B-cell maturation antigen-specific chimeric antigen receptor T cells for multiple myeloma: Clinical experience and future perspectives.


Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
15 10 2020
Historique:
received: 12 11 2019
revised: 04 03 2020
accepted: 24 03 2020
pubmed: 10 4 2020
medline: 13 4 2021
entrez: 10 4 2020
Statut: ppublish

Résumé

Despite major advances in the treatment of multiple myeloma (MM), it remains a largely incurable disease with long-term control often dependent on continuous therapy. More effective, better tolerated treatments are therefore required to achieve durable remissions and to improve the quality of life of MM patients. Adoptive immunotherapy employing T cells expressing chimeric antigen receptors (CAR) is currently among the most promising treatment approaches in cancer. Within the target portfolio for MM immunotherapy, B-cell maturation antigen (BCMA) is among the most widely studied target antigens. BCMA is consistently expressed on MM cells and, importantly, is not expressed in critical healthy tissue. For this reason, it is an ideal target for MM immunotherapy. Several clinical trials evaluating different BCMA-targeting CAR constructs have been initiated and early results are very promising. However, in this rapidly developing clinical landscape, the ultimate role of BCMA-specific CAR-T cell therapy remains unclear. In this review, we will summarize currently available clinical data on BCMA-directed CAR-T cells and discuss potential future perspective for this promising treatment approach in MM.

Identifiants

pubmed: 32270481
doi: 10.1002/ijc.33002
doi:

Substances chimiques

B-Cell Maturation Antigen 0
Receptors, Chimeric Antigen 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2029-2041

Informations de copyright

© 2020 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.

