PMID: 35672651