Generation of TCR-Expressing Innate Lymphoid-like Helper Cells that Induce Cytotoxic T Cell-Mediated Anti-leukemic Cell Response

Ueda, N.; Uemura, Y.; Zhang, R.; Kitayama, S.; Iriguchi, S.; Kawai, Y.; Yasui, Y.; Tatsumi, M.; Ueda, T.; Liu, T.-Y.; Mizoro, Yasutaka; Okada, C.; Watanabe, A.; Nakanishi, M.; Senju, S.; Nishimura, Y.; Kuzushima, K.; Kiyoi, H.; Naoe, T.; Kaneko, S.

doi:10.1016/j.stemcr.2018.04.025

Article (Scientific journals)

Generation of TCR-Expressing Innate Lymphoid-like Helper Cells that Induce Cytotoxic T Cell-Mediated Anti-leukemic Cell Response

Ueda, N.; Uemura, Y.; Zhang, R. et al.

2018 • In Stem Cell Reports, 10 (6), p. 1935-1946

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/247967

DOI
10.1016/j.stemcr.2018.04.025

PubMed
29805109

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Keywords :

CD40L; DC activation; T cell differentiation; CD3 antigen; CD4 antigen; CD40 ligand; CD8 antigen; T lymphocyte receptor; WT1 protein; Article; T lymphocyte activation; Biomarkers; Cell Differentiation; Dendritic Cells; Gene Expression; Humans; Immunity, Innate; Immunophenotyping; Induced Pluripotent Stem Cells; Leukemia, Myelogenous, Chronic, BCR-ABL Positive; Receptors, Antigen, T-Cell; T-Cell Antigen Receptor Specificity; T-Lymphocytes, Cytotoxic; T-Lymphocytes, Helper-Inducer; WT1 Proteins

Abstract :

[en] CD4+ T helper (Th) cell activation is essential for inducing cytotoxic T lymphocyte (CTL) responses against malignancy. We reprogrammed a Th clone specific for chronic myelogenous leukemia (CML)-derived b3a2 peptide to pluripotency and re-differentiated the cells into original TCR-expressing T-lineage cells (iPS-T cells) with gene expression patterns resembling those of group 1 innate lymphoid cells. CD4 gene transduction into iPS-T cells enhanced b3a2 peptide-specific responses via b3a2 peptide-specific TCR. iPS-T cells upregulated CD40 ligand (CD40L) expression in response to interleukin-2 and interleukin-15. In the presence of Wilms tumor 1 (WT1) peptide, antigen-specific dendritic cells (DCs) conditioned by CD4-modified CD40Lhigh iPS-T cells stimulated WT1-specific CTL priming, which eliminated WT1 peptide-expressing CML cells in vitro and in vivo. Thus, CD4 modification of CD40Lhigh iPS-T cells generates innate lymphoid helper-like cells inducing bcr-abl-specific TCR signaling that mediates effectiveanti-leukemic CTL responses via DC maturation, showing potential for adjuvant immunotherapy against leukemia. Kaneko and colleagues describe the generation of CD4+ T helper clone-derived iPSCs and differentiation of the cells into T-lineage cells, which had molecular signatures and functional properties more consistent with group 1 innate lymphoid cells. CD4 transduction and CD40 ligand high population purification of the regenerated cells enhanced the antigen-specific adjuvant responses via dendritic cells in an antigen-specific manner. © 2018 The Authors

Disciplines :

Immunology & infectious disease

Author, co-author :

Ueda, N.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Uemura, Y.; National Cancer Center > Exploratory Oncology Research & Clinical Trial Center > Division of Cancer Immunotherapy

Zhang, R.; National Cancer Center > Exploratory Oncology Research & Clinical Trial Center > Division of Cancer Immunotherapy

Kitayama, S.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Iriguchi, S.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Kawai, Y.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Yasui, Y.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Tatsumi, M.; Aichi Cancer Center Research Institute > Division of Immunology

Ueda, T.; Kyoto University > Center for iPS Cell Research and Application > Department of Cell Growth and Differentiation

Liu, T.-Y.; Aichi Cancer Center Research Institute > Division of Immunology

More authors (10 more)

Language :

English

Title :

Generation of TCR-Expressing Innate Lymphoid-like Helper Cells that Induce Cytotoxic T Cell-Mediated Anti-leukemic Cell Response

Publication date :

June 2018

Journal title :

Stem Cell Reports

eISSN :

