Augmenting the landscape of chimeric antigen receptor T-cell therapy

References

• Sadelain M, Brentjens R, Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013 Apr;3(4):388–398. doi: 10.1158/2159-8290.CD-12-0548
   PubMed Web of Science ®Google Scholar
• Eshhar Z, Waks T, Gross G, et al. 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. Proc Natl Acad Sci USA. 1993;90(2):720–724. doi: 10.1073/pnas.90.2.720
   PubMed Web of Science ®Google Scholar
• Majzner RG, Mackall CL. Clinical lessons learned from the first leg of the CAR T cell journey. Nat Med. 2019;25:1341–1355. doi: 10.1038/s41591-019-0564-6
   PubMed Web of Science ®Google Scholar
• Melief CJM. Tumor eradication by adoptive transfer of cytotoxic T lymphocytes. Adv Cancer Res. 1992;58:143–175. doi: 10.1016/s0065-230x(08)60294-8
   PubMed Web of Science ®Google Scholar
• Benmebarek MR, Karches CH, Cadilha BL, et al. Killing mechanisms of chimeric antigen receptor (CAR) T cells. Int J Mol Sci. 2019;20(6). doi: 10.3390/ijms20061283
   PubMed Web of Science ®Google Scholar
• Jensen MC, Riddell SR. Designing chimeric antigen receptors to effectively and safely target tumors. Curr Opin Immunol. 2015;33:9–15. doi: 10.1016/j.coi.2015.01.002
   PubMed Web of Science ®Google Scholar
• Tokarew N, Ogonek J, Endres S, et al. Teaching an old dog new tricks: next-generation CAR T cells. Br J Cancer. 2019;120:26–37. doi: 10.1038/s41416-018-0325-1
   PubMed Web of Science ®Google Scholar
• Espie D, Donnadieu E. New insights into CAR T cell-mediated killing of tumor cells. Front Immunol. 2022 15;13:1016208. doi: 10.3389/fimmu.2022.1016208
   PubMed Web of Science ®Google Scholar
• Kravets VG, Zhang Y, Sun H. Chimeric-antigen-receptor (CAR) T cells and the factors influencing their therapeutic efficacy. J Immunol Res Ther. 2017;2(1):100–113.
   PubMedGoogle Scholar
• Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor–modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368:1509–1518. doi: 10.1056/NEJMoa1215134
   PubMed Web of Science ®Google Scholar
• Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor–modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725–733. doi: 10.1056/nejmoa1103849
   PubMed Web of Science ®Google Scholar
• Dagar G, Gupta A, Masoodi T, et al. Harnessing the potential of CAR-T cell therapy: progress, challenges, and future directions in hematological and solid tumor treatments. J Transl Med. 2023;21(1):449. doi: 10.1186/s12967-023-04292-3
   PubMed Web of Science ®Google Scholar
• Novartis five-year Kymriah® data show durable remission and long-term survival maintained in children and young adults with advanced B-cell ALL | Novartis [Internet]. [cited 2024 Jun 11]. Available from: https://www.novartis.com/news/media-releases/novartis-five-year-kymriah-data-show-durable-remission-and-long-term-survival-maintained-children-and-young-adults-advanced-b-cell-all
   Google Scholar
• YESCARTA® (axicabtagene ciloleucel) efficacy information | HCP [Internet]. [cited 2024 Jun 11]. Available from: https://www.yescartahcp.com/3l-large-b-cell-lymphoma/efficacy
   Google Scholar
• BristoL Myers Squibb - Bristol Myers Squibb’s Breyanzi (lisocabtagene maraleucel) delivers deep and durable responses in relapsed or refractory follicular lymphoma and mantle cell lymphoma in TRANSCEND clinical trials presented at ICML 2023 [Internet]. [cited 2024 Jun 11]. Available from: https://news.bms.com/news/details/2023/Bristol-Myers-Squibbs-Breyanzi-lisocabtagene-maraleucel-Delivers-Deep-and-Durable-Responses-in-Relapsed-or-Refractory-Follicular-Lymphoma-and-Mantle-Cell-Lymphoma-in-TRANSCEND-Clinical-Trials-Presented-at-ICML-2023/default.aspx
