Targeting HLA-E-overexpressing cancers with a NKG2A/C switch receptor.

CAR T cells HLA-E NK cells NKG2 receptor family Pre-clinical research cancer immunotherapy glioblastoma

Journal

Med (New York, N.Y.)
ISSN: 2666-6340
Titre abrégé: Med
Pays: United States
ID NLM: 101769215

Informations de publication

Date de publication:
10 Oct 2024
Historique:
received: 30 01 2024
revised: 06 06 2024
accepted: 23 09 2024
medline: 19 10 2024
pubmed: 19 10 2024
entrez: 18 10 2024
Statut: aheadofprint

Résumé

Human leukocyte antigen (HLA)-E is overexpressed by a large proportion of solid tumors, including malignant glioblastoma, and acts as a major checkpoint for NKG2A We engineered a chimeric A/C switch receptor, combining the high HLA-E binding affinity of the NKG2A receptor ectodomain with the activating signaling of the NKG2C receptor endodomain. The cytotoxic function of A/C switch-transduced NK and T cells was evaluated against tumor cells with varying levels of HLA-E expression. In vivo efficacy was assessed using a xenograft model of glioblastoma. A/C switch-transduced NK and T cells exhibited superior and specific cytotoxicity against tumor cells with medium to high HLA-E expression. A/C switch-expressing human T cells demonstrated enhanced anti-tumor function in a glioblastoma xenograft model. The activity of the modified T cells was governed by an equilibrium between A/C switch levels and HLA-E expression, creating a therapeutic window to minimize on-target, off-tumor toxicities. Normal cells remained insensitive to A/C switch T cells, even after interferon (IFN)-γ pretreatment to induce HLA-E expression. The A/C switch receptor effectively targets tumor cells expressing high levels of HLA-E, either alone or in combination with other engineered specificities, to overcome the suppressive NKG2A/HLA-E checkpoint. This approach offers a promising therapeutic strategy with a favorable safety profile for targeting HLA-E-overexpressing tumors. This work was funded by The Research Council of Norway, the Norwegian Cancer Society, and the National Cancer Institute.

Sections du résumé

BACKGROUND BACKGROUND
Human leukocyte antigen (HLA)-E is overexpressed by a large proportion of solid tumors, including malignant glioblastoma, and acts as a major checkpoint for NKG2A
METHODS METHODS
We engineered a chimeric A/C switch receptor, combining the high HLA-E binding affinity of the NKG2A receptor ectodomain with the activating signaling of the NKG2C receptor endodomain. The cytotoxic function of A/C switch-transduced NK and T cells was evaluated against tumor cells with varying levels of HLA-E expression. In vivo efficacy was assessed using a xenograft model of glioblastoma.
FINDINGS RESULTS
A/C switch-transduced NK and T cells exhibited superior and specific cytotoxicity against tumor cells with medium to high HLA-E expression. A/C switch-expressing human T cells demonstrated enhanced anti-tumor function in a glioblastoma xenograft model. The activity of the modified T cells was governed by an equilibrium between A/C switch levels and HLA-E expression, creating a therapeutic window to minimize on-target, off-tumor toxicities. Normal cells remained insensitive to A/C switch T cells, even after interferon (IFN)-γ pretreatment to induce HLA-E expression.
CONCLUSIONS CONCLUSIONS
The A/C switch receptor effectively targets tumor cells expressing high levels of HLA-E, either alone or in combination with other engineered specificities, to overcome the suppressive NKG2A/HLA-E checkpoint. This approach offers a promising therapeutic strategy with a favorable safety profile for targeting HLA-E-overexpressing tumors.
FUNDING BACKGROUND
This work was funded by The Research Council of Norway, the Norwegian Cancer Society, and the National Cancer Institute.

Identifiants

pubmed: 39423821
pii: S2666-6340(24)00377-5
doi: 10.1016/j.medj.2024.09.010
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests K.-J.M. is a consultant and has research support from Fate Therapeutics. K.-J.M. has research support from Oncopeptides. K.-J.M. and Q.H. are consultants at Vycellix. All relationships have been approved by Oslo University Hospital, University of Oslo and Karolinska Institute. M. Sadelain reports research funding from Takeda Pharmaceuticals, Atara Biotherapeutics, Fate Therapeutics, and Mnemo Therapeutics, all of which are unrelated to the present research. M. Sadelain is a scientific cofounder of Mnemo Therapeutics.

Auteurs

Michelle Sætersmoen (M)

Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.

Ivan S Kotchetkov (IS)

Department of Neurology, Memorial Sloan Kettering Cancer Center, New York, NY, USA; Center for Cell Engineering and Immunology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Lamberto Torralba-Raga (L)

Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.

Jorge Mansilla-Soto (J)

Center for Cell Engineering and Immunology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Ebba Sohlberg (E)

Center for Infectious Medicine, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, Sweden.

Silje Zandstra Krokeide (SZ)

Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway.

Quirin Hammer (Q)

Center for Infectious Medicine, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, Sweden.

Michel Sadelain (M)

Center for Cell Engineering and Immunology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Karl-Johan Malmberg (KJ)

Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway. Electronic address: k.j.malmberg@medisin.uio.no.

Classifications MeSH