Identification of a Drosophila glucose receptor using Ca2+ imaging of single chemosensory neurons

PLoS One. 2013;8(2):e56304. doi: 10.1371/journal.pone.0056304. Epub 2013 Feb 13.

Abstract

Evaluation of food compounds by chemosensory cells is essential for animals to make appropriate feeding decisions. In the fruit fly Drosophila melanogaster, structurally diverse chemicals are detected by multimeric receptors composed of members of a large family of Gustatory receptor (Gr) proteins. Putative sugar and bitter receptors are expressed in distinct subsets of Gustatory Receptor Neurons (GRN) of taste sensilla, thereby assigning distinct taste qualities to sugars and bitter tasting compounds, respectively. Here we report a Ca(2+) imaging method that allows association of ligand-mediated responses to a single GRN. We find that different sweet neurons exhibit distinct response profiles when stimulated with various sugars, and likewise, different bitter neurons exhibit distinct response profiles when stimulated with a set of bitter chemicals. These observations suggest that individual neurons within a taste modality are represented by distinct repertoires of sweet and bitter taste receptors, respectively. Furthermore, we employed this novel method to identify glucose as the primary ligand for the sugar receptor Gr61a, which is not only expressed in sweet sensing neurons of classical chemosensory sensilla, but also in two supersensitive neurons of atypical taste sensilla. Thus, single cell Ca(2+) imaging can be employed as a powerful tool to identify ligands for orphan Gr proteins.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Arabinose / metabolism
  • Arabinose / pharmacology
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Chemoreceptor Cells / drug effects
  • Chemoreceptor Cells / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Fructose / metabolism
  • Fructose / pharmacology
  • Glucose / metabolism
  • Glucose / pharmacology
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Maltose / metabolism
  • Maltose / pharmacology
  • Microscopy, Confocal
  • Mutation
  • Neurons / drug effects
  • Neurons / metabolism*
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Sensilla / drug effects
  • Sensilla / metabolism
  • Single-Cell Analysis / methods
  • Sucrose / metabolism
  • Sucrose / pharmacology
  • Taste

Substances

  • Drosophila Proteins
  • Gr61a protein, Drosophila
  • Luminescent Proteins
  • Receptors, Cell Surface
  • glucose receptor
  • gustatory receptor, Drosophila
  • Fructose
  • Sucrose
  • Maltose
  • Arabinose
  • Glucose
  • Calcium