1. Immunology and Inflammation
  2. Neuroscience
Download icon

Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition

  1. C Leopold kurz
  2. Bernard Charroux
  3. Delphine Chaduli
  4. Annelise Viallat-Lieutaud
  5. Julien Royet  Is a corresponding author
  1. Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, France
Research Article
  • Cited 19
  • Views 2,781
  • Annotations
Cite this article as: eLife 2017;6:e21937 doi: 10.7554/eLife.21937

Abstract

As infectious diseases pose a threat to host integrity, eukaryotes have evolved mechanisms to eliminate pathogens. In addition to develop strategies reducing infection, animals can engage in behaviours that lower the impact of the infection. The molecular mechanisms by which microbes impact host behaviour are not well understood. We demonstrate that bacterial infection of Drosophila females reduces oviposition and that peptidoglycan, the component that activates Drosophila antibacterial response, is also the elicitor of this behavioral change. We show that peptidoglycan regulates egg laying rate by activating NF-B signaling pathway in octopaminergic neurons and that, a dedicated peptidoglycan degrading enzyme acts in these neurons to buffer this behavioural response. This study shows that a unique ligand and signaling cascade are used in immune cells to mount an immune response and in neurons to control fly behavior following infection. This may represent a case of behavioural immunity.

Article and author information

Author details

  1. C Leopold kurz

    Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, Marseilles, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Bernard Charroux

    Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, Mraseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Delphine Chaduli

    Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Annelise Viallat-Lieutaud

    Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, Mraseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Julien Royet

    Aix-Marseille Université, Centre National de la Recherche Scientifique, UMR 7288, Institut de Biologie du Développement de Marseille, Marseilles, France
    For correspondence
    julien.royet@univ-amu.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5671-4833

Funding

Centre National de la Recherche Scientifique (24567)

  • Julien Royet

Equipe Fondation pour la Recherche Médicale (DEQ20140329541)

  • Julien Royet

Investissements d'avenir-Labex INFORM (ANR-11-LABx-0054)

  • Julien Royet

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: September 29, 2016
  2. Accepted: February 26, 2017
  3. Accepted Manuscript published: March 7, 2017 (version 1)
  4. Version of Record published: March 24, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 2,781
    Page views
  • 616
    Downloads
  • 19
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Developmental Biology
    2. Immunology and Inflammation
    Chew Leng Lim et al.
    Research Article Updated

    There is strong evidence that the pro-inflammatory microenvironment during post-partum mammary involution promotes parity-associated breast cancer. Estrogen exposure during mammary involution drives tumor growth through neutrophils’ activity. However, how estrogen and neutrophils influence mammary involution are unknown. Combined analysis of transcriptomic, protein, and immunohistochemical data in BALB/c mice showed that estrogen promotes involution by exacerbating inflammation, cell death and adipocytes repopulation. Remarkably, 88% of estrogen-regulated genes in mammary tissue were mediated through neutrophils, which were recruited through estrogen-induced CXCR2 signalling in an autocrine fashion. While neutrophils mediate estrogen-induced inflammation and adipocytes repopulation, estrogen-induced mammary cell death was via lysosome-mediated programmed cell death through upregulation of cathepsin B, Tnf and Bid in a neutrophil-independent manner. Notably, these multifaceted effects of estrogen are mostly mediated by ERα and unique to the phase of mammary involution. These findings are important for the development of intervention strategies for parity-associated breast cancer.

    1. Cell Biology
    2. Immunology and Inflammation
    Daniel Blumenthal et al.
    Research Article Updated

    T cell activation by dendritic cells (DCs) involves forces exerted by the T cell actin cytoskeleton, which are opposed by the cortical cytoskeleton of the interacting antigen-presenting cell. During an immune response, DCs undergo a maturation process that optimizes their ability to efficiently prime naïve T cells. Using atomic force microscopy, we find that during maturation, DC cortical stiffness increases via a process that involves actin polymerization. Using stimulatory hydrogels and DCs expressing mutant cytoskeletal proteins, we find that increasing stiffness lowers the agonist dose needed for T cell activation. CD4+ T cells exhibit much more profound stiffness dependency than CD8+ T cells. Finally, stiffness responses are most robust when T cells are stimulated with pMHC rather than anti-CD3ε, consistent with a mechanosensing mechanism involving receptor deformation. Taken together, our data reveal that maturation-associated cytoskeletal changes alter the biophysical properties of DCs, providing mechanical cues that costimulate T cell activation.