Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis

Laura J. Myhill*, Sophie Stolzenbach, Tina V.A. Hansen, Kerstin Skovgaard, C. Rune Stensvold, Lee O.Brien Andersen, Peter Nejsum, Helena Mejer, Stig M. Thamsborg, Andrew R. Williams

*Corresponding author for this work

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Abstract

Diet composition may play a crucial role in shaping host immune responses and commensal gut microbiota populations. Bioactive dietary components, such as inulin, have been extensively studied for their bioactive properties, particularly in modulating gut immune function and reducing inflammation. It has been shown that colonization with gastrointestinal parasitic worms (helminths) may alleviate chronic inflammation through promotion of T-helper cell type (Th) 2 and T-regulatory immune responses and alterations in the gut microbiome. In this study, we investigated if dietary inulin could modulate mucosal immune function in pigs during colonization with the porcine whipworm Trichuris suis. T. Suis infection induced a typical Th2-biased immune response characterized by transcriptional changes in Th2-and barrier function-related genes, accompanied by intestinal remodeling through increased epithelial goblet and tuft cell proliferation. We observed that inulin also up-regulated Th2-related immune genes (IL13, IL5), and suppressed Th1-related pro-inflammatory genes (IFNG, IL1A, IL8) in the colon. Notably, inulin augmented the T. Suis-induced responses with increased transcription of key Th2 and mucosal barrier genes (e.g., IL13, TFF3), and synergistically suppressed pro-inflammatory genes, such as IFNG and CXCL9. 16S rRNA sequencing of proximal colon digesta samples revealed that inulin supplementation reduced the abundance of bacterial phyla linked to inflammation, such as Proteobacteria and Firmicutes, and simultaneously increased Actinobacteria and Bacteroidetes. Interestingly, pigs treated with both inulin and T. Suis displayed the highest Bacteroidetes: Firmicutes ratio and the lowest gut pH, suggesting an interaction of diet and helminth infection that stimulates the growth of beneficial bacterial species. Overall, our data demonstrate that T. Suis infection and inulin co-operatively enhance anti-inflammatory immune responses, which is potentially mediated by changes in microbiota composition. Our results highlight the intricate interactions between diet, immune function and microbiota composition in a porcine helminth infection model. This porcine model should facilitate further investigations into the use of bioactive diets as immunomodulatory mediators against inflammatory conditions, and how diet and parasites may influence gut health.

Original languageEnglish
Article number2557
JournalFrontiers in Immunology
Volume9
Number of pages15
ISSN1664-3224
DOIs
Publication statusPublished - 2018

Keywords

  • Gut microbiota
  • Helminth infection
  • Mucosal immunity
  • Porcine models
  • Prebiotics