2213-6711

Publisher :

Cell Press

Volume :

Issue :

Pages :

1935-1946

Peer reviewed :

Peer Reviewed verified by ORBi

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Bibliography

Bennett, S.R., Carbone, F.R., Karamalis, F., Flavell, R.A., Miller, J.F., Heath, W.R., Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393 (1998), 478–480.
Bennett, S.R., Carbone, F.R., Karamalis, F., Miller, J.F., Heath, W.R., Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J. Exp. Med. 186 (1997), 65–70.
Boise, L.H., Minn, A.J., Noel, P.J., June, C.H., Accavitti, M.A., Lindsten, T., Thompson, C.B., CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 3 (1995), 87–98.
Cai, A., Keskin, D.B., DeLuca, D.S., Alonso, A., Zhang, W., Zhang, G.L., Hammond, N.N., Nardi, V., Stone, R.M., Neuberg, D., et al. Mutated BCR-ABL generates immunogenic T-cell epitopes in CML patients. Clin. Cancer Res. 18 (2012), 5761–5772.
Carbone, E., Ruggiero, G., Terrazzano, G., Palomba, C., Manzo, C., Fontana, S., Spits, H., Karre, K., Zappacosta, S., A new mechanism of NK cell cytotoxicity activation: the CD40-CD40 ligand interaction. J. Exp. Med. 185 (1997), 2053–2060.
Cording, S., Medvedovic, J., Aychek, T., Eberl, G., Innate lymphoid cells in defense, immunopathology and immunotherapy. Nat. Immunol 17 (2016), 755–757.
Fransen, M.F., Sluijter, M., Morreau, H., Arens, R., Melief, C.J., Local activation of CD8 T cells and systemic tumor eradication without toxicity via slow release and local delivery of agonistic CD40 antibody. Clin. Cancer Res. 17 (2011), 2270–2280.
Groom, J.R., Luster, A.D., CXCR3 in T cell function. Exp. Cell Res. 317 (2011), 620–631.
Janeway, C.A. Jr., The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu. Rev. Immunol. 10 (1992), 645–674.
Kaneko, S., Onodera, M., Fujiki, Y., Nagasawa, T., Nakauchi, H., Simplified retroviral vector gcsap with murine stem cell virus long terminal repeat allows high and continued expression of enhanced green fluorescent protein by human hematopoietic progenitors engrafted in nonobese diabetic/severe combined immunodeficient mice. Hum. Gene Ther. 12 (2001), 35–44.
Kim, H.J., Cantor, H., CD4 T-cell subsets and tumor immunity: the helpful and the not-so-helpful. Cancer Immunol. Res. 2 (2014), 91–98.
Kitayama, S., Zhang, R., Liu, T.Y., Ueda, N., Iriguchi, S., Yasui, Y., Kawai, Y., Tatsumi, M., Hirai, N., Mizoro, Y., et al. Cellular adjuvant properties, direct cytotoxicity of re-differentiated Valpha24 invariant NKT-like cells from human induced pluripotent stem cells. Stem Cell Rep 6 (2016), 213–227.
Komlosi, Z.I., Kovacs, N., van de Veen, W., Kirsch, A.I., Fahrner, H.B., Wawrzyniak, M., Rebane, A., Stanic, B., Palomares, O., Ruckert, B., et al. Human CD40 ligand-expressing type 3 innate lymphoid cells induce IL-10-producing immature transitional regulatory B cells. J. Allergy Clin. Immunol., 2017, 10.1016/j.jaci.2017.07.046.
Kreiter, S., Vormehr, M., van de Roemer, N., Diken, M., Lower, M., Diekmann, J., Boegel, S., Schrors, B., Vascotto, F., Castle, J.C., et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 520 (2015), 692–696.
Li, L., Leid, M., Rothenberg, E.V., An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 329 (2010), 89–93.
Magri, G., Miyajima, M., Bascones, S., Mortha, A., Puga, I., Cassis, L., Barra, C.M., Comerma, L., Chudnovskiy, A., Gentile, M., et al. Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat. Immunol 15 (2014), 354–364.
McKenzie, A.N., Spits, H., Eberl, G., Innate lymphoid cells in inflammation and immunity. Immunity 41 (2014), 366–374.
Molldrem, J.J., Lee, P.P., Wang, C., Felio, K., Kantarjian, H.M., Champlin, R.E., Davis, M.M., Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat. Med. 6 (2000), 1018–1023.