   Google Scholar
• TECARTUS® Efficacy Response Data for R/R B-cell ALL [Internet]. [cited 2024 Jun 11]. Available from: https://www.tecartushcp.com/car-t-cell-therapy/acute-lymphoblastic-leukemia/response
   Google Scholar
• Bristol Myers Squibb - Bristol Myers Squibb’s Abecma (idecabtagene vicleucel) becomes first CAR T cell therapy approved in the European Union in earlier lines for triple-class exposed relapsed and refractory multiple myeloma [Internet]. [cited 2024 Jun 11]. Available from: https://news.bms.com/news/details/2024/Bristol-Myers-Squibbs-Abecma-idecabtagene-vicleucel-Becomes-First-CAR-T-Cell-Therapy-Approved-in-the-European-Union-in-Earlier-Lines-for-Triple-Class-Exposed-Relapsed-and-Refractory-Multiple-Myeloma/
   Google Scholar
• About CARVYKTI® (ciltacabtagene autoleucel) [Internet]. [cited 2024 Jun 11]. Available from: https://www.carvykti.com/about-carvykti/
   Google Scholar
• Cao X, Li W, Yu Y, et al. China enters CAR-T cell therapy era. Innov (Camb). 2021 16;3(1):100197. doi: 10.1016/j.xinn.2021.100197
   PubMedGoogle Scholar
• Keam SJ. Equecabtagene autoleucel: first approval. Mol Diagn Ther. 2023;27(6):781–787. doi: 10.1007/s40291-023-00673-y
   PubMed Web of Science ®Google Scholar
• ImmunoACT - India’s pioneer in cell & gene therapies [Internet]. [cited 2024 Jun 11]. Available from: https://www.immunoact.com/
   Google Scholar
• Siegel RL, Miller KD, Wagle NS, et al. Cancer statistics. CA Cancer J Clin. 2023 Jan;73(1):17–48. doi: 10.3322/caac.21763
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Dudley ME, Feldman SA, et al. 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. 2012;119:2709–2720. doi: 10.1182/blood-2011-10-384388
   PubMed Web of Science ®Google Scholar
• Ahmad A, Uddin S, Steinho M. CAR-T cell therapies: an overview of clinical studies supporting their approved use against acute lymphoblastic leukemia and large b-cell lymphomas. Int J Mol Sci. 2020 May 30;21(11):3906. doi: 10.3390/ijms21113906
   PubMed Web of Science ®Google Scholar
• Guzman G, Reed MR, Bielamowicz K, et al. CAR-T therapies in solid tumors: opportunities and challenges. Curr Oncol Rep. 2023;25:479–489. doi: 10.1007/s11912-023-01380-x
   PubMed Web of Science ®Google Scholar
• Daei Sorkhabi A, Mohamed Khosroshahi L, Sarkesh A, et al. The current landscape of CAR T-cell therapy for solid tumors: mechanisms, research progress, challenges, and counterstrategies;14. Front Immunol. 2023 Mar 20;14:1113882. doi: 10.3389/fimmu.2023.1113882
   PubMed Web of Science ®Google Scholar
• Home | ClinicalTrials.gov [Internet]. [cited 2024 Jun 11]. Available from: https://www.clinicaltrials.gov/
   Google Scholar
• Patel U, Abernathy J, Savani BN, et al. CAR T cell therapy in solid tumors: a review of current clinical trials. EJHaem. 2021 Dec 7;3(Suppl 1):24–31. doi: 10.1002/jha2.356
   PubMedGoogle Scholar
• CAR T-cell therapy market size & growth insights | 2032 [Internet]. [cited 2024 Jun 11]. Available from: https://www.alliedmarketresearch.com/car-t-cell-therapy-market-A16971
   Google Scholar
• Wang X, Rivière I. Clinical manufacturing of CAR T cells: foundation of a promising therapy. Mol Ther Oncolytics. 2016 Jun 15;3:16015. doi: 10.1038/mto.2016.15
