How to integrate CD19 specific chimeric antigen receptor T cells with other CD19 targeting agents in diffuse large B-cell lymphoma?
CAR T cells
CD19 targeting agents
DLBCL
Journal
Hematological oncology
ISSN: 1099-1069
Titre abrégé: Hematol Oncol
Pays: England
ID NLM: 8307268
Informations de publication
Date de publication:
08 Nov 2023
08 Nov 2023
Historique:
revised:
12
10
2023
received:
07
08
2023
accepted:
13
10
2023
medline:
8
11
2023
pubmed:
8
11
2023
entrez:
8
11
2023
Statut:
aheadofprint
Résumé
About one third of patients with diffuse large B-cell lymphoma (DLBCL) have a relapsing/refractory (R/R) disease after first line chemo-immunotherapy, with particularly poor outcomes observed in patients with primary refractory disease and early relapse. CD19 specific chimeric antigen receptor (CAR) T cell therapy is a game changer that results in durable and complete response rates in almost half of the patients with R/R DLBCL. Other emerging CD19-targeting therapies include monoclonal antibodies, bispecific antibodies and targeting antibody-drug conjugates, which also show encouraging results. However, the timing and sequencing of different anti-CD19-targeting agents and how they might interfere with subsequent CAR T cell treatment is still unclear. In this review, we summarize the results of the pivotal clinical trials as well as evidence from real-world series of the use of different CD19-targeting approved agents. We discuss the effect of various therapies on CD19 expression and its implications for treatment sequencing.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Swiss National Science Foundation
ID : 310030_220070
Pays : Switzerland
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Flowers CR, Odejide OO. Sequencing therapy in relapsed DLBCL. Hematology. 2022;2022(1):146-154. https://doi.org/10.1182/hematology.2022000332
Sehn LH, Salles G. Diffuse large B-cell lymphoma. N Engl J Med. 2021;384(9):842-858. Longo DL, ed. https://doi.org/10.1056/NEJMra2027612
Crump M, Neelapu SS, Farooq U, et al. Outcomes in refractory diffuse large B-cell lymphoma: results from the international SCHOLAR-1 study. Blood. 2017;130(16):1800-1808. https://doi.org/10.1182/blood-2017-03-769620
Wang Y, Farooq U, Link BK, et al. Late relapses in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. J Clin Oncol. 2019;37(21):1819-1827. https://doi.org/10.1200/JCO.19.00014
Gisselbrecht C, Glass B, Mounier N, et al. Salvage regimens with autologous transplantation for relapsed large B-cell lymphoma in the rituximab era. J Clin Oncol. 2010;28(27):4184-4190. https://doi.org/10.1200/JCO.2010.28.1618
Sermer D, Elavalakanar P, Abramson JS, Palomba ML, Salles G, Arnason J. Targeting CD19 for diffuse large B cell lymphoma in the era of CARs: other modes of transportation. Blood Rev. 2022;57:101002. Published online. https://doi.org/10.1016/j.blre.2022.101002
Abramson JS, Ghosh N, Smith SM. ADCs, BiTEs, CARs, and small molecules: a new era of targeted therapy in non-hodgkin lymphoma. Am Soc Clin Oncol Educ Book. 2020(40):302-313. https://doi.org/10.1200/EDBK_279043
Sureda A, Lugtenburg PJ, Kersten MJ, et al. Cellular therapy in lymphoma. Hematol Oncol. 2023. Published online June 29, 2023:hon.3200. https://doi.org/10.1002/hon.3200
Boardman AP, Salles G. CAR T-cell therapy in large B cell lymphoma. Hematol Oncol. 2023;41(Suppl 1):112-118. https://doi.org/10.1002/hon.3153
Nagler A, Perriello VM, Falini L, Falini B. How I treat refractory/relapsed diffuse large B-cell lymphomas with CD19 -directed chimeric antigen receptor T cells. Br J Haematol. 2023;201(3):396-410. https://doi.org/10.1111/bjh.18724
Bailly S, Cartron G, Chaganti S, et al. Targeting CD19 in diffuse large B-cell lymphoma: an expert opinion paper. Hematol Oncol. 2022;40(4):505-517. https://doi.org/10.1002/hon.3013
Neelapu SS, Jacobson CA, Oluwole OO, et al. Outcomes of older patients in ZUMA-1, a pivotal study of axicabtagene ciloleucel in refractory large B-cell lymphoma. Blood. 2020;135(23):2106-2109. https://doi.org/10.1182/blood.2019004162
