FOXO1 enhances CAR T cell stemness, metabolic fitness and efficacy.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
10 Apr 2024
10 Apr 2024
Historique:
received:
13
02
2023
accepted:
27
02
2024
medline:
11
4
2024
pubmed:
11
4
2024
entrez:
10
4
2024
Statut:
aheadofprint
Résumé
Chimeric antigen receptor (CAR) T cell therapy has transformed the treatment of haematological malignancies such as acute lymphoblastic leukaemia, B cell lymphoma and multiple myeloma
Identifiants
pubmed: 38600376
doi: 10.1038/s41586-024-07242-1
pii: 10.1038/s41586-024-07242-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Maude, S. L. et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371, 1507–1517 (2014).
pubmed: 25317870
pmcid: 4267531
doi: 10.1056/NEJMoa1407222
Kalos, M. et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3, 95ra73 (2011).
pubmed: 21832238
pmcid: 3393096
doi: 10.1126/scitranslmed.3002842
Rodriguez-Otero, P. et al. Ide-cel or standard regimens in relapsed and refractory multiple myeloma. N. Engl. J. Med. 388, 1002–1014 (2023).
pubmed: 36762851
doi: 10.1056/NEJMoa2213614
San-Miguel, J. et al. Cilta-cel or standard care in lenalidomide-refractory multiple myeloma. N. Engl. J. Med. 389, 335–347 (2023).
pubmed: 37272512
doi: 10.1056/NEJMoa2303379
Mardiana, S., Solomon, B. J., Darcy, P. K. & Beavis, P. A. Supercharging adoptive T cell therapy to overcome solid tumor-induced immunosuppression. Sci. Transl. Med. 11, eaaw2293 (2019).
pubmed: 31167925
doi: 10.1126/scitranslmed.aaw2293
Chan, J. D. et al. Cellular networks controlling T cell persistence in adoptive cell therapy. Nat. Rev. Immunol. 21, 769–784 (2021).
pubmed: 33879873
doi: 10.1038/s41577-021-00539-6
van Bruggen, J. A. C. et al. Chronic lymphocytic leukemia cells impair mitochondrial fitness in CD8
pubmed: 31076448
pmcid: 7022375
doi: 10.1182/blood.2018885863
Fraietta, J. A. et al. Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia. Nat. Med. 24, 563–571 (2018).
pubmed: 29713085
pmcid: 6117613
doi: 10.1038/s41591-018-0010-1
Blank, C. U. et al. Defining T cell exhaustion. Nat. Rev. Immunol. 19, 665–674 (2019).
pubmed: 31570879
pmcid: 7286441
doi: 10.1038/s41577-019-0221-9
Giraldo, N. A. et al. Tumor-infiltrating and peripheral blood T-cell immunophenotypes predict early relapse in localized clear cell renal cell carcinoma. Clin. Cancer Res. 23, 4416–4428 (2017).
pubmed: 28213366
doi: 10.1158/1078-0432.CCR-16-2848
Sade-Feldman, M. et al. Defining T cell states associated with response to checkpoint immunotherapy in melanoma. Cell 175, 998–1013.e20 (2019).
doi: 10.1016/j.cell.2018.10.038
Giuffrida, L. et al. IL-15 preconditioning augments CAR T cell responses to checkpoint blockade for improved treatment of solid tumors. Mol. Ther. 28, 2379–2393 (2020).
pubmed: 32735774
pmcid: 7647667
doi: 10.1016/j.ymthe.2020.07.018
Klebanoff, C. A. et al. Central memory self/tumor-reactive CD8
pubmed: 15980149
pmcid: 1172264
doi: 10.1073/pnas.0503726102
Siddiqui, I. et al. Intratumoral Tcf1
pubmed: 30635237
doi: 10.1016/j.immuni.2018.12.021
Guo, Y. et al. Phase I study of chimeric antigen receptor-modified T cells in patients with EGFR-positive advanced biliary tract cancers. Clin. Cancer Res. 24, 1277–1286 (2018).
pubmed: 29138340
doi: 10.1158/1078-0432.CCR-17-0432
Soriano-Baguet, L. & Brenner, D. Metabolism and epigenetics at the heart of T cell function. Trends Immunol. 44, 231–244 (2023).
pubmed: 36774330
doi: 10.1016/j.it.2023.01.002
Weber, E. W. et al. Transient rest restores functionality in exhausted CAR-T cells through epigenetic remodeling. Science 372, eaba1786 (2021).
pubmed: 33795428
pmcid: 8049103
doi: 10.1126/science.aba1786
Hirabayashi, K. et al. Dual-targeting CAR-T cells with optimal co-stimulation and metabolic fitness enhance antitumor activity and prevent escape in solid tumors. Nat. Cancer 2, 904–918 (2021).
