1. Immunology and Inflammation
  2. Neuroscience
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Intestinal infection regulates behavior and learning via neuroendocrine signaling

  1. Jogender Singh
  2. Alejandro Aballay  Is a corresponding author
  1. Oregon Health and Science University, United States
Research Article
  • Cited 19
  • Views 3,804
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Cite this article as: eLife 2019;8:e50033 doi: 10.7554/eLife.50033

Abstract

The recognition of pathogens and subsequent activation of defense responses are critical for the survival of organisms. The nematode Caenorhabditis elegans recognizes pathogenic bacteria and elicits defense responses by activating immune pathways and pathogen avoidance. Here we show that chemosensation of phenazines produced by pathogenic Pseudomonas aeruginosa, which leads to rapid activation of DAF-7/TGF-β in ASJ neurons, is insufficient for the elicitation of pathogen avoidance behavior. Instead, intestinal infection and bloating of the lumen, which depend on the virulence of P. aeruginosa, regulates both pathogen avoidance and aversive learning by modulating not only the DAF-7/TGF-β pathway but also the G-protein coupled receptor NPR-1 pathway, which also controls aerotaxis behavior. Modulation of these neuroendocrine pathways by intestinal infection serves as a systemic feedback that enables animals to avoid virulent bacteria. These results reveal how feedback from the intestine during infection can modulate the behavior, learning, and microbial perception of the host.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Jogender Singh

    Department of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alejandro Aballay

    Department of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, United States
    For correspondence
    aballay@ohsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5975-3352

Funding

National Institute of General Medical Sciences (GM0709077)

  • Alejandro Aballay

National Institute of Allergy and Infectious Diseases (AI117911)

  • Alejandro Aballay

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yuichi Iino, University of Tokyo, Japan

Publication history

  1. Received: July 9, 2019
  2. Accepted: October 31, 2019
  3. Accepted Manuscript published: November 1, 2019 (version 1)
  4. Version of Record published: November 29, 2019 (version 2)

Copyright

© 2019, Singh & Aballay

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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