Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice

Abstract Despite the initial successes of the Bacillus Calmette-Guerin (BCG) vaccine in children, its efficacy against tuberculosis is highly variable. There is a lack of understanding about how mental conditions influence BCG vaccination. Here, we used the chronic social defeat stress (CSDS) model...

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Main Authors: Rohit Tyagi, Xi Chen, Atika Dhar, Bing Yang, Wei Zhou, Aikebaier Reheman, Yingying Lei, Gang Cao
Format: Article
Language:English
Published: BMC 2023-12-01
Series:Animal Diseases
Subjects:
Online Access:https://doi.org/10.1186/s44149-023-00102-x
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author Rohit Tyagi
Xi Chen
Atika Dhar
Bing Yang
Wei Zhou
Aikebaier Reheman
Yingying Lei
Gang Cao
author_facet Rohit Tyagi
Xi Chen
Atika Dhar
Bing Yang
Wei Zhou
Aikebaier Reheman
Yingying Lei
Gang Cao
author_sort Rohit Tyagi
collection DOAJ
description Abstract Despite the initial successes of the Bacillus Calmette-Guerin (BCG) vaccine in children, its efficacy against tuberculosis is highly variable. There is a lack of understanding about how mental conditions influence BCG vaccination. Here, we used the chronic social defeat stress (CSDS) model to explore the effects of depression on BCG vaccination efficacy. We observed higher lung and spleen bacterial loads and a lower organ index in depressed compared to BCG mice. Meanwhile, a relatively lower T cell protective efficacy was observed in both compared to control and BCG mice via a mycobacterium growth inhibition assay (MGIA). Cytokine expression of IL-12p40, IL-1β, IL-17, TNF-α and IFN-γ was reduced, whereas the expression of IL-10 and IL-5 was increased in the spleen of both compared to BCG mice. Moreover, the proportions of CD4+IFN-γ+, CD8+IFN-γ+ T lymphocytes and CD4+ effector/central memory T cells were reduced in the splenocytes of the depressed BCG mice. Depression promotes CD4+ regulatory T cells (Treg) and myeloid-derived suppressor cell (MDSC) generation in depressed mice, contributing to the reduced pro-inflammatory immune response upon BCG vaccination. This study provides insight into the decreased protective immunity by BCG vaccination attributable to depression in mice.
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spelling doaj.art-4e043cb78e90408f82f27624064d31ad2023-12-24T12:13:20ZengBMCAnimal Diseases2731-04422023-12-013111210.1186/s44149-023-00102-xChronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in miceRohit Tyagi0Xi Chen1Atika Dhar2Bing Yang3Wei Zhou4Aikebaier Reheman5Yingying Lei6Gang Cao7National Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Institute of ImmunologyNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityAbstract Despite the initial successes of the Bacillus Calmette-Guerin (BCG) vaccine in children, its efficacy against tuberculosis is highly variable. There is a lack of understanding about how mental conditions influence BCG vaccination. Here, we used the chronic social defeat stress (CSDS) model to explore the effects of depression on BCG vaccination efficacy. We observed higher lung and spleen bacterial loads and a lower organ index in depressed compared to BCG mice. Meanwhile, a relatively lower T cell protective efficacy was observed in both compared to control and BCG mice via a mycobacterium growth inhibition assay (MGIA). Cytokine expression of IL-12p40, IL-1β, IL-17, TNF-α and IFN-γ was reduced, whereas the expression of IL-10 and IL-5 was increased in the spleen of both compared to BCG mice. Moreover, the proportions of CD4+IFN-γ+, CD8+IFN-γ+ T lymphocytes and CD4+ effector/central memory T cells were reduced in the splenocytes of the depressed BCG mice. Depression promotes CD4+ regulatory T cells (Treg) and myeloid-derived suppressor cell (MDSC) generation in depressed mice, contributing to the reduced pro-inflammatory immune response upon BCG vaccination. This study provides insight into the decreased protective immunity by BCG vaccination attributable to depression in mice.https://doi.org/10.1186/s44149-023-00102-xBCGVaccine efficacyTregImmune suppressionDepression
spellingShingle Rohit Tyagi
Xi Chen
Atika Dhar
Bing Yang
Wei Zhou
Aikebaier Reheman
Yingying Lei
Gang Cao
Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
Animal Diseases
BCG
Vaccine efficacy
Treg
Immune suppression
Depression
title Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
title_full Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
title_fullStr Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
title_full_unstemmed Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
title_short Chronic social defeat stress-induced depression reduces BCG efficacy by promoting regulatory T-cell levels in mice
title_sort chronic social defeat stress induced depression reduces bcg efficacy by promoting regulatory t cell levels in mice
topic BCG
Vaccine efficacy
Treg
Immune suppression
Depression
url https://doi.org/10.1186/s44149-023-00102-x
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