Majzner RG, Rietberg SP, Sotillo E, et al. Tuning the antigen density requirement for CAR T-cell activity. Cancer Discov. 2020;10(5):702-723. https://doi.org/10.1158/2159-8290.CD-19-0945
Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439-448. https://doi.org/10.1056/NEJMoa1709866
Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377(26):2531-2544. https://doi.org/10.1056/NEJMoa1707447
Smith R, Shen R. Complexities in comparing the impact of costimulatory domains on approved CD19 CAR functionality. J Transl Med. 2023;21(1):515. https://doi.org/10.1186/s12967-023-04372-4
Schuster 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
Abramson 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. Published online. 2020;396(10254):839-852. https://doi.org/10.1016/s0140-6736(20)31366-0
Chong EA, Ruella M, Schuster SJ. Five-year outcomes for refractory B-cell lymphomas with CAR T-cell therapy. N Engl J Med. 2021;384(7):673-674. https://doi.org/10.1056/NEJMc2030164
Neelapu SS, Jacobson CA, Ghobadi A, et al. 5-Year follow-up supports curative potential of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1). Blood. 2023:2022018893. Published online February 23, 2023:blood. https://doi.org/10.1182/blood.2022018893
Bethge 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. 2022:2021015209. Published online March 22, 2022:blood. https://doi.org/10.1182/blood.2021015209
Casadei B, Argnani L, Guadagnuolo S, et al. Real world evidence of CAR T-cell therapies for the treatment of relapsed/refractory B-cell non-hodgkin lymphoma: a monocentric experience. Cancers. 2021;13(19):4789. https://doi.org/10.3390/cancers13194789
Vercellino L, Di Blasi R, Kanoun S, et al. Predictive factors of early progression after CAR T-cell therapy in relapsed/refractory diffuse large B-cell lymphoma. Blood Adv. 2020;4(22):5607-5615. https://doi.org/10.1182/bloodadvances.2020003001
Bachy E, Le Gouill 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
Locke 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
Bishop MR, Dickinson M, Purtill D, et al. Second-line tisagenlecleucel or standard care in aggressive B-cell lymphoma. N Engl J Med. 2022;386(7):629-639. https://doi.org/10.1056/NEJMoa2116596
Lisocabtagene K. Maraleucel versus standard of care with salvage chemotherapy followed by autologous stem cell transplantation as second-line treatment in patients with relapsed or refractory large B-cell lymphoma (TRANSFORM): results from an interim analysis of an open-label, randomised, phase 3 trial. Lancet. 2022. Published online.
Westin JR, Oluwole OO, Kersten MJ, et al. Survival with axicabtagene ciloleucel in large B-cell lymphoma. N Engl J Med. 2023;389(2):148-157. https://doi.org/10.1056/NEJMoa2301665
Bommier C, Lambert J, Thieblemont C. Comparing apples and oranges: the ZUMA-7, TRANSFORM and BELINDA trials. Hematol Oncol. 2022;40(5):1090-1093. https://doi.org/10.1002/hon.3001
Houot R, Bachy E, Cartron G, et al. Axicabtagene ciloleucel in large B cell lymphoma ineligible for autologous stem cell transplantation: the phase 2 ALYCANTE trial. Nat Med. 2023;14. Published online September. https://doi.org/10.1038/s41591-023-02572-5
Sehgal A, Hoda D, Riedell PA, et al. Lisocabtagene maraleucel as second-line therapy in adults with relapsed or refractory large B-cell lymphoma who were not intended for haematopoietic stem cell transplantation (PILOT): an open-label, phase 2 study. Lancet Oncol. 2022;23(8):1066-1077. https://doi.org/10.1016/S1470-2045(22)00339-4
Neelapu SS, Dickinson M, Munoz J, et al. Axicabtagene ciloleucel as first-line therapy in high-risk large B-cell lymphoma: the phase 2 ZUMA-12 trial. Nat Med. 2022;28(4):735-742. https://doi.org/10.1038/s41591-022-01731-4
Westin J, Jacobson CA, Chavez JC, et al. ZUMA-23: A Global, Phase 3, Randomized Controlled Study of Axicabtagene Ciloleucel versus Standard of Care as First-Line Therapy in Patients with High-Risk Large B-Cell Lymphoma.