pubmed: 34746799
pmcid: 8570569
doi: 10.1038/s43018-021-00244-2
Hurton, L. V. et al. Tethered IL-15 augments antitumor activity and promotes a stem-cell memory subset in tumor-specific T cells. Proc. Natl Acad. Sci. USA 113, E7788–E7797 (2016).
pubmed: 27849617
pmcid: 5137758
doi: 10.1073/pnas.1610544113
Kagoya, Y. et al. BET bromodomain inhibition enhances T cell persistence and function in adoptive immunotherapy models. J. Clin. Invest. 126, 3479–3494 (2016).
pubmed: 27548527
pmcid: 5004946
doi: 10.1172/JCI86437
Seo, H. et al. BATF and IRF4 cooperate to counter exhaustion in tumor-infiltrating CAR T cells. Nat. Immunol. 22, 983–995 (2021).
pubmed: 34282330
pmcid: 8319109
doi: 10.1038/s41590-021-00964-8
Lynn, R. C. et al. c-Jun overexpression in CAR T cells induces exhaustion resistance. Nature 576, 293–300 (2019).
pubmed: 31802004
pmcid: 6944329
doi: 10.1038/s41586-019-1805-z
Alizadeh, D. et al. IL15 enhances CAR-T cell antitumor activity by reducing mTORC1 activity and preserving their stem cell memory phenotype. Cancer Immunol. Res. 7, 759–772 (2019).
pubmed: 30890531
pmcid: 6687561
doi: 10.1158/2326-6066.CIR-18-0466
Tejera, M. M., Kim, E. H., Sullivan, J. A., Plisch, E. H. & Suresh, M. FoxO1 controls effector-to-memory transition and maintenance of functional CD8 T cell memory. J. Immunol. 191, 187–199 (2013).
pubmed: 23733882
doi: 10.4049/jimmunol.1300331
Kerdiles, Y. M. et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10, 176–184 (2009).
pubmed: 19136962
pmcid: 2856471
doi: 10.1038/ni.1689
Chen, Z. et al. In vivo CD8
pubmed: 33636129
pmcid: 8054351
doi: 10.1016/j.cell.2021.02.019
Yang, C. Y. et al. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8
pubmed: 22057289
doi: 10.1038/ni.2158
Utzschneider, D. T. et al. Active maintenance of T cell memory in acute and chronic viral infection depends on continuous expression of FOXO1. Cell Rep. 22, 3454–3467 (2018).
pubmed: 29590615
pmcid: 5942184
doi: 10.1016/j.celrep.2018.03.020
Klotz, L. O. et al. Redox regulation of FoxO transcription factors. Redox Biol. 6, 51–72 (2015).
pubmed: 26184557
pmcid: 4511623
doi: 10.1016/j.redox.2015.06.019
Beavis, P. A. et al. Targeting the adenosine 2A receptor enhances chimeric antigen receptor T cell efficacy. J. Clin. Invest. 127, 929–941 (2017).
pubmed: 28165340
pmcid: 5330718
doi: 10.1172/JCI89455
Dong, E. et al. IFN-γ surmounts PD-L1/PD1 inhibition to CAR-T cell therapy by upregulating ICAM-1 on tumor cells. Signal Transduct. Target. Ther. 6, 20 (2021).
pubmed: 33454722
pmcid: 7811529
doi: 10.1038/s41392-020-00357-7
Chmielewski, M., Kopecky, C., Hombach, A. A. & Abken, H. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res. 71, 5697–5706 (2011).
pubmed: 21742772
doi: 10.1158/0008-5472.CAN-11-0103
Larson, R. C. et al. CAR T cell killing requires the IFNγR pathway in solid but not liquid tumours. Nature 604, 563–570 (2022).
pubmed: 35418687
doi: 10.1038/s41586-022-04585-5
Mardiana, S. et al. A multifunctional role for adjuvant anti-4-1BB therapy in augmenting antitumor response by chimeric antigen receptor T cells. Cancer Res. 77, 1296–1309 (2017).
pubmed: 28082401
doi: 10.1158/0008-5472.CAN-16-1831
Kantari-Mimoun, C. et al. CAR T-cell entry into tumor islets is a two-step process dependent on IFNγ and ICAM-1. Cancer Immunol. Res. 9, 1425–1438 (2021).
pubmed: 34686489
doi: 10.1158/2326-6066.CIR-20-0837
Monteiro, L. B., Davanzo, G. G., de Aguiar, C. F. & Moraes-Vieira, P. M. M. Using flow cytometry for mitochondrial assays. MethodsX 7, 100938 (2020).
pubmed: 32551241
pmcid: 7289760
doi: 10.1016/j.mex.2020.100938
Jang, K. J. et al. Mitochondrial function provides instructive signals for activation-induced B-cell fates. Nat. Commun. 6, 6750 (2015).
pubmed: 25857523
doi: 10.1038/ncomms7750
Rad, S. M. A., Poudel, A., Tan, G. M. Y. & McLellan, A. D. Promoter choice: Who should drive the CAR in T cells? PLoS ONE 15, e0232915 (2020).
