Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner

Tropheryma whipplei, the agent of Whipple’s disease, is an intracellular pathogen that replicates in macrophages. The phagocytic and cellular processes leading to the formation of T. whipplei replicative vacuole remain poorly understood. Macrophage microbicidal activity is largely related to macro/a...

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Main Authors: Emilie Reyne, Jeffrey Arrindell, Eloïne Bestion, Soraya Mezouar, Benoit Desnues
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Autophagy Reports
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Online Access:https://www.tandfonline.com/doi/10.1080/27694127.2025.2475527
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author Emilie Reyne
Jeffrey Arrindell
Eloïne Bestion
Soraya Mezouar
Benoit Desnues
author_facet Emilie Reyne
Jeffrey Arrindell
Eloïne Bestion
Soraya Mezouar
Benoit Desnues
author_sort Emilie Reyne
collection DOAJ
description Tropheryma whipplei, the agent of Whipple’s disease, is an intracellular pathogen that replicates in macrophages. The phagocytic and cellular processes leading to the formation of T. whipplei replicative vacuole remain poorly understood. Macrophage microbicidal activity is largely related to macro/autophagy which is also essential for cell homeostasis. Here, we show that T. whipplei uptake by macrophages involved LC3-associated phagocytosis (LAP). Bacteria then escaped into the cytosol from where they were recaptured by xenophagy. We also demonstrate that T. whipplei blocked the autophagic flux to build its replicative compartment. Inhibition of LAP resulted in the decrease of interleukin (IL)-10 secretion and the restoration of the autophagy flux, suggesting that modulation of autophagy during infection alters immune response and promote persistence. Our results provide new insight in the intracellular fate of the bacteria during macrophage infection and suggest the possible involvement of previously unknown virulence factors in T. whipplei infection.
format Article
id doaj-art-cf873125922f47528d84fc9446fbbf54
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issn 2769-4127
language English
publishDate 2025-12-01
publisher Taylor & Francis Group
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series Autophagy Reports
spelling doaj-art-cf873125922f47528d84fc9446fbbf542025-08-20T03:05:52ZengTaylor & Francis GroupAutophagy Reports2769-41272025-12-014110.1080/27694127.2025.2475527Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent mannerEmilie Reyne0Jeffrey Arrindell1Eloïne Bestion2Soraya Mezouar3Benoit Desnues4Aix-Marseille Univ, MEPHI, Marseille, FranceAix-Marseille Univ, MEPHI, Marseille, FranceGenoscience Pharma, 13006 Marseille, FranceAix-Marseille Univ, ADES, CNRS, EFS, Marseille, FranceAix-Marseille Univ, MEPHI, Marseille, FranceTropheryma whipplei, the agent of Whipple’s disease, is an intracellular pathogen that replicates in macrophages. The phagocytic and cellular processes leading to the formation of T. whipplei replicative vacuole remain poorly understood. Macrophage microbicidal activity is largely related to macro/autophagy which is also essential for cell homeostasis. Here, we show that T. whipplei uptake by macrophages involved LC3-associated phagocytosis (LAP). Bacteria then escaped into the cytosol from where they were recaptured by xenophagy. We also demonstrate that T. whipplei blocked the autophagic flux to build its replicative compartment. Inhibition of LAP resulted in the decrease of interleukin (IL)-10 secretion and the restoration of the autophagy flux, suggesting that modulation of autophagy during infection alters immune response and promote persistence. Our results provide new insight in the intracellular fate of the bacteria during macrophage infection and suggest the possible involvement of previously unknown virulence factors in T. whipplei infection.https://www.tandfonline.com/doi/10.1080/27694127.2025.2475527AutophagyImmune escapeLC3-associated phagocytosis (LAP)MacrophageTropheryma whippleiWhipple’s disease
spellingShingle Emilie Reyne
Jeffrey Arrindell
Eloïne Bestion
Soraya Mezouar
Benoit Desnues
Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
Autophagy Reports
Autophagy
Immune escape
LC3-associated phagocytosis (LAP)
Macrophage
Tropheryma whipplei
Whipple’s disease
title Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
title_full Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
title_fullStr Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
title_full_unstemmed Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
title_short Tropheryma whipplei escapes LAPosome and modulates macrophage response in a xenophagy-dependent manner
title_sort tropheryma whipplei escapes laposome and modulates macrophage response in a xenophagy dependent manner
topic Autophagy
Immune escape
LC3-associated phagocytosis (LAP)
Macrophage
Tropheryma whipplei
Whipple’s disease
url https://www.tandfonline.com/doi/10.1080/27694127.2025.2475527
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