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Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids

Escherichia coli strain Nissle has been used as a probiotic and therapeutic agent for over a century. Reports suggest that Nissle protects mice from enterohemorrhagic E. coli (EHEC) O157:H7 strains; however, mice are not very susceptible to O157:H7 and are not accurate models for O157:H7 infection i...

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Autores principales: Pradhan, Suman, Weiss, Alison Ann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7343996/
https://www.ncbi.nlm.nih.gov/pubmed/32636253
http://dx.doi.org/10.1128/mBio.01470-20
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author Pradhan, Suman
Weiss, Alison Ann
author_facet Pradhan, Suman
Weiss, Alison Ann
author_sort Pradhan, Suman
collection PubMed
description Escherichia coli strain Nissle has been used as a probiotic and therapeutic agent for over a century. Reports suggest that Nissle protects mice from enterohemorrhagic E. coli (EHEC) O157:H7 strains; however, mice are not very susceptible to O157:H7 and are not accurate models for O157:H7 infection in humans. Also, Nissle is closely related to uropathogenic E. coli (UPEC) strain CFT073, suggesting that Nissle could have pathogenic potential. To assess the safety of and protection conferred by Nissle, we modeled infection in stem cell-derived human intestinal organoids (HIOs). HIOs replicate the structure and function of human intestinal tissue. HIOs have a lumen enclosed by a single cell layer of differentiated epithelium, which is surrounded by a diffuse mesenchymal layer. An epithelial barrier which excludes the luminal contents from the surrounding cell layers and medium develops. Nissle appeared to be nonpathogenic; 10(3) CFU were microinjected into the lumen, and after 3 days, 10(7) CFU were recovered and the epithelial barrier remained intact. In contrast, microinjected EHEC and UPEC bacteria destroyed the epithelial barrier. To assess the protection conferred by Nissle, HIOs microinjected with Nissle were challenged after 18 to 24 h with EHEC or UPEC. Preincubation with Nissle prevented the loss of the epithelial barrier function, the loss of E-cadherin expression, the increased production of reactive oxygen species, and apoptosis. Nissle did not replicate in the HIO coculture, while the pathogenic strains did replicate, suggesting that Nissle conferred protection via activation of host defenses and not by eliminating competing strains. Nissle was shown to be susceptible to some Shiga toxin phage, and Nissle lysogens could produce Shiga toxin.
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spelling pubmed-73439962020-07-10 Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids Pradhan, Suman Weiss, Alison Ann mBio Research Article Escherichia coli strain Nissle has been used as a probiotic and therapeutic agent for over a century. Reports suggest that Nissle protects mice from enterohemorrhagic E. coli (EHEC) O157:H7 strains; however, mice are not very susceptible to O157:H7 and are not accurate models for O157:H7 infection in humans. Also, Nissle is closely related to uropathogenic E. coli (UPEC) strain CFT073, suggesting that Nissle could have pathogenic potential. To assess the safety of and protection conferred by Nissle, we modeled infection in stem cell-derived human intestinal organoids (HIOs). HIOs replicate the structure and function of human intestinal tissue. HIOs have a lumen enclosed by a single cell layer of differentiated epithelium, which is surrounded by a diffuse mesenchymal layer. An epithelial barrier which excludes the luminal contents from the surrounding cell layers and medium develops. Nissle appeared to be nonpathogenic; 10(3) CFU were microinjected into the lumen, and after 3 days, 10(7) CFU were recovered and the epithelial barrier remained intact. In contrast, microinjected EHEC and UPEC bacteria destroyed the epithelial barrier. To assess the protection conferred by Nissle, HIOs microinjected with Nissle were challenged after 18 to 24 h with EHEC or UPEC. Preincubation with Nissle prevented the loss of the epithelial barrier function, the loss of E-cadherin expression, the increased production of reactive oxygen species, and apoptosis. Nissle did not replicate in the HIO coculture, while the pathogenic strains did replicate, suggesting that Nissle conferred protection via activation of host defenses and not by eliminating competing strains. Nissle was shown to be susceptible to some Shiga toxin phage, and Nissle lysogens could produce Shiga toxin. American Society for Microbiology 2020-07-07 /pmc/articles/PMC7343996/ /pubmed/32636253 http://dx.doi.org/10.1128/mBio.01470-20 Text en Copyright © 2020 Pradhan and Weiss. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Pradhan, Suman
Weiss, Alison Ann
Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title_full Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title_fullStr Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title_full_unstemmed Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title_short Probiotic Properties of Escherichia coli Nissle in Human Intestinal Organoids
title_sort probiotic properties of escherichia coli nissle in human intestinal organoids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7343996/
https://www.ncbi.nlm.nih.gov/pubmed/32636253
http://dx.doi.org/10.1128/mBio.01470-20
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