   PubMed Web of Science ®Google Scholar
• Vormittag P, Gunn R, Ghorashian S, et al. Review: a guide to manufacturing CAR T cell therapies. Curr Opin Biotechnol. 2018 Oct;53:164–181. doi: 10.1016/j.copbio.2018.01.025
   PubMed Web of Science ®Google Scholar
• Zhang Y, Iii ROW, Tucker HO. Formulation strategies in immunotherapeutic pharmaceutical products. World J Clin Oncol. 2020 May 24;11(5):275–282. doi: 10.5306/wjco.v11.i5.275
   PubMed Web of Science ®Google Scholar
• Jackson Z, Roe A, Sharma AA, et al. Automated manufacture of autologous CD19 CAR-T cells for treatment of non-Hodgkin lymphoma. Front Immunol. 2020 Aug 7;11:1941. doi: 10.3389/fimmu.2020.01941
   PubMed Web of Science ®Google Scholar
• Mock U, Nickolay L, Philip B, et al. Automated manufacturing of chimeric antigen receptor T cells for adoptive immunotherapy using CliniMACS prodigy. Cytotherapy. 2016;18:1002–1011. doi: 10.1016/j.jcyt.2016.05.009
   PubMed Web of Science ®Google Scholar
• Blache U, Popp G, Dünkel A, et al. Potential solutions for manufacture of CAR T cells in cancer immunotherapy. Nat Commun. 2022;13:5225. doi: 10.1038/s41467-022-32866-0
   PubMed Web of Science ®Google Scholar
• Lock D, Monjezi R, Brandes C, et al. Automated, scaled, transposon-based production of CAR T cells. J Immunother Cancer. 2022 Sep;10(9):e005189. doi: 10.1136/jitc-2022-005189
   PubMed Web of Science ®Google Scholar
• Gil L, Grajek M. Artificial intelligence and chimeric antigen receptor T-cell therapy. 2022. Acta Haematol Pol. 2022;53(3):176–179. doi: 10.5603/AHP.a2022.0019
   Google Scholar
• Hort S, Herbst L, Bäckel N, et al. Toward rapid, widely available autologous CAR-T cell therapy – artificial intelligence and automation enabling the smart manufacturing hospital. Front Med. 2022 Jun 6;9:913287. doi: 10.3389/fmed.2022.913287
   Web of Science ®Google Scholar
• Zhang P, Zhang G, Wan X. Challenges and new technologies in adoptive cell therapy. J Hematol Oncol. 2023 Aug 18;16(1):97. doi: 10.1186/s13045-023-01492-8
   PubMed Web of Science ®Google Scholar
• Fda, Cber. Testing of retroviral vector-based human gene therapy products for replication competent retrovirus during product manufacture and patient follow-up; guidance for industry. 2020 [cited 2024 Jun 11]. Available from: https://www.fda.gov/vaccines-blood-biologics/guidance-compliance-
   Google Scholar
• Volokhov DV, Graham LJ, Brorson KA, et al. Mycoplasma testing of cell substrates and biologics: review of alternative non-microbiological techniques. Mol Cell Probes. 2011;25:69–77. doi: 10.1016/j.mcp.2011.01.002
   PubMed Web of Science ®Google Scholar
• Li Y, Huo Y, Yu L, et al. Quality control and nonclinical research on CAR-T cell products: general principles and key issues. Eng. 2019;5:122–131. doi: 10.1016/j.eng.2018.12.003
   Google Scholar
• Watanabe N, Mo F, McKenna MK. Impact of manufacturing procedures on CAR T cell functionality. Front Immunol. 2022 Apr 13;13:876339. doi: 10.3389/fimmu.2022.876339
   PubMed Web of Science ®Google Scholar
• Gajra A, Zalenski A, Sannareddy A, et al. Barriers to chimeric antigen receptor T-Cell (CAR-T) therapies in clinical practice. Pharmaceut Med. 2022;36:163–171. doi: 10.1007/s40290-022-00428-w
   PubMed Web of Science ®Google Scholar
• Cliff ERS, Kelkar AH, Russler-Germain DA, et al. High cost of chimeric antigen receptor T-cells: challenges and solutions. Am Soc Clin Oncol Educ Book. 2023 Jun;43:e397912. doi: 10.1200/EDBK_397912
