GM-CSF disruption in CART cells modulates T cell activation and enhances CART cell anti-tumor activity.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
06
06
2021
accepted:
04
04
2022
revised:
31
03
2022
pubmed:
21
4
2022
medline:
7
6
2022
entrez:
20
4
2022
Statut:
ppublish
Résumé
Inhibitory myeloid cells and their cytokines play critical roles in limiting chimeric antigen receptor T (CART) cell therapy by contributing to the development of toxicities and resistance following infusion. We have previously shown that neutralization of granulocyte-macrophage colony-stimulating factor (GM-CSF) prevents these toxicities and enhances CART cell functions by inhibiting myeloid cell activation. In this report, we study the direct impact of GM-CSF disruption during the production of CD19-directed CART cells on their effector functions, independent of GM-CSF modulation of myeloid cells. In this study, we show that antigen-specific activation of GM-CSF
Identifiants
pubmed: 35440691
doi: 10.1038/s41375-022-01572-7
pii: 10.1038/s41375-022-01572-7
pmc: PMC9234947
mid: NIHMS1795688
doi:
Substances chimiques
Cytokines
0
Granulocyte-Macrophage Colony-Stimulating Factor
83869-56-1
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1635-1645Subventions
Organisme : NCI NIH HHS
ID : K12 CA090628
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA201127
Pays : United States
Organisme : NCI NIH HHS
ID : R37 CA266344
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002377
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
June CH, Sadelain M. Chimeric antigen receptor therapy. N Engl J Med. 2018;379:64–73.
doi: 10.1056/NEJMra1706169
Anagnostou T, Riaz IB, Hashmi SK, Murad MH, Kenderian SS. Anti-CD19 chimeric antigen receptor T-cell therapy in acute lymphocytic leukaemia: a systematic review and meta-analysis. Lancet Haematol. 2020;7:e816–e826.
doi: 10.1016/S2352-3026(20)30277-5
Khadka RH, Sakemura R, Kenderian SS, Johnson AJ. Management of cytokine release syndrome: an update on emerging antigen-specific T cell engaging immunotherapies. Immunotherapy. 2019;11:851–7.
doi: 10.2217/imt-2019-0074
Teachey DT, Lacey SF, Shaw PA, Melenhorst JJ, Maude SL, Frey N, et al. Identification of predictive biomarkers for cytokine release syndrome after chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Cancer Discov. 2016;6:664–79.
doi: 10.1158/2159-8290.CD-16-0040
Locke FL, Ghobadi A, Jacobson CA, Miklos DB, Lekakis LJ, Oluwole OO, et al. Long-term safety and activity of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1): a single-arm, multicentre, phase 1–2 trial. Lancet Oncol. 2019;20:31–42.
doi: 10.1016/S1470-2045(18)30864-7
Schuster SJ, Svoboda J, Chong EA, Nasta SD, Mato AR, Anak O, et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017;377:2545–54.
doi: 10.1056/NEJMoa1708566
Sakemura R, Cox MJ, Hefazi M, Siegler EL, Kenderian SS. Resistance to CART cell therapy: lessons learned from the treatment of hematological malignancies. Leuk Lymphoma. 2021;62:1–18.
doi: 10.1080/10428194.2021.1894648
Cox MJ, Kenderian SS. Omics analyses provide insights to CART cell therapy resistance. J Transl Genet Genom 2021;5:80–8.
Sterner RM, Kenderian SS. Myeloid cell and cytokine interactions with chimeric antigen receptor-T-cell therapy: implication for future therapies. Curr Opin Hematol. 2020;27:41–48.
doi: 10.1097/MOH.0000000000000559
Stroncek DF, Ren J, Lee DW, Tran M, Frodigh SE, Sabatino M, et al. Myeloid cells in peripheral blood mononuclear cell concentrates inhibit the expansion of chimeric antigen receptor T cells. Cytotherapy. 2016;18:893–901.
doi: 10.1016/j.jcyt.2016.04.003
Ruella M, Klichinsky M, Kenderian SS, Shestova O, Ziober A, Kraft DO, et al. Overcoming the immunosuppressive tumor microenvironment of Hodgkin Lymphoma using chimeric antigen receptor T cells. Cancer Disco. 2017;7:1154–67.
doi: 10.1158/2159-8290.CD-16-0850
Jain MD, Zhao H, Wang X, Atkins R, Menges M, Reid K, et al. Tumor interferon signaling and suppressive myeloid cells associate with CAR T cell failure in large B cell lymphoma. Blood. 2021;137:2621–33.
doi: 10.1182/blood.2020007445
Neelapu SS, Locke FL, Bartlett NL, Lekakis LJ, Miklos DB, Jacobson CA, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377:2531–44.
doi: 10.1056/NEJMoa1707447
Shi Y, Liu CH, Roberts AI, Das J, Xu G, Ren G, et al. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don’t know. Cell Res. 2006;16:126–33.
doi: 10.1038/sj.cr.7310017
Tugues S, Amorim A, Spath S, Martin-Blondel G, Schreiner B, De Feo D, et al. Graft-versus-host disease, but not graft-versus-leukemia immunity, is mediated by GM-CSF-licensed myeloid cells. Sci Transl Med. 2018;10.
Sterner RM, Sakemura R, Cox MJ, Yang N, Khadka RH, Forsman CL, et al. GM-CSF inhibition reduces cytokine release syndrome and neuroinflammation but enhances CAR-T cell function in xenografts. Blood. 2019;133:697–709.
doi: 10.1182/blood-2018-10-881722
Sterner RM, Cox MJ, Sakemura R, Kenderian SS. Using CRISPR/Cas9 to knock out GM-CSF in CAR-T cells. J. Vis. Exp. 2019;149:e59629.
