[Review] CAR T-cell therapy for multiple myeloma: state of the art and prospects

1.Gandhi UH Cornell RF Lakshman A et al.

Outcomes of patients with multiple myeloma refractory to CD38-targeted monoclonal antibody therapy.

Leukemia. 33: 2266-22752.Maher J Brentjens RJ Gunset G Rivière I Sadelain M

Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta/CD28 receptor.

Nat Biotechnol. 20: 70-753.O'Connor BP Raman VS Erickson LD et al.

BCMA is essential for the survival of long-lived bone marrow plasma cells.

J Exp Med. 199: 91-984.Tai YT Acharya C An G et al.

APRIL and BCMA promote human multiple myeloma growth and immunosuppression in the bone marrow microenvironment.

Blood. 127: 3225-32365.Friedman KM Garrett TE Evans JW et al.

Effective targeting of multiple B-cell maturation antigen-expressing hematological malignances by anti-B-cell maturation antigen chimeric antigen receptor T cells.

Hum Gene Ther. 29: 585-6016.Bu DX Singh R Choi EE et al.

Pre-clinical validation of B cell maturation antigen (BCMA) as a target for T cell immunotherapy of multiple myeloma.

Oncotarget. 9: 25764-257807.Carpenter RO Evbuomwan MO Pittaluga S et al.

B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma.

Clin Cancer Res. 19: 2048-20608.Ali SA Shi V Maric I et al.

T cells expressing an anti-B-cell maturation antigen chimeric antigen receptor cause remissions of multiple myeloma.

Blood. 128: 1688-17009.Brudno JN Maric I Hartman SD et al.

T cells genetically modified to express an anti-B-cell maturation antigen chimeric antigen receptor cause remissions of poor-prognosis relapsed multiple myeloma.

J Clin Oncol. 36: 2267-228010.Cohen AD Garfall AL Stadtmauer EA et al.

B cell maturation antigen-specific CAR T cells are clinically active in multiple myeloma.

J Clin Invest. 129: 2210-222111.Raje N Berdeja J Lin Y et al.

Anti-BCMA CAR T-cell therapy bb2121 in relapsed or refractory multiple myeloma.

N Engl J Med. 380: 1726-173712.Alsina M Shah N Raje N et al.

Updated results from the phase 1 CRB-402 study of anti-BCMA CAR T-cell therapy bb21217 in patients with relapsed and refractory multiple myeloma: correlation of expansion and duration of response with T-cell phenotypes.

Blood. 136 : 13013.Madduri D Berdeja J Usmani S et al.

CARTITUDE-1: phase 1b/2 study of ciltacabtagene autoleucel, a B-cell maturation antigen-directed chimeric antigen receptor T-cell therapy, in relapsed/refractory multiple myeloma.

Blood. 136 : 17714.Wang B Zhao W Liu J et al.

Long-term follow-up of a phase 1, first-in-human open-label study of LCAR-B38M, a structurally differentiated chimeric antigen receptor T (CAR-T) cell therapy targeting B-cell maturation antigen (BCMA), in patients (pts) with relapsed/refractory multiple myeloma (RRMM).

Blood. 134 : 57915.Zhao WH Liu J Wang BY et al.

A phase 1, open-label study of LCAR-B38M, a chimeric antigen receptor T cell therapy directed against B cell maturation antigen, in patients with relapsed or refractory multiple myeloma.

J Hematol Oncol. 11: 14116.Zudaire E Madduri D Usmani S et al.

Translational analysis from CARTITUDE-1, an ongoing phase 1b/2 study of JNJ-4528 BCMA-targeted CAR-T cell therapy in relapsed and/or refractory multiple myeloma (R/R MM), indicates preferential expansion of CD8+ T cell central memory cell subset.

Blood. 134 : 92817.Mailankody S Jakubowiak A Htut M et al.

Orvacabtagene autoleucel (orva-cel), a B-cell maturation antigen (BCMA)-directed CAR T cell therapy for patients (pts) with relapsed/refractory multiple myeloma (RRMM): update of the phase 1/2 EVOLVE study (NCT03430011).

Proc Am Soc Clin Oncol. 38 850418.Mailankody S Ghosh A Staehr M et al.