Cite this

Myhill, L. J., Stolzenbach, S., Hansen, T. V. A., Skovgaard, K., Stensvold, C. R., Andersen, L. O. B., ... Williams, A. R. (2018). Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis. Frontiers in Immunology, 9, [2557]. https://doi.org/10.3389/fimmu.2018.02557
Myhill, Laura J. ; Stolzenbach, Sophie ; Hansen, Tina V.A. ; Skovgaard, Kerstin ; Stensvold, C. Rune ; Andersen, Lee O.Brien ; Nejsum, Peter ; Mejer, Helena ; Thamsborg, Stig M. ; Williams, Andrew R. / Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis. In: Frontiers in Immunology. 2018 ; Vol. 9.
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title = "Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis",
abstract = "Diet composition may play a crucial role in shaping host immune responses and commensal gut microbiota populations. Bioactive dietary components, such as inulin, have been extensively studied for their bioactive properties, particularly in modulating gut immune function and reducing inflammation. It has been shown that colonization with gastrointestinal parasitic worms (helminths) may alleviate chronic inflammation through promotion of T-helper cell type (Th) 2 and T-regulatory immune responses and alterations in the gut microbiome. In this study, we investigated if dietary inulin could modulate mucosal immune function in pigs during colonization with the porcine whipworm Trichuris suis. T. Suis infection induced a typical Th2-biased immune response characterized by transcriptional changes in Th2-and barrier function-related genes, accompanied by intestinal remodeling through increased epithelial goblet and tuft cell proliferation. We observed that inulin also up-regulated Th2-related immune genes (IL13, IL5), and suppressed Th1-related pro-inflammatory genes (IFNG, IL1A, IL8) in the colon. Notably, inulin augmented the T. Suis-induced responses with increased transcription of key Th2 and mucosal barrier genes (e.g., IL13, TFF3), and synergistically suppressed pro-inflammatory genes, such as IFNG and CXCL9. 16S rRNA sequencing of proximal colon digesta samples revealed that inulin supplementation reduced the abundance of bacterial phyla linked to inflammation, such as Proteobacteria and Firmicutes, and simultaneously increased Actinobacteria and Bacteroidetes. Interestingly, pigs treated with both inulin and T. Suis displayed the highest Bacteroidetes: Firmicutes ratio and the lowest gut pH, suggesting an interaction of diet and helminth infection that stimulates the growth of beneficial bacterial species. Overall, our data demonstrate that T. Suis infection and inulin co-operatively enhance anti-inflammatory immune responses, which is potentially mediated by changes in microbiota composition. Our results highlight the intricate interactions between diet, immune function and microbiota composition in a porcine helminth infection model. This porcine model should facilitate further investigations into the use of bioactive diets as immunomodulatory mediators against inflammatory conditions, and how diet and parasites may influence gut health.",
keywords = "Gut microbiota, Helminth infection, Mucosal immunity, Porcine models, Prebiotics",
author = "Myhill, {Laura J.} and Sophie Stolzenbach and Hansen, {Tina V.A.} and Kerstin Skovgaard and Stensvold, {C. Rune} and Andersen, {Lee O.Brien} and Peter Nejsum and Helena Mejer and Thamsborg, {Stig M.} and Williams, {Andrew R.}",
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Myhill, LJ, Stolzenbach, S, Hansen, TVA, Skovgaard, K, Stensvold, CR, Andersen, LOB, Nejsum, P, Mejer, H, Thamsborg, SM & Williams, AR 2018, 'Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis', Frontiers in Immunology, vol. 9, 2557. https://doi.org/10.3389/fimmu.2018.02557

Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis. / Myhill, Laura J.; Stolzenbach, Sophie; Hansen, Tina V.A.; Skovgaard, Kerstin; Stensvold, C. Rune; Andersen, Lee O.Brien; Nejsum, Peter; Mejer, Helena; Thamsborg, Stig M.; Williams, Andrew R.

In: Frontiers in Immunology, Vol. 9, 2557, 2018.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Mucosal barrier and Th2 immune responses are enhanced by dietary inulin in pigs infected with trichuris suis

AU - Myhill, Laura J.

AU - Stolzenbach, Sophie

AU - Hansen, Tina V.A.

AU - Skovgaard, Kerstin

AU - Stensvold, C. Rune

AU - Andersen, Lee O.Brien

AU - Nejsum, Peter

AU - Mejer, Helena

AU - Thamsborg, Stig M.

AU - Williams, Andrew R.

