Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)

Abstract Background Prenatal exposure to intrauterine inflammation (IUI) is a crucial event in preterm birth (PTB) pathophysiology, increasing the incidence of neurodevelopmental disorders. Gut microbiota and metabolite profile alterations have been reported to be involved in PTB pathophysiology. Me...

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Main Authors: Bei Jia, Lijun Tang, Huibing Liu, Wenqian Chen, Qian Chen, Mei Zhong, Ailan Yin
Format: Article
Language:English
Published: BMC 2024-01-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-023-04603-8
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author Bei Jia
Lijun Tang
Huibing Liu
Wenqian Chen
Qian Chen
Mei Zhong
Ailan Yin
author_facet Bei Jia
Lijun Tang
Huibing Liu
Wenqian Chen
Qian Chen
Mei Zhong
Ailan Yin
author_sort Bei Jia
collection DOAJ
description Abstract Background Prenatal exposure to intrauterine inflammation (IUI) is a crucial event in preterm birth (PTB) pathophysiology, increasing the incidence of neurodevelopmental disorders. Gut microbiota and metabolite profile alterations have been reported to be involved in PTB pathophysiology. Method and results In this study, IUI-exposed PTB mouse model was established and verified by PTB rate and other perinatal adverse reactions; LPS-indued IUI significantly increased the rates of PTB, apoptosis and inflammation in placenta tissue samples. LPS-induced IUI caused no significant differences in species richness and evenness but significantly altered the species abundance distribution. Non-targeted metabolomics analysis indicated that the metabolite profile of the preterm mice was altered, and differential metabolites were associated with signaling pathways including pyruvate metabolism. Furthermore, a significant positive correlation between Parasutterella excrementihominis and S4572761 (Nb-p-coumaroyltryptamine) and Mreference-1264 (pyruvic acid), respectively, was observed. Lastly, pyruvic acid treatment partially improved LPS-induced IUI phenotypes and decreased PTB rates and decreased the apoptosis and inflammation in placenta tissue samples. Conclusion This study revealed an association among gut microbiota dysbiosis, metabolite profile alterations, and LPS-induced IUI and PTB in mice models. Our investigation revealed the possible involvement of gut microbiota in the pathophysiology of LPS-induced IUI and PTB, which might be mediated by metabolites such as pyruvic acid. Future studies should be conducted to verify the findings through larger sample-sized animal studies and clinical investigations.
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spelling doaj.art-8b52cf0db5c741aba1a5c6b851fae30a2024-01-07T12:42:12ZengBMCJournal of Translational Medicine1479-58762024-01-0122111610.1186/s12967-023-04603-8Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)Bei Jia0Lijun Tang1Huibing Liu2Wenqian Chen3Qian Chen4Mei Zhong5Ailan Yin6Department of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityDepartment of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical UniversityAbstract Background Prenatal exposure to intrauterine inflammation (IUI) is a crucial event in preterm birth (PTB) pathophysiology, increasing the incidence of neurodevelopmental disorders. Gut microbiota and metabolite profile alterations have been reported to be involved in PTB pathophysiology. Method and results In this study, IUI-exposed PTB mouse model was established and verified by PTB rate and other perinatal adverse reactions; LPS-indued IUI significantly increased the rates of PTB, apoptosis and inflammation in placenta tissue samples. LPS-induced IUI caused no significant differences in species richness and evenness but significantly altered the species abundance distribution. Non-targeted metabolomics analysis indicated that the metabolite profile of the preterm mice was altered, and differential metabolites were associated with signaling pathways including pyruvate metabolism. Furthermore, a significant positive correlation between Parasutterella excrementihominis and S4572761 (Nb-p-coumaroyltryptamine) and Mreference-1264 (pyruvic acid), respectively, was observed. Lastly, pyruvic acid treatment partially improved LPS-induced IUI phenotypes and decreased PTB rates and decreased the apoptosis and inflammation in placenta tissue samples. Conclusion This study revealed an association among gut microbiota dysbiosis, metabolite profile alterations, and LPS-induced IUI and PTB in mice models. Our investigation revealed the possible involvement of gut microbiota in the pathophysiology of LPS-induced IUI and PTB, which might be mediated by metabolites such as pyruvic acid. Future studies should be conducted to verify the findings through larger sample-sized animal studies and clinical investigations.https://doi.org/10.1186/s12967-023-04603-8Preterm birth (PTB)Intrauterine inflammation (IUI)Gut microbiotaMetabolitesPyruvic acid
spellingShingle Bei Jia
Lijun Tang
Huibing Liu
Wenqian Chen
Qian Chen
Mei Zhong
Ailan Yin
Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
Journal of Translational Medicine
Preterm birth (PTB)
Intrauterine inflammation (IUI)
Gut microbiota
Metabolites
Pyruvic acid
title Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
title_full Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
title_fullStr Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
title_full_unstemmed Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
title_short Potential roles of the interactions between gut microbiota and metabolites in LPS-induced intrauterine inflammation (IUI) and associated preterm birth (PTB)
title_sort potential roles of the interactions between gut microbiota and metabolites in lps induced intrauterine inflammation iui and associated preterm birth ptb
topic Preterm birth (PTB)
Intrauterine inflammation (IUI)
Gut microbiota
Metabolites
Pyruvic acid
url https://doi.org/10.1186/s12967-023-04603-8
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