A STING antagonist modulating the interaction with STIM1 blocks ER-to-Golgi trafficking and inhibits lupus pathology.


Journal

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

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 02 12 2020
revised: 15 03 2021
accepted: 15 03 2021
pubmed: 5 4 2021
medline: 30 11 2021
entrez: 4 4 2021
Statut: ppublish

Résumé

Nucleic acids are potent stimulators of type I interferon (IFN-I) and antiviral defense, but may also promote pathological inflammation. A range of diseases are characterized by elevated IFN-I, including systemic lupus erythematosus (lupus). The DNA-activated cGAS-STING pathway is a major IFN-I-inducing pathway, and activation of signaling is dependent on trafficking of STING from the ER to the Golgi. Here we used cell culture systems, a mouse lupus model, and material from lupus patients, to explore the mode of action of a STING antagonistic peptide, and its ability to modulate disease processes. We report that the peptide ISD017 selectively inhibits all known down-stream activities of STING, including IFN-I, inflammatory cytokines, autophagy, and apoptosis. ISD017 blocks the essential trafficking of STING from the ER to Golgi through a mechanism dependent on the STING ER retention factor STIM1. Importantly, ISD017 blocks STING activity in vivo and ameliorates disease development in a mouse model for lupus. Finally, ISD017 treatment blocks pathological cytokine responses in cells from lupus patients with elevated IFN-I levels. These data hold promise for beneficial use of STING-targeting therapy in lupus. The Novo Nordisk Foundation, The European Research Council, The Lundbeck Foundation, European Union under the Horizon 2020 Research, Deutsche Forschungsgemeinschaft, Chulalongkorn University.

Sections du résumé

BACKGROUND BACKGROUND
Nucleic acids are potent stimulators of type I interferon (IFN-I) and antiviral defense, but may also promote pathological inflammation. A range of diseases are characterized by elevated IFN-I, including systemic lupus erythematosus (lupus). The DNA-activated cGAS-STING pathway is a major IFN-I-inducing pathway, and activation of signaling is dependent on trafficking of STING from the ER to the Golgi.
METHODS METHODS
Here we used cell culture systems, a mouse lupus model, and material from lupus patients, to explore the mode of action of a STING antagonistic peptide, and its ability to modulate disease processes.
FINDINGS RESULTS
We report that the peptide ISD017 selectively inhibits all known down-stream activities of STING, including IFN-I, inflammatory cytokines, autophagy, and apoptosis. ISD017 blocks the essential trafficking of STING from the ER to Golgi through a mechanism dependent on the STING ER retention factor STIM1. Importantly, ISD017 blocks STING activity in vivo and ameliorates disease development in a mouse model for lupus. Finally, ISD017 treatment blocks pathological cytokine responses in cells from lupus patients with elevated IFN-I levels.
INTERPRETATION CONCLUSIONS
These data hold promise for beneficial use of STING-targeting therapy in lupus.
FUNDING BACKGROUND
The Novo Nordisk Foundation, The European Research Council, The Lundbeck Foundation, European Union under the Horizon 2020 Research, Deutsche Forschungsgemeinschaft, Chulalongkorn University.

Identifiants

pubmed: 33813142
pii: S2352-3964(21)00107-9
doi: 10.1016/j.ebiom.2021.103314
pmc: PMC8047499
pii:
doi:

Substances chimiques

Membrane Proteins 0
Neoplasm Proteins 0
STIM1 protein, human 0
STING1 protein, human 0
Stromal Interaction Molecule 1 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103314

Subventions

Organisme : European Research Council
ID : 786602
Pays : International

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest TP, CKH, LØ, and SRP own shares in ISD Immunotech, which owns the patent for ISD017 (WO2014166502A2). The patent was the patent was issued by CKH. None of the other authors have conflicts to declare.

Auteurs

Thaneas Prabakaran (T)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Anne Troldborg (A)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark; Department of Clinical Medicine, Aarhus University, Aarhus DK-8000, Denmark; Department of Rheumatology, Aarhus University Hospital, Aarhus N 8200, Denmark.

Sarinya Kumpunya (S)

Center of Excellence in Systems Biology, Research Affairs, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand; Inter-Department Program of Biomedical Sciences, Faculty of Graduate, Chulalongkorn University, Bangkok, Thailand.

Isara Alee (I)

Center of Excellence in Systems Biology, Research Affairs, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand; Inter-Department Program of Biomedical Sciences, Faculty of Graduate, Chulalongkorn University, Bangkok, Thailand.

Emilija Marinković (E)

Institute for Immunology, Faculty of Medicine, Technical University Dresden, Dresden, Germany.

Samuel J Windross (SJ)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Ramya Nandakumar (R)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Ryo Narita (R)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Bao-Cun Zhang (BC)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Mikkel Carstensen (M)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Pichpisith Vejvisithsakul (P)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark; Section for Translational Medicine, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.

Mikkel H S Marqvorsen (MHS)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Marie B Iversen (MB)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Christian K Holm (CK)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark.

Lars J Østergaard (LJ)

Department of Clinical Medicine, Aarhus University, Aarhus DK-8000, Denmark; Department of Infectious Diseases, Aarhus University Hospital, Aarhus N 8200, Denmark.

Finn Skou Pedersen (FS)

Department of Molecular Biology and Genetics, Aarhus University, Aarhus DK-8000, Denmark.

Trairak Pisitkun (T)

Center of Excellence in Systems Biology, Research Affairs, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.

Rayk Behrendt (R)

Institute for Immunology, Faculty of Medicine, Technical University Dresden, Dresden, Germany.

Prapaporn Pisitkun (P)

Section for Translational Medicine, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand; Division of Allergy, Immunology, and Rheumatology, Department of Medicine, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.

Søren R Paludan (SR)

Department of Biomedicine, Aarhus University, Aarhus DK-8000, Denmark. Electronic address: srp@biomed.au.dk.

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