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Effect of Akkermansia muciniphila, Faecalibacterium prausnitzii, and Their Extracellular Vesicles on the Serotonin System in Intestinal Epithelial Cells

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Abstract

The gastrointestinal (GI) tract is an essential reservoir of serotonin or 5-hydroxytryptamine (5-HT), which possesses a set of bacterial species communities. Intestinal microbiota has the ability to modulate the host’s serotonin system. In this regard, we evaluated the effect of Akkermansia muciniphila and Faecalibacterium prausnitzii along with their extracellular vesicles (EVs) on serotonin system-related genes in human epithelial colorectal adenocarcinoma (Caco-2) cells. The differentiated Caco-2 cells were treated with A. muciniphila and F. prausnitzii with the multiplicity of infection ratio of 1 and 10 and the EV concentration of 1 μg/mL and 50 μg/mL, respectively. After 24 h, the serotonin level was quantified using an ELISA kit and also the gene expression of serotonin system-related genes was examined using the quantitative real-time PCR method. According to the results, treatment with A. muciniphila and F. prausnitzii-derived EVs increased the serotonin level, while none of the bacteria could affect the serotonin level in the Caco-2 cells. Both bacteria had significant effects on the mRNA expression of serotonin system-related genes in the Caco-2 cells. Moreover, we observed that A. muciniphila and F. prausnitzii-derived EVs could impact the expression of major genes involved in the serotonin system. Our findings showed that A. muciniphila and F. prausnitzii along with their EVs could modulate serotonin system-related genes; hence, they may be useful in microbiota modulation therapies to maintain the homeostasis of the serotonin system.

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Acknowledgements

The authors would like to thank the laboratory staff of Microbiology Research Center (MRC) and Department of Mycobacteriology and Pulmonary Research of Pasteur Institute of Iran.

Funding

This study was funded by Pasteur Institute of Iran (Grant No. B-9325).

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Authors and Affiliations

  1. Department of Mycobacteriology and Pulmonary Research, Pasteur Institute of Iran, Tehran, Iran

    Rezvan Yaghoubfar, Ava Behrouzi, Fatemeh Ashrafian, Farzam Vaziri, Seyed Ali Nojoumi, Abolfazl Fateh & Seyed Davar Siadat

  2. Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran

    Rezvan Yaghoubfar, Ava Behrouzi, Fatemeh Ashrafian, Farzam Vaziri, Seyed Ali Nojoumi, Abolfazl Fateh & Seyed Davar Siadat

  3. Department of Microbiology, School of Medicine, Shahed University, Tehran, Iran

    Ehsan Zare Banadkoki

  4. Systems Biomedicine Unit, Pasteur Institute of Iran, Tehran, Iran

    Arezou Lari

  5. Department of Biochemistry, Pasteur Institute of Iran, Tehran, Iran

    Shohreh Khatami

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  1. Rezvan Yaghoubfar
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Contributions

R.Y., A.B., F.A., and F.A. performed the experiments; E.Z.B.K. and A.L. had role in acquisition of data; A.L. and F.V. analyzed the data; A.N. and A.F. read and approved final manuscript; S.D.S. and SH.KH. designed and supervised the study, read, and approved manuscript.

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Correspondence to Abolfazl Fateh or Shohreh Khatami.

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Yaghoubfar, R., Behrouzi, A., Zare Banadkoki, E. et al. Effect of Akkermansia muciniphila, Faecalibacterium prausnitzii, and Their Extracellular Vesicles on the Serotonin System in Intestinal Epithelial Cells. Probiotics & Antimicro. Prot. 13, 1546–1556 (2021). https://doi.org/10.1007/s12602-021-09786-4

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