Manriquez-Roman C, Siegler EL, Kenderian SS. CRISPR takes the front seat in CART-cell development. BioDrugs. 2021;35:113–24.
doi: 10.1007/s40259-021-00473-y
Sachdeva M, Duchateau P, Depil S, Poirot L, Valton J. Granulocyte-macrophage colony-stimulating factor inactivation in CAR T-cells prevents monocyte-dependent release of key cytokine release syndrome mediators. J Biol Chem. 2019;294:5430–7.
doi: 10.1074/jbc.AC119.007558
Zhang J, Roberts AI, Liu C, Ren G, Xu G, Zhang L, et al. A novel subset of helper T cells promotes immune responses by secreting GM-CSF. Cell Death Differ. 2013;20:1731–41.
doi: 10.1038/cdd.2013.130
Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics. 2010;26:589–95.
doi: 10.1093/bioinformatics/btp698
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–303.
doi: 10.1101/gr.107524.110
Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, et al. A global reference for human genetic variation. Nature. 2015;526:68–74.
doi: 10.1038/nature15393
Stemmer M, Thumberger T, Del Sol Keyer M, Wittbrodt J, Mateo JL. CCTop: an intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS One. 2015;10:e0124633.
doi: 10.1371/journal.pone.0124633
Brinkman EK, Chen T, Amendola M, van Steensel B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 2014;42:e168–e168.
doi: 10.1093/nar/gku936
Iyer V, Boroviak K, Thomas M, Doe B, Riva L, Ryder E, et al. No unexpected CRISPR-Cas9 off-target activity revealed by trio sequencing of gene-edited mice. PLoS Genet. 2018;14:e1007503.
doi: 10.1371/journal.pgen.1007503
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
doi: 10.1186/s13059-014-0550-8
Zhang Y, Li H, Wang X, Gao X, Liu X. Regulation of T cell development and activation by creatine kinase B. PLoS One. 2009;4:e5000.
doi: 10.1371/journal.pone.0005000
Juric V, Chen CC, Lau LF. Fas-mediated apoptosis is regulated by the extracellular matrix protein CCN1 (CYR61) in vitro and in vivo. Mol Cell Biol. 2009;29:3266–79.
doi: 10.1128/MCB.00064-09
Yamamoto TN, Lee PH, Vodnala SK, Gurusamy D, Kishton RJ, Yu Z, et al. T cells genetically engineered to overcome death signaling enhance adoptive cancer immunotherapy. J Clin Investig. 2019;129:1551–65.
doi: 10.1172/JCI121491
Michelozzi IM, Gomez-Castaneda E, Pohle RVC, Rodriguez F, Sufi J, Puigdevall P, et al. The Enhanced Functionality of Low-Affinity CD19 CAR T Cells Is Associated with Activation Priming and Polyfunctional Cytokine Phenotype. Blood 2020;136:52–53.
doi: 10.1182/blood-2020-141249
Tschumi BO, Dumauthioz N, Marti B, Zhang L, Schneider P, Mach JP, et al. CART cells are prone to Fas- and DR5-mediated cell death. J Immunother Cancer. 2018;6:71.
doi: 10.1186/s40425-018-0385-z
Benmebarek MR, Karches CH, Cadilha BL, Lesch S, Endres S, Kobold S. Killing mechanisms of chimeric antigen receptor (CAR) T cells. Int J Mol Sci. 2019;20:1283.
doi: 10.3390/ijms20061283
Gomes-Silva D, Mukherjee M, Srinivasan M, Krenciute G, Dakhova O, Zheng Y, et al. Tonic 4-1BB costimulation in chimeric antigen receptors impedes T cell survival and is vector-dependent. Cell Rep. 2017;21:17–26.
doi: 10.1016/j.celrep.2017.09.015
Kunkele A, Johnson AJ, Rolczynski LS, Chang CA, Hoglund V, Kelly-Spratt KS, et al. Functional tuning of CARs reveals signaling threshold above which CD8+ CTL antitumor potency is attenuated due to cell Fas-FasL-dependent AICD. Cancer Immunol Res. 2015;3:368–79.
doi: 10.1158/2326-6066.CIR-14-0200
Siegler EL, Simone BW, Sakemura R, Tapper EE, Horvei P, Cox MJ, et al. Efficient gene editing of CART cells with CRISPR-Cas12a for enhanced antitumor efficacy. Blood. 2020;136:6–7.
doi: 10.1182/blood-2020-141115
Ghezraoui H, Piganeau M, Renouf B, Renaud JB, Sallmyr A, Ruis B, et al. Chromosomal translocations are mediated by canonical NHEJ in human cells. Cancer Discov. 2014;4:OF12.
doi: 10.1158/2159-8290.CD-RW2014-197
Stadtmauer EA, Cohen AD, Weber K, Lacey SF, Gonzalez VE, Melenhorst JJ, et al. First-in-human assessment of feasibility and safety of multiplexed genetic engineering of autologous T cells expressing NY-ESO -1 TCR and CRISPR/Cas9 gene edited to eliminate endogenous TCR and PD-1 (NYCE T cells) in advanced multiple myeloma (MM) and sarcoma. Blood. 2019;134:49.
doi: 10.1182/blood-2019-122374
Yi Y, Chai X, Zheng L, Zhang Y, Shen J, Hu B, et al. CRISPR-edited CART with GM-CSF knockout and auto secretion of IL6 and IL1 blockers in patients with hematologic malignancy. Cell Disco. 2021;7:27.
doi: 10.1038/s41421-021-00255-4