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Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes

INTRODUCTION: Glutathione peroxidase is abundant in eukaryotes as an important antioxidant enzyme. However, prokaryotic glutathione peroxidase has not been thoroughly studied. Listeria monocytogenes is a facultative intracellular pathogen that is capable of causing listeriosis in animals as well as...

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Autores principales: Zhang, Yu, Guo, Qian, Fang, Xiaowei, Yuan, Mei, Hu, Wenjie, Liang, Xiongyan, Liu, Jing, Yang, Yuying, Fang, Chun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10073551/
https://www.ncbi.nlm.nih.gov/pubmed/37032864
http://dx.doi.org/10.3389/fmicb.2023.1122623
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author Zhang, Yu
Guo, Qian
Fang, Xiaowei
Yuan, Mei
Hu, Wenjie
Liang, Xiongyan
Liu, Jing
Yang, Yuying
Fang, Chun
author_facet Zhang, Yu
Guo, Qian
Fang, Xiaowei
Yuan, Mei
Hu, Wenjie
Liang, Xiongyan
Liu, Jing
Yang, Yuying
Fang, Chun
author_sort Zhang, Yu
collection PubMed
description INTRODUCTION: Glutathione peroxidase is abundant in eukaryotes as an important antioxidant enzyme. However, prokaryotic glutathione peroxidase has not been thoroughly studied. Listeria monocytogenes is a facultative intracellular pathogen that is capable of causing listeriosis in animals as well as humans. Despite the fact that L. monocytogenes encodes a putative glutathione peroxidase, GSH-Px (encoded by lmo0983)), the functions of the enzyme are still unknown. Here we revealed the unusual roles of L. monocytogenes GSH-Px in bacterial antioxidants and pathogenicity. METHODS: L. monocytogenes Lm850658 was taken as the parental strain to construct the gsh-px deletion strain and related complement strain. The effect of the gsh-px gene on the resistance of L. monocytogenes to oxidative stress was determined by measuring the concentrations of glutathione and assaying the stress survival rates under different oxidative conditions. In addition, the pathogenicity of L. monocytogenes was determined by cellular adhesion and invasion assays and mice virulence tests, and the expression of virulence factors was determined by Western blot. RESULTS: Deficiency of GSH-Px not only increased glutathione concentrations in L. monocytogenes but also enhanced its resistance to oxidative stress when exposed to copper and iron ions. In addition, the absence of gsh-px significantly improved the adhesion and invasion efficiency of L. monocytogenes to Caco-2 cells. More importantly, L. monocytogenes lacking GSH-Px could colonize and proliferate more efficiently in mice livers and spleens, enhancing the pathogenicity of L. monocytogenes by increasing the expression of virulence factors like InlA, InlB, and LLO. DISCUSSION: Taken together, we confirmed that GSH-Px of L. monocytogenes has a counter-intuitive effect on the antioxidant capacity and pathogenicity.
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spelling pubmed-100735512023-04-06 Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes Zhang, Yu Guo, Qian Fang, Xiaowei Yuan, Mei Hu, Wenjie Liang, Xiongyan Liu, Jing Yang, Yuying Fang, Chun Front Microbiol Microbiology INTRODUCTION: Glutathione peroxidase is abundant in eukaryotes as an important antioxidant enzyme. However, prokaryotic glutathione peroxidase has not been thoroughly studied. Listeria monocytogenes is a facultative intracellular pathogen that is capable of causing listeriosis in animals as well as humans. Despite the fact that L. monocytogenes encodes a putative glutathione peroxidase, GSH-Px (encoded by lmo0983)), the functions of the enzyme are still unknown. Here we revealed the unusual roles of L. monocytogenes GSH-Px in bacterial antioxidants and pathogenicity. METHODS: L. monocytogenes Lm850658 was taken as the parental strain to construct the gsh-px deletion strain and related complement strain. The effect of the gsh-px gene on the resistance of L. monocytogenes to oxidative stress was determined by measuring the concentrations of glutathione and assaying the stress survival rates under different oxidative conditions. In addition, the pathogenicity of L. monocytogenes was determined by cellular adhesion and invasion assays and mice virulence tests, and the expression of virulence factors was determined by Western blot. RESULTS: Deficiency of GSH-Px not only increased glutathione concentrations in L. monocytogenes but also enhanced its resistance to oxidative stress when exposed to copper and iron ions. In addition, the absence of gsh-px significantly improved the adhesion and invasion efficiency of L. monocytogenes to Caco-2 cells. More importantly, L. monocytogenes lacking GSH-Px could colonize and proliferate more efficiently in mice livers and spleens, enhancing the pathogenicity of L. monocytogenes by increasing the expression of virulence factors like InlA, InlB, and LLO. DISCUSSION: Taken together, we confirmed that GSH-Px of L. monocytogenes has a counter-intuitive effect on the antioxidant capacity and pathogenicity. Frontiers Media S.A. 2023-03-22 /pmc/articles/PMC10073551/ /pubmed/37032864 http://dx.doi.org/10.3389/fmicb.2023.1122623 Text en Copyright © 2023 Zhang, Guo, Fang, Yuan, Hu, Liang, Liu, Yang and Fang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Zhang, Yu
Guo, Qian
Fang, Xiaowei
Yuan, Mei
Hu, Wenjie
Liang, Xiongyan
Liu, Jing
Yang, Yuying
Fang, Chun
Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title_full Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title_fullStr Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title_full_unstemmed Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title_short Destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of Listeria monocytogenes
title_sort destroying glutathione peroxidase improves the oxidative stress resistance and pathogenicity of listeria monocytogenes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10073551/
https://www.ncbi.nlm.nih.gov/pubmed/37032864
http://dx.doi.org/10.3389/fmicb.2023.1122623
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