Induction of the ISR by AB5 subtilase cytotoxin drives type-I IFN expression in pDCs via STING activation

D Daniela Barros (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) B Beatriz H. Ferreira (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) P Paulina Garcia-Gonzalez (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) F Francesco Carbone (Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163) M Marine Luka (Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163) F Fátima Leite-Pinheiro (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) M Mariana D. Machado (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) T Theopisti Nikolaou (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) A Angelo Pilotti (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) E Eliot Goguet (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) P Paulo Antas (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) A Andreia Mendes (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) L Lichen Zhang (School of Medical Technology, Henan Key Laboratory of Immunology and Targeted Therapy, Xinxiang Medical University) M Marina Cresci (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) L Lou Galliot (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) J Julien P. Gigan (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) M Marisa Reverendo (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) B Bing Su M Miwako Narita (Laboratory of Hematology and Oncology, Graduate School of Health Sciences, Niigata University) A Adrienne W. Paton (Research Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide) J James C. Paton (Research Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide) S Stéphane Rocchi (Université Côte d’Azur, INSERM) F Frédéric Rieux-Laucat (Université de Paris Cité, Imagine Institute Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163) R Rafael J. Argüello (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) B Béatrice Nal (Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)) Y Yinming Liang (School of Medical Technology, Henan Key Laboratory of Immunology and Targeted Therapy, Xinxiang Medical University) M Mickaël Ménager (Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163) E Evelina Gatti (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) C Catarina R. Almeida (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro) P Philippe Pierre (Institute of Biomedicine, Department of Medical Sciences, University of Aveiro)

Abstract

We demonstrate that exposure to the AB5 subtilase cytotoxin (SubAB) induces the unfolded protein response (UPR) in human peripheral blood mononuclear cells, concomitant with a proinflammatory response across distinct cell subsets. Notably, SubAB selectively induces type-I interferon (IFN) expression in plasmacytoid dendritic cells, acting synergistically with Toll-like receptor 7 stimulation. The induction of type-I IFN in response to SubAB relies on stimulator of interferon genes (STING) activation, coupled with protein synthesis inhibition mediated by protein kinase R-like endoplasmic reticulum kinase (PERK) and phosphorylation of the eukaryotic translation initiation factor 2 subunit-alpha. By impeding mRNA translation through the integrated stress response, SubAB precipitates the downregulation of the negative innate signaling feedback regulator Tax1-binding protein 1. This downregulation is necessary to unleash TANK-binding kinase 1 signaling associated with STING activation. These findings shed light on how UPR-inducing conditions may regulate the immune system during infection or pathogenesis.

Article Details

Volume / Issue Vol. 122, Issue 21
Published May 27, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (30)

D

Daniela Barros

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

B

Beatriz H. Ferreira

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

P

Paulina Garcia-Gonzalez

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

F

Francesco Carbone

Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163

M

Marine Luka

Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163

F

Fátima Leite-Pinheiro

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

M

Mariana D. Machado

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

T

Theopisti Nikolaou

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

A

Angelo Pilotti

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

E

Eliot Goguet

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

P

Paulo Antas

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

A

Andreia Mendes

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

L

Lichen Zhang

School of Medical Technology, Henan Key Laboratory of Immunology and Targeted Therapy, Xinxiang Medical University

M

Marina Cresci

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

L

Lou Galliot

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

J

Julien P. Gigan

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

M

Marisa Reverendo

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

B

Bing Su

M

Miwako Narita

Laboratory of Hematology and Oncology, Graduate School of Health Sciences, Niigata University

A

Adrienne W. Paton

Research Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide

J

James C. Paton

Research Centre for Infectious Diseases, Department of Molecular and Biomedical Science, University of Adelaide

S

Stéphane Rocchi

Université Côte d’Azur, INSERM

F

Frédéric Rieux-Laucat

Université de Paris Cité, Imagine Institute Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR 1163

R

Rafael J. Argüello

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

B

Béatrice Nal

Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML)

Y

Yinming Liang

School of Medical Technology, Henan Key Laboratory of Immunology and Targeted Therapy, Xinxiang Medical University

M

Mickaël Ménager

Université de Paris Cité, Imagine Institute, Laboratory of Inflammatory Responses and Transcriptomic Networks in Diseases, Atip-Avenir Team, INSERM U1163

E

Evelina Gatti

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

C

Catarina R. Almeida

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro

P

Philippe Pierre

Institute of Biomedicine, Department of Medical Sciences, University of Aveiro