doi: 10.1371/journal.pone.0232915
Wherry, E. J. et al. Molecular signature of CD8
pubmed: 17950003
doi: 10.1016/j.immuni.2007.09.006
Shan, Q. et al. Tcf1–CTCF cooperativity shapes genomic architecture to promote CD8
pubmed: 35882936
pmcid: 9579964
doi: 10.1038/s41590-022-01263-6
Delpoux, A. et al. FOXO1 constrains activation and regulates senescence in CD8 T cells. Cell Rep. 34, 108674 (2021).
pubmed: 33503413
doi: 10.1016/j.celrep.2020.108674
Melenhorst, J. J. et al. Decade-long leukaemia remissions with persistence of CD4
pubmed: 35110735
pmcid: 9166916
doi: 10.1038/s41586-021-04390-6
Klebanoff, C. A. et al. Inhibition of AKT signaling uncouples T cell differentiation from expansion for receptor-engineered adoptive immunotherapy. JCI Insight 2, e95103 (2017).
pubmed: 29212954
pmcid: 5752304
doi: 10.1172/jci.insight.95103
Kousteni, S. FoxO1, the transcriptional chief of staff of energy metabolism. Bone 50, 437–443 (2012).
pubmed: 21816244
doi: 10.1016/j.bone.2011.06.034
Huang, Q. et al. The primordial differentiation of tumor-specific memory CD8
pubmed: 36208623
doi: 10.1016/j.cell.2022.09.020
Reinhard, K. et al. An RNA vaccine drives expansion and efficacy of claudin-CAR-T cells against solid tumors. Science 367, 446–453 (2020).
pubmed: 31896660
doi: 10.1126/science.aay5967
Piechocki, M. P., Ho, Y. S., Pilon, S. & Wei, W. Z. Human ErbB-2 (Her-2) transgenic mice: a model system for testing Her-2 based vaccines. J. Immunol. 171, 5787–5794 (2003).
pubmed: 14634087
doi: 10.4049/jimmunol.171.11.5787
Darcy, P. K. et al. Redirected perforin-dependent lysis of colon carcinoma by ex vivo genetically engineered CTL. J. Immunol. 164, 3705–3712 (2000).
pubmed: 10725729
doi: 10.4049/jimmunol.164.7.3705
DeLuca, D. S. et al. RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 28, 1530–1532 (2012).
pubmed: 22539670
pmcid: 3356847
doi: 10.1093/bioinformatics/bts196
Zerbino, D. R. et al. Ensembl 2018. Nucleic Acids Res. 46, D754–D761 (2018).
pubmed: 29155950
doi: 10.1093/nar/gkx1098
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308
doi: 10.1093/bioinformatics/btp616
McCarthy, D. J., Chen, Y. & Smyth, G. K. Differential expression analysis of multifactor RNA-seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297 (2012).
pubmed: 22287627
pmcid: 3378882
doi: 10.1093/nar/gks042
Korotkevich, G., Sukhov, V. & Sergushichev, A. Fast gene set enrichment analysis. Preprint at bioRxiv https://doi.org/10.1101/060012 (2019).
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517
pmcid: 1239896
doi: 10.1073/pnas.0506580102
Liberzon, A. et al. Molecular signatures database (MSigDB) 3.0. Bioinformatics 27, 1739–1740 (2011).
pubmed: 21546393
pmcid: 3106198
doi: 10.1093/bioinformatics/btr260
Liberzon, A. et al. The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 1, 417–425 (2015).
pubmed: 26771021
pmcid: 4707969
doi: 10.1016/j.cels.2015.12.004
Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).
pubmed: 10592173
pmcid: 102409
doi: 10.1093/nar/28.1.27
Pont, F., Tosolini, M. & Fournie, J. J. Single-cell signature explorer for comprehensive visualization of single cell signatures across scRNA-seq datasets. Nucleic Acids Res. 47, e133 (2019).
pubmed: 31294801
pmcid: 6868346
doi: 10.1093/nar/gkz601
Gaspar, J. M. NGmerge: merging paired-end reads via novel empirically-derived models of sequencing errors. BMC Bioinformatics 19, 536 (2018).
pubmed: 30572828
pmcid: 6302405
doi: 10.1186/s12859-018-2579-2
Pohl, A. & Beato, M. bwtool: a tool for bigWig files. Bioinformatics 30, 1618–1619 (2014).
pubmed: 24489365
pmcid: 4029031
doi: 10.1093/bioinformatics/btu056
Schep, A. N., Wu, B., Buenrostro, J. D. & Greenleaf, W. J. chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat. Methods 14, 975–978 (2017).
pubmed: 28825706
pmcid: 5623146
doi: 10.1038/nmeth.4401
Castro-Mondragon, J. A. et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 50, D165–D173 (2022).
pubmed: 34850907
doi: 10.1093/nar/gkab1113