Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses

Oriana Rossi, Lisette A. van Berkel, Florian Chain, M. Tanweer Khan, Nico Taverne, Harry Sokol, Sylvia H. Duncan, Harry J. Flint, Hermie J. M. Harmsen, Philippe Langella, Janneke N. Samsom, Jerry M. Wells

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Abstract

Faecalibacterium prausnitzii strain A2-165 was previously reported to have anti-inflammatory properties and prevent colitis in a TNBS model. We compared the immunomodulatory properties of strain A2-165 to four different F. prausnitzii isolates and eight abundant intestinal commensals using human dendritic cells (DCs) and mouse BMDCs in vitro. Principal component analysis revealed that the cytokine response to F. prausnitzii A2-165 is distinct from the other strains in eliciting high amounts of IL-10 secretion. The mouse DNBS model of relapsing IBD was used to compare the protective effects of F. prausnitzii A2-165 and Clostridium hathewayi, a low secretor of IL-10, on the Th1-driven inflammatory response to DNBS; attenuation of disease parameters was only observed with F. prausnitzii. In an in vivo mouse model of nasal tolerance to ovalbumin, F. prausnitzii A2-165 enhanced ovalbumin-specific T cell proliferation and reduced the proportion of IFN-γ(+) T cells in CLNs. Similarly, in vitro F. prausnitzii A2-165 stimulated BMDCs increased ovalbumin-specific T cell proliferation and reduced the number of IFN-γ(+) T cells. These mechanisms may contribute to the anti-inflammatory effects of F. prausnitzii in colitis and support the notion that this abundant bacterium might contribute to immune homeostasis in the intestine via its anti-inflammatory properties.

Original languageEnglish
Article number18507
Pages (from-to)1-12
Number of pages12
JournalScientific Reports
Volume6
Early online date4 Jan 2016
DOIs
Publication statusPublished - Jan 2016

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varespladib methyl
Interleukin-10
Dendritic Cells
T-Lymphocytes
Ovalbumin
Anti-Inflammatory Agents
Colitis
Cell Proliferation
Clostridium
Faecalibacterium prausnitzii
Principal Component Analysis
Nose
Intestines
Homeostasis
Cytokines
Bacteria

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Rossi, O., van Berkel, L. A., Chain, F., Tanweer Khan, M., Taverne, N., Sokol, H., ... Wells, J. M. (2016). Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Scientific Reports, 6, 1-12. [18507]. https://doi.org/10.1038/srep18507

Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. / Rossi, Oriana; van Berkel, Lisette A.; Chain, Florian; Tanweer Khan, M.; Taverne, Nico; Sokol, Harry; Duncan, Sylvia H.; Flint, Harry J.; Harmsen, Hermie J. M.; Langella, Philippe; Samsom, Janneke N.; Wells, Jerry M.

In: Scientific Reports, Vol. 6, 18507, 01.2016, p. 1-12.

Research output: Contribution to journalArticle

Rossi, O, van Berkel, LA, Chain, F, Tanweer Khan, M, Taverne, N, Sokol, H, Duncan, SH, Flint, HJ, Harmsen, HJM, Langella, P, Samsom, JN & Wells, JM 2016, 'Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses', Scientific Reports, vol. 6, 18507, pp. 1-12. https://doi.org/10.1038/srep18507
Rossi, Oriana ; van Berkel, Lisette A. ; Chain, Florian ; Tanweer Khan, M. ; Taverne, Nico ; Sokol, Harry ; Duncan, Sylvia H. ; Flint, Harry J. ; Harmsen, Hermie J. M. ; Langella, Philippe ; Samsom, Janneke N. ; Wells, Jerry M. / Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. In: Scientific Reports. 2016 ; Vol. 6. pp. 1-12.
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title = "Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses",
abstract = "Faecalibacterium prausnitzii strain A2-165 was previously reported to have anti-inflammatory properties and prevent colitis in a TNBS model. We compared the immunomodulatory properties of strain A2-165 to four different F. prausnitzii isolates and eight abundant intestinal commensals using human dendritic cells (DCs) and mouse BMDCs in vitro. Principal component analysis revealed that the cytokine response to F. prausnitzii A2-165 is distinct from the other strains in eliciting high amounts of IL-10 secretion. The mouse DNBS model of relapsing IBD was used to compare the protective effects of F. prausnitzii A2-165 and Clostridium hathewayi, a low secretor of IL-10, on the Th1-driven inflammatory response to DNBS; attenuation of disease parameters was only observed with F. prausnitzii. In an in vivo mouse model of nasal tolerance to ovalbumin, F. prausnitzii A2-165 enhanced ovalbumin-specific T cell proliferation and reduced the proportion of IFN-γ(+) T cells in CLNs. Similarly, in vitro F. prausnitzii A2-165 stimulated BMDCs increased ovalbumin-specific T cell proliferation and reduced the number of IFN-γ(+) T cells. These mechanisms may contribute to the anti-inflammatory effects of F. prausnitzii in colitis and support the notion that this abundant bacterium might contribute to immune homeostasis in the intestine via its anti-inflammatory properties.",
author = "Oriana Rossi and {van Berkel}, {Lisette A.} and Florian Chain and {Tanweer Khan}, M. and Nico Taverne and Harry Sokol and Duncan, {Sylvia H.} and Flint, {Harry J.} and Harmsen, {Hermie J. M.} and Philippe Langella and Samsom, {Janneke N.} and Wells, {Jerry M.}",
note = "Acknowledgements This work was financially supported by the EC FP7 Cross-talk project (PITN-GA-2008-215553). The authors thank the Histology Platform from GABI research unit and especially Abdelhak Boukadiri for their technical support in the histology sample preparation and Marl{\`e}ne H{\'e}ry, Charline Pontlevoy, Jerome Pottier and Andr{\'e} Tiffoche (UE0907 IERP, Jouy en Josas) for their help during animal experiments. The authors thank Rafael Mu{\~n}oz-Tamayo (INRA) for his help in performing the PCA.",
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AU - Chain, Florian