Clinical responses and pharmacokinetics of MCARH171, a human-derived BCMA targeted CAR T cell therapy in relapsed/refractory multiple myeloma: final results of a phase 1 clinical trial.

Blood. 132 : 95919.Green D Pont M Sather B et al.

Fully human BCMA targeted chimeric antigen receptor T cells administered in a defined composition demonstrate potency at low doses in advanced stage high risk multiple myeloma.

Blood. 132 101120.Costello C Cohen A Patel K et al.

Phase 1/2 study of the safety and response of P-BCMA-101 CAR-T cells in patients with relapsed/refractory (R/R) multiple myeloma (MM) (PRIME) with novel therapeutic strategies.

Blood. 136 : 29-3021.Hao S Jin J Jiang S et al.

Two-year follow-up of investigator-initiated phase 1 trials of the safety and efficacy of fully human Anti-BCMA CAR T Cells (CT053) in relapsed/refractory multiple myeloma.

Blood. 136 : 27-2822.Li C Wang J Wang D et al.

Efficacy and safety of fully human BCMA targeting CAR T-cell therapy in relapsed/refractory MM.

Blood. 134 : 92923.Mailankody S Matous J Liedtke M et al.

Universal: an allogeneic first-in-human study of the anti-BCMA ALLO-715 and the anti-CD52 ALLO-647 in relapsed/refractory multiple myeloma.

Blood. 136 : 24-2524.Lin Y Raje N Berdeja J et al.

Idecabtagene vicleucel (ide-cel, bb2121), a BCMA-directed CAR T cell therapy, in patients with relapsed and refractory multiple myeloma: updated results from phase 1 CRB-401 study.

Blood. 136 : 26-2725.Munshi N Anderson Jr, LD Shah N et al.

Idecabtagene vicleucel (ide-cel; bb2121), a BCMA-targeted CAR T-cell therapy, in patients with relapsed and refractory multiple myeloma (RRMM): initial KarMMa results.

Proc Am Soc Clin Oncol. 38 850326.Kansagra A Lin Y Berdeja J et al.

Characterization of cytokine release syndrome in the KarMMa study of idecabtagene vicleucel (ide-cel, bb2121) for relapsed and refractory multiple myeloma.

Blood. 136 137827.Madduri D Usmani S Jagannath S et al.

Results from CARTITUDE-1: a phase 1b/2 study of JNJ-4528, a CAR-T cell therapy directed against B-cell maturation antigen (BCMA), in patients with relapsed and/or refractory multiple myeloma (R/R MM).

Blood. 134 : 57728.Shah N Ayers D Davies F et al.

A matching-adjusted indirect comparison of efficacy outcomes for idecabtagene vicleucel (ide-cel, bb2121), a BCMA-directed CAR T cell therapy versus conventional care in triple-class-exposed relapsed and refractory multiple myeloma.

Blood. 136 165329.Delforge M Shah N Rodriguez Otero P et al.

Health state utility valuation in patients with triple-class-exposed relapsed and refractory multiple myeloma treated with the BCMA-directed CAR T cell therapy, idecabtagene vicleucel (ide-cel, bb2121): results from the KarMMa trial.

Blood. 136 : 14-1530.Martin 3rd, T Lin Y Agha M et al.

Health-related quality of life in the CARTITUDE-1 study of ciltacabtagene autoleucel for relapsed/refractory multiple myeloma.

Blood. 136 229131.Berdeja J Raje N Siegel D et al.

Efficacy and safety of idecabtagene vicleucel (ide-cel, bb2121) in elderly patients with relapsed and refractory multiple myeloma: KarMMa subgroup analysis.

Blood. 136 : 16-1732.Raje N Siegel D Jagannath S et al.

Idecabtagene vicleucel (ide-cel, bb2121) in relapsed and refractory multiple myeloma: analyses of high-risk subgroups in the KarMMa study.

Blood. 136 323433.Xu J Chen LJ Yang SS et al.

Exploratory trial of a biepitopic CAR T-targeting B cell maturation antigen in relapsed/refractory multiple myeloma.

Proc Natl Acad Sci USA. 116: 9543-955134.Colonna M Navarro G DeVries T et al.

Orvacabtagene autoleucel (orva-cel; JCARH125): a fully human BCMA-targeted second-generation CAR T cell product characterized by a predominant central memory phenotype with high in vitro and in vivo proliferative potential and sustained in vivo persistence.

