Light and hydrogen peroxide inhibit C. elegans Feeding through gustatory receptor orthologs and pharyngeal neurons

Neuron. 2015 Feb 18;85(4):804-18. doi: 10.1016/j.neuron.2014.12.061. Epub 2015 Jan 29.

Abstract

While gustatory sensing of the five primary flavors (sweet, salty, sour, bitter, and savory) has been extensively studied, pathways that detect non-canonical taste stimuli remain relatively unexplored. In particular, while reactive oxygen species cause generalized damage to biological systems, no gustatory mechanism to prevent ingestion of such material has been identified in any organism. We observed that light inhibits C. elegans feeding and used light as a tool to uncover molecular and neural mechanisms for gustation. Light can generate hydrogen peroxide, and we discovered that hydrogen peroxide similarly inhibits feeding. The gustatory receptor family members LITE-1 and GUR-3 are required for the inhibition of feeding by light and hydrogen peroxide. The I2 pharyngeal neurons increase calcium in response to light and hydrogen peroxide, and these responses require GUR-3 and a conserved antioxidant enzyme peroxiredoxin PRDX-2. Our results demonstrate a gustatory mechanism that mediates the detection and blocks ingestion of a non-canonical taste stimulus, hydrogen peroxide.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Dose-Response Relationship, Radiation
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Feeding Behavior* / drug effects
  • Feeding Behavior* / physiology
  • Feeding Behavior* / radiation effects
  • Hydrogen Peroxide / pharmacology*
  • Laser Therapy
  • Light*
  • Locomotion / drug effects
  • Locomotion / radiation effects
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mutation / genetics
  • Neurons* / drug effects
  • Neurons* / physiology
  • Neurons* / radiation effects
  • Optogenetics
  • Oxidants / pharmacology*
  • Peroxiredoxins / genetics
  • Peroxiredoxins / metabolism
  • Pharynx / cytology*
  • Reaction Time / drug effects
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • Drosophila Proteins
  • Membrane Proteins
  • Oxidants
  • Receptors, Cell Surface
  • gustatory receptor, Drosophila
  • lite-1 protein, C elegans
  • Hydrogen Peroxide
  • PRDX-2 protein, C elegans
  • Peroxiredoxins
  • Calcium