Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress-induced depressive-like behavior

doi:10.1111/ejn.15192

. 2021 Jun;53(11):3598-3611.

doi: 10.1111/ejn.15192. Epub 2021 May 10.

Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress-induced depressive-like behavior

Jingjing Rao¹, Ruining Xie², Li Lin², Jian Jiang², Lei Du², Xindie Zeng², Gongying Li³, Chunmei Wang⁴, Yi Qiao²

Affiliations

¹ Cheeloo College of Medicine, Shandong University, Jinan, China.
² Department of Public Health, Jining Medical University, Jining, China.
³ Department of Mental Health, Jining Medical University, Jining, China.
⁴ Neurobiology Institute, Jining Medical University, Jining, China.

PMID: 33742731
DOI: 10.1111/ejn.15192

Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress-induced depressive-like behavior

Jingjing Rao et al. Eur J Neurosci. 2021 Jun.

. 2021 Jun;53(11):3598-3611.

doi: 10.1111/ejn.15192. Epub 2021 May 10.

Authors

Jingjing Rao¹, Ruining Xie², Li Lin², Jian Jiang², Lei Du², Xindie Zeng², Gongying Li³, Chunmei Wang⁴, Yi Qiao²

Affiliations

¹ Cheeloo College of Medicine, Shandong University, Jinan, China.
² Department of Public Health, Jining Medical University, Jining, China.
³ Department of Mental Health, Jining Medical University, Jining, China.
⁴ Neurobiology Institute, Jining Medical University, Jining, China.

PMID: 33742731
DOI: 10.1111/ejn.15192

Abstract

The gut-microbiota-brain axis is the most important complex and bidirectional pathway between the gastrointestinal tract and the central nervous system. This study investigated the potential of microbe-induced gut-to-brain signaling to modulate the effect of stress on depressive-like behavior, intestinal barrier, and neuroinflammation. Result showed that fecal microbiota transplantation increased the consumption of sucrose solutions and decreased the immobility time in forced swimming test. This treatment also increased Firmicutes and decreased Bacteroidetes and Desulfobacterota at phylum levels; reduced the loss of villi and epithelial cells; suppressed the inflammatory cell infiltration in the ileum; increased the expression of ZO-1, occludin; protected the mucosal layer function; and suppressed the high levels of inflammasomes (NLRP3, ASC, caspase-1, and IL-1β) in rat brain. In summary, fecal microbiota transplantation improves the depressive-like behavior, alters the gut microbiota imbalance, and alleviates the intestinal tract inflammation, intestinal mucosa disruption, and neuroinflammation in rats induced by chronic unpredictable mild stress.

Keywords: depression; fecal microbiota transplantation; gut mucosa barrier; gut-microbiota-brain axis; inflammation.

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References

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[1] Alcocer-Gómez, E., Casas-Barquero, N., Williams, M. R., Romero-Guillena, S. L., Cañadas-Lozano, D., Bullón, P., Sánchez-Alcazar, J. A., Navarro-Pando, J. M., & Cordero, M. D. (2017). Antidepressants induce autophagy dependent-NLRP3-inflammasome inhibition in Major depressive disorder. Pharmacological Research, 121, 114-121. https://doi.org/10.1016/j.phrs.2017.04.028

[2] Alcocer-Gómez, E., Casas-Barquero, N., Williams, M. R., Romero-Guillena, S. L., Cañadas-Lozano, D., Bullón, P., Sánchez-Alcazar, J. A., Navarro-Pando, J. M., & Cordero, M. D. (2017). Antidepressants induce autophagy dependent-NLRP3-inflammasome inhibition in Major depressive disorder. Pharmacological Research, 121, 114-121. https://doi.org/10.1016/j.phrs.2017.04.028

[3] Assimakopoulos, S. F., Papageorgiou, I., & Charonis, A. (2011). Enterocytes' tight junctions: From molecules to diseases. World Journal of Gastrointestinal Pathophysiology, 2, 123-137. https://doi.org/10.4291/wjgp.v2.i6.123

[4] Assimakopoulos, S. F., Papageorgiou, I., & Charonis, A. (2011). Enterocytes' tight junctions: From molecules to diseases. World Journal of Gastrointestinal Pathophysiology, 2, 123-137. https://doi.org/10.4291/wjgp.v2.i6.123

[5] Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011). Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain, Behavior, and Immunity, 25, 397-407. https://doi.org/10.1016/j.bbi.2010.10.023

[6] Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011). Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain, Behavior, and Immunity, 25, 397-407. https://doi.org/10.1016/j.bbi.2010.10.023

[7] Carabotti, M., Scirocco, A., Maselli, M. A., & Severi, C. (2015). The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Annals of Gastroenterology, 28, 203-209.

[8] Carabotti, M., Scirocco, A., Maselli, M. A., & Severi, C. (2015). The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Annals of Gastroenterology, 28, 203-209.

[9] Carlessi, A. S., Borba, L. A., Zugno, A. I., Quevedo, J., & Réus, G. Z. (2019). Gut microbiota-brain axis in depression: The role of neuroinflammation. European Journal of Neuroscience. https://doi.org/10.1111/ejn.14631

[10] Carlessi, A. S., Borba, L. A., Zugno, A. I., Quevedo, J., & Réus, G. Z. (2019). Gut microbiota-brain axis in depression: The role of neuroinflammation. European Journal of Neuroscience. https://doi.org/10.1111/ejn.14631

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Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress-induced depressive-like behavior

Affiliations

Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress-induced depressive-like behavior

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