Horton HM, Bernett MJ, Pong E, et al. Potent in vitro and in vivo activity of an fc-engineered anti-CD19 monoclonal antibody against lymphoma and leukemia. Cancer Res. 2008;68(19):8049-8057. https://doi.org/10.1158/0008-5472.CAN-08-2268
Awan FT, Lapalombella R, Trotta R, et al. CD19 targeting of chronic lymphocytic leukemia with a novel Fc-domain-engineered monoclonal antibody. Blood. 2010;115(6):1204-1213. https://doi.org/10.1182/blood-2009-06-229039
Salles G, Duell J, González Barca E, et al. Tafasitamab plus lenalidomide in relapsed or refractory diffuse large B-cell lymphoma (L-MIND): a multicentre, prospective, single-arm, phase 2 study. Lancet Oncol. 2020;21(7):978-988. Published online July 2020 PMID: 32511983. https://doi.org/10.1016/s1470-2045(20)30225-4
Duell J, Maddocks KJ, González-Barca E, et al. Long-term outcomes from the Phase II L-MIND study of tafasitamab (MOR208) plus lenalidomide in patients with relapsed or refractory diffuse large B-cell lymphoma. Haematologica. 2021;106(9):2417-2426. https://doi.org/10.3324/haematol.2020.275958
Zinzani PL, Rodgers T, Marino D, et al. RE-MIND: comparing tafasitamab + lenalidomide (L-MIND) with a real-world lenalidomide monotherapy cohort in relapsed or refractory diffuse large B-cell lymphoma. Clin Cancer Res. 2021;27(22):6124-6134. https://doi.org/10.1158/1078-0432.CCR-21-1471
Cordoba R, Prawitz T, Westley T, et al. Tafasitamab plus lenalidomide versus 3 rituximab-based treatments for non-transplant eligible relapsed/refractory diffuse large B-cell lymphoma: a matching-adjusted indirect comparison. Adv Ther. 2022;39(6):2668-2687. https://doi.org/10.1007/s12325-022-02094-5
Zammarchi F, Corbett S, Adams L, et al. ADCT-402, a PBD dimer-containing antibody drug conjugate targeting CD19-expressing malignancies. Blood. 2018;131(10):1094-1105. https://doi.org/10.1182/blood-2017-10-813493
Hartley JA, Flynn MJ, Bingham JP, et al. Pre-clinical pharmacology and mechanism of action of SG3199, the pyrrolobenzodiazepine (PBD) dimer warhead component of antibody-drug conjugate (ADC) payload tesirine. Sci Rep. 2018;8(1):10479. https://doi.org/10.1038/s41598-018-28533-4
Caimi PF, Ai W, Alderuccio JP, et al. Loncastuximab tesirine in relapsed or refractory diffuse large B-cell lymphoma (LOTIS-2): a multicentre, open-label, single-arm, phase 2 trial. Lancet Oncol. 2021;22(6):790-800. Published online. https://doi.org/10.1016/S1470-2045(21)00139-X
Hamadani M, Chen L, Song Y, et al. Matching-adjusted indirect comparison of the efficacy of loncastuximab tesirine versus treatment in the chemoimmunotherapy era for relapsed/refractory diffuse large B-cell lymphoma. Clin Lymphoma, Myeloma & Leukemia. 2022;22(8):e738-e744. https://doi.org/10.1016/j.clml.2022.04.006
Schlereth B, Quadt C, Dreier T, et al. T-cell activation and B-cell depletion in chimpanzees treated with a bispecific anti-CD19/anti-CD3 single-chain antibody construct. Cancer Immunol Immunother CII. 2006;55(5):503-514. https://doi.org/10.1007/s00262-005-0001-1
Goebeler ME, Knop S, Viardot A, et al. Bispecific T-cell engager (BiTE) antibody construct blinatumomab for the treatment of patients with relapsed/refractory non-Hodgkin lymphoma: final results from a phase I study. J Clin Oncol. 2016;34(10):1104-1111. https://doi.org/10.1200/JCO.2014.59.1586