Références

Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378:439-448.
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;377:2531-2544.
Schuster SJ, Bishop MR, Tam CS, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-cell lymphoma. N Engl J Med. 2019;380:45-56.
Garfall AL, Maus MV, Hwang WT, et al. Chimeric antigen receptor T cells against CD19 for multiple myeloma. N Engl J Med. 2015;373:1040-1047.
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. 2018;3:120505.
Tian C, Yang H, Zhu L, Zhang Q, Cao Z, Zhang Y. Anti-CD138 chimeric antigen receptor-modified T cell therapy for multiple myeloma with extensive extramedullary involvement. Ann Hematol. 2017;96:1407-1410.
Ramos CA, Savoldo B, Torrano V, et al. Clinical responses with T lymphocytes targeting malignancy-associated kappa light chains. J Clin Invest. 2016;126:2588-2596.
Laabi Y, Gras MP, Brouet JC, Berger R, Larsen CJ, Tsapis A. The BCMA gene, preferentially expressed during B lymphoid maturation, is bidirectionally transcribed. Nucleic Acids Res. 1994;22:1147-1154.
Laabi Y, Gras MP, Carbonnel F, et al. A new gene, BCM, on chromosome 16 is fused to the interleukin 2 gene by a t(4;16)(q26;p13) translocation in a malignant T cell lymphoma. EMBO J. 1992;11:3897-3904.
Mackay F, Schneider P, Rennert P, Browning J. BAFF and APRIL: a tutorial on B cell survival. Annu Rev Immunol. 2003;21:231-264.
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. 2004;199:91-98.
Xu S, Lam KP. B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol Cell Biol. 2001;21:4067-4074.
Novak AJ, Darce JR, Arendt BK, et al. Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival. Blood. 2004;103:689-694.
Tai YT, Acharya C, An G, et al. APRIL and BCMA promote human multiple myeloma growth and immunosuppression in the bone marrow microenvironment. Blood. 2016;127:3225-3236.
Laurent SA, Hoffmann FS, Kuhn PH, et al. Gamma-Secretase directly sheds the survival receptor BCMA from plasma cells. Nat Commun. 2015;6:7333.
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. 2013;19:2048-2060.
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. 2016;128:1688-1700.
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. 2018;29:585-601.
Turtle CJ, Hanafi LA, Berger C, et al. Immunotherapy of non-Hodgkin's lymphoma with a defined ratio of CD8+ and CD4+ CD19-specific chimeric antigen receptor-modified T cells. Sci Transl Med. 2016;8:355ra116.
Smith EL, Staehr M, Masakayan R, et al. Development and evaluation of an optimal human single-chain variable fragment-derived BCMA-targeted CAR T cell vector. Mol Ther. 2018;26:1447-1456.
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. 2018;9:25764-25780.
Mailankody S, Htut M, Lee KP, et al. JCARH125, anti-BCMA CAR T-cell therapy for relapsed/refractory multiple myeloma: initial proof of concept results from a phase 1/2 multicenter study (EVOLVE). Blood. 2018;132:957-957.
Green DJ, Pont M, Sather BD, 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. 2018;132:1011-1011.
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. 2018;11:141.
Gregory T, Cohen AD, Costello CL, et al. Efficacy and safety of P-Bcma-101 CAR-T cells in patients with relapsed/refractory (r/r) multiple myeloma (MM). Blood. 2018;132:1012-1012.
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. 2018;36:2267-2280.
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. 2019;130:2210-2221.
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 I clinical trial. Blood. 2018;132:959.
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. 2019;380:1726-1737.
Shah N, Alsina M, Siegel DS, et al. Initial results from a phase 1 clinical study of bb21217, a next-generation anti Bcma CAR T therapy. Blood. 2018;132:488-488.
Madduri D, Usmani SZ, 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. 2019;134:577-577.
Jiang S, Jin J, Hao S, et al. Low dose of human scFv-derived BCMA-targeted CAR-T cells achieved fast response and high complete remission in patients with relapsed/refractory multiple myeloma. Blood. 2018;132:960-960.
Liu Y, Chen Z, Fang H, et al. Durable remission achieved from Bcma-directed CAR-T therapy against relapsed or refractory multiple myeloma. Blood. 2018;132:956-956.
Li C, Wang Q, Zhu H, et al. T cells expressing anti B-cell maturation antigen chimeric antigen receptors for plasma cell malignancies. Blood. 2018;132:1013-1013.
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. 2018;132:1009.
Neelapu SS, Tummala S, Kebriaei P, et al. Chimeric antigen receptor T-cell therapy - assessment and management of toxicities. Nat Rev Clin Oncol. 2018;15:47-62.
Lee DW, Santomasso BD, Locke FL, et al. ASBMT consensus grading for cytokine release syndrome and neurological toxicity associated with immune effector cells. Biol Blood Marrow Transplant. 2018;25:625-638.
Fraietta JA, Nobles CL, Sammons MA, et al. Disruption of TET2 promotes the therapeutic efficacy of CD19-targeted T cells. Nature. 2018;558:307-312.
Bonini C, Ferrari G, Verzeletti S, et al. HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science. 1997;276:1719-1724.
Hoyos V, Savoldo B, Quintarelli C, et al. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia. 2010;24:1160-1170.
Straathof KC, Pule MA, Yotnda P, et al. An inducible caspase 9 safety switch for T-cell therapy. Blood. 2005;105:4247-4254.
Sakemura R, Terakura S, Watanabe K, et al. A Tet-on inducible system for controlling CD19-chimeric antigen receptor expression upon drug administration. Cancer Immunol Res. 2016;4:658-668.
Paszkiewicz PJ, Frassle SP, Srivastava S, et al. Targeted antibody-mediated depletion of murine CD19 CAR T cells permanently reverses B cell aplasia. J Clin Invest. 2016;126:4262-4272.
Schubert ML, Hoffmann JM, Dreger P, Muller-Tidow C, Schmitt M. Chimeric antigen receptor transduced T cells: tuning up for the next generation. Int J Cancer. 2018;142:1738-1747.