PY - 2018

Y1 - 2018

N2 - Diet composition may play a crucial role in shaping host immune responses and commensal gut microbiota populations. Bioactive dietary components, such as inulin, have been extensively studied for their bioactive properties, particularly in modulating gut immune function and reducing inflammation. It has been shown that colonization with gastrointestinal parasitic worms (helminths) may alleviate chronic inflammation through promotion of T-helper cell type (Th) 2 and T-regulatory immune responses and alterations in the gut microbiome. In this study, we investigated if dietary inulin could modulate mucosal immune function in pigs during colonization with the porcine whipworm Trichuris suis. T. Suis infection induced a typical Th2-biased immune response characterized by transcriptional changes in Th2-and barrier function-related genes, accompanied by intestinal remodeling through increased epithelial goblet and tuft cell proliferation. We observed that inulin also up-regulated Th2-related immune genes (IL13, IL5), and suppressed Th1-related pro-inflammatory genes (IFNG, IL1A, IL8) in the colon. Notably, inulin augmented the T. Suis-induced responses with increased transcription of key Th2 and mucosal barrier genes (e.g., IL13, TFF3), and synergistically suppressed pro-inflammatory genes, such as IFNG and CXCL9. 16S rRNA sequencing of proximal colon digesta samples revealed that inulin supplementation reduced the abundance of bacterial phyla linked to inflammation, such as Proteobacteria and Firmicutes, and simultaneously increased Actinobacteria and Bacteroidetes. Interestingly, pigs treated with both inulin and T. Suis displayed the highest Bacteroidetes: Firmicutes ratio and the lowest gut pH, suggesting an interaction of diet and helminth infection that stimulates the growth of beneficial bacterial species. Overall, our data demonstrate that T. Suis infection and inulin co-operatively enhance anti-inflammatory immune responses, which is potentially mediated by changes in microbiota composition. Our results highlight the intricate interactions between diet, immune function and microbiota composition in a porcine helminth infection model. This porcine model should facilitate further investigations into the use of bioactive diets as immunomodulatory mediators against inflammatory conditions, and how diet and parasites may influence gut health.

AB - Diet composition may play a crucial role in shaping host immune responses and commensal gut microbiota populations. Bioactive dietary components, such as inulin, have been extensively studied for their bioactive properties, particularly in modulating gut immune function and reducing inflammation. It has been shown that colonization with gastrointestinal parasitic worms (helminths) may alleviate chronic inflammation through promotion of T-helper cell type (Th) 2 and T-regulatory immune responses and alterations in the gut microbiome. In this study, we investigated if dietary inulin could modulate mucosal immune function in pigs during colonization with the porcine whipworm Trichuris suis. T. Suis infection induced a typical Th2-biased immune response characterized by transcriptional changes in Th2-and barrier function-related genes, accompanied by intestinal remodeling through increased epithelial goblet and tuft cell proliferation. We observed that inulin also up-regulated Th2-related immune genes (IL13, IL5), and suppressed Th1-related pro-inflammatory genes (IFNG, IL1A, IL8) in the colon. Notably, inulin augmented the T. Suis-induced responses with increased transcription of key Th2 and mucosal barrier genes (e.g., IL13, TFF3), and synergistically suppressed pro-inflammatory genes, such as IFNG and CXCL9. 16S rRNA sequencing of proximal colon digesta samples revealed that inulin supplementation reduced the abundance of bacterial phyla linked to inflammation, such as Proteobacteria and Firmicutes, and simultaneously increased Actinobacteria and Bacteroidetes. Interestingly, pigs treated with both inulin and T. Suis displayed the highest Bacteroidetes: Firmicutes ratio and the lowest gut pH, suggesting an interaction of diet and helminth infection that stimulates the growth of beneficial bacterial species. Overall, our data demonstrate that T. Suis infection and inulin co-operatively enhance anti-inflammatory immune responses, which is potentially mediated by changes in microbiota composition. Our results highlight the intricate interactions between diet, immune function and microbiota composition in a porcine helminth infection model. This porcine model should facilitate further investigations into the use of bioactive diets as immunomodulatory mediators against inflammatory conditions, and how diet and parasites may influence gut health.

KW - Gut microbiota

KW - Helminth infection

KW - Mucosal immunity

KW - Porcine models

KW - Prebiotics

U2 - 10.3389/fimmu.2018.02557

DO - 10.3389/fimmu.2018.02557

M3 - Journal article

VL - 9

JO - Frontiers in Immunology

JF - Frontiers in Immunology

SN - 1664-3224

M1 - 2557

ER -