Naito, T., Tanaka, H., Naoe, Y., Taniuchi, I., Transcriptional control of T-cell development. Int. Immunol. 23 (2011), 661–668.
Neofytou, E., O'Brien, C.G., Couture, L.A., Wu, J.C., Hurdles to clinical translation of human induced pluripotent stem cells. J. Clin. Invest 125 (2015), 2551–2557.
Nishimura, T., Kaneko, S., Kawana-Tachikawa, A., Tajima, Y., Goto, H., Zhu, D., Nakayama-Hosoya, K., Iriguchi, S., Uemura, Y., Shimizu, T., et al. Generation of rejuvenated antigen-specific T cells by reprogramming to pluripotency and redifferentiation. Cell Stem Cell 12 (2013), 114–126.
Rezvani, K., Grube, M., Brenchley, J.M., Sconocchia, G., Fujiwara, H., Price, D.A., Gostick, E., Yamada, K., Melenhorst, J., Childs, R., et al. Functional leukemia-associated antigen-specific memory CD8+ T cells exist in healthy individuals and in patients with chronic myelogenous leukemia before and after stem cell transplantation. Blood 102 (2003), 2892–2900.
Ridge, J.P., Di Rosa, F., Matzinger, P., A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 393 (1998), 474–478.
Schoenberger, S.P., Toes, R.E., van der Voort, E.I., Offringa, R., Melief, C.J., T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393 (1998), 480–483.
Sonnenberg, G.F., Artis, D., Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 21 (2015), 698–708.
Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J.P., Eberl, G., Koyasu, S., Locksley, R.M., McKenzie, A.N., Mebius, R.E., et al. Innate lymphoid cells – a proposal for uniform nomenclature. Nat. Rev. Immunol. 13 (2013), 145–149.
Summers deLuca, L., Gommerman, J.L., Fine-tuning of dendritic cell biology by the TNF superfamily. Nat. Rev. Immunol. 12 (2012), 339–351.
Tabata, H., Kanai, T., Yoshizumi, H., Nishiyama, S., Fujimoto, S., Matsuda, I., Yasukawa, M., Matsushita, S., Nishimura, Y., Characterization of self-glutamic acid decarboxylase 65-reactive CD4+ T-cell clones established from Japanese patients with insulin-dependent diabetes mellitus. Hum. Immunol. 59 (1998), 549–560.
Ueda, N., Zhang, R., Tatsumi, M., Liu, T.Y., Kitayama, S., Yasui, Y., Sugai, S., Iwama, T., Senju, S., Okada, S., et al. BCR-ABL-specific CD4+ T-helper cells promote the priming of antigen-specific cytotoxic T cells via dendritic cells. Cell. Mol. Immunol 15 (2016), 15–26.
Vizcardo, R., Masuda, K., Yamada, D., Ikawa, T., Shimizu, K., Fujii, S., Koseki, H., Kawamoto, H., Regeneration of human tumor antigen-specific T cells from iPSCs derived from mature CD8(+) T cells. Cell Stem Cell 12 (2013), 31–36.
Wakao, H., Yoshikiyo, K., Koshimizu, U., Furukawa, T., Enomoto, K., Matsunaga, T., Tanaka, T., Yasutomi, Y., Yamada, T., Minakami, H., et al. Expansion of functional human mucosal-associated invariant T cells via reprogramming to pluripotency and redifferentiation. Cell Stem Cell 12 (2013), 546–558.
Wiesel, M., Oxenius, A., From crucial to negligible: functional CD8(+) T-cell responses and their dependence on CD4(+) T-cell help. Eur. J. Immunol. 42 (2012), 1080–1088.
Yamada, D., Iyoda, T., Vizcardo, R., Shimizu, K., Sato, Y., Endo, T.A., Kitahara, G., Okoshi, M., Kobayashi, M., Sakurai, M., et al. Efficient regeneration of human Valpha24+ invariant natural killer T cells and their anti-tumor activity in vivo. Stem Cells 34 (2016), 2852–2860.
Zhang, R., Liu, T., Senju, S., Haruta, M., Hirosawa, N., Suzuki, M., Tatsumi, M., Ueda, N., Maki, H., Nakatsuka, R., et al. Generation of mouse pluripotent stem cell-derived proliferating myeloid cells as an unlimited source of functional antigen-presenting cells. Cancer Immunol. Res. 3 (2015), 668–677.