Insect odorant response sensitivity is tuned by metabotropically autoregulated olfactory receptors

PLoS One. 2013;8(3):e58889. doi: 10.1371/journal.pone.0058889. Epub 2013 Mar 12.

Abstract

Insects possess one of the most exquisitely sensitive olfactory systems in the animal kingdom, consisting of three different types of chemosensory receptors: ionotropic glutamate-like receptors (IRs), gustatory receptors (GRs) and odorant receptors (ORs). Both insect ORs and IRs are ligand-gated ion channels, but ORs possess a unique configuration composed of an odorant-specific protein OrX and a ubiquitous coreceptor (Orco). In addition, these two ionotropic receptors confer different tuning properties for the neurons in which they are expressed. Unlike IRs, neurons expressing ORs are more sensitive and can also be sensitized by sub-threshold concentrations of stimuli. What is the mechanistic basis for these differences in tuning? We show that intrinsic regulation of Orco enhances neuronal response to odorants and sensitizes the ORs. We also demonstrate that inhibition of metabotropic regulation prevents receptor sensitization. Our results indicate that Orco-mediated regulation of OR sensitivity provides tunable ionotropic receptors capable of detecting odors over a wider range of concentrations, providing broadened sensitivity over IRs themselves.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Cyclic AMP / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / metabolism
  • Homeostasis
  • Insecta / physiology*
  • Odorants*
  • Olfactory Receptor Neurons / metabolism*
  • Receptors, Ionotropic Glutamate / metabolism
  • Receptors, Odorant / metabolism*
  • Sensory Thresholds
  • Signal Transduction
  • Stimulation, Chemical

Substances

  • Drosophila Proteins
  • Receptors, Ionotropic Glutamate
  • Receptors, Odorant
  • Cyclic AMP

Grant support

This study was supported by the Max Planck Society (SLL, BSH, DW), the International Max Planck Research School (MNG), and iChem (6th Programme of the EU; SBO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.