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.
Highlights
The human gastrointestinal (GI) tract has a complex bacterial community, which regulates the host production of several signaling molecules, including serotonin or 5-hydroxytryptamine (5-HT), hormones, and neurotransmitters[1,2,3]
Since recent studies have highlighted the relationship between the gut microbiota and the serotonergic system, in this study, for the first time, we aimed to evaluate the effects of A. muciniphila and its extracellular vesicles (EVs) on the serotonergic system in different anatomical regions of mice and in human colon carcinoma cells (Caco-2 cell line)
In order to determine the effect of A. muciniphila and its EVs on serotonin system in mice, C57BL/6J ones were treated with A. muciniphila and its EVs every day for 4 weeks
Summary
The human gastrointestinal (GI) tract has a complex bacterial community, which regulates the host production of several signaling molecules, including serotonin or 5-hydroxytryptamine (5-HT), hormones, and neurotransmitters[1,2,3]. Since GI is an important reservoir of serotonin, interactions between the microbiota and the serotonergic system play a fundamental role in the pathogenesis of gut disorders through the serotonin-gut microbiota axis In this regard, a published study showed that the gut microbes crucially affect the production of colonic serotonin, given the effect of short-chain fatty acids (SCFAs) on enterochromaffin cells; this finding indicates the importance of the gut microbiota in the regulation of serotonergic system in the h ost[7]. Our recent laboratory study showed that A. muciniphila-derived EVs regulated the intestinal immunity and maintenance of immune homeostasis in the gut better than the bacterium itself[25]. Little is known about the potential of these EVs
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