   PubMedGoogle Scholar
• De Luca M, Cossu G. Cost and availability of novel cell and gene therapies. EMBO Rep. 2023 Feb 6;24(2):e56661. doi: 10.15252/embr.202256661
   PubMed Web of Science ®Google Scholar
• Whittington MD, Ollendorf DA, Campbell JD. Accounting for all costs in the total cost of chimeric antigen receptor T-cell immunotherapy. JAMA Oncol. 2018 Dec 1;4(12):1784–1785. doi: 10.1001/jamaoncol.2018.4625
   PubMed Web of Science ®Google Scholar
• Jagannath S, Joseph N, Crivera C, et al. Total car-T cost of care beyond the price of car-T cell therapy in patients with multiple myeloma. Blood. 2021;138(Supplement 1):4964–4964. doi: 10.1182/blood-2021-153438
   Google Scholar
• Thielen FW, Heine RJSD, van den Berg S, et al. Towards sustainability and affordability of expensive cell and gene therapies? Applying a cost-based pricing model to estimate prices for libmeldy and zolgensma. Cytotherapy. 2022;24:1245–1258. doi: 10.1016/j.jcyt.2022.09.002
   PubMed Web of Science ®Google Scholar
• Spink K, Steinsapir A. The long road to affordability: a cost of goods analysis for an autologous CAR-T process. Cell Gene Ther Insights. 2018;4:1105–1116. doi: 10.18609/cgti.2018.108
   Google Scholar
• Kilgore KM, Mohammadi I, Schroeder A, et al. Medicare patients receiving chimeric antigen receptor T-cell therapy for non-Hodgkin lymphoma: a first real-world look at patient characteristics, healthcare utilization and costs. Blood. 2019;134(Supplement_1):793. doi: 10.1182/blood-2019-124364
   PubMedGoogle Scholar
• Norelli M, Camisa B, Barbiera G, et al. Monocyte-derived IL-1 and IL-6 are differentially required for cytokine-release syndrome and neurotoxicity due to CAR T cells. Nat Med. 2018 Jun;24(6):739–748. doi: 10.1038/s41591-018-0036-4
   PubMed Web of Science ®Google Scholar
• Wang Z, Han W. Biomarkers of cytokine release syndrome and neurotoxicity related to CAR-T cell therapy. Biomark Res. 2018 Jan 22;6:4. doi: 10.1186/s40364-018-0116-0
   PubMed Web of Science ®Google Scholar
• Turtle CJ, Hanafi LA, Berger C, et al. CD19 CAR-T cells of defined CD4+: CD8+ composition in adult B cell ALL patients. J Clin Invest. 2016 Jun 1;126(6):2123–2138. doi: 10.1172/JCI85309
   PubMed Web of Science ®Google Scholar
• Jones SA, Jenkins BJ. Recent insights into targeting the IL-6 cytokine family in inflammatory diseases and cancer. Nat Rev Immunol. 2018 Dec;18(12):773–789. doi: 10.1038/s41577-018-0066-7
   PubMed Web of Science ®Google Scholar
• Kankeu Fonkoua LA, Sirpilla O, Sakemura R, et al. CAR T cell therapy and the tumor microenvironment: current challenges and opportunities. Mol Ther Oncolytics. 2022;25:69–77. doi: 10.1016/j.omto.2022.03.009
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013 Nov;19(11):1423–1437. doi: 10.1038/nm.3394
   PubMed Web of Science ®Google Scholar
• Yan T, Zhu L, Chen J. Current advances and challenges in CAR T-Cell therapy for solid tumors: tumor-associated antigens and the tumor microenvironment. Exp Hematol Oncol. 2023 Jan 27;12(1):14. doi: 10.1186/s40164-023-00373-7
   PubMed Web of Science ®Google Scholar
• Lyu L, Feng Y, Chen X, et al. The global chimeric antigen receptor T (CAR-T) cell therapy patent landscape. Nat Biotechnol. 2020;38:1387–1394. doi: 10.1038/s41587-020-00749-8
   PubMed Web of Science ®Google Scholar
• Le RQ, Li L, Yuan W, et al. FDA approval summary: tocilizumab for treatment of chimeric antigen receptor T cell-induced severe or life-threatening cytokine release syndrome. Oncology. 2018 Aug;23(8):943–947. doi: 10.1634/theoncologist.2018-0028
