Coagulation factor VIIa enhances programmed death-ligand 1 expression and its stability in breast cancer cells to promote breast cancer immune evasion.


Journal

Journal of thrombosis and haemostasis : JTH
ISSN: 1538-7836
Titre abrégé: J Thromb Haemost
Pays: England
ID NLM: 101170508

Informations de publication

Date de publication:
12 2023
Historique:
received: 25 08 2022
revised: 02 08 2023
accepted: 03 08 2023
medline: 27 11 2023
pubmed: 15 8 2023
entrez: 14 8 2023
Statut: ppublish

Résumé

Immunotherapy for breast cancer has not gained significant success. Coagulation factor VIIa (FVIIa)-tissue factor (TF) mediated activation of protease-activated receptor 2 (PAR2) is shown to promote metastasis and secretion of the immune-modulatory cytokines but the role of FVIIa in cancer immunology is still not well understood. Here, we aim to investigate whether FVIIa protects breast cancer cells from CD8 T-cell-mediated killing. Peripheral blood mononuclear cell-derived CD8 T cells were cocultured with vehicle or FVIIa pretreated MDAMB468 cells. The proliferation and activity of CD8 T cells were measured by flow cytometry and ELISA. An allograft model, using wild-type or TF/PAR2-deleted 4T1 cells, was employed to determine the effect of FVIIa on breast cancer immune evasion in vivo. Here, we demonstrate that TF-FVIIa induces programmed death-ligand 1 (PD-L1) in breast cancer cells by activating PAR2. PAR2 activation triggers large tumor suppressor kinase 1 (LATS1) inactivation leading to loss of yes-associated protein (YAP)/transcriptional coactivator with PDZ-binding motif (TAZ) phosphorylation and subsequent nuclear localization of YAP/TAZ. YAP/TAZ inhibition reduces PD-L1 expression and increases CD8 T-cell activity. We further demonstrate that, apart from transcriptional induction of PD-L1, PAR2 activation also increases PD-L1 stability by enhancing its glycosylation through N-glycosyltransferases STT3A and STT3B. In a mouse model of breast cancer, tumor cell-specific PAR2 depletion leads to PD-L1 downregulation and increases anti-PD-1 immunotherapy efficacy. In conclusion, we showed that FVIIa-mediated signaling cascade in cancer cells serves as a tumor intrinsic mechanism of immunosuppression to promote cancer immune evasion.

Sections du résumé

BACKGROUND
Immunotherapy for breast cancer has not gained significant success. Coagulation factor VIIa (FVIIa)-tissue factor (TF) mediated activation of protease-activated receptor 2 (PAR2) is shown to promote metastasis and secretion of the immune-modulatory cytokines but the role of FVIIa in cancer immunology is still not well understood.
OBJECTIVES
Here, we aim to investigate whether FVIIa protects breast cancer cells from CD8 T-cell-mediated killing.
METHODS
Peripheral blood mononuclear cell-derived CD8 T cells were cocultured with vehicle or FVIIa pretreated MDAMB468 cells. The proliferation and activity of CD8 T cells were measured by flow cytometry and ELISA. An allograft model, using wild-type or TF/PAR2-deleted 4T1 cells, was employed to determine the effect of FVIIa on breast cancer immune evasion in vivo.
RESULTS
Here, we demonstrate that TF-FVIIa induces programmed death-ligand 1 (PD-L1) in breast cancer cells by activating PAR2. PAR2 activation triggers large tumor suppressor kinase 1 (LATS1) inactivation leading to loss of yes-associated protein (YAP)/transcriptional coactivator with PDZ-binding motif (TAZ) phosphorylation and subsequent nuclear localization of YAP/TAZ. YAP/TAZ inhibition reduces PD-L1 expression and increases CD8 T-cell activity. We further demonstrate that, apart from transcriptional induction of PD-L1, PAR2 activation also increases PD-L1 stability by enhancing its glycosylation through N-glycosyltransferases STT3A and STT3B.
CONCLUSION
In a mouse model of breast cancer, tumor cell-specific PAR2 depletion leads to PD-L1 downregulation and increases anti-PD-1 immunotherapy efficacy. In conclusion, we showed that FVIIa-mediated signaling cascade in cancer cells serves as a tumor intrinsic mechanism of immunosuppression to promote cancer immune evasion.

Identifiants

pubmed: 37579880
pii: S1538-7836(23)00632-3
doi: 10.1016/j.jtha.2023.08.008
pii:
doi:

Substances chimiques

CD274 protein, human 0
B7-H1 Antigen 0
Factor VIIa EC 3.4.21.21
Thromboplastin 9035-58-9
Receptor, PAR-2 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3522-3538

Informations de copyright

Copyright © 2023 International Society on Thrombosis and Haemostasis. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interests There are no competing interests to disclose.

Auteurs

Subhojit Paul (S)

School of Biological Sciences, Indian Association for the Cultivation of Science, Kolkata, India.

Kaushik Das (K)

Department of Cellular and Molecular Biology, The University of Texas Health Science Center at Tyler, Tyler, Texas.

Arnab Ghosh (A)

School of Biological Sciences, Indian Association for the Cultivation of Science, Kolkata, India.

Akash Chatterjee (A)

School of Biological Sciences, Indian Association for the Cultivation of Science, Kolkata, India.

Avinandan Bhoumick (A)

School of Biological Sciences, Indian Association for the Cultivation of Science, Kolkata, India.

Abhimanyu Basu (A)

Department of General Surgery, Institute of Postgraduate Medical Education and Research, Kolkata, West Bengal, India.

Prosenjit Sen (P)

School of Biological Sciences, Indian Association for the Cultivation of Science, Kolkata, India. Electronic address: bcps@iacs.res.in.

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Classifications MeSH