<i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells
The gut microbiota contributes to human health and disease; however, the mechanisms by which commensal bacteria interact with the host are still unclear. To date, a number of in vitro systems have been designed to investigate the host–microbe interactions. In most of the intestinal models, the enter...
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| Format: | Article |
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MDPI AG
2022-11-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/10/11/2263 |
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| author | Thomas Gautier Nelly Fahet Zohreh Tamanai-Shacoori Nolwenn Oliviero Marielle Blot Aurélie Sauvager Agnes Burel Sandrine David-Le Gall Sophie Tomasi Sophie Blat Latifa Bousarghin |
| author_facet | Thomas Gautier Nelly Fahet Zohreh Tamanai-Shacoori Nolwenn Oliviero Marielle Blot Aurélie Sauvager Agnes Burel Sandrine David-Le Gall Sophie Tomasi Sophie Blat Latifa Bousarghin |
| author_sort | Thomas Gautier |
| collection | DOAJ |
| description | The gut microbiota contributes to human health and disease; however, the mechanisms by which commensal bacteria interact with the host are still unclear. To date, a number of in vitro systems have been designed to investigate the host–microbe interactions. In most of the intestinal models, the enteroendocrine cells, considered as a potential link between gut bacteria and several human diseases, were missing. In the present study, we have generated a new model by adding enteroendocrine cells (ECC) of L-type (NCI-H716) to the one that we have previously described including enterocytes, mucus, and M cells. After 21 days of culture with the other cells, enteroendocrine-differentiated NCI-H716 cells showed neuropods at their basolateral side and expressed their specific genes encoding proglucagon (<i>GCG</i>) and chromogranin A (<i>CHGA</i>). We showed that this model could be stimulated by commensal bacteria playing a key role in health, <i>Roseburia intestinalis</i> and <i>Bacteroides fragilis</i>, but also by a pathogenic strain such as <i>Salmonella Heidelberg</i>. Moreover, using cell-free supernatants of <i>B. fragilis</i> and <i>R. intestinalis</i>, we have shown that <i>R. intestinalis</i> supernatant induced a significant increase in <i>IL-8</i> and <i>PYY</i> but not in <i>GCG</i> gene expression, while <i>B. fragilis</i> had no impact. Our data indicated that <i>R. intestinalis</i> produced short chain fatty acids (SCFAs) such as butyrate whereas <i>B. fragilis</i> produced more propionate. However, these SCFAs were probably not the only metabolites implicated in <i>PYY</i> expression since butyrate alone had no effect. In conclusion, our new quadricellular model of gut epithelium could be an effective tool to highlight potential beneficial effects of bacteria or their metabolites, in order to develop new classes of probiotics. |
| first_indexed | 2024-03-09T18:08:03Z |
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| id | doaj.art-87fde38c4fce485dbd5ac696fda26911 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T18:08:03Z |
| publishDate | 2022-11-01 |
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| spelling | doaj.art-87fde38c4fce485dbd5ac696fda269112023-11-24T09:17:27ZengMDPI AGMicroorganisms2076-26072022-11-011011226310.3390/microorganisms10112263<i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine CellsThomas Gautier0Nelly Fahet1Zohreh Tamanai-Shacoori2Nolwenn Oliviero3Marielle Blot4Aurélie Sauvager5Agnes Burel6Sandrine David-Le Gall7Sophie Tomasi8Sophie Blat9Latifa Bousarghin10Institut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceISCR (Institut des Sciences Chimiques de Rennes)-UMR CNRS 6226, Univ Rennes, CNRS, F-35000 Rennes, FranceISCR (Institut des Sciences Chimiques de Rennes)-UMR CNRS 6226, Univ Rennes, CNRS, F-35000 Rennes, FrancePlateforme Microscopie Electronique MRic/ISFR Biosit/Campus Santé, Univ Rennes, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceISCR (Institut des Sciences Chimiques de Rennes)-UMR CNRS 6226, Univ Rennes, CNRS, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceInstitut NUMECAN, INSERM, Univ Rennes, INRAE, F-35000 Rennes, FranceThe gut microbiota contributes to human health and disease; however, the mechanisms by which commensal bacteria interact with the host are still unclear. To date, a number of in vitro systems have been designed to investigate the host–microbe interactions. In most of the intestinal models, the enteroendocrine cells, considered as a potential link between gut bacteria and several human diseases, were missing. In the present study, we have generated a new model by adding enteroendocrine cells (ECC) of L-type (NCI-H716) to the one that we have previously described including enterocytes, mucus, and M cells. After 21 days of culture with the other cells, enteroendocrine-differentiated NCI-H716 cells showed neuropods at their basolateral side and expressed their specific genes encoding proglucagon (<i>GCG</i>) and chromogranin A (<i>CHGA</i>). We showed that this model could be stimulated by commensal bacteria playing a key role in health, <i>Roseburia intestinalis</i> and <i>Bacteroides fragilis</i>, but also by a pathogenic strain such as <i>Salmonella Heidelberg</i>. Moreover, using cell-free supernatants of <i>B. fragilis</i> and <i>R. intestinalis</i>, we have shown that <i>R. intestinalis</i> supernatant induced a significant increase in <i>IL-8</i> and <i>PYY</i> but not in <i>GCG</i> gene expression, while <i>B. fragilis</i> had no impact. Our data indicated that <i>R. intestinalis</i> produced short chain fatty acids (SCFAs) such as butyrate whereas <i>B. fragilis</i> produced more propionate. However, these SCFAs were probably not the only metabolites implicated in <i>PYY</i> expression since butyrate alone had no effect. In conclusion, our new quadricellular model of gut epithelium could be an effective tool to highlight potential beneficial effects of bacteria or their metabolites, in order to develop new classes of probiotics.https://www.mdpi.com/2076-2607/10/11/2263hormone-producing cellsquadricellular modelgut commensal bacteriabutyrateproglucagonpeptide tyrosine tyrosine |
| spellingShingle | Thomas Gautier Nelly Fahet Zohreh Tamanai-Shacoori Nolwenn Oliviero Marielle Blot Aurélie Sauvager Agnes Burel Sandrine David-Le Gall Sophie Tomasi Sophie Blat Latifa Bousarghin <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells Microorganisms hormone-producing cells quadricellular model gut commensal bacteria butyrate proglucagon peptide tyrosine tyrosine |
| title | <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells |
| title_full | <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells |
| title_fullStr | <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells |
| title_full_unstemmed | <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells |
| title_short | <i>Roseburia intestinalis</i> Modulates PYY Expression in a New a Multicellular Model including Enteroendocrine Cells |
| title_sort | i roseburia intestinalis i modulates pyy expression in a new a multicellular model including enteroendocrine cells |
| topic | hormone-producing cells quadricellular model gut commensal bacteria butyrate proglucagon peptide tyrosine tyrosine |
| url | https://www.mdpi.com/2076-2607/10/11/2263 |
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