   Google Scholar
• Le RQ, Li L, Yuan W, et al. Tocilizumab for treatment of severe or life-threatening chimeric antigen receptor T cell-induced cytokine release syndrome—FDA approval summary/biol blood marrow transplant. Biol Blood Marrow Transplant. 2018;24(3):S119–S290. doi: 10.1016/j.bbmt.2017.12.104
   PubMed Web of Science ®Google Scholar
• Liu S, Deng B, Yin Z, et al. Corticosteroids do not influence the efficacy and kinetics of CAR-T cells for B-cell acute lymphoblastic leukemia. Blood Cancer J. 2020 Feb 6;10(2):15. doi: 10.1038/s41408-020-0280-y
   PubMed Web of Science ®Google Scholar
• Brattås MK, Reikvam H, Tvedt THA, et al. Dasatinib as an investigational drug for the treatment of Philadelphia chromosome-positive acute lymphoblastic leukemia in adults. Expert Opin Investig Drugs. 2019 May;28(5):411–420. doi: 10.1080/13543784.2019.1597052
   PubMed Web of Science ®Google Scholar
• Li AM, Hucks GE, Dinofia AM, et al. Checkpoint inhibitors augment CD19-directed chimeric antigen receptor (CAR) T cell therapy in relapsed B-cell acute lymphoblastic leukemia. Blood. 2018;132:556–556. doi: 10.1182/blood-2018-99-112572
   Web of Science ®Google Scholar
• Fedorov VD, Themeli M, Sadelain M. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci Transl Med. 2013 Dec 11;5(215):215ra172. doi: 10.1126/scitranslmed.3006597
   PubMed Web of Science ®Google Scholar
• Dimitri A, Herbst F, Fraietta JA. Engineering the next-generation of CAR T-cells with CRISPR-Cas9 gene editing. Mol Cancer. 2022 Mar 18;21(1):78. doi: 10.1186/s12943-022-01559-z
   PubMed Web of Science ®Google Scholar
• Zhou X, Dotti G, Krance RA, et al. Inducible caspase-9 suicide gene controls adverse effects from alloreplete T cells after haploidentical stem cell transplantation. Blood. 2015 Jun 25;125(26):4103–4113. doi: 10.1182/blood-2015-02-628354
   PubMed Web of Science ®Google Scholar
• Qin H, Ramakrishna S, Nguyen S, et al. Preclinical development of bivalent chimeric antigen receptors targeting both CD19 and CD22. Mol Ther Oncolytics. 2018 Nov 6;11:127–137. doi: 10.1016/j.omto.2018.10.006
   PubMed Web of Science ®Google Scholar
• Martyniszyn A, Krahl AC, André MC, et al. CD20-CD19 bispecific CAR T cells for the treatment of B-cell malignancies. Hum Gene Ther. 2017 Dec;28(12):1147–1157. doi: 10.1089/hum.2017.126
   PubMed Web of Science ®Google Scholar
• Ruella M, Barrett DM, Kenderian SS, et al. Dual CD19 and CD123 targeting prevents antigen-loss relapses after CD19-directed immunotherapies. J Clin Investig. 2016;126:3814–3826. doi: 10.1172/JCI87366
   PubMed Web of Science ®Google Scholar
• Fousek K, Watanabe J, George A, et al. Targeting primary Pre-B cell acute lymphoblastic leukemia and CD19-negative relapses using trivalent CAR T cells. Blood. 2017;130:4614–4614. doi: 10.1182/blood.V130
   Web of Science ®Google Scholar
• Edeline J, Houot R, Marabelle A, et al. CAR-T cells and BiTEs in solid tumors: challenges and perspectives. J Hematol Oncol. 2021 Apr 19;14(1):65. doi: 10.1186/s13045-021-01067-5
   PubMed Web of Science ®Google Scholar
• Slaney CY, Wang P, Darcy PK, et al. CARs versus BiTEs: a comparison between T cell–redirection strategies for cancer treatment. Cancer Discov. 2018;8:924–934. doi: 10.1158/2159-8290.CD-18-0297
   PubMed Web of Science ®Google Scholar
• BLINCYTO® (blinatumomab) for injection.
