In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice

Alterations in the gut microbiota composition and diversity seem to play a role in the development of chronic diseases, including inflammatory bowel disease (IBD), leading to gut barrier disruption and induction of proinflammatory immune responses. This opens the door for the use of novel health-pro...

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Main Authors: Bernardo Cuffaro, Aka L. W. Assohoun, Denise Boutillier, Lenka Súkeníková, Jérémy Desramaut, Samira Boudebbouze, Sophie Salomé-Desnoulez, Jiří Hrdý, Anne-Judith Waligora-Dupriet, Emmanuelle Maguin, Corinne Grangette
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/9/9/2104
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author Bernardo Cuffaro
Aka L. W. Assohoun
Denise Boutillier
Lenka Súkeníková
Jérémy Desramaut
Samira Boudebbouze
Sophie Salomé-Desnoulez
Jiří Hrdý
Anne-Judith Waligora-Dupriet
Emmanuelle Maguin
Corinne Grangette
author_facet Bernardo Cuffaro
Aka L. W. Assohoun
Denise Boutillier
Lenka Súkeníková
Jérémy Desramaut
Samira Boudebbouze
Sophie Salomé-Desnoulez
Jiří Hrdý
Anne-Judith Waligora-Dupriet
Emmanuelle Maguin
Corinne Grangette
author_sort Bernardo Cuffaro
collection DOAJ
description Alterations in the gut microbiota composition and diversity seem to play a role in the development of chronic diseases, including inflammatory bowel disease (IBD), leading to gut barrier disruption and induction of proinflammatory immune responses. This opens the door for the use of novel health-promoting bacteria. We selected five <i>Parabacteroides distasonis</i> strains isolated from human adult and neonates gut microbiota. We evaluated in vitro their immunomodulation capacities and their ability to reinforce the gut barrier and characterized in vivo their protective effects in an acute murine model of colitis. The in vitro beneficial activities were highly strain dependent: two strains exhibited a potent anti-inflammatory potential and restored the gut barrier while a third strain reinstated the epithelial barrier. While their survival to in vitro gastric conditions was variable, the levels of <i>P. distasonis</i> DNA were higher in the stools of bacteria-treated animals. The strains that were positively scored in vitro displayed a strong ability to rescue mice from colitis. We further showed that two strains primed dendritic cells to induce regulatory T lymphocytes from naïve CD4<sup>+</sup> T cells. This study provides better insights on the functionality of commensal bacteria and crucial clues to design live biotherapeutics able to target inflammatory chronic diseases such as IBD.
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spelling doaj.art-3a4c293489b0476a8928ce453fc6385a2023-11-20T13:54:38ZengMDPI AGCells2073-44092020-09-0199210410.3390/cells9092104In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in MiceBernardo Cuffaro0Aka L. W. Assohoun1Denise Boutillier2Lenka Súkeníková3Jérémy Desramaut4Samira Boudebbouze5Sophie Salomé-Desnoulez6Jiří Hrdý7Anne-Judith Waligora-Dupriet8Emmanuelle Maguin9Corinne Grangette10Université de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Centre d’Infection et d’Immunité de Lille, 59000 Lille, FranceInstitut Micalis, MIHA Team, Université Paris-Saclay, INRAE, AgroParisTech, 78350 Jouy-en-Josas, FranceUniversité de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Centre d’Infection et d’Immunité de Lille, 59000 Lille, FranceInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University and General University Hospital, 121 08 Prague, Czech RepublicUniversité de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Centre d’Infection et d’Immunité de Lille, 59000 Lille, FranceInstitut Micalis, MIHA Team, Université Paris-Saclay, INRAE, AgroParisTech, 78350 Jouy-en-Josas, FranceUniversité de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, US 41-UMS 2014-PLBS, 59000 Lille, FranceInstitute of Immunology and Microbiology, First Faculty of Medicine, Charles University and General University Hospital, 121 08 Prague, Czech RepublicUMR-S1139 INSERM, Faculté de Pharmacie de Paris, Université de Paris, 75006 Paris, FranceInstitut Micalis, MIHA Team, Université Paris-Saclay, INRAE, AgroParisTech, 78350 Jouy-en-Josas, FranceUniversité de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019-UMR 9017-CIIL-Centre d’Infection et d’Immunité de Lille, 59000 Lille, FranceAlterations in the gut microbiota composition and diversity seem to play a role in the development of chronic diseases, including inflammatory bowel disease (IBD), leading to gut barrier disruption and induction of proinflammatory immune responses. This opens the door for the use of novel health-promoting bacteria. We selected five <i>Parabacteroides distasonis</i> strains isolated from human adult and neonates gut microbiota. We evaluated in vitro their immunomodulation capacities and their ability to reinforce the gut barrier and characterized in vivo their protective effects in an acute murine model of colitis. The in vitro beneficial activities were highly strain dependent: two strains exhibited a potent anti-inflammatory potential and restored the gut barrier while a third strain reinstated the epithelial barrier. While their survival to in vitro gastric conditions was variable, the levels of <i>P. distasonis</i> DNA were higher in the stools of bacteria-treated animals. The strains that were positively scored in vitro displayed a strong ability to rescue mice from colitis. We further showed that two strains primed dendritic cells to induce regulatory T lymphocytes from naïve CD4<sup>+</sup> T cells. This study provides better insights on the functionality of commensal bacteria and crucial clues to design live biotherapeutics able to target inflammatory chronic diseases such as IBD.https://www.mdpi.com/2073-4409/9/9/2104microbiotaprobioticsholobiontlive biotherapeutic products (LBP)IBDimmune response
spellingShingle Bernardo Cuffaro
Aka L. W. Assohoun
Denise Boutillier
Lenka Súkeníková
Jérémy Desramaut
Samira Boudebbouze
Sophie Salomé-Desnoulez
Jiří Hrdý
Anne-Judith Waligora-Dupriet
Emmanuelle Maguin
Corinne Grangette
In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
Cells
microbiota
probiotics
holobiont
live biotherapeutic products (LBP)
IBD
immune response
title In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
title_full In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
title_fullStr In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
title_full_unstemmed In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
title_short In Vitro Characterization of Gut Microbiota-Derived Commensal Strains: Selection of <i>Parabacteroides distasonis</i> Strains Alleviating TNBS-Induced Colitis in Mice
title_sort in vitro characterization of gut microbiota derived commensal strains selection of i parabacteroides distasonis i strains alleviating tnbs induced colitis in mice
topic microbiota
probiotics
holobiont
live biotherapeutic products (LBP)
IBD
immune response
url https://www.mdpi.com/2073-4409/9/9/2104
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