Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p

PepT1, a proton-coupled oligopeptide transporter, is crucial for intestinal homeostasis. It is mainly expressed in small intestine enterocytes, facilitating the absorption of di/tri-peptides from dietary proteins. In the colon, PepT1 expression is minimal to prevent excessive responses to proinflamm...

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Autores: Olivo-Martinez, Yenifer, Martínez-Ruiz, Sergio, Cordero, Cecilia, Badía Palacín, Josefa, Baldomà Llavinés, Laura
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:2445/217674
Acceso en línea:https://hdl.handle.net/2445/217674
Access Level:acceso abierto
Palabra clave:Microbiota intestinal
Intestins
Probiòtics
Gastrointestinal microbiome
Intestines
Probiotics
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spelling Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3pOlivo-Martinez, YeniferMartínez-Ruiz, SergioCordero, CeciliaBadía Palacín, JosefaBaldomà Llavinés, LauraMicrobiota intestinalIntestinsProbiòticsGastrointestinal microbiomeIntestinesProbioticsPepT1, a proton-coupled oligopeptide transporter, is crucial for intestinal homeostasis. It is mainly expressed in small intestine enterocytes, facilitating the absorption of di/tri-peptides from dietary proteins. In the colon, PepT1 expression is minimal to prevent excessive responses to proinflammatory peptides from the gut microbiota. However, increased colonic PepT1 is linked to chronic inflammatory diseases and colitis-associated cancer. Despite promising results from animal studies on the benefits of extracellular vesicles (EVs) from beneficial gut commensals in treating IBD, applying probiotic EVs as a postbiotic strategy in humans requires a thorough understanding of their mechanisms. Here, we investigate the potential of EVs of the probiotic Nissle 1917 (EcN) and the commensal EcoR12 in preventing altered PepT1 expression under inflammatory conditions, using an interleukin (IL)-1-induced inflammation model in Caco-2 cells. The effects are evaluated by analyzing the expression of PepT1 (mRNA and protein) and miR-193a-3p and miR-92b, which regulate, respectively, PepT1 mRNA translation and degradation. The influence of microbiota EVs on PepT1 expression is also analyzed in the presence of bacterial peptides that are natural substrates of colonic PepT1 to clarify how the regulatory mechanisms function under both physiological andpathological conditions. The main finding is that EcN EVs significantly decreases PepT1 protein via upregulation of miR-193a-3p. Importantly, this regulatory effect is strain-specific and only activates in cells exposed to IL-1β, suggesting that EcN EVs does not control PepT1 expression under basal conditions but can play a pivotal role in response to inflammation as a stressor. By this mechanism,EcN EVs may reduce inflammation in response to microbiota in chronic intestinal disorders by limiting the uptake of bacterial proinflammatory peptides.MDPI2025202520242025info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersion1 p.application/pdfhttps://hdl.handle.net/2445/217674Articles publicats en revistes (Bioquímica i Fisiologia)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésReproducció del document publicat a: https://doi.org/doi: 10.3390/nu16162719Nutrients, 2024, vol. 16, num.2719https://doi.org/doi: 10.3390/nu16162719cc-by (c) Olivo-Martínez, Y. et al., 2024http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:2445/2176742026-05-29T05:05:01Z
dc.title.none.fl_str_mv Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
title Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
spellingShingle Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
Olivo-Martinez, Yenifer
Microbiota intestinal
Intestins
Probiòtics
Gastrointestinal microbiome
Intestines
Probiotics
title_short Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
title_full Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
title_fullStr Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
title_full_unstemmed Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
title_sort Extracellular Vesicles of the Probiotic Escherichia coli Nissle 1917 Reduce PepT1 Levels in IL-1β Treated Caco-2 Cells via Upregulation of miR-193a-3p
dc.creator.none.fl_str_mv Olivo-Martinez, Yenifer
Martínez-Ruiz, Sergio
Cordero, Cecilia
Badía Palacín, Josefa
Baldomà Llavinés, Laura
author Olivo-Martinez, Yenifer
author_facet Olivo-Martinez, Yenifer
Martínez-Ruiz, Sergio
Cordero, Cecilia
Badía Palacín, Josefa
Baldomà Llavinés, Laura
author_role author
author2 Martínez-Ruiz, Sergio
Cordero, Cecilia
Badía Palacín, Josefa
Baldomà Llavinés, Laura
author2_role author
author
author
author
dc.subject.none.fl_str_mv Microbiota intestinal
Intestins
Probiòtics
Gastrointestinal microbiome
Intestines
Probiotics
topic Microbiota intestinal
Intestins
Probiòtics
Gastrointestinal microbiome
Intestines
Probiotics
description PepT1, a proton-coupled oligopeptide transporter, is crucial for intestinal homeostasis. It is mainly expressed in small intestine enterocytes, facilitating the absorption of di/tri-peptides from dietary proteins. In the colon, PepT1 expression is minimal to prevent excessive responses to proinflammatory peptides from the gut microbiota. However, increased colonic PepT1 is linked to chronic inflammatory diseases and colitis-associated cancer. Despite promising results from animal studies on the benefits of extracellular vesicles (EVs) from beneficial gut commensals in treating IBD, applying probiotic EVs as a postbiotic strategy in humans requires a thorough understanding of their mechanisms. Here, we investigate the potential of EVs of the probiotic Nissle 1917 (EcN) and the commensal EcoR12 in preventing altered PepT1 expression under inflammatory conditions, using an interleukin (IL)-1-induced inflammation model in Caco-2 cells. The effects are evaluated by analyzing the expression of PepT1 (mRNA and protein) and miR-193a-3p and miR-92b, which regulate, respectively, PepT1 mRNA translation and degradation. The influence of microbiota EVs on PepT1 expression is also analyzed in the presence of bacterial peptides that are natural substrates of colonic PepT1 to clarify how the regulatory mechanisms function under both physiological andpathological conditions. The main finding is that EcN EVs significantly decreases PepT1 protein via upregulation of miR-193a-3p. Importantly, this regulatory effect is strain-specific and only activates in cells exposed to IL-1β, suggesting that EcN EVs does not control PepT1 expression under basal conditions but can play a pivotal role in response to inflammation as a stressor. By this mechanism,EcN EVs may reduce inflammation in response to microbiota in chronic intestinal disorders by limiting the uptake of bacterial proinflammatory peptides.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/217674
url https://hdl.handle.net/2445/217674
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/doi: 10.3390/nu16162719
Nutrients, 2024, vol. 16, num.2719
https://doi.org/doi: 10.3390/nu16162719
dc.rights.none.fl_str_mv cc-by (c) Olivo-Martínez, Y. et al., 2024
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Olivo-Martínez, Y. et al., 2024
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 1 p.
application/pdf
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
dc.source.none.fl_str_mv Articles publicats en revistes (Bioquímica i Fisiologia)
reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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