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TIGIT and PD-1 Mark Intratumoral T Cells with Reduced Effector Function in B-cell Non-Hodgkin Lymphoma

Sarah E. Josefsson, Klaus Beiske, Yngvild N. Blaker, Mette S. Førsund, Harald Holte, Bjørn Østenstad, Eva Kimby, Hakan Köksal, Sébastien Wälchli, Baoyan Bai, Erlend B. Smeland, Ronald Levy, Arne Kolstad, Kanutte Huse and June H. Myklebust
Sarah E. Josefsson
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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Klaus Beiske
3Department of Pathology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway.
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Yngvild N. Blaker
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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Mette S. Førsund
3Department of Pathology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway.
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Harald Holte
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
4Department of Oncology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway.
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Bjørn Østenstad
4Department of Oncology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway.
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Eva Kimby
5Department of Hematology, Karolinska Institutet, Stockholm, Sweden.
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Hakan Köksal
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
6Section for Cellular Therapy, Department for Cancer Treatment, Oslo University Hospital, Oslo, Norway.
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Sébastien Wälchli
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
6Section for Cellular Therapy, Department for Cancer Treatment, Oslo University Hospital, Oslo, Norway.
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Baoyan Bai
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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Erlend B. Smeland
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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Ronald Levy
7Division of Oncology, Stanford School of Medicine, Stanford, California.
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Arne Kolstad
4Department of Oncology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway.
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Kanutte Huse
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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June H. Myklebust
1Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.
2KG Jebsen Centre for B-cell Malignancies, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.
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  • For correspondence: June.Helen.Myklebust@rr-research.no
DOI: 10.1158/2326-6066.CIR-18-0351 Published March 2019
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Abstract

Checkpoint blockade can reverse T-cell exhaustion and promote antitumor responses. Although blocking the PD-1 pathway has been successful in Hodgkin lymphoma, response rates have been modest in B-cell non-Hodgkin lymphoma (NHL). Coblockade of checkpoint receptors may therefore be necessary to optimize antitumor T-cell responses. Here, characterization of coinhibitory receptor expression in intratumoral T cells from different NHL types identified TIGIT and PD-1 as frequently expressed coinhibitory receptors. Tumors from NHL patients were enriched in CD8+ and CD4+ T effector memory cells that displayed high coexpression of TIGIT and PD-1, and coexpression of these checkpoint receptors identified T cells with reduced production of IFNγ, TNFα, and IL2. The suppressed cytokine production could be improved upon in vitro culture in the absence of ligands. Whereas PD-L1 was expressed by macrophages, the TIGIT ligands CD155 and CD112 were expressed by lymphoma cells in 39% and 50% of DLBCL cases and in some mantle cell lymphoma cases, as well as by endothelium and follicular dendritic cells in all NHLs investigated. Collectively, our results show that TIGIT and PD-1 mark dysfunctional T cells and suggest that TIGIT and PD-1 coblockade should be further explored to elicit potent antitumor responses in patients with NHL.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Received May 29, 2018.
  • Revision received October 10, 2018.
  • Accepted January 11, 2019.
  • Published first January 18, 2019.
  • ©2019 American Association for Cancer Research.
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Cancer Immunology Research: 7 (3)
March 2019
Volume 7, Issue 3
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TIGIT and PD-1 Mark Intratumoral T Cells with Reduced Effector Function in B-cell Non-Hodgkin Lymphoma
Sarah E. Josefsson, Klaus Beiske, Yngvild N. Blaker, Mette S. Førsund, Harald Holte, Bjørn Østenstad, Eva Kimby, Hakan Köksal, Sébastien Wälchli, Baoyan Bai, Erlend B. Smeland, Ronald Levy, Arne Kolstad, Kanutte Huse and June H. Myklebust
Cancer Immunol Res March 1 2019 (7) (3) 355-362; DOI: 10.1158/2326-6066.CIR-18-0351

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TIGIT and PD-1 Mark Intratumoral T Cells with Reduced Effector Function in B-cell Non-Hodgkin Lymphoma
Sarah E. Josefsson, Klaus Beiske, Yngvild N. Blaker, Mette S. Førsund, Harald Holte, Bjørn Østenstad, Eva Kimby, Hakan Köksal, Sébastien Wälchli, Baoyan Bai, Erlend B. Smeland, Ronald Levy, Arne Kolstad, Kanutte Huse and June H. Myklebust
Cancer Immunol Res March 1 2019 (7) (3) 355-362; DOI: 10.1158/2326-6066.CIR-18-0351
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