   Google Scholar
• Roybal KT, Rupp LJ, Morsut L, et al. Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell. 2016 Feb 11;164(4):770–779. doi: 10.1016/j.cell.2016.01.011
   PubMed Web of Science ®Google Scholar
• Chen YY. Increasing T cell versatility with SUPRA CARs. Cell. 2018 May 31;173(6):1316–1317. doi: 10.1016/j.cell.2018.05.030
   PubMed Web of Science ®Google Scholar
• Kueberuwa G, Kalaitsidou M, Cheadle E, et al. CD19 CAR T cells expressing IL-12 eradicate lymphoma in fully lymphoreplete mice through induction of host immunity. Mol Ther Oncolytics. 2018;8:41–51. doi: 10.1016/j.omto.2017.12.003
   PubMed Web of Science ®Google Scholar
• Chmielewski M, Abken H. TRUCKS, the fourth‐generation CAR T cells: current developments and clinical translation. Adv Cell Gene Ther. 2020;3. doi: 10.1002/acg2.84
   Google Scholar
• Lin H, Cheng J, Mu W, et al. Advances in Universal CAR-T cell therapy. Front Immunol. 2021 Oct 6;12:744823. doi: 10.3389/fimmu.2021.744823
   PubMedGoogle Scholar
• Hu Y, Zhou Y, Zhang M, et al. CRISPR/Cas9-engineered universal CD19/CD22 dual-targeted CAR-T cell therapy for relapsed/refractory B-cell acute lymphoblastic leukemia. Clin Cancer Res. 2021 May 15;27(10):2764–2772. doi: 10.1158/1078-0432.CCR-20-3863
   PubMed Web of Science ®Google Scholar
• Razeghian E, Nasution MKM, Rahman HS, et al. A deep insight into CRISPR/Cas9 application in CAR-T cell-based tumor immunotherapies. Stem Cell Res Ther. 2021 Jul 28;12(1):428. doi: 10.1186/s13287-021-02510-7
   PubMed Web of Science ®Google Scholar
• Xie G, Dong H, Liang Y, et al. CAR-NK cells: a promising cellular immunotherapy for cancer. EBioMedicine. 2020 Sep;59:102975. doi: 10.1016/j.ebiom.2020.102975
   PubMed Web of Science ®Google Scholar
• Klichinsky M, Ruella M, Shestova O, et al. Human chimeric antigen receptor macrophages for cancer immunotherapy. Nat Biotechnol. 2020;38:947–953. doi: 10.1038/s41587-020-0462-y
   PubMed Web of Science ®Google Scholar
• Querques I, Mades A, Zuliani C, et al. A highly soluble sleeping beauty transposase improves control of gene insertion. Nat Biotechnol. 2019 Dec;37(12):1502–1512. doi: 10.1038/s41587-019-0291-z
   PubMed Web of Science ®Google Scholar
• Ptáčková P, Musil J, Štach M, et al. A new approach to CAR T-cell gene engineering and cultivation using piggyBac transposon in the presence of IL-4, IL-7 and IL-21. Cytotherapy. 2018 Apr;20(4):507–520. doi: 10.1016/j.jcyt.2017.10.001
   PubMed Web of Science ®Google Scholar
• Walters AA, Kinnear E, Shattock RJ, et al. Comparative analysis of enzymatically produced novel linear DNA constructs with plasmids for use as DNA vaccines. Gene Ther. 2014 Jul;21(7):645–652. doi: 10.1038/gt.2014.37
   PubMed Web of Science ®Google Scholar
• Bishop DC, Caproni L, Gowrishankar K, et al. CAR T cell generation by piggyBac transposition from linear doggybone DNA vectors requires transposon DNA-flanking regions. Mol Ther Methods Clin Dev. 2020;17:359–368. doi: 10.1016/j.omtm.2019.12.020
   PubMed Web of Science ®Google Scholar
• Labbé RP, Vessillier S, Rafiq QA. Lentiviral vectors for T cell engineering: clinical applications, bioprocessing and future perspectives. Viruses. 2021 Aug 2;13(8):1528. doi: 10.3390/v13081528
   PubMed Web of Science ®Google Scholar
• Ansorge S, Lanthier S, Transfiguracion J, et al. Development of a scalable process for high-yield lentiviral vector production by transient transfection of HEK293 suspension cultures. J Gene Med. 2009;11:868–876. doi: 10.1002/jgm.1370
