Evaluation of the Impact of BaP Exposure on the Gut Microbiota and Allergic Responses in an OVA-Sensitized Mouse Model
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Evaluation of the Impact of BaP Exposure on the Gut Microbiota and Allergic Responses in an OVA-Sensitized Mouse Model. / Du, Beibei; Xiao, Xiaojun; Wang, Huailing; Li, Wenxi; Xia, Zhongkui; Yang, Pingchang; Huang, Shau Ku; Yuan, Ruyi; Liu, Jie; Han, Mo; Zou, Yuanqiang; Zhu, Jiahui; He, Dongdong; Lyu, Jinli; Jin, Xin; Xu, Xun; Wang, Jian; Yang, Huanming; Xiao, Liang; Liu, Xiaoyu; Kristiansen, Karsten.
In: Environmental Health Perspectives, Vol. 131, No. 6, 2023.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Evaluation of the Impact of BaP Exposure on the Gut Microbiota and Allergic Responses in an OVA-Sensitized Mouse Model
AU - Du, Beibei
AU - Xiao, Xiaojun
AU - Wang, Huailing
AU - Li, Wenxi
AU - Xia, Zhongkui
AU - Yang, Pingchang
AU - Huang, Shau Ku
AU - Yuan, Ruyi
AU - Liu, Jie
AU - Han, Mo
AU - Zou, Yuanqiang
AU - Zhu, Jiahui
AU - He, Dongdong
AU - Lyu, Jinli
AU - Jin, Xin
AU - Xu, Xun
AU - Wang, Jian
AU - Yang, Huanming
AU - Xiao, Liang
AU - Liu, Xiaoyu
AU - Kristiansen, Karsten
PY - 2023
Y1 - 2023
N2 - BACKGROUND: Exposure to environmental pollutants, including benzo[a]pyrene (BaP), has been implicated in allergic diseases and intestinal microbiota homeostasis, but the environment-microbiota-immunity triangular relationship and to what extent BaP-induced remodeling of the gut microbiota contributes to intestinal allergic inflammation remain to be established. OBJECTIVES: We investigated the impact of BaP on intestinal allergic inflammation and examined the relationship between this effect and gut microbiota dysbiosis. We explored the potential ability of intestinal bacteria to degrade BaP and alleviate cytotoxicity as a detoxification strategy to counteract the effects of BaP exposure. METHODS: We combined microbiome shotgun metagenomics with animal histological and intestinal allergic inflammatory responses to assess the effects of BaP (formula presented ) in a 23-d toxicity test in antigen-induced allergic female mice. In addition, genome annotation, quantitative analysis of BaP, and in vitro cytotoxicity-tests using CaCo-2 cells were conducted to infer the role of intestinal bacteria in BaP detoxification. RESULTS: BaP exposure impacted the taxonomic composition and the functional potential of the gut microbiota and aggravated antigen-induced intestinal allergic inflammatory responses. The level of inflammatory cytokines correlated with the abundance of specific bacterial taxa, including Lachnospiraceae bacterium 28-4 and Alistipes inops. We identified 614 bacteria harboring genes implicated in the degradation of BaP, and 4 of these bacterial strains were shown to significantly reduce the cytotoxicity of BaP to CaCo-2 cells in vitro. DISCUSSION: Using allergic female mice as a model, we investigated the relationship between BaP, microbiota, and host immune reactions, highlighting the role of gut bacteria in BaP-aggravated allergic reactions. Our findings offer novel insight toward establishing the causal relationship between BaP exposure and the occurrence of allergic disorders. Identifying gut bacteria that degrade BaP may provide new strategies for ameliorating BaP cytotoxicity. https://doi.org/10.1289/EHP11874.
AB - BACKGROUND: Exposure to environmental pollutants, including benzo[a]pyrene (BaP), has been implicated in allergic diseases and intestinal microbiota homeostasis, but the environment-microbiota-immunity triangular relationship and to what extent BaP-induced remodeling of the gut microbiota contributes to intestinal allergic inflammation remain to be established. OBJECTIVES: We investigated the impact of BaP on intestinal allergic inflammation and examined the relationship between this effect and gut microbiota dysbiosis. We explored the potential ability of intestinal bacteria to degrade BaP and alleviate cytotoxicity as a detoxification strategy to counteract the effects of BaP exposure. METHODS: We combined microbiome shotgun metagenomics with animal histological and intestinal allergic inflammatory responses to assess the effects of BaP (formula presented ) in a 23-d toxicity test in antigen-induced allergic female mice. In addition, genome annotation, quantitative analysis of BaP, and in vitro cytotoxicity-tests using CaCo-2 cells were conducted to infer the role of intestinal bacteria in BaP detoxification. RESULTS: BaP exposure impacted the taxonomic composition and the functional potential of the gut microbiota and aggravated antigen-induced intestinal allergic inflammatory responses. The level of inflammatory cytokines correlated with the abundance of specific bacterial taxa, including Lachnospiraceae bacterium 28-4 and Alistipes inops. We identified 614 bacteria harboring genes implicated in the degradation of BaP, and 4 of these bacterial strains were shown to significantly reduce the cytotoxicity of BaP to CaCo-2 cells in vitro. DISCUSSION: Using allergic female mice as a model, we investigated the relationship between BaP, microbiota, and host immune reactions, highlighting the role of gut bacteria in BaP-aggravated allergic reactions. Our findings offer novel insight toward establishing the causal relationship between BaP exposure and the occurrence of allergic disorders. Identifying gut bacteria that degrade BaP may provide new strategies for ameliorating BaP cytotoxicity. https://doi.org/10.1289/EHP11874.
U2 - 10.1289/EHP11874
DO - 10.1289/EHP11874
M3 - Journal article
C2 - 37267060
AN - SCOPUS:85160899307
VL - 131
JO - Environmental Health Perspectives
JF - Environmental Health Perspectives
SN - 0091-6765
IS - 6
ER -
ID: 357056598