Grueneberg ganglion neurons are finely tuned cold sensors.
The Grueneberg ganglion is a newly appreciated nasal subsystem with neural connections to the olfactory forebrain, but its functional role has not been well defined. Here, we assess whether Grueneberg ganglion neurons (GGNs) function as thermosensors. By investigating the effect of acute temperature changes on the cytosolic Ca(2+) concentration of genetically labeled mouse GGNs (either gender), we demonstrate that GGNs are thermosensory neurons specialized to detect a temperature decline within a given temperature window. Furthermore, GGNs comprise a relatively homogeneous cell population with respect to temperature sensitivity. GGNs do not respond to ligands of the temperature-sensitive TRP channels TRPM8 and TRPA1, suggesting a novel mechanism for temperature sensing. One possibility is a cGMP-mediated mechanism, as GGNs express the receptor guanylyl cyclase GC-G, the cGMP-sensitive phosphodiesterase PDE2 and the cGMP-sensitive channel CNGA3. Surprisingly, Cnga3-null mice show normal cooling-induced Ca(2+) responses although cGMP-dependent Ca(2+) increases are absent in these mice. Rather, the cooling-induced Ca(2+) response of GGNs depends critically on the activity of a tetrodotoxin-sensitive voltage-gated sodium channel whereas the cGMP-dependent Ca(2+) signal does not. These findings establish the Grueneberg ganglion as a sensory organ mediating cold-evoked neural responses, possibly in conjunction with the sensing of other stress- or fear-related chemical social cues.
Schmid
Andreas
A
Department of Physiology, University of Saarland School of Medicine, Homburg, Germany.
Pyrski
Martina
M
Biel
Martin
M
Leinders-Zufall
Trese
T
Zufall
Frank
F
D015056:1-Methyl-3-isobutylxanthine / Q000494:pharmacology; D000818:Animals; D000831:Animals, Newborn; D002118:Calcium / Q000378:metabolism; D020013:Calcium Signaling / Q000187:drug effects / Q000235:genetics; D003080:Cold Temperature; D005576:Colforsin / Q000494:pharmacology; D006152:Cyclic GMP / Q000031:analogs & derivatives / Q000494:pharmacology; D054815:Cyclic Nucleotide-Gated Cation Channels / Q000172:deficiency / Q000378:metabolism; D017950:Ganglia, Sensory / Q000166:cytology*; D049452:Green Fluorescent Proteins / Q000235:genetics; D066298:In Vitro Techniques; D017879:Isothiocyanates / Q000494:pharmacology; D051379:Mice; D008822:Mice, Transgenic; D018613:Microscopy, Confocal / Q000379:methods; D009296:Nasal Cavity / Q000294:innervation*; D009830:Olfactory Bulb / Q000502:physiology; D051842:Olfactory Marker Protein / Q000235:genetics / Q000378:metabolism; D009833:Olfactory Pathways / Q000502:physiology; D010726:Phosphodiesterase Inhibitors / Q000494:pharmacology; D011744:Pyrimidinones / Q000494:pharmacology; D011984:Sensory Receptor Cells / Q000187:drug effects / Q000502:physiology*; D026941:Sodium Channel Blockers / Q000494:pharmacology; D000074025:TRPA1 Cation Channel; D013779:Tetrodotoxin / Q000494:pharmacology; D013697:Thermosensing / Q000502:physiology*; D013997:Time Factors; D050051:Transient Receptor Potential Channels / Q000172:deficiency
C518237:Cnga3 protein, mouse; D054815:Cyclic Nucleotide-Gated Cation Channels; D017879:Isothiocyanates; D051842:Olfactory Marker Protein; C497598:Omp protein, mouse; D010726:Phosphodiesterase Inhibitors; D011744:Pyrimidinones; D026941:Sodium Channel Blockers; D000074025:TRPA1 Cation Channel; D050051:Transient Receptor Potential Channels; C475685:Trpa1 protein, mouse; D049452:Green Fluorescent Proteins; D005576:Colforsin; C016276:8-bromocyclic GMP; D013779:Tetrodotoxin; C041942:2,3,4-tri-O-acetylarabinopyranosyl isothiocyanate; C490483:icilin; D006152:Cyclic GMP; D002118:Calcium; D015056:1-Methyl-3-isobutylxanthine