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Pulmonary Th17 Antifungal Immunity Is Regulated by the Gut Microbiome

Jeremy P. McAleer, Nikki L. H. Nguyen, Kong Chen, Pawan Kumar, David M. Ricks, Matthew Binnie, Rachel A. Armentrout, Derek A. Pociask, Aaron Hein, Amy Yu, Amit Vikram, Kyle Bibby, Yoshinori Umesaki, Amariliz Rivera, Dean Sheppard, Wenjun Ouyang, Lora V. Hooper and Jay K. Kolls
J Immunol July 1, 2016, 197 (1) 97-107; DOI: https://doi.org/10.4049/jimmunol.1502566
Jeremy P. McAleer
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Nikki L. H. Nguyen
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
†Department of Genetics, Louisiana State University Health Sciences Center, New Orleans, LA 70112;
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Kong Chen
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Pawan Kumar
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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  • ORCID record for Pawan Kumar
David M. Ricks
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
†Department of Genetics, Louisiana State University Health Sciences Center, New Orleans, LA 70112;
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Matthew Binnie
‡Division of Respirology, Department of Medicine, University of Toronto, Ontario M5B 1W8, Canada;
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Rachel A. Armentrout
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Derek A. Pociask
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Aaron Hein
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Amy Yu
†Department of Genetics, Louisiana State University Health Sciences Center, New Orleans, LA 70112;
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Amit Vikram
§Department of Civil and Environmental Engineering, University of Pittsburgh, Pittsburgh, PA 15261;
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Kyle Bibby
§Department of Civil and Environmental Engineering, University of Pittsburgh, Pittsburgh, PA 15261;
¶Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA 15260;
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Yoshinori Umesaki
‖Yakult Central Institute for Microbiological Research, Kunitachi-shi, Tokyo 186-8650, Japan;
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Amariliz Rivera
#Department of Pediatrics, Center for Immunity and Inflammation, New Jersey Medical School, Newark, NJ 07101;
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Dean Sheppard
**Lung Biology Center, University of California, San Francisco, San Francisco, CA 94143;
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Wenjun Ouyang
††Department of Immunology, Genentech, South San Francisco, CA 94080; and
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Lora V. Hooper
‡‡Department of Immunology, Howard Hughes Medical Institute, The University of Texas Southwestern Medical Center, Dallas, TX 75390
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Jay K. Kolls
*Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, Pittsburgh, PA 15224;
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Abstract

Commensal microbiota are critical for the development of local immune responses. In this article, we show that gut microbiota can regulate CD4 T cell polarization during pulmonary fungal infections. Vancomycin drinking water significantly decreased lung Th17 cell numbers during acute infection, demonstrating that Gram-positive commensals contribute to systemic inflammation. We next tested a role for RegIIIγ, an IL-22–inducible antimicrobial protein with specificity for Gram-positive bacteria. Following infection, increased accumulation of Th17 cells in the lungs of RegIIIγ−/− and Il22−/− mice was associated with intestinal segmented filamentous bacteria (SFB) colonization. Although gastrointestinal delivery of rRegIIIγ decreased lung inflammatory gene expression and protected Il22−/− mice from weight loss during infection, it had no direct effect on SFB colonization, fungal clearance, or lung Th17 immunity. We further show that vancomycin only decreased lung IL-17 production in mice colonized with SFB. To determine the link between gut microbiota and lung immunity, serum-transfer experiments revealed that IL-1R ligands increase the accumulation of lung Th17 cells. These data suggest that intestinal microbiota, including SFB, can regulate pulmonary adaptive immune responses.

This article is featured in In This Issue, p.1

Footnotes

  • This work was supported by National Institute of Allergy and Infectious Diseases, National Institutes of Health Award R37-HL079142 (to J.K.K.) and Grant R01 DK070855 (to L.V.H.); J.P.M. was supported in part by Fellowship F32AI096772. L.V.H. also receives support from the Howard Hughes Medical Institute.

  • The sequences presented in this article have been submitted to the Metagenomics RAST server under accession number 4541676.3.

  • The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    B6
    C57BL/6
    BSS
    balanced salt solution
    DC
    dendritic cell
    GF
    germ-free
    IL-1RA
    IL-1R antagonist
    o.p.
    oropharyngeal
    OTU
    operational taxonomic unit
    SFB
    segmented filamentous bacteria
    siLP
    small intestinal lamina propria
    Treg
    regulatory T cell
    WT
    wild-type.

  • Received December 9, 2015.
  • Accepted April 25, 2016.
  • Copyright © 2016 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 197 (1)
The Journal of Immunology
Vol. 197, Issue 1
1 Jul 2016
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Pulmonary Th17 Antifungal Immunity Is Regulated by the Gut Microbiome
Jeremy P. McAleer, Nikki L. H. Nguyen, Kong Chen, Pawan Kumar, David M. Ricks, Matthew Binnie, Rachel A. Armentrout, Derek A. Pociask, Aaron Hein, Amy Yu, Amit Vikram, Kyle Bibby, Yoshinori Umesaki, Amariliz Rivera, Dean Sheppard, Wenjun Ouyang, Lora V. Hooper, Jay K. Kolls
The Journal of Immunology July 1, 2016, 197 (1) 97-107; DOI: 10.4049/jimmunol.1502566

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Pulmonary Th17 Antifungal Immunity Is Regulated by the Gut Microbiome
Jeremy P. McAleer, Nikki L. H. Nguyen, Kong Chen, Pawan Kumar, David M. Ricks, Matthew Binnie, Rachel A. Armentrout, Derek A. Pociask, Aaron Hein, Amy Yu, Amit Vikram, Kyle Bibby, Yoshinori Umesaki, Amariliz Rivera, Dean Sheppard, Wenjun Ouyang, Lora V. Hooper, Jay K. Kolls
The Journal of Immunology July 1, 2016, 197 (1) 97-107; DOI: 10.4049/jimmunol.1502566
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