Abstract

The mouse Grueneberg ganglion (GG) is an olfactory subsystem located at the tip of the nose close to the entry of the naris. It comprises neurons that are both sensitive to cold temperature and play an important role in the detection of alarm pheromones (APs). This chemical modality may be essential for species survival. Interestingly, GG neurons display an atypical mammalian olfactory morphology with neurons bearing deeply invaginated cilia mostly covered by ensheathing glial cells. We had previously noticed their morphological resemblance with the chemosensory amphid neurons found in the anterior region of the head of Caenorhabditis elegans (C. elegans). We demonstrate here further molecular and functional similarities. Thus, we found an orthologous expression of molecular signaling elements that was furthermore restricted to similar specific subcellular localizations. Calcium imaging also revealed a ligand selectivity for the methylated thiazole odorants that amphid neurons are known to detect. Cellular responses from GG neurons evoked by chemical or temperature stimuli were also partially cGMP-dependent. In addition, we found that, although behaviors depending on temperature sensing in the mouse, such as huddling and thermotaxis did not implicate the GG, the thermosensitivity modulated the chemosensitivity at the level of single GG neurons. Thus, the striking similarities with the chemosensory amphid neurons of C. elegans conferred to the mouse GG neurons unique multimodal sensory properties.

Highlights

  • Organisms have evolved specialized populations of sensory receptor neurons to detect the chemical information that is present in their environment (Ache and Young, 2005)

  • We focused on the cyclic guanosine monophosphate (cGMP)-dependent proteins and verified by immunohistochemistry their neuronal expression and localization in mouse GG neurons (Figure 1C)

  • We looked for the presence of the particulate guanylyl cyclase G (GC-G), a potential transmembrane receptor (Fleischer et al, 2009; Liu et al, 2009), the cyclic nucleotide-gated channels 3 (CNGA3) (Liu et al, 2009) as well as downstream regulatory elements such as the phosphodiesterase 2A (PDE2A) (Fleischer et al, 2009; Liu et al, 2009; Matsuo et al, 2012) and the cGMPdependent protein kinase of type 2 (Liu et al, 2009)

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Summary

INTRODUCTION

Organisms have evolved specialized populations of sensory receptor neurons to detect the chemical information that is present in their environment (Ache and Young, 2005). Amphid neurons include three principal olfactory classes named amphid wing neurons of type A (AWA), B (AWB), and C (AWC) (Figure 1A) They play a fundamental role in mate identification, in food finding and in noxious conditions avoidance by odortaxis (Bargmann, 2006). The olfactory sensory neurons are dispatched in four distinct subsystems: the main olfactory epithelium (MOE), the septal organ of Masera (SO), the vomeronasal organ (VNO) and the most recently described Grueneberg ganglion (GG) (Gruneberg, 1973) (Figure 1B) These subsystems are implicated in the detection of molecules carrying chemical messages, such as odorants and pheromones that play a role in behaviors ranging from food finding to social communication (Munger et al, 2009). GG neurons, through their position at the tip of the nose, are able to integrate multiple sensory inputs thereby allowing an animal to assess additional aspects of its olfactory environment

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