Tryptophan metabolism promotes immune evasion in human pancreatic β cells.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 13 03 2023
revised: 18 07 2023
accepted: 18 07 2023
medline: 18 9 2023
pubmed: 4 8 2023
entrez: 3 8 2023
Statut: ppublish

Résumé

To resist the autoimmune attack characteristic of type 1 diabetes, insulin producing pancreatic β cells need to evade T-cell recognition. Such escape mechanisms may be conferred by low HLA class I (HLA-I) expression and upregulation of immune inhibitory molecules such as Programmed cell Death Ligand 1 (PD-L1). The expression of PD-L1, HLA-I and CXCL10 was evaluated in the human β cell line, ECN90, and in primary human and mouse pancreatic islets. Most genes were determined by real-time RT-PCR, flow cytometry and Western blot. Activator and inhibitor of the AKT signaling were used to modulate PD-L1 induction. Key results were validated by monitoring activity of CD8+ Jurkat T cells presenting β cell specific T-cell receptor and transduced with reporter genes in contact culture with the human β cell line, ECN90. In this study, we identify tryptophan (TRP) as an agonist of PD-L1 induction through the AKT signaling pathway. TRP also synergistically enhanced PD-L1 expression on β cells exposed to interferon-γ. Conversely, interferon-γ-mediated induction of HLA-I and CXCL10 genes was down-regulated upon TRP treatment. Finally, TRP and its derivatives inhibited the activation of islet-reactive CD8+ T cells by β cells. Collectively, our findings indicate that TRP could induce immune tolerance to β cells by promoting their immune evasion through HLA-I downregulation and PD-L1 upregulation. Dutch Diabetes Research Foundation, DON Foundation, the Laboratoire d'Excellence consortium Revive (ANR-10-LABX-0073), Agence Nationale de la Recherche (ANR-19-CE15-0014-01), Fondation pour la Recherche Médicale (EQ U201903007793-EQU20193007831), Innovative Medicines InitiativeINNODIA and INNODIA HARVEST, Aides aux Jeunes Diabetiques (AJD) and Juvenile Diabetes Research Foundation Ltd (JDRF).

Sections du résumé

BACKGROUND BACKGROUND
To resist the autoimmune attack characteristic of type 1 diabetes, insulin producing pancreatic β cells need to evade T-cell recognition. Such escape mechanisms may be conferred by low HLA class I (HLA-I) expression and upregulation of immune inhibitory molecules such as Programmed cell Death Ligand 1 (PD-L1).
METHODS METHODS
The expression of PD-L1, HLA-I and CXCL10 was evaluated in the human β cell line, ECN90, and in primary human and mouse pancreatic islets. Most genes were determined by real-time RT-PCR, flow cytometry and Western blot. Activator and inhibitor of the AKT signaling were used to modulate PD-L1 induction. Key results were validated by monitoring activity of CD8+ Jurkat T cells presenting β cell specific T-cell receptor and transduced with reporter genes in contact culture with the human β cell line, ECN90.
FINDINGS RESULTS
In this study, we identify tryptophan (TRP) as an agonist of PD-L1 induction through the AKT signaling pathway. TRP also synergistically enhanced PD-L1 expression on β cells exposed to interferon-γ. Conversely, interferon-γ-mediated induction of HLA-I and CXCL10 genes was down-regulated upon TRP treatment. Finally, TRP and its derivatives inhibited the activation of islet-reactive CD8+ T cells by β cells.
INTERPRETATION CONCLUSIONS
Collectively, our findings indicate that TRP could induce immune tolerance to β cells by promoting their immune evasion through HLA-I downregulation and PD-L1 upregulation.
FUNDING BACKGROUND
Dutch Diabetes Research Foundation, DON Foundation, the Laboratoire d'Excellence consortium Revive (ANR-10-LABX-0073), Agence Nationale de la Recherche (ANR-19-CE15-0014-01), Fondation pour la Recherche Médicale (EQ U201903007793-EQU20193007831), Innovative Medicines InitiativeINNODIA and INNODIA HARVEST, Aides aux Jeunes Diabetiques (AJD) and Juvenile Diabetes Research Foundation Ltd (JDRF).

Identifiants

pubmed: 37536063
pii: S2352-3964(23)00305-5
doi: 10.1016/j.ebiom.2023.104740
pmc: PMC10412781
pii:
doi:

Substances chimiques

Tryptophan 8DUH1N11BX
Interferon-gamma 82115-62-6
B7-H1 Antigen 0
Proto-Oncogene Proteins c-akt EC 2.7.11.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104740

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare that they have no conflicts of interest with the contents of this article.

Auteurs

Latif Rachdi (L)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France. Electronic address: latif.rachdi@inserm.fr.

Zhicheng Zhou (Z)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

Claire Berthault (C)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

Chloe Lourenço (C)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

Alexis Fouque (A)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

Thomas Domet (T)

Assistance Publique Hôpitaux de Paris, Cell Therapy Unit, Saint Louis Hospital, Paris 75010, France.

Mathieu Armanet (M)

Assistance Publique Hôpitaux de Paris, Cell Therapy Unit, Saint Louis Hospital, Paris 75010, France.

Sylvaine You (S)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

Mark Peakman (M)

Department of Immunobiology, School of Immunology and Microbial Sciences, King's College London, London SE1 9RT, UK.

Roberto Mallone (R)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France; Assistance Publique Hôpitaux de Paris, Service de Diabétologie et Immunologie Clinique, Cochin Hospital, Paris 75014, France.

Raphael Scharfmann (R)

Université Paris Cité, Institut Cochin, CNRS, INSERM, Paris 75014, France.

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Classifications MeSH