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Fermentable Dietary Fiber Promotes Helminth Infection and Exacerbates Host Inflammatory Responses

Laura J. Myhill, Sophie Stolzenbach, Helena Mejer, Simon R. Jakobsen, Tina V. A. Hansen, Daniel Andersen, Susanne Brix, Lars H. Hansen, Lukasz Krych, Dennis S. Nielsen, Peter Nejsum, Stig M. Thamsborg and Andrew R. Williams
J Immunol June 1, 2020, 204 (11) 3042-3055; DOI: https://doi.org/10.4049/jimmunol.1901149
Laura J. Myhill
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Sophie Stolzenbach
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Helena Mejer
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Simon R. Jakobsen
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Tina V. A. Hansen
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Daniel Andersen
†Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby DK-2800, Denmark;
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Susanne Brix
†Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby DK-2800, Denmark;
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Lars H. Hansen
‡Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Frederiksberg C DK-1871, Denmark;
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Lukasz Krych
§Department of Food Sciences, Faculty of Science, University of Copenhagen, Frederiksberg C DK-1958, Denmark; and
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Dennis S. Nielsen
§Department of Food Sciences, Faculty of Science, University of Copenhagen, Frederiksberg C DK-1958, Denmark; and
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Peter Nejsum
¶Department of Clinical Medicine, Aarhus University, Aarhus DK-8200, Denmark
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Stig M. Thamsborg
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Andrew R. Williams
*Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C DK-1870, Denmark;
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Key Points

  • Inulin enhanced susceptibility to Trichuris muris infection in C57BL/6 mice.

  • The combination of inulin and infection caused colonic inflammation and dysbiosis.

  • Neutralization of IFN-γ restored worm expulsion in inulin-fed mice.

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Abstract

Fermentable dietary fibers promote the growth of beneficial bacteria, can enhance mucosal barrier integrity, and reduce chronic inflammation. However, effects on intestinal type 2 immune function remain unclear. In this study, we used the murine whipworm Trichuris muris to investigate the effect of the fermentable fiber inulin on host responses to infection regimes that promote distinct Th1 and Th2 responses in C57BL/6 mice. In uninfected mice, dietary inulin stimulated the growth of beneficial bacteria, such as Bifidobacterium (Actinobacteria) and Akkermansia (Verrucomicrobia). Despite this, inulin prevented worm expulsion in normally resistant mice, instead resulting in chronic infection, whereas mice fed an equivalent amount of nonfermentable fiber (cellulose) expelled worms normally. Lack of expulsion in the mice fed inulin was accompanied by a significantly Th1-skewed immune profile characterized by increased T-bet+ T cells and IFN-γ production in mesenteric lymph nodes, increased expression of Ido1 in the cecum, and a complete absence of mast cell and IgE production. Furthermore, the combination of dietary inulin and high-dose T. muris infection caused marked dysbiosis, with expansion of the Firmicutes and Proteobacteria phyla, near elimination of Bacteroidetes, and marked reductions in cecal short-chain fatty acids. Neutralization of IFN-γ during infection abrogated Ido1 expression and was sufficient to restore IgE production and worm expulsion in inulin-fed mice. Our results indicate that, whereas inulin promoted gut health in otherwise healthy mice, during T. muris infection, it exacerbated inflammatory responses and dysbiosis. Thus, the positive effects of fermentable fiber on gut inflammation appear to be context dependent, revealing a novel interaction between diet and infection.

This article is featured in In This Issue, p.2865

Footnotes

  • This work was supported by The Danish Council for Independent Research: Technology and Production Sciences (Grant DFF-4184-00377), The Lundbeck Foundation (Grant R252-2017-1731), and the Carlsberg Foundation (Grant CF17-0422). P.N. was supported by the Independent Research Fund Denmark (Grant DFF-6111-00521).

  • The microarray data presented in this article have been submitted to the Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE136492 and the microbiota sequencing data have been submitted to the Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra/) under accession number PRJNA614961.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    DC
    dendritic cell
    E/S
    excretory/secretory
    GSEA
    Gene Set Enrichment Analysis
    MLN
    mesenteric lymph node
    OTU
    operational taxonomic unit
    PCoA
    principal coordinates analysis
    PERMANOVA
    permutational multivariate ANOVA
    p.i.
    postinfection
    SCFA
    short-chain fatty acid.

  • Received September 19, 2019.
  • Accepted March 24, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 204 (11)
The Journal of Immunology
Vol. 204, Issue 11
1 Jun 2020
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Fermentable Dietary Fiber Promotes Helminth Infection and Exacerbates Host Inflammatory Responses
Laura J. Myhill, Sophie Stolzenbach, Helena Mejer, Simon R. Jakobsen, Tina V. A. Hansen, Daniel Andersen, Susanne Brix, Lars H. Hansen, Lukasz Krych, Dennis S. Nielsen, Peter Nejsum, Stig M. Thamsborg, Andrew R. Williams
The Journal of Immunology June 1, 2020, 204 (11) 3042-3055; DOI: 10.4049/jimmunol.1901149

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Fermentable Dietary Fiber Promotes Helminth Infection and Exacerbates Host Inflammatory Responses
Laura J. Myhill, Sophie Stolzenbach, Helena Mejer, Simon R. Jakobsen, Tina V. A. Hansen, Daniel Andersen, Susanne Brix, Lars H. Hansen, Lukasz Krych, Dennis S. Nielsen, Peter Nejsum, Stig M. Thamsborg, Andrew R. Williams
The Journal of Immunology June 1, 2020, 204 (11) 3042-3055; DOI: 10.4049/jimmunol.1901149
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