Mutants in Drosophila TRPC channels reduce olfactory sensitivity to carbon dioxide

PLoS One. 2012;7(11):e49848. doi: 10.1371/journal.pone.0049848. Epub 2012 Nov 19.

Abstract

Background: Members of the canonical Transient Receptor Potential (TRPC) class of cationic channels function downstream of Gαq and PLCβ in Drosophila photoreceptors for transducing visual stimuli. Gαq has recently been implicated in olfactory sensing of carbon dioxide (CO(2)) and other odorants. Here we investigated the role of PLCβ and TRPC channels for sensing CO(2) in Drosophila.

Methodology/principal findings: Through behavioral assays it was demonstrated that Drosophila mutants for plc21c, trp and trpl have a reduced sensitivity for CO(2). Immuno-histochemical staining for TRP, TRPL and TRPγ indicates that all three channels are expressed in Drosophila antennae including the sensory neurons that express CO(2) receptors. Electrophysiological recordings obtained from the antennae of protein null alleles of TRP (trp(343)) and TRPL (trpl(302)), showed that the sensory response to multiple concentrations of CO(2) was reduced. However, trpl(302); trp(343) double mutants still have a residual response to CO(2). Down-regulation of TRPC channels specifically in CO(2) sensing olfactory neurons reduced the response to CO(2) and this reduction was obtained even upon down-regulation of the TRPCs in adult olfactory sensory neurons. Thus the reduced response to CO(2) obtained from the antennae of TRPC RNAi strains is not due to a developmental defect.

Conclusion: These observations show that reduction in TRPC channel function significantly reduces the sensitivity of the olfactory response to CO(2) concentrations of 5% or less in adult Drosophila. It is possible that the CO(2) receptors Gr63a and Gr21a activate the TRPC channels through Gαq and PLC21C.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carbon Dioxide / metabolism*
  • Carbon Dioxide / pharmacology
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / physiology
  • Drosophila* / genetics
  • Drosophila* / physiology
  • Gene Expression Regulation
  • Mutation
  • Olfactory Pathways / metabolism
  • Olfactory Pathways / physiology*
  • Phospholipase C beta / genetics
  • Phospholipase C beta / metabolism
  • Photoreceptor Cells, Invertebrate / metabolism
  • Receptors, Cell Surface* / genetics
  • Receptors, Cell Surface* / metabolism
  • Sensory Receptor Cells / metabolism
  • TRPC Cation Channels* / chemistry
  • TRPC Cation Channels* / genetics
  • TRPC Cation Channels* / physiology
  • Vision, Ocular

Substances

  • Drosophila Proteins
  • Gr21a protein, Drosophila
  • Gr63a protein, Drosophila
  • Receptors, Cell Surface
  • TRPC Cation Channels
  • carbon dioxide receptor
  • Carbon Dioxide
  • Phospholipase C beta

Grant support

This work was supported by the Department of Biotechnology, Govt. of India and National Centre for Biological Sciences, Tata Institute of Fundamental Research. The National Centre for Biological Sciences (NCBS) imaging facilities used for this work were supported by the NCBS Central Image-Flow Facility and Department of Science and Technology, Govt. of India (No.SR/S5/NM-36/2005). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.