FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance

Abstract Background Leishmania is the causal parasite of leishmaniasis, a neglected tropical disease affecting millions of individuals worldwide, and its dissemination is linked to climate change. Despite the complexity and effectiveness of the immune response, the parasite has developed many strate...

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Main Authors: Ikram Hammi, Julien Giron-Michel, Myriam Riyad, Khadija Akarid, Damien Arnoult
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-024-06593-y
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author Ikram Hammi
Julien Giron-Michel
Myriam Riyad
Khadija Akarid
Damien Arnoult
author_facet Ikram Hammi
Julien Giron-Michel
Myriam Riyad
Khadija Akarid
Damien Arnoult
author_sort Ikram Hammi
collection DOAJ
description Abstract Background Leishmania is the causal parasite of leishmaniasis, a neglected tropical disease affecting millions of individuals worldwide, and its dissemination is linked to climate change. Despite the complexity and effectiveness of the immune response, the parasite has developed many strategies to evade it and take control of the host cell to replicate. These evasion strategies start at early stages of infection by hijacking immune receptors to mitigate the cellular response. In this study, we examined whether Leishmania uses the Fc receptor FcγRIIA/CD32a and its downstream signaling pathways to evade the host immune response. Methods Regarding in vivo studies, CD32a transgenic mice and the corresponding wild types were infected with Leishmania major Friedlin strain. For the in vitro experiments, BMDMs isolated from WT or CD32a transgenic mice and control or CD32a knockdown differentiated THP-1s were infected with two species of Leishmania, Leishmania major and L. tropica. Results In vivo, expression of FcγRIIA/CD32a was found to accelerate the signs of inflammation while simultaneously preventing the formation of necrotic lesions after Leishmania infection. In infected macrophages, the presence of FcγRIIA/CD32a did not affect the secretion of proinflammatory cytokines, while the balance between ITAMa and ITAMi proteins was disturbed with improved Fyn and Lyn activation. Unexpectedly, infection with L. tropica but not L. major triggered an intracytoplasmic processing of FcγRIIA/CD32a. Conclusions Our observations underscore the significance of FcγRIIA/CD32a in cutaneous leishmaniasis and its potential use as a therapeutic target. Graphical Abstract
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spelling doaj-art-448229ecbd9d493793ee5ead83ff1ef42025-08-20T02:40:21ZengBMCParasites & Vectors1756-33052024-12-0117111210.1186/s13071-024-06593-yFcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balanceIkram Hammi0Julien Giron-Michel1Myriam Riyad2Khadija Akarid3Damien Arnoult4Health & Environment Laboratory, Ain Chock Faculty of Sciences, Hassan II University of Casablanca (UH2C)INSERM UMR-S-MD 1197, Ministère des Armées et Université Paris SaclayLaboratory of Cellular and Molecular Pathology, Faculty of Medicine and Pharmacy, UH2CHealth & Environment Laboratory, Ain Chock Faculty of Sciences, Hassan II University of Casablanca (UH2C)INSERM UMR-S-MD 1197, Ministère des Armées et Université Paris SaclayAbstract Background Leishmania is the causal parasite of leishmaniasis, a neglected tropical disease affecting millions of individuals worldwide, and its dissemination is linked to climate change. Despite the complexity and effectiveness of the immune response, the parasite has developed many strategies to evade it and take control of the host cell to replicate. These evasion strategies start at early stages of infection by hijacking immune receptors to mitigate the cellular response. In this study, we examined whether Leishmania uses the Fc receptor FcγRIIA/CD32a and its downstream signaling pathways to evade the host immune response. Methods Regarding in vivo studies, CD32a transgenic mice and the corresponding wild types were infected with Leishmania major Friedlin strain. For the in vitro experiments, BMDMs isolated from WT or CD32a transgenic mice and control or CD32a knockdown differentiated THP-1s were infected with two species of Leishmania, Leishmania major and L. tropica. Results In vivo, expression of FcγRIIA/CD32a was found to accelerate the signs of inflammation while simultaneously preventing the formation of necrotic lesions after Leishmania infection. In infected macrophages, the presence of FcγRIIA/CD32a did not affect the secretion of proinflammatory cytokines, while the balance between ITAMa and ITAMi proteins was disturbed with improved Fyn and Lyn activation. Unexpectedly, infection with L. tropica but not L. major triggered an intracytoplasmic processing of FcγRIIA/CD32a. Conclusions Our observations underscore the significance of FcγRIIA/CD32a in cutaneous leishmaniasis and its potential use as a therapeutic target. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06593-yLeishmaniasisFc receptorsFcγRIIAImmune responseITAM
spellingShingle Ikram Hammi
Julien Giron-Michel
Myriam Riyad
Khadija Akarid
Damien Arnoult
FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
Parasites & Vectors
Leishmaniasis
Fc receptors
FcγRIIA
Immune response
ITAM
title FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
title_full FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
title_fullStr FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
title_full_unstemmed FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
title_short FcRγIIA attenuates pathology of cutaneous leishmaniasis and modulates ITAMa/i balance
title_sort fcrγiia attenuates pathology of cutaneous leishmaniasis and modulates itama i balance
topic Leishmaniasis
Fc receptors
FcγRIIA
Immune response
ITAM
url https://doi.org/10.1186/s13071-024-06593-y
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