Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling
Recent studies have shown that the gut microbiome changes brain function, behavior, and psychiatric and neurological disorders. The Gut–Brain Axis (GBA) provides a neuronal pathway to explain this. But exactly how do commensal bacteria signal through the epithelial layer of the large intestine to ac...
Main Authors: | , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-11-01
|
Series: | Nutrients |
Subjects: | |
Online Access: | https://www.mdpi.com/2072-6643/14/22/4856 |
_version_ | 1797464276704690176 |
---|---|
author | John E. Piletz Jason Cooper Kevin Chidester Kyle Erson Sydney Melton Anthony Osemeka Megan Patterson Kyndall Strickland Jing Xuan Wan Kaitlin Williams |
author_facet | John E. Piletz Jason Cooper Kevin Chidester Kyle Erson Sydney Melton Anthony Osemeka Megan Patterson Kyndall Strickland Jing Xuan Wan Kaitlin Williams |
author_sort | John E. Piletz |
collection | DOAJ |
description | Recent studies have shown that the gut microbiome changes brain function, behavior, and psychiatric and neurological disorders. The Gut–Brain Axis (GBA) provides a neuronal pathway to explain this. But exactly how do commensal bacteria signal through the epithelial layer of the large intestine to activate GBA nerve afferents? An in vitro model is described. We differentiated two human cell lines: <i>Caco2Bbe1</i> into mature epithelium on 0.4-micron filters and then <i>SH-SY5Y</i> into mature neurons in 24-well plates. These were co-cultured by placing the epithelium-laden filters 1 mm above the neurons. Twenty-four hours later they were tri-cultured by apical addition of 10<sup>7</sup><i>Lactobacillus rhamnosus</i> or <i>Lactobacillus fermentum</i> which settled on the epithelium. Alone, the <i>Caco2bbe1</i> cells stimulated neurite outgrowth in underlying <i>SH-SY5Y</i>. Beyond this, the lactobacilli were well tolerated and stimulated further neurite outgrowth by 24 h post-treatment, though not passing through the filters. The results provide face validity for a first-of-kind model of transepithelial intestinal lumen-to nerve signaling. The model displays the tight junctional barrier characteristics found in the large intestine while at the same time translating stimulatory signals from the bacteria through epithelial cells to attracted neurons. The model is easy to set-up with components widely available. |
first_indexed | 2024-03-09T18:05:06Z |
format | Article |
id | doaj.art-3800b73d88194ef9ac47b1942ba0cdc8 |
institution | Directory Open Access Journal |
issn | 2072-6643 |
language | English |
last_indexed | 2024-03-09T18:05:06Z |
publishDate | 2022-11-01 |
publisher | MDPI AG |
record_format | Article |
series | Nutrients |
spelling | doaj.art-3800b73d88194ef9ac47b1942ba0cdc82023-11-24T09:32:17ZengMDPI AGNutrients2072-66432022-11-011422485610.3390/nu14224856Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve SignalingJohn E. Piletz0Jason Cooper1Kevin Chidester2Kyle Erson3Sydney Melton4Anthony Osemeka5Megan Patterson6Kyndall Strickland7Jing Xuan Wan8Kaitlin Williams9Office of Global Education, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USADepartment of Biology, Mississippi College, Clinton, MS 39058, USARecent studies have shown that the gut microbiome changes brain function, behavior, and psychiatric and neurological disorders. The Gut–Brain Axis (GBA) provides a neuronal pathway to explain this. But exactly how do commensal bacteria signal through the epithelial layer of the large intestine to activate GBA nerve afferents? An in vitro model is described. We differentiated two human cell lines: <i>Caco2Bbe1</i> into mature epithelium on 0.4-micron filters and then <i>SH-SY5Y</i> into mature neurons in 24-well plates. These were co-cultured by placing the epithelium-laden filters 1 mm above the neurons. Twenty-four hours later they were tri-cultured by apical addition of 10<sup>7</sup><i>Lactobacillus rhamnosus</i> or <i>Lactobacillus fermentum</i> which settled on the epithelium. Alone, the <i>Caco2bbe1</i> cells stimulated neurite outgrowth in underlying <i>SH-SY5Y</i>. Beyond this, the lactobacilli were well tolerated and stimulated further neurite outgrowth by 24 h post-treatment, though not passing through the filters. The results provide face validity for a first-of-kind model of transepithelial intestinal lumen-to nerve signaling. The model displays the tight junctional barrier characteristics found in the large intestine while at the same time translating stimulatory signals from the bacteria through epithelial cells to attracted neurons. The model is easy to set-up with components widely available.https://www.mdpi.com/2072-6643/14/22/4856entericnervous systemcholinergicprobioticsgutbrain |
spellingShingle | John E. Piletz Jason Cooper Kevin Chidester Kyle Erson Sydney Melton Anthony Osemeka Megan Patterson Kyndall Strickland Jing Xuan Wan Kaitlin Williams Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling Nutrients enteric nervous system cholinergic probiotics gut brain |
title | Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling |
title_full | Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling |
title_fullStr | Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling |
title_full_unstemmed | Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling |
title_short | Transepithelial Effect of Probiotics in a Novel Model of Gut Lumen to Nerve Signaling |
title_sort | transepithelial effect of probiotics in a novel model of gut lumen to nerve signaling |
topic | enteric nervous system cholinergic probiotics gut brain |
url | https://www.mdpi.com/2072-6643/14/22/4856 |
work_keys_str_mv | AT johnepiletz transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT jasoncooper transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT kevinchidester transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT kyleerson transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT sydneymelton transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT anthonyosemeka transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT meganpatterson transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT kyndallstrickland transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT jingxuanwan transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling AT kaitlinwilliams transepithelialeffectofprobioticsinanovelmodelofgutlumentonervesignaling |