The IL-25-dependent tuft cell circuit driven by intestinal helminths requires macrophage migration inhibitory factor (MIF).


Journal

Mucosal immunology
ISSN: 1935-3456
Titre abrégé: Mucosal Immunol
Pays: United States
ID NLM: 101299742

Informations de publication

Date de publication:
06 2022
Historique:
received: 08 04 2021
accepted: 10 02 2022
revised: 31 01 2022
pubmed: 16 3 2022
medline: 1 12 2022
entrez: 15 3 2022
Statut: ppublish

Résumé

Macrophage migration inhibitory factor (MIF) is a key innate immune mediator with chemokine- and cytokine-like properties in the inflammatory pathway. While its actions on macrophages are well-studied, its effects on other cell types are less understood. Here we report that MIF is required for expansion of intestinal tuft cells during infection with the helminth Nippostrongylus brasiliensis. MIF-deficient mice show defective innate responses following infection, lacking intestinal epithelial tuft cell hyperplasia or upregulation of goblet cell RELMβ, and fail to expand eosinophil, type 2 innate lymphoid cell (ILC2) and macrophage (M2) populations. Similar effects were observed in MIF-sufficient wild-type mice given the MIF inhibitor 4-IPP. MIF had no direct effect on epithelial cells in organoid cultures, and MIF-deficient intestinal stem cells could generate tuft cells in vitro in the presence of type 2 cytokines. In vivo the lack of MIF could be fully compensated by administration of IL-25, restoring tuft cell differentiation and goblet cell expression of RELM-β, demonstrating its requirement upstream of the ILC2-tuft cell circuit. Both ILC2s and macrophages expressed the MIF receptor CXCR4, indicating that MIF may act as an essential co-factor on both cell types to activate responses to IL-25 in helminth infection.

Identifiants

pubmed: 35288645
doi: 10.1038/s41385-022-00496-w
pii: S1933-0219(22)01751-2
pmc: PMC9705247
doi:

Substances chimiques

Macrophage Migration-Inhibitory Factors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1243-1256

Subventions

Organisme : Wellcome Trust
ID : 106122
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 107490
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104111
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2022. The Author(s).

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Auteurs

Fumi Varyani (F)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.
Institute of Immunology and Infection Research, University of Edinburgh, Edinburgh, UK.

Stephan Löser (S)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.

Kara J Filbey (KJ)

Institute of Immunology and Infection Research, University of Edinburgh, Edinburgh, UK.
Lydia Becker Institute for Immunology and Inflammation, University of Manchester, Manchester, UK.

Yvonne Harcus (Y)

Institute of Immunology and Infection Research, University of Edinburgh, Edinburgh, UK.

Claire Drurey (C)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.

Marta Campillo Poveda (MC)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.

Orhan Rasid (O)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.

Madeleine P J White (MPJ)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.

Danielle J Smyth (DJ)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK.
Division of Cell Signalling and Immunology, University of Dundee, Dundee, UK.

François Gerbe (F)

IGF, University of Montpellier, CNRS, Inserm, Montpellier, France.

Philippe Jay (P)

IGF, University of Montpellier, CNRS, Inserm, Montpellier, France.

Rick M Maizels (RM)

Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, UK. rick.maizels@glasgow.ac.uk.

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