Blood. 136 : 11-1235.Neelapu SS Locke FL Bartlett NL et al.

Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma.

N Engl J Med. 377: 2531-254436.Yan L Yan Z Shang J et al.

Sequential CD19- and BCMA-specific chimeric antigen receptor T cell treatment for RRMM: report from a single center study.

Blood. 134 : 57837.Martin M Thompson E Brown W et al.

Idecabtagene vicleucel (ide-cel, bb2121) responders are characterized by early and temporally consistent activation and expansion of CAR T cells with a T effector phenotype.

Blood. 136 231538.Piasecki J DeVries T Radhakrishnan A et al.

Association of baseline and postinfusion biomarkers with safety and efficacy endpoints in patients treated with orvacabtagene autoleucel (orva-cel; JCARH125) in the phase 1/2 EVOLVE study (NCT03430011).

Blood. 136 : 2-339.Lin Y Martin 3rd, T Cohen A et al.

Cytokine release syndrome in patients with relapsed/refractory multiple myeloma treated with ciltacabtagene autoleucel in the phase 1b/2 CARTITUDE-1 study.

Blood. 136 : 45-4640.Lee DW Santomasso BD Locke FL et al.

ASTCT consensus grading for cytokine release syndrome and neurologic toxicity associated with immune effector cells.

Biol Blood Marrow Transplant. 25: 625-63841.Maude SL Frey N Shaw PA et al.

Chimeric antigen receptor T cells for sustained remissions in leukemia.

N Engl J Med. 371: 1507-151742.Santomasso BD Park JH Salloum D et al.

Clinical and biological correlates of neurotoxicity associated with CAR T-cell therapy in patients with B-cell acute lymphoblastic leukemia.

Cancer Discov. 8: 958-97143.Sterner RM Sakemura R Cox MJ et al.

GM-CSF inhibition reduces cytokine release syndrome and neuroinflammation but enhances CAR-T cell function in xenografts.

Blood. 133: 697-70944.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. 24: 739-74845.Jiang H Dong B Gao L et al.

Clinical results of a multicenter study of the first-in-human dual BCMA and CD19 targeted novel platform fast CAR-T cell therapy for patients with relapsed/refractory multiple myeloma.

Blood. 136 : 25-2646.Yan Z Cao J Cheng H et al.

A combination of humanised anti-CD19 and anti-BCMA CAR T cells in patients with relapsed or refractory multiple myeloma: a single-arm, phase 2 trial.

Lancet Haematol. 6: e521-e52947.

A bispecific CAR T-cell therapy targeting BCMA and CD38 for relapsed/refractory multiple myeloma: updated results from a phase 1 dose-climbing trial.

Blood. 134 : 93048.Popat R Zweegman S Cavet J et al.

Phase 1 first-in-human study of AUTO2, the first chimeric antigen receptor (CAR) T cell targeting APRIL for patients with relapsed/refractory multiple myeloma (RRMM).

Blood. 134 311249.Cowan A Pont M Sather B et al.

Efficacy and safety of fully human BCMA CAR T cells in combination with a gamma secretase inhibitor to increase BCMA surface expression in patients with relapsed or refractory multiple myeloma.

Blood. 134 : 20450.Leblay N Maity R Barakat E et al.

Cite-seq profiling of T-cells in multiple myeloma patients undergoing BCMA targeting CAR T or BiTEs immunotherapy.

Blood. 136 : 11-1251.Garfall AL Dancy EK Cohen AD et al.

T-cell phenotypes associated with effective CAR T-cell therapy in postinduction vs relapsed multiple myeloma.

Blood Adv. 3: 2812-281552.Gattinoni L Lugli E Ji Y et al.

A human memory T cell subset with stem cell-like properties.

Nat Med. 17: 1290-129753.Yeku OO Purdon TJ Koneru M Spriggs D Brentjens RJ

Armored CAR T cells enhance antitumor efficacy and overcome the tumor microenvironment.

Sci Rep. 71054154.Krejcik J Frerichs KA Nijhof IS et al.

Monocytes and granulocytes reduce CD38 expression levels on myeloma cells in patients treated with daratumumab.