Dufner V, Sayehli CM, Chatterjee M, et al. Long-term outcome of patients with relapsed/refractory B-cell non-Hodgkin lymphoma treated with blinatumomab. Blood Adv. 2019;3(16):2491-2498. https://doi.org/10.1182/bloodadvances.2019000025
Sun LL, Ellerman D, Mathieu M, et al. Anti-CD20/CD3 T cell-dependent bispecific antibody for the treatment of B cell malignancies. Sci Transl Med. 2015;7(287):287ra70. https://doi.org/10.1126/scitranslmed.aaa4802
Bacac M, Colombetti S, Herter S, et al. CD20-TCB with obinutuzumab pretreatment as next-generation treatment of hematologic malignancies. Clin Cancer Res Off J Am Assoc Cancer Res. 2018;24(19):4785-4797. https://doi.org/10.1158/1078-0432.CCR-18-0455
Thieblemont C, Phillips T, Ghesquieres H, et al. Epcoritamab, a novel, subcutaneous CD3xCD20 bispecific T-cell-engaging antibody, in relapsed or refractory large B-cell lymphoma: dose expansion in a phase I/II trial. J Clin Oncol. 2023;41(12):2238-2247. https://doi.org/10.1200/JCO.22.01725
Budde 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
Hutchings M, Morschhauser F, Iacoboni G, et al. Glofitamab, a novel, bivalent CD20-targeting T-cell-engaging bispecific antibody, induces durable complete remissions in relapsed or refractory B-cell lymphoma: a phase I trial. J Clin Oncol. 2021;39(18):1959-1970. https://doi.org/10.1200/JCO.20.03175
Zhou S, Liu M, Ren F, Meng X, Yu J. The landscape of bispecific T cell engager in cancer treatment. Biomark Res. 2021;9(1):38. https://doi.org/10.1186/s40364-021-00294-9
Delage L, Manzoni D, Quinquenet C, et al. Molecular analysis of a CD19-negative diffuse large B-cell lymphoma. Haematologica. 2019;104(3):e114-e116. https://doi.org/10.3324/haematol.2018.203521
Hicks SW, Tarantelli C, Wilhem A, et al. The novel CD19-targeting antibody-drug conjugate huB4-DGN462 shows improved anti-tumor activity compared to SAR3419 in CD19-positive lymphoma and leukemia models. Haematologica. 2019;104(8):1633-1639. https://doi.org/10.3324/haematol.2018.211011
Arribas AJ, Napoli S, Cascione L, et al. Resistance to PI3Kδ inhibitors in marginal zone lymphoma can be reverted by targeting the IL-6/PDGFRA axis. Haematologica. 2022;107(11):2685-2697. https://doi.org/10.3324/haematol.2021.279957
Tarantelli C, Spriano F, Golino G, et al. The antibody-drug conjugate (ADC) loncastuximab tesirine (ADCT-402) targeting CD19 SHOWS strong in vitro anti-lymphoma activity both as single agents and in combination. Hematol Oncol. 2019;37(S2):129-130. https://doi.org/10.1002/hon.90_2629
Caimi PF, Ardeshna KM, Reid E, et al. The AntiCD19 antibody drug immunoconjugate loncastuximab achieves responses in DLBCL relapsing after AntiCD19 CAR-T cell therapy. Clin Lymphoma, Myeloma & Leukemia. 2022;22(5):e335-e339. https://doi.org/10.1016/j.clml.2021.11.005
Spiegel 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
Majzner RG, Mackall CL. Tumor antigen escape from CAR T-cell therapy. Cancer Discov. 2018;8(10):1219-1226. https://doi.org/10.1158/2159-8290.CD-18-0442
Sotillo 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
Shalabi H, Kraft IL, Wang HW, et al. Sequential loss of tumor surface antigens following chimeric antigen receptor T-cell therapies in diffuse large B-cell lymphoma. Haematologica. 2018;103(5):e215-e218. https://doi.org/10.3324/haematol.2017.183459
