Transient receptor potential channels encode volatile chemicals sensed by rat trigeminal ganglion neurons

PLoS One. 2013 Oct 21;8(10):e77998. doi: 10.1371/journal.pone.0077998. eCollection 2013.

Abstract

Primary sensory afferents of the dorsal root and trigeminal ganglia constantly transmit sensory information depicting the individual's physical and chemical environment to higher brain regions. Beyond the typical trigeminal stimuli (e.g. irritants), environmental stimuli comprise a plethora of volatile chemicals with olfactory components (odorants). In spite of a complete loss of their sense of smell, anosmic patients may retain the ability to roughly discriminate between different volatile compounds. While the detailed mechanisms remain elusive, sensory structures belonging to the trigeminal system seem to be responsible for this phenomenon. In order to gain a better understanding of the mechanisms underlying the activation of the trigeminal system by volatile chemicals, we investigated odorant-induced membrane potential changes in cultured rat trigeminal neurons induced by the odorants vanillin, heliotropyl acetone, helional, and geraniol. We observed the dose-dependent depolarization of trigeminal neurons upon application of these substances occurring in a stimulus-specific manner and could show that distinct neuronal populations respond to different odorants. Using specific antagonists, we found evidence that TRPA1, TRPM8, and/or TRPV1 contribute to the activation. In order to further test this hypothesis, we used recombinantly expressed rat and human variants of these channels to investigate whether they are indeed activated by the odorants tested. We additionally found that the odorants dose-dependently inhibit two-pore potassium channels TASK1 and TASK3 heterologously expressed In Xenopus laevis oocytes. We suggest that the capability of various odorants to activate different TRP channels and to inhibit potassium channels causes neuronal depolarization and activation of distinct subpopulations of trigeminal sensory neurons, forming the basis for a specific representation of volatile chemicals in the trigeminal ganglia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyclic Monoterpenes
  • Animals
  • Benzaldehydes / pharmacology
  • Cells, Cultured
  • Humans
  • Nerve Tissue Proteins
  • Neurons / drug effects
  • Neurons / metabolism*
  • Potassium Channels, Tandem Pore Domain / antagonists & inhibitors
  • Potassium Channels, Tandem Pore Domain / genetics
  • Potassium Channels, Tandem Pore Domain / metabolism
  • Rats
  • TRPA1 Cation Channel
  • TRPC Cation Channels / antagonists & inhibitors
  • TRPC Cation Channels / genetics
  • TRPC Cation Channels / metabolism
  • TRPM Cation Channels / antagonists & inhibitors
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism
  • TRPV Cation Channels / antagonists & inhibitors
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism
  • Terpenes / pharmacology
  • Transient Receptor Potential Channels / antagonists & inhibitors
  • Transient Receptor Potential Channels / genetics
  • Transient Receptor Potential Channels / metabolism*
  • Trigeminal Ganglion / cytology*
  • Volatile Organic Compounds / pharmacology*

Substances

  • Acyclic Monoterpenes
  • Benzaldehydes
  • Kcnk9 protein, rat
  • Nerve Tissue Proteins
  • Potassium Channels, Tandem Pore Domain
  • TRPA1 Cation Channel
  • TRPC Cation Channels
  • TRPM Cation Channels
  • TRPV Cation Channels
  • Terpenes
  • Transient Receptor Potential Channels
  • Trpa1 protein, rat
  • Trpm8 protein, rat
  • Trpv1 protein, rat
  • Volatile Organic Compounds
  • potassium channel subfamily K member 3
  • vanillin
  • geraniol

Grants and funding

This project was funded by grants from the Deutsche Forschungsgesellschaft [SFB 874 H.H.] and the Ruhr University Research School. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.