MITD1 is a brain-specific interferon-inducible factor that inhibits flavivirus replication

J Jim Zoladek (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) M Marion Cannac (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) M Maël Seite (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) E Emma Davies (Medical Research Council-University of Glasgow Centre for Virus Research) J Jordan Quellec (Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier) J Jonathan Barthelemy (Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier) K Kamila Gorna (UMR Virologie, Laboratoire de Santé Animale, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement (INRAE), Anses, Ecole Nationale Vétérinaire d’Alfort) S Sophie Desgraupes (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) I Ines Bribes (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) S Sara Salinas (Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier) M Muriel Coulpier (UMR Virologie, Laboratoire de Santé Animale, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement (INRAE), Anses, Ecole Nationale Vétérinaire d’Alfort) N Nathalie J. Arhel (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier) M Massimo Palmarini (Medical Research Council-University of Glasgow Centre for Virus Research) Y Yannick Simonin (Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier) S Sam J. Wilson (Medical Research Council-University of Glasgow Centre for Virus Research) S Sébastien Nisole (Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier)

Abstract

West Nile virus (WNV) and Usutu virus (USUV) are closely related mosquito-borne neurotropic flaviviruses that share common transmission cycle and can infect humans. However, while human infections by WNV are widespread, infections by USUV are comparatively less frequent, less severe, and currently limited to Africa and Europe. To identify human host factors that contribute to the pathogenic signatures of these two flaviviruses, we carried out an arrayed expression screen of over 1,300 interferon-stimulated genes (ISGs). Several ISGs known to target flaviviruses, including IFI6, SHFL, and RTP4 were among the strongest hits. Interestingly, we also found MITD1, an ISG with no previously reported antiviral activity, among the strongest hits. We demonstrated that the antiviral activity of MITD1 was not limited to USUV and WNV, since it also inhibited Zika and dengue virus replication. We found MITD1 to interfere with viral RNA replication by sequestering specific endosomal sorting complexes required for transport-III (ESCRT-III) proteins involved in the formation of viral replication factories. MITD1 expression was not increased by type I interferon (IFN-I) in most human cells and mouse tissues that we examined, although WNV and USUV replication was strongly inhibited by IFN-I. Strikingly, MITD1 was induced in the brain of USUV-infected mice and importantly, in human monocyte-derived microglia. Using human microglial-like cells, we confirmed that MITD1 is an essential mediator of the anti-flavivirus activity of IFN-I in these cells. We conclude that MITD1 plays a key role in the cellular defenses against neurotropic flaviviruses.

Article Details

Volume / Issue Vol. 122, Issue 12
Published March 25, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (16)

J

Jim Zoladek

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

M

Marion Cannac

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

M

Maël Seite

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

E

Emma Davies

Medical Research Council-University of Glasgow Centre for Virus Research

J

Jordan Quellec

Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier

J

Jonathan Barthelemy

Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier

K

Kamila Gorna

UMR Virologie, Laboratoire de Santé Animale, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement (INRAE), Anses, Ecole Nationale Vétérinaire d’Alfort

S

Sophie Desgraupes

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

I

Ines Bribes

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

S

Sara Salinas

Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier

M

Muriel Coulpier

UMR Virologie, Laboratoire de Santé Animale, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement (INRAE), Anses, Ecole Nationale Vétérinaire d’Alfort

N

Nathalie J. Arhel

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier

M

Massimo Palmarini

Medical Research Council-University of Glasgow Centre for Virus Research

Y

Yannick Simonin

Pathogenesis and Control of Chronic and Emerging Infections, INSERM, Établissement français du sang (EFS), Université de Montpellier

S

Sam J. Wilson

Medical Research Council-University of Glasgow Centre for Virus Research

S

Sébastien Nisole

Viral Trafficking, Restriction and Innate Signaling, CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier, Université de Montpellier