Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice

Abstract Several studies have reported that the host-microbe interactions in the gut modulate the host serotonin or 5-hydroxytryptamine (5-HT) system. Here, we evaluated the effects of Akkermansia muciniphila and its extracellular vesicles (EVs) on genes pertaining to the serotonergic system in the...

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Autores principales: Rezvan Yaghoubfar, Ava Behrouzi, Fatemeh Ashrafian, Arefeh Shahryari, Hamid Reza Moradi, Samira Choopani, Shima Hadifar, Farzam Vaziri, Seyed Ali Nojoumi, Abolfazl Fateh, Shohreh Khatami, Seyed Davar Siadat
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Publicado: Nature Portfolio 2020
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spelling oai:doaj.org-article:a206ccd1ca9d4ccc9a27367a61667f9d2021-12-02T13:33:59ZModulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice10.1038/s41598-020-79171-82045-2322https://doaj.org/article/a206ccd1ca9d4ccc9a27367a61667f9d2020-12-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-79171-8https://doaj.org/toc/2045-2322Abstract Several studies have reported that the host-microbe interactions in the gut modulate the host serotonin or 5-hydroxytryptamine (5-HT) system. Here, we evaluated the effects of Akkermansia muciniphila and its extracellular vesicles (EVs) on genes pertaining to the serotonergic system in the colon and hippocampus of mice. Male C57BL/6J mice were administered viable A. muciniphila and its EVs for 4 weeks. The serotonin levels in the colon, hippocampus, and serum of mice, as well as the human colon carcinoma cells (Caco-2), were measured by ELISA assays. Also, the effects of A. muciniphila and its EVs on the expression of serotonin system genes in the colon and hippocampus were examined. A. muciniphila and its EVs may have a biological effect on the induction of serotonin levels in the colon and hippocampus of mice. Also, EVs increased the serotonin level in the Caco-2 cell line. In contrast, both treatments decreased the serotonin level in the serum. Both the bacterium and its EVs had significant effects on the mRNA expression of genes, involved in serotonin signaling/metabolism in the colon and hippocampus of mice. Moreover, A. muciniphila and its EVs affected the mRNA expression of inflammatory cytokines (Il-10 and Tnf-α) in the colon, however, there is no significant difference in inflammatory cell infiltrate in the histopathology of the colon. The presence of A. muciniphila and its EVs in the gut promotes serotonin concentration, they also affect serotonin signaling/metabolism through the gut-brain axis and may be considered in new therapeutic strategies to ameliorate serotonin-related disorders.Rezvan YaghoubfarAva BehrouziFatemeh AshrafianArefeh ShahryariHamid Reza MoradiSamira ChoopaniShima HadifarFarzam VaziriSeyed Ali NojoumiAbolfazl FatehShohreh KhatamiSeyed Davar SiadatNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-12 (2020)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Rezvan Yaghoubfar
Ava Behrouzi
Fatemeh Ashrafian
Arefeh Shahryari
Hamid Reza Moradi
Samira Choopani
Shima Hadifar
Farzam Vaziri
Seyed Ali Nojoumi
Abolfazl Fateh
Shohreh Khatami
Seyed Davar Siadat
Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
description Abstract Several studies have reported that the host-microbe interactions in the gut modulate the host serotonin or 5-hydroxytryptamine (5-HT) system. Here, we evaluated the effects of Akkermansia muciniphila and its extracellular vesicles (EVs) on genes pertaining to the serotonergic system in the colon and hippocampus of mice. Male C57BL/6J mice were administered viable A. muciniphila and its EVs for 4 weeks. The serotonin levels in the colon, hippocampus, and serum of mice, as well as the human colon carcinoma cells (Caco-2), were measured by ELISA assays. Also, the effects of A. muciniphila and its EVs on the expression of serotonin system genes in the colon and hippocampus were examined. A. muciniphila and its EVs may have a biological effect on the induction of serotonin levels in the colon and hippocampus of mice. Also, EVs increased the serotonin level in the Caco-2 cell line. In contrast, both treatments decreased the serotonin level in the serum. Both the bacterium and its EVs had significant effects on the mRNA expression of genes, involved in serotonin signaling/metabolism in the colon and hippocampus of mice. Moreover, A. muciniphila and its EVs affected the mRNA expression of inflammatory cytokines (Il-10 and Tnf-α) in the colon, however, there is no significant difference in inflammatory cell infiltrate in the histopathology of the colon. The presence of A. muciniphila and its EVs in the gut promotes serotonin concentration, they also affect serotonin signaling/metabolism through the gut-brain axis and may be considered in new therapeutic strategies to ameliorate serotonin-related disorders.
format article
author Rezvan Yaghoubfar
Ava Behrouzi
Fatemeh Ashrafian
Arefeh Shahryari
Hamid Reza Moradi
Samira Choopani
Shima Hadifar
Farzam Vaziri
Seyed Ali Nojoumi
Abolfazl Fateh
Shohreh Khatami
Seyed Davar Siadat
author_facet Rezvan Yaghoubfar
Ava Behrouzi
Fatemeh Ashrafian
Arefeh Shahryari
Hamid Reza Moradi
Samira Choopani
Shima Hadifar
Farzam Vaziri
Seyed Ali Nojoumi
Abolfazl Fateh
Shohreh Khatami
Seyed Davar Siadat
author_sort Rezvan Yaghoubfar
title Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
title_short Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
title_full Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
title_fullStr Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
title_full_unstemmed Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
title_sort modulation of serotonin signaling/metabolism by akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice
publisher Nature Portfolio
publishDate 2020
url https://doaj.org/article/a206ccd1ca9d4ccc9a27367a61667f9d
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