   PubMed Web of Science ®Google Scholar
• Comisel R-M, Kara B, Fiesser FH, et al. Lentiviral vector bioprocess economics for cell and gene therapy commercialization. Biochem Eng J. 2021;167:107868. doi: 10.1016/j.bej.2020.107868
   Web of Science ®Google Scholar
• Foster JB, Barrett DM, Karikó K. The emerging role of in vitro-transcribed mRNA in adoptive T cell immunotherapy. Mol Ther. 2019;27:747–756. doi: 10.1016/j.ymthe.2019.01.018
   PubMed Web of Science ®Google Scholar
• Wu J, Wu W, Zhou B, et al. Chimeric antigen receptor therapy meets mRNA technology. Trends Biotechnol. 2024 Feb;42(2):228–240. doi: 10.1016/j.tibtech.2023.08.005
   PubMed Web of Science ®Google Scholar
• Van Hoecke L, Verbeke R, Dewitte H, et al. mRNA in cancer immunotherapy: beyond a source of antigen. Mol Cancer. 2021 Mar 3;20(1):48. doi: 10.1186/s12943-021-01329-3
   PubMed Web of Science ®Google Scholar
• Rabinovich PM, Komarovskaya ME, Ye ZJ, et al. Synthetic messenger RNA as a tool for gene therapy. Hum Gene Ther. 2006 Oct;17(10):1027–1035. doi: 10.1089/hum.2006.17.1027
   PubMed Web of Science ®Google Scholar
• Smits E, Ponsaerts P, Lenjou M, et al. RNA-based gene transfer for adult stem cells and T cells. Leukemia. 2004;18:1898–1902. doi: 10.1038/sj.leu.2403463
   PubMed Web of Science ®Google Scholar
• Krug C, Birkholz K, Paulus A, et al. Stability and activity of MCSP-specific chimeric antigen receptors (CARs) depend on the scFv antigen-binding domain and the protein backbone. Cancer Immunol Immun. 2015;64:1623–1635. doi: 10.1007/s00262-015-1767-4
   PubMed Web of Science ®Google Scholar
• Schutsky K, Song DG, Lynn R, et al. Rigorous optimization and validation of potent RNA CAR T cell therapy for the treatment of common epithelial cancers expressing folate receptor. Oncotarget. 2015;6:28911–28928. doi: 10.18632/oncotarget.5029
   PubMed Web of Science ®Google Scholar
• Birkholz K, Hombach A, Krug C, et al. Transfer of mRNA encoding recombinant immunoreceptors reprograms CD4+ and CD8+ T cells for use in the adoptive immunotherapy of cancer. Gene Ther. 2009;16:596–604. doi: 10.1038/gt.2008.189
   PubMed Web of Science ®Google Scholar
• Singh N, Liu X, Hulitt J, et al. Nature of tumor control by permanently and transiently modified GD2 chimeric antigen receptor T cells in xenograft models of neuroblastoma. Cancer Immunol Res. 2014;2:1059–1070. doi: 10.1158/2326-6066.CIR-14-0051
   PubMedGoogle Scholar
• Caruso HG, Torikai H, Zhang L, et al. Redirecting T-cell specificity to EGFR using mRNA to self-limit expression of chimeric antigen receptor. J Immunother. 2016;39:205–217. doi: 10.1097/CJI.0000000000000126
   PubMed Web of Science ®Google Scholar
• Kenderian SS, Ruella M, Shestova O, et al. CD33-specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia. 2015;29:1637–1647. doi: 10.1038/leu.2015.52
   PubMed Web of Science ®Google Scholar
• Cummins KD, Frey N, Nelson AM, et al. Treating relapsed/refractory (RR) AML with biodegradable anti-CD123 CAR modified T cells. Blood. 2017;130:1359–1359. doi: 10.1182/blood.V130.Suppl_1.1359.1359
   Web of Science ®Google Scholar
• Panjwani MK, Smith JB, Schutsky K, et al. Feasibility and safety of RNA-transfected CD20-specific chimeric antigen receptor T cells in dogs with spontaneous B cell lymphoma. Mol Ther. 2016;24:1602–1614. doi: 10.1038/mt.2016.146
   PubMed Web of Science ®Google Scholar
