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Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway

Intestinal melatonin exerts diverse biological effects on the body. Our previous research showed that the abundance of the butyrate-producing bacteria, Roseburia, is positively related to the expression of colonic mucosal melatonin. However, the detailed relationship is unclear. Therefore, we aimed...

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Detalles Bibliográficos
Autores principales: Song, Lijin, He, Meibo, Sun, Qinghua, Wang, Yujing, Zhang, Jindong, Fang, Yuan, Liu, Shuangjiang, Duan, Liping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8746519/
https://www.ncbi.nlm.nih.gov/pubmed/35010992
http://dx.doi.org/10.3390/nu14010117
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author Song, Lijin
He, Meibo
Sun, Qinghua
Wang, Yujing
Zhang, Jindong
Fang, Yuan
Liu, Shuangjiang
Duan, Liping
author_facet Song, Lijin
He, Meibo
Sun, Qinghua
Wang, Yujing
Zhang, Jindong
Fang, Yuan
Liu, Shuangjiang
Duan, Liping
author_sort Song, Lijin
collection PubMed
description Intestinal melatonin exerts diverse biological effects on the body. Our previous research showed that the abundance of the butyrate-producing bacteria, Roseburia, is positively related to the expression of colonic mucosal melatonin. However, the detailed relationship is unclear. Therefore, we aimed to explore whether Roseburia regulates intestinal melatonin and its underlying mechanisms. Male Sprague–Dawley germfree rats were orally administered with or without Roseburia hominis. R. hominis treatment significantly increased the intestinal melatonin level. The concentrations of propionate and butyrate in the intestinal contents were significantly elevated after gavage of R. hominis. Propionate or butyrate treatment increased melatonin, 5-hydroxytryptamine (5-HT), arylalkylamine N-acetyltransferase (AANAT), and phosphorylated cAMP-response element-binding protein (p-CREB) levels. When pretreated with telotristat ethyl, the inhibitor of tryptophan hydroxylase (TPH), or siRNA of Aanat, or 666-15, i.e., an inhibitor of CREB, propionate, or butyrate, could not promote melatonin production in the pheochromocytoma cell line BON-1. Metabolomics analysis showed that propionate and butyrate stimulation regulated levels of some metabolites and some metabolic pathways in BON-1 cell supernatants. In conclusion, propionate and butyrate, i.e., metabolites of R. hominis, can promote intestinal melatonin synthesis by increasing 5-HT levels and promoting p-CREB-mediated Aanat transcription, thereby offering a potential target for ameliorating intestinal diseases.
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spelling pubmed-87465192022-01-11 Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway Song, Lijin He, Meibo Sun, Qinghua Wang, Yujing Zhang, Jindong Fang, Yuan Liu, Shuangjiang Duan, Liping Nutrients Article Intestinal melatonin exerts diverse biological effects on the body. Our previous research showed that the abundance of the butyrate-producing bacteria, Roseburia, is positively related to the expression of colonic mucosal melatonin. However, the detailed relationship is unclear. Therefore, we aimed to explore whether Roseburia regulates intestinal melatonin and its underlying mechanisms. Male Sprague–Dawley germfree rats were orally administered with or without Roseburia hominis. R. hominis treatment significantly increased the intestinal melatonin level. The concentrations of propionate and butyrate in the intestinal contents were significantly elevated after gavage of R. hominis. Propionate or butyrate treatment increased melatonin, 5-hydroxytryptamine (5-HT), arylalkylamine N-acetyltransferase (AANAT), and phosphorylated cAMP-response element-binding protein (p-CREB) levels. When pretreated with telotristat ethyl, the inhibitor of tryptophan hydroxylase (TPH), or siRNA of Aanat, or 666-15, i.e., an inhibitor of CREB, propionate, or butyrate, could not promote melatonin production in the pheochromocytoma cell line BON-1. Metabolomics analysis showed that propionate and butyrate stimulation regulated levels of some metabolites and some metabolic pathways in BON-1 cell supernatants. In conclusion, propionate and butyrate, i.e., metabolites of R. hominis, can promote intestinal melatonin synthesis by increasing 5-HT levels and promoting p-CREB-mediated Aanat transcription, thereby offering a potential target for ameliorating intestinal diseases. MDPI 2021-12-28 /pmc/articles/PMC8746519/ /pubmed/35010992 http://dx.doi.org/10.3390/nu14010117 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Song, Lijin
He, Meibo
Sun, Qinghua
Wang, Yujing
Zhang, Jindong
Fang, Yuan
Liu, Shuangjiang
Duan, Liping
Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title_full Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title_fullStr Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title_full_unstemmed Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title_short Roseburia hominis Increases Intestinal Melatonin Level by Activating p-CREB-AANAT Pathway
title_sort roseburia hominis increases intestinal melatonin level by activating p-creb-aanat pathway
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8746519/
https://www.ncbi.nlm.nih.gov/pubmed/35010992
http://dx.doi.org/10.3390/nu14010117
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