Plaks 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
Dodero A, Bramanti S, Pennisi M, et al. Patients outcome after chimeric antigen receptor (CAR) T-cells failure in aggressive B-cell lymphomas: role of immunotherapy and prognostic factors. Blood. 2022;140(Suppl 1):9468-9469. https://doi.org/10.1182/blood-2022-163651
Alarcon Tomas A, Fein JA, Fried S, et al. Outcomes of first therapy after CD19-CAR-T treatment failure in large B-cell lymphoma. Leukemia. 2023;37(1):154-163. https://doi.org/10.1038/s41375-022-01739-2
Sworder BJ, Kurtz DM, Alig SK, et al. Determinants of resistance to engineered T cell therapies targeting CD19 in large B cell lymphomas. Cancer Cell. 2023;41(1):210-225.e5. https://doi.org/10.1016/j.ccell.2022.12.005
Duell J, Obr A, Augustin M, et al. CD19 expression is maintained in DLBCL patients after treatment with tafasitamab plus lenalidomide in the L-MIND study. Leuk Lymphoma. 2022;63(2):468-472. https://doi.org/10.1080/10428194.2021.1986219
Thapa B, Caimi PF, Ardeshna KM, et al. CD19 antibody-drug conjugate therapy in DLBCL does not preclude subsequent responses to CD19-directed CAR T-cell therapy. Blood Adv. 2020;4(16):3850-3852. https://doi.org/10.1182/bloodadvances.2020002587
Sakemura RL, Manriquez-Roman C, Horvei P, et al. CD19 antigen occupancy on cancer cells with the CD19 monoclonal antibody tafasitamab improves the activation, antitumor efficacy, and safety profile of CART19 cell therapy. Blood. 2022;140((Suppl 1)):2362-2364. https://doi.org/10.1182/blood-2022-158273
Fitzgerald KN, Quesada AE, von Keudell G, et al. CD19 epitope masking by tafasitamab leads to delays in subsequent use of CD19 CAR T-cell therapy in two patients with aggressive mature B-cell lymphomas. Leuk Lymphoma. 2022;63(3):751-754. https://doi.org/10.1080/10428194.2021.1992622
Tabbara N, Gaut D, Oliai C, Lewis T, de Vos S. Anti-CD19 CAR T-cell therapy remission despite prior anti-CD19 antibody tafasitamab in relapsed/refractory DLBCL. Leuk Res Rep. 2021;16:100260. https://doi.org/10.1016/j.lrr.2021.100260
Iqbal M, Khurana A, Chavez J, et al. Efficacy of CD19 directed therapies in large B-cell lymphoma (LBCL) relapsing after chimeric antigen receptor (CAR) T-cell therapy. Blood. 2022;140(Suppl 1):10396-10398. https://doi.org/10.1182/blood-2022-169689
Brudno JN, Kochenderfer JN. Limited utility of chimeric antigen receptor (CAR) T-cell retreatment: experience with a human anti-CD19 CAR. Bone Marrow Transpl. 2023;58(10):1157-1159. https://doi.org/10.1038/s41409-023-02041-0
Holland EM, Molina JC, Dede K, et al. Efficacy of second CAR-T (CART2) infusion limited by poor CART expansion and antigen modulation. J Immunother Cancer. 2022;10(5):e004483. https://doi.org/10.1136/jitc-2021-004483
Shah BD, Jacobson C, Solomon SR, et al. Allogeneic CAR-T PBCAR0191 with intensified lymphodepletion is highly active in patients with relapsed/refractory B-cell malignancies. Blood. 2021;138((Suppl 1)):302. https://doi.org/10.1182/blood-2021-150609
Di Blasi R, Le Gouill S, Bachy E, et al. Outcomes of patients with aggressive B-cell lymphoma after failure of anti-CD19 CAR T-cell therapy: a DESCAR-T analysis. Blood. 2022;140(24):2584-2593. https://doi.org/10.1182/blood.2022016945