• Inoo K, Inagaki R, Fujiwara K, et al. Immunological quality and performance of tumor vessel-targeting CAR-T cells prepared by mRNA-EP for clinical research. Mol Ther Oncolytics. 2016;3:16024. doi: 10.1038/mto.2016.24
   PubMed Web of Science ®Google Scholar
• Billingsley MM, Singh N, Ravikumar P, et al. Ionizable lipid nanoparticle-mediated mRNA delivery for human CAR T cell engineering. Nano Lett. 2020;20:1578–1589. doi: 10.1021/acs.nanolett.9b04246
   PubMed Web of Science ®Google Scholar
• Parayath NN, Stephan SB, Koehne AL, et al. In vitro-transcribed antigen receptor mRNA nanocarriers for transient expression in circulating T cells in vivo. Nat Commun. 2020 Nov 27;11(1):6080. doi: 10.1038/s41467-020-19486-2
   PubMed Web of Science ®Google Scholar
• Rurik JG, Tombácz I, Yadegari A, et al. CAR T cells produced in vivo to treat cardiac injury. Science (1979). 2022;375:91–96. doi: 10.1126/science.abm0594
   PubMed Web of Science ®Google Scholar
• Maus MV, Haas AR, Beatty GL, et al. T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol Res. 2013;1:26–31. doi: 10.1158/2326-6066.CIR-13-0006
   PubMed Web of Science ®Google Scholar
• Tchou J, Zhao Y, Levine BL, et al. Safety and efficacy of intratumoral injections of chimeric antigen receptor (CAR) T cells in metastatic breast cancer. Cancer Immunol Res. 2017;5:1152–1161. doi: 10.1158/2326-6066.CIR-17-0189
   PubMed Web of Science ®Google Scholar
• Beatty GL, O’Hara MH, Lacey SF, et al. Activity of mesothelin-specific chimeric antigen receptor T cells against pancreatic carcinoma metastases in a phase 1 trial. Gastroenterology. 2018;155:29–32. doi: 10.1053/j.gastro.2018.03.029
   PubMed Web of Science ®Google Scholar
• Lin L, Cho S-F, Xing L, et al. Preclinical evaluation of CD8+ anti-BCMA mRNA CAR T cells for treatment of multiple myeloma. Leukemia. 2021;35:752–763. doi: 10.1038/s41375-020-0951-5
   PubMed Web of Science ®Google Scholar
• Shah PD, Huang AC, Xu X, et al. Phase I trial of autologous RNA-electroporated cMET-directed CAR T cells administered intravenously in patients with melanoma and breast carcinoma. Cancer Res Commun. 2023;3:821–829. doi: 10.1158/2767-9764.CRC-22-0486
   PubMedGoogle Scholar
• Deo S, Desai K, Patare A, et al. Evaluation of self-amplifying mRNA platform for protein expression and genetic stability: implication for mRNA therapies. Biochem Biophys Res Commun. 2023;680:108–118. doi: 10.1016/j.bbrc.2023.09.016
   PubMed Web of Science ®Google Scholar
• Zhao Y, Moon E, Carpenito C, et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res. 2010;70:9053. doi: 10.1158/0008-5472.CAN-10-2880
   PubMed Web of Science ®Google Scholar
• Anderson BR, Muramatsu H, Nallagatla SR, et al. Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Res. 2010;38:5884–5892. doi: 10.1093/nar/gkq347
   PubMed Web of Science ®Google Scholar
• Karikó K, Muramatsu H, Ludwig J, et al. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA. Nucleic Acids Res. 2011;39:e142. doi: 10.1093/nar/gkr695
   PubMed Web of Science ®Google Scholar
• Jayaraman J, Mellody MP, Hou AJ, et al. CAR-T design: elements and their synergistic function. EBioMedicine. 2020;58:102931. doi: 10.1016/j.ebiom.2020.102931
   PubMed Web of Science ®Google Scholar
• Rafiq S, Hackett CS, Brentjens RJ. Engineering strategies to overcome the current roadblocks in CAR T cell therapy. Nat Rev Clin Oncol. 2019;17(3):147–167. doi: 10.1038/s41571-019-0297-y
   PubMed Web of Science ®Google Scholar