Clin Cancer Res. 23: 7498-751155.Wang X Walter M Urak R et al.

Lenalidomide enhances the function of CS1 chimeric antigen receptor-redirected T cells against multiple myeloma.

Clin Cancer Res. 24: 106-11956.Di Stasi A Tey SK Dotti G et al.

Inducible apoptosis as a safety switch for adoptive cell therapy.

N Engl J Med. 365: 1673-168357.van der Schans JJ van de Donk NWCJ Mutis T

Dual targeting to overcome current challenges in multiple myeloma CAR T-cell treatment.

Front Oncol. 10136258.Globerson Levin A Rawet Slobodkin M Waks T et al.

Treatment of multiple myeloma using chimeric antigen receptor T cells with dual specificity.

Cancer Immunol Res. 8: 1485-149559.Juillerat A Marechal A Filhol JM et al.

Design of chimeric antigen receptors with integrated controllable transient functions.

Sci Rep. 61895060.Drent E Themeli M Poels R et al.

A rational strategy for reducing on-target off-tumor effects of CD38-chimeric antigen receptors by affinity optimization.

Mol Ther. 25: 1946-195861.Tan AHJ Vinanica N Campana D

Chimeric antigen receptor-T cells with cytokine neutralizing capacity.

Blood Adv. 4: 1419-143162.Chung DJ Pronschinske KB Shyer JA et al.

T-cell exhaustion in multiple myeloma relapse after autotransplant: optimal timing of immunotherapy.

Cancer Immunol Res. 4: 61-7163.Sommer C Boldajipour B Kuo TC et al.

Preclinical evaluation of allogeneic CAR T cells targeting BCMA for the treatment of multiple myeloma.

Mol Ther. 27: 1126-113864.Mahtur R Zhang Z He J et al.

Universal SLAMF7-specific CAR T-cells as treatment or multiple myeloma.

Blood. 130 : 50265.Khurana A Hatchcock M Habermann TM et al.

Lines of therapy before autologous stem cell transplant (ASCT) and CAR-T affect outcomes in aggressive Non-Hodgkin's lymphoma (NHL).

Blood. 136 : 29-3066.Franssen LE Raymakers RA Buijs A et al.

Outcome of allogeneic transplantation in newly diagnosed and relapsed/refractory multiple myeloma: long-term follow-up in a single institution.

Eur J Haematol. 97: 479-48867.Shi X Yan L Shang J et al.

Tandom autologous transplantation and combined infusion of CD19 and BCMA-specific chimeric antigen receptor T cells for high risk MM: initial safety and efficacy report from a clinical pilot study.

Blood. 132 100968.Garfall AL Stadtmauer EA Hwang WT et al.

Anti-CD19 CAR T cells with high-dose melphalan and autologous stem cell transplantation for refractory multiple myeloma.

JCI Insight. 412768469.Topp MS Duell J Zugmaier G et al.

Anti-B-cell maturation antigen BiTE molecule AMG 420 induces responses in multiple myeloma.

J Clin Oncol. 38: 775-78370.Garfall AL Usmani S Mateos MV et al.

Updated phase 1 results of teclistamab, a B-cell maturation antigen (BCMA) x CD3 bispecific antibody, in relapsed and/or refractory multiple myeloma (RRMM).

Blood. 136 : 2771.Samur M Fulciniti M Aktas-Samur A et al.

Biallelic loss of BCMA triggers resistance to anti-BCMA CAR T-cell therapy in multiple myeloma.

Blood. 136 : 1473.Chari A Vogl DT Jagannath S et al.

Selinexor-based regimens for the treatment of myeloma refractory to chimeric antigen receptor T cell therapy.

Br J Haematol. 189: e126-e13074.Cohen AD Garfall AL Dogan A et al.

Serial treatment of relapsed/refractory multiple myeloma with different BCMA-targeting therapies.

Blood Adv. 3: 2487-249075.Ran T Eichmüller SB Schmidt P Schlander M

Cost of decentralized CAR T-cell production in an academic nonprofit setting.

Int J Cancer. 147: 3438-344576.Gross G Gorochov G Waks T Eshhar Z

Generation of effector T cells expressing chimeric T cell receptor with antibody type-specificity.

Transplant Proc. 21: 127-130

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