Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota

Avian meningitis <i>Escherichia coli</i> (<i>E. coli</i>) can cause acute bacterial meningitis which threatens poultry health, causes great economic losses in the poultry industry, and has recently been speculated as a potential zoonotic pathogen. Melatonin can counteract bac...

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Main Authors: Dong Zhang, Shu Xu, Hucong Wu, Jiaqi Liu, Yiting Wang, Guoqiang Zhu
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/1/298
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author Dong Zhang
Shu Xu
Hucong Wu
Jiaqi Liu
Yiting Wang
Guoqiang Zhu
author_facet Dong Zhang
Shu Xu
Hucong Wu
Jiaqi Liu
Yiting Wang
Guoqiang Zhu
author_sort Dong Zhang
collection DOAJ
description Avian meningitis <i>Escherichia coli</i> (<i>E. coli</i>) can cause acute bacterial meningitis which threatens poultry health, causes great economic losses in the poultry industry, and has recently been speculated as a potential zoonotic pathogen. Melatonin can counteract bacterial meningitis-induced disruption of the blood–brain barrier (BBB), neuroinflammation, and reduce mortality. There are increasing data showing that melatonin’s beneficial effects on bacterial meningitis are associated with intestinal microbiota. In this study, our data showed that melatonin alleviated neurological symptoms, enhanced survival rate, protected the integrity of the BBB, reduced the bacterial load in various tissues and blood, and inhibited inflammation and neutrophil infiltration of brain tissue in an APEC TW-XM-meningitis mice model. The results of 16S rRNA showed that melatonin pretreatment significantly maintained the composition of intestinal microbiota in APEC-meningitis mice. The abundance and diversity of intestinal microbiota were disturbed in APEC TW-XM-meningitis mice, with a decreased ratio of <i>Firmicutes</i> to <i>Bacteroides</i> and an increased the abundance of <i>Proteobacteria</i>. Melatonin pretreatment could significantly improve the composition and abundance of harmful bacteria and alleviate the decreased abundance of beneficial bacteria. Importantly, melatonin failed to affect the meningitis neurologic symptoms caused by APEC TW-XM infection in antibiotic-pretreated mice. In conclusion, the results suggest that melatonin can effectively prevent meningitis induced by APEC TW-XM infection in mice, depending on the intestinal microbiota. This finding is helpful to further explore the specific target mechanism of melatonin-mediated intestinal microbiota in the prevention of and protection against <i>Escherichia coli</i> meningitis.
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spelling doaj.art-726750f9b5e047e48c42887b69374d8e2023-11-16T15:31:23ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-12-0124129810.3390/ijms24010298Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal MicrobiotaDong Zhang0Shu Xu1Hucong Wu2Jiaqi Liu3Yiting Wang4Guoqiang Zhu5College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaAvian meningitis <i>Escherichia coli</i> (<i>E. coli</i>) can cause acute bacterial meningitis which threatens poultry health, causes great economic losses in the poultry industry, and has recently been speculated as a potential zoonotic pathogen. Melatonin can counteract bacterial meningitis-induced disruption of the blood–brain barrier (BBB), neuroinflammation, and reduce mortality. There are increasing data showing that melatonin’s beneficial effects on bacterial meningitis are associated with intestinal microbiota. In this study, our data showed that melatonin alleviated neurological symptoms, enhanced survival rate, protected the integrity of the BBB, reduced the bacterial load in various tissues and blood, and inhibited inflammation and neutrophil infiltration of brain tissue in an APEC TW-XM-meningitis mice model. The results of 16S rRNA showed that melatonin pretreatment significantly maintained the composition of intestinal microbiota in APEC-meningitis mice. The abundance and diversity of intestinal microbiota were disturbed in APEC TW-XM-meningitis mice, with a decreased ratio of <i>Firmicutes</i> to <i>Bacteroides</i> and an increased the abundance of <i>Proteobacteria</i>. Melatonin pretreatment could significantly improve the composition and abundance of harmful bacteria and alleviate the decreased abundance of beneficial bacteria. Importantly, melatonin failed to affect the meningitis neurologic symptoms caused by APEC TW-XM infection in antibiotic-pretreated mice. In conclusion, the results suggest that melatonin can effectively prevent meningitis induced by APEC TW-XM infection in mice, depending on the intestinal microbiota. This finding is helpful to further explore the specific target mechanism of melatonin-mediated intestinal microbiota in the prevention of and protection against <i>Escherichia coli</i> meningitis.https://www.mdpi.com/1422-0067/24/1/298bacterial meningitisAPEC TW-XMmelatoninblood–brain barrierinflammationintestinal microbiota
spellingShingle Dong Zhang
Shu Xu
Hucong Wu
Jiaqi Liu
Yiting Wang
Guoqiang Zhu
Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
International Journal of Molecular Sciences
bacterial meningitis
APEC TW-XM
melatonin
blood–brain barrier
inflammation
intestinal microbiota
title Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
title_full Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
title_fullStr Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
title_full_unstemmed Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
title_short Melatonin Is Neuroprotective in <i>Escherichia coli</i> Meningitis Depending on Intestinal Microbiota
title_sort melatonin is neuroprotective in i escherichia coli i meningitis depending on intestinal microbiota
topic bacterial meningitis
APEC TW-XM
melatonin
blood–brain barrier
inflammation
intestinal microbiota
url https://www.mdpi.com/1422-0067/24/1/298
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AT hucongwu melatoninisneuroprotectiveiniescherichiacoliimeningitisdependingonintestinalmicrobiota
AT jiaqiliu melatoninisneuroprotectiveiniescherichiacoliimeningitisdependingonintestinalmicrobiota
AT yitingwang melatoninisneuroprotectiveiniescherichiacoliimeningitisdependingonintestinalmicrobiota
AT guoqiangzhu melatoninisneuroprotectiveiniescherichiacoliimeningitisdependingonintestinalmicrobiota