Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota

BackgroundSalmonella enterica Serovar Typhimurium (S. Typhimurium) infection can cause inflammation and oxidative stress in the body, leading to gastroenteritis, fever and other diseases in humans and animals. More and more studies have emphasized the broad prospects of probiotics in improving infla...

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Main Authors: Haihua Li, Xinyi Ma, Zhiyuan Shang, Xuejiao Liu, Jiayun Qiao
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483705/full
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author Haihua Li
Xinyi Ma
Zhiyuan Shang
Xuejiao Liu
Jiayun Qiao
author_facet Haihua Li
Xinyi Ma
Zhiyuan Shang
Xuejiao Liu
Jiayun Qiao
author_sort Haihua Li
collection DOAJ
description BackgroundSalmonella enterica Serovar Typhimurium (S. Typhimurium) infection can cause inflammation and oxidative stress in the body, leading to gastroenteritis, fever and other diseases in humans and animals. More and more studies have emphasized the broad prospects of probiotics in improving inflammation and oxidative stress, but the ability and mechanism of Lactobacillus acidophilus (LA) to alleviate the inflammatory/oxidative reaction caused by pathogens are still unclear.Methods and resultsIn this study, we treated the mice with LA for 14 days, infected them with S. Typhimurium for 24 h, and sacrificed the mice to collect samples. We found that the early intervention of LA alleviated the pathological injury and reversed the down-regulation of the duodenal and hepatic tight junction protein mRNA levels caused by S. Typhimurium infection. Compared with S. Typhimurium group, LA early intervention increased the expression of antioxidant enzymes, but decreased the levels of serum malondialdehyde (MDA), interleukin-8 and tumor necrosis factor-α (TNF-α). Additionally, LA early intervention significantly increased Nrf2 mRNA expression in the liver and decreased Keap1 mRNA expression in the duodenum compared to the S. Typhimurium group. Furthermore, early LA treatment reduced the abundance of Bacteroides acidificiens, increased the abundance of Akkermansia, and alleviated the decrease in SCFAs levels in the cecum of S. Typhimurium-infected mice. Spearman correlation analysis showed that there was a certain correlation between cecal flora and serum indicators and short chain fatty acids.ConclusionTaken together, the results indicate that LA early intervention may alleviates S. Typhimurium-induced inflammation and oxidative responses in mice by activating the p62-Keap1-Nrf2 signaling pathway and regulating the gut microbial community.Significance and impact of the studyExploring the ability of LA to resist animal oxidative stress and microflora regulation caused by pathogenic microbes, so as to provide more options for developing healthy disease-resistant feed additives.
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spelling doaj-art-02a054470b0a41288ad2c910235d05922025-01-16T19:27:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14837051483705Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiotaHaihua Li0Xinyi Ma1Zhiyuan Shang2Xuejiao Liu3Jiayun Qiao4Tianjin Key Laboratory of Agricultural Animal Breeding and Healthy Husbandry, College of Animal Science and Veterinary Medicine, Tianjin Agricultural University, Tianjin, ChinaTianjin Key Laboratory of Conservation and Utilization of Animal Diversity, College of Life Sciences, Tianjin Normal University, Tianjin, ChinaXiaoyi Seventh Middle School, Xiaoyi, ChinaTianjin Key Laboratory of Agricultural Animal Breeding and Healthy Husbandry, College of Animal Science and Veterinary Medicine, Tianjin Agricultural University, Tianjin, ChinaTianjin Key Laboratory of Conservation and Utilization of Animal Diversity, College of Life Sciences, Tianjin Normal University, Tianjin, ChinaBackgroundSalmonella enterica Serovar Typhimurium (S. Typhimurium) infection can cause inflammation and oxidative stress in the body, leading to gastroenteritis, fever and other diseases in humans and animals. More and more studies have emphasized the broad prospects of probiotics in improving inflammation and oxidative stress, but the ability and mechanism of Lactobacillus acidophilus (LA) to alleviate the inflammatory/oxidative reaction caused by pathogens are still unclear.Methods and resultsIn this study, we treated the mice with LA for 14 days, infected them with S. Typhimurium for 24 h, and sacrificed the mice to collect samples. We found that the early intervention of LA alleviated the pathological injury and reversed the down-regulation of the duodenal and hepatic tight junction protein mRNA levels caused by S. Typhimurium infection. Compared with S. Typhimurium group, LA early intervention increased the expression of antioxidant enzymes, but decreased the levels of serum malondialdehyde (MDA), interleukin-8 and tumor necrosis factor-α (TNF-α). Additionally, LA early intervention significantly increased Nrf2 mRNA expression in the liver and decreased Keap1 mRNA expression in the duodenum compared to the S. Typhimurium group. Furthermore, early LA treatment reduced the abundance of Bacteroides acidificiens, increased the abundance of Akkermansia, and alleviated the decrease in SCFAs levels in the cecum of S. Typhimurium-infected mice. Spearman correlation analysis showed that there was a certain correlation between cecal flora and serum indicators and short chain fatty acids.ConclusionTaken together, the results indicate that LA early intervention may alleviates S. Typhimurium-induced inflammation and oxidative responses in mice by activating the p62-Keap1-Nrf2 signaling pathway and regulating the gut microbial community.Significance and impact of the studyExploring the ability of LA to resist animal oxidative stress and microflora regulation caused by pathogenic microbes, so as to provide more options for developing healthy disease-resistant feed additives.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483705/fullLactobacillus acidophilusSalmonella Typhimuriuminflammatory responsesoxidative responsesp62-Keap1-Nrf2 signaling pathwaycecal microbiota
spellingShingle Haihua Li
Xinyi Ma
Zhiyuan Shang
Xuejiao Liu
Jiayun Qiao
Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
Frontiers in Microbiology
Lactobacillus acidophilus
Salmonella Typhimurium
inflammatory responses
oxidative responses
p62-Keap1-Nrf2 signaling pathway
cecal microbiota
title Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
title_full Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
title_fullStr Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
title_full_unstemmed Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
title_short Lactobacillus acidophilus alleviate Salmonella enterica Serovar Typhimurium-induced murine inflammatory/oxidative responses via the p62-Keap1-Nrf2 signaling pathway and cecal microbiota
title_sort lactobacillus acidophilus alleviate salmonella enterica serovar typhimurium induced murine inflammatory oxidative responses via the p62 keap1 nrf2 signaling pathway and cecal microbiota
topic Lactobacillus acidophilus
Salmonella Typhimurium
inflammatory responses
oxidative responses
p62-Keap1-Nrf2 signaling pathway
cecal microbiota
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483705/full
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