Fraietta JA, Lacey SF, Orlando EJ, et al. Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia. Nat Med. 2018;24:563-571.
Gagelmann N, Ayuk F, Atanackovic D, Kroger N. B cell maturation antigen-specific chimeric antigen receptor T cells for relapsed or refractory multiple myeloma: a meta-analysis. Eur J Haematol. 2019;129:2210-2221.
Wasch R, Munder M, Marks R. Teaming up for CAR-T cell therapy. Haematologica. 2019;104:2335-2336.
Zelle-Rieser C, Thangavadivel S, Biedermann R, et al. T cells in multiple myeloma display features of exhaustion and senescence at the tumor site. J Hematol Oncol. 2016;9:116.
Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer. 2012;12:671-684.
Cieri N, Camisa B, Cocchiarella F, et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood. 2013;121:573-584.
Hoffmann JM, Schubert ML, Wang L, et al. Differences in expansion potential of naive chimeric antigen receptor T cells from healthy donors and untreated chronic lymphocytic leukemia patients. Front Immunol. 2017;8:1956.
Xu Y, Zhang M, Ramos CA, et al. Closely related T-memory stem cells correlate with in vivo expansion of CAR.CD19-T cells and are preserved by IL-7 and IL-15. Blood. 2014;123:3750-3759.
Gattinoni L, Klebanoff CA, Restifo NP. Pharmacologic induction of CD8+ T cell memory: better living through chemistry. Sci Transl Med. 2009;1:11ps12.
Gargett T, Brown MP. Different cytokine and stimulation conditions influence the expansion and immune phenotype of third-generation chimeric antigen receptor T cells specific for tumor antigen GD2. Cytotherapy. 2015;17:487-495.
Stock S, Hoffmann JM, Schubert ML, et al. Influence of retronectin-mediated T-cell activation on expansion and phenotype of CD19-specific chimeric antigen receptor T cells. Hum Gene Ther. 2018;29:1167-1182.
Yu SS, Nukaya I, Enoki T, et al. In vivo persistence of genetically modified T cells generated ex vivo using the fibronectin CH296 stimulation method. Cancer Gene Ther. 2008;15:508-516.
Lucas CL, Zhang Y, Venida A, et al. Heterozygous splice mutation in PIK3R1 causes human immunodeficiency with lymphoproliferation due to dominant activation of PI3K. J Exp Med. 2014;211:2537-2547.
Soond DR, Bjorgo E, Moltu K, et al. PI3K p110delta regulates T-cell cytokine production during primary and secondary immune responses in mice and humans. Blood. 2010;115:2203-2213.
Bowers JS, Majchrzak K, Nelson MH, et al. PI3Kdelta inhibition enhances the antitumor fitness of adoptively transferred CD8(+) T cells. Front Immunol. 2017;8:1221.
Crompton JG, Sukumar M, Roychoudhuri R, et al. Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res. 2015;75:296-305.
Stock S, Ubelhart R, Schubert ML, et al. Idelalisib for optimized CD19-specific chimeric antigen receptor T cells in chronic lymphocytic leukemia patients. Int J Cancer. 2019;145:1312-1324.
Kebriaei P, Singh H, Huls MH, et al. Phase I trials using sleeping beauty to generate CD19-specific CAR T cells. J Clin Invest. 2016;126:3363-3376.
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;126:2123-2138.
Schuster SJ, Svoboda J, Chong EA, et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017;377:2545-2554.
Lesokhin AM, Ansell SM, Armand P, et al. Nivolumab in patients with relapsed or refractory hematologic malignancy: preliminary results of a phase Ib study. J Clin Oncol. 2016;34:2698-2704.
Badros A, Hyjek E, Ma N, et al. Pembrolizumab, pomalidomide, and low-dose dexamethasone for relapsed/refractory multiple myeloma. Blood. 2017;130:1189-1197.
Bernabei L, Garfall AL, Melenhorst JJ, et al. PD-1 inhibitor combinations as salvage therapy for relapsed/refractory multiple myeloma (MM) patients progressing after BCMA-directed CAR T cells. Blood. 2018;132:1973-1973.
Otahal P, Prukova D, Kral V, et al. Lenalidomide enhances antitumor functions of chimeric antigen receptor modified T cells. Onco Targets Ther. 2016;5:e1115940.
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. 2018;24:106-119.
Works M, Soni N, Hauskins C, et al. Anti-B-cell maturation antigen chimeric antigen receptor T cell function against multiple myeloma is enhanced in the presence of lenalidomide. Mol Cancer Ther. 2019;18:2246-2257.
Moreaux J, Cremer FW, Reme T, et al. The level of TACI gene expression in myeloma cells is associated with a signature of microenvironment dependence versus a plasmablastic signature. Blood. 2005;106:1021-1030.
Lee L, Draper B, Chaplin N, et al. An APRIL-based chimeric antigen receptor for dual targeting of BCMA and TACI in multiple myeloma. Blood. 2018;131:746-758.
Qin H, Ramakrishna S, Nguyen S, et al. Preclinical development of bivalent chimeric antigen receptors targeting both CD19 and CD22. Mol Ther Oncol. 2018;11:127-137.

Auteurs

Leopold Sellner (L)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Heidelberg, Germany.

Fuli Fan (F)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.

Nicola Giesen (N)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
CCU Molecular Hematology/Oncology, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Maria-Luisa Schubert (ML)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.

Hartmut Goldschmidt (H)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Heidelberg, Germany.

Carsten Müller-Tidow (C)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Heidelberg, Germany.

Peter Dreger (P)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Heidelberg, Germany.

Marc S Raab (MS)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
CCU Molecular Hematology/Oncology, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Michael Schmitt (M)

Department of Internal Medicine V, Heidelberg University Hospital, Heidelberg, Germany.
National Center for Tumor Diseases (NCT), German Cancer Consortium (DKTK), Heidelberg, Germany.

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