Serotonergic chemosensory neurons modify the C. elegans immune response by regulating G-protein signaling in epithelial cells

PLoS Pathog. 2013;9(12):e1003787. doi: 10.1371/journal.ppat.1003787. Epub 2013 Dec 12.

Abstract

The nervous and immune systems influence each other, allowing animals to rapidly protect themselves from changes in their internal and external environment. However, the complex nature of these systems in mammals makes it difficult to determine how neuronal signaling influences the immune response. Here we show that serotonin, synthesized in Caenorhabditis elegans chemosensory neurons, modulates the immune response. Serotonin released from these cells acts, directly or indirectly, to regulate G-protein signaling in epithelial cells. Signaling in these cells is required for the immune response to infection by the natural pathogen Microbacterium nematophilum. Here we show that serotonin signaling suppresses the innate immune response and limits the rate of pathogen clearance. We show that C. elegans uses classical neurotransmitters to alter the immune response. Serotonin released from sensory neurons may function to modify the immune system in response to changes in the animal's external environment such as the availability, or quality, of food.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / immunology*
  • Caenorhabditis elegans / microbiology
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Epithelial Cells / immunology*
  • Epithelial Cells / metabolism
  • GTP-Binding Protein alpha Subunits, Gi-Go / genetics*
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism
  • Gene Expression Regulation
  • Immunity, Innate / drug effects
  • Immunity, Innate / genetics*
  • RGS Proteins / genetics*
  • RGS Proteins / metabolism
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / metabolism
  • Serotonergic Neurons / immunology*
  • Serotonin / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / immunology

Substances

  • Caenorhabditis elegans Proteins
  • EGL-10 protein, C elegans
  • GOA-1 protein, C elegans
  • RGS Proteins
  • Serotonin
  • GTP-Binding Proteins
  • GTP-Binding Protein alpha Subunits, Gi-Go