Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota

Fructus gardeniae (FG) is a traditional Chinese medicine and health food for thousands of years of application throughout Chinese history and is still widely used in clinical Chinese medicine. FG has a beneficial impact on anxiety, depression, insomnia, and psychiatric disorders; however, its mechan...

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Main Authors: Dong Liu, Qianfei Wang, Ying Li, Zhenshuang Yuan, Zhiliang Liu, Junli Guo, Xin Li, Weichao Zhang, Yulei Tao, Jianqiang Mei
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1167312/full
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author Dong Liu
Dong Liu
Qianfei Wang
Ying Li
Zhenshuang Yuan
Zhiliang Liu
Junli Guo
Xin Li
Weichao Zhang
Yulei Tao
Jianqiang Mei
author_facet Dong Liu
Dong Liu
Qianfei Wang
Ying Li
Zhenshuang Yuan
Zhiliang Liu
Junli Guo
Xin Li
Weichao Zhang
Yulei Tao
Jianqiang Mei
author_sort Dong Liu
collection DOAJ
description Fructus gardeniae (FG) is a traditional Chinese medicine and health food for thousands of years of application throughout Chinese history and is still widely used in clinical Chinese medicine. FG has a beneficial impact on anxiety, depression, insomnia, and psychiatric disorders; however, its mechanism of action requires further investigation. This study aimed to investigate the effects and mechanisms of FG on sleep deprivation (SD)-induced anxiety-like behavior in rats. A model of SD-induced anxiety-like behavior in rats was established by intraperitoneal injection of p-chlorophenylalanine (PCPA). This was accompanied by neuroinflammation and metabolic abnormalities in the hippocampus and disturbance of intestinal microbiota. However reduced SD-induced anxiety-like behavior and decreased levels of pro-inflammatory cytokines including TNF-α and IL-1β were observed in the hippocampus of rats after 7 days of FG intervention. In addition, metabolomic analysis demonstrated that FG was able to modulate levels of phosphatidylserine 18, Phosphatidylinositol 18, sn-glycero-3-phosphocholine, deoxyguanylic acid, xylose, betaine and other metabolites in the hippocampus. The main metabolic pathways of hippocampal metabolites after FG intervention involve carbon metabolism, glycolysis/gluconeogenesis, pentose phosphate, and glycerophospholipid metabolism. 16S rRNA sequencing illustrated that FG ameliorated the dysbiosis of gut microbiota in anxious rats, mainly increased the abundance of Muribaculaceae and Lactobacillus, and decreased the abundance of Lachnospiraceae_NK4A136_group. In addition, the correlation analysis demonstrated that there was a close relationship between hippocampal metabolites and intestinal microbiota. In conclusion, FG improved the anxiety behavior and inhibited of neuroinflammation in sleep-deprived rats, and the mechanism may be related to the FG regulation of hippocampal metabolites and intestinal microflora composition.
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spelling doaj.art-05459376526d4ffa81c63904acf12baf2023-06-12T04:28:57ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-06-011310.3389/fcimb.2023.11673121167312Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiotaDong Liu0Dong Liu1Qianfei Wang2Ying Li3Zhenshuang Yuan4Zhiliang Liu5Junli Guo6Xin Li7Weichao Zhang8Yulei Tao9Jianqiang Mei10Department of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Traditional Chinese Medicine, Hebei General Hospital, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Pharmacy, The First Affiliated Hospital, and College of Clinical Medicine of Henan University of Science and Technology, Luoyang, ChinaSchool of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing, ChinaDepartment of Emergency, Hebei Yiling Hospital, Shijiazhang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaDepartment of Emergency, The First Affiliated Hospital of Hebei University of Chinese Medicine, Shijiazhuang, Hebei, ChinaFructus gardeniae (FG) is a traditional Chinese medicine and health food for thousands of years of application throughout Chinese history and is still widely used in clinical Chinese medicine. FG has a beneficial impact on anxiety, depression, insomnia, and psychiatric disorders; however, its mechanism of action requires further investigation. This study aimed to investigate the effects and mechanisms of FG on sleep deprivation (SD)-induced anxiety-like behavior in rats. A model of SD-induced anxiety-like behavior in rats was established by intraperitoneal injection of p-chlorophenylalanine (PCPA). This was accompanied by neuroinflammation and metabolic abnormalities in the hippocampus and disturbance of intestinal microbiota. However reduced SD-induced anxiety-like behavior and decreased levels of pro-inflammatory cytokines including TNF-α and IL-1β were observed in the hippocampus of rats after 7 days of FG intervention. In addition, metabolomic analysis demonstrated that FG was able to modulate levels of phosphatidylserine 18, Phosphatidylinositol 18, sn-glycero-3-phosphocholine, deoxyguanylic acid, xylose, betaine and other metabolites in the hippocampus. The main metabolic pathways of hippocampal metabolites after FG intervention involve carbon metabolism, glycolysis/gluconeogenesis, pentose phosphate, and glycerophospholipid metabolism. 16S rRNA sequencing illustrated that FG ameliorated the dysbiosis of gut microbiota in anxious rats, mainly increased the abundance of Muribaculaceae and Lactobacillus, and decreased the abundance of Lachnospiraceae_NK4A136_group. In addition, the correlation analysis demonstrated that there was a close relationship between hippocampal metabolites and intestinal microbiota. In conclusion, FG improved the anxiety behavior and inhibited of neuroinflammation in sleep-deprived rats, and the mechanism may be related to the FG regulation of hippocampal metabolites and intestinal microflora composition.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1167312/fullfructus gardeniaesleep deprivationanxietyinflammationhippocampal metabolomicsgut microbiota
spellingShingle Dong Liu
Dong Liu
Qianfei Wang
Ying Li
Zhenshuang Yuan
Zhiliang Liu
Junli Guo
Xin Li
Weichao Zhang
Yulei Tao
Jianqiang Mei
Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
Frontiers in Cellular and Infection Microbiology
fructus gardeniae
sleep deprivation
anxiety
inflammation
hippocampal metabolomics
gut microbiota
title Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
title_full Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
title_fullStr Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
title_full_unstemmed Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
title_short Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
title_sort fructus gardeniae ameliorates anxiety like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota
topic fructus gardeniae
sleep deprivation
anxiety
inflammation
hippocampal metabolomics
gut microbiota
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1167312/full
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