AU - Tanweer Khan, M.

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AU - Samsom, Janneke N.

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N1 - Acknowledgements This work was financially supported by the EC FP7 Cross-talk project (PITN-GA-2008-215553). The authors thank the Histology Platform from GABI research unit and especially Abdelhak Boukadiri for their technical support in the histology sample preparation and Marlène Héry, Charline Pontlevoy, Jerome Pottier and André Tiffoche (UE0907 IERP, Jouy en Josas) for their help during animal experiments. The authors thank Rafael Muñoz-Tamayo (INRA) for his help in performing the PCA.

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N2 - Faecalibacterium prausnitzii strain A2-165 was previously reported to have anti-inflammatory properties and prevent colitis in a TNBS model. We compared the immunomodulatory properties of strain A2-165 to four different F. prausnitzii isolates and eight abundant intestinal commensals using human dendritic cells (DCs) and mouse BMDCs in vitro. Principal component analysis revealed that the cytokine response to F. prausnitzii A2-165 is distinct from the other strains in eliciting high amounts of IL-10 secretion. The mouse DNBS model of relapsing IBD was used to compare the protective effects of F. prausnitzii A2-165 and Clostridium hathewayi, a low secretor of IL-10, on the Th1-driven inflammatory response to DNBS; attenuation of disease parameters was only observed with F. prausnitzii. In an in vivo mouse model of nasal tolerance to ovalbumin, F. prausnitzii A2-165 enhanced ovalbumin-specific T cell proliferation and reduced the proportion of IFN-γ(+) T cells in CLNs. Similarly, in vitro F. prausnitzii A2-165 stimulated BMDCs increased ovalbumin-specific T cell proliferation and reduced the number of IFN-γ(+) T cells. These mechanisms may contribute to the anti-inflammatory effects of F. prausnitzii in colitis and support the notion that this abundant bacterium might contribute to immune homeostasis in the intestine via its anti-inflammatory properties.

AB - Faecalibacterium prausnitzii strain A2-165 was previously reported to have anti-inflammatory properties and prevent colitis in a TNBS model. We compared the immunomodulatory properties of strain A2-165 to four different F. prausnitzii isolates and eight abundant intestinal commensals using human dendritic cells (DCs) and mouse BMDCs in vitro. Principal component analysis revealed that the cytokine response to F. prausnitzii A2-165 is distinct from the other strains in eliciting high amounts of IL-10 secretion. The mouse DNBS model of relapsing IBD was used to compare the protective effects of F. prausnitzii A2-165 and Clostridium hathewayi, a low secretor of IL-10, on the Th1-driven inflammatory response to DNBS; attenuation of disease parameters was only observed with F. prausnitzii. In an in vivo mouse model of nasal tolerance to ovalbumin, F. prausnitzii A2-165 enhanced ovalbumin-specific T cell proliferation and reduced the proportion of IFN-γ(+) T cells in CLNs. Similarly, in vitro F. prausnitzii A2-165 stimulated BMDCs increased ovalbumin-specific T cell proliferation and reduced the number of IFN-γ(+) T cells. These mechanisms may contribute to the anti-inflammatory effects of F. prausnitzii in colitis and support the notion that this abundant bacterium might contribute to immune homeostasis in the intestine via its anti-inflammatory properties.

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