From In Vitro Data to In Vivo Interspecies Danger Communication: A Study of Chemosensing via the Mouse Grueneberg Ganglion

SIMPLE SUMMARY: The mouse olfactory system is essential for danger detection with a critical role in the Grueneberg ganglion subsystem. This organ, which is localized at the tip of the nose, is implicated in the recognition of kairomones, or chemical cues released by predators which allow interspecies communication. These kairomones, which are present in the secretions of predators, will induce fear-related behaviours in mice. It is not yet known how the Grueneberg ganglion neurons can detect these molecules; however, three specific bitter taste receptors, known as TAS2Rs, that are present in the Grueneberg ganglion play a role in this detection. Here, using in vitro, ex vivo and in vivo experimental approaches, we identified two novel and potent sources of kairomones that are recognized by the mouse Grueneberg ganglion neurons, namely the biological secretions from the raccoon (Procyon lotor) and the skunk (Mephitis mephitis). ABSTRACT: In the wild, mice have developed survival strategies to detect volatile cues that warn them of potential danger. Specific olfactory neurons found in the Grueneberg ganglion olfactory subsystem can detect alarm pheromones emitted by stressed conspecifics, as well as kairomones involuntarily released by their predators. These volatile chemical cues allow intra- and interspecies communication of danger, respectively. Alarm pheromones, kairomones and bitter taste ligands share a common chemical motif containing sulfur or nitrogen. Interestingly, three specific bitter taste receptors (TAS2Rs) have been found in the Grueneberg ganglion neurons that are implicated in danger signalling pathways. We have recently developed a TAS2R–expressing heterologous system that mimics the Grueneberg ganglion neuron responses after kairomone stimulation. Here, we demonstrated by in vitro, ex vivo and in vivo experiments that the biological secretions from the raccoon (Procyon lotor) and the skunk (Mephitis mephitis) were acting as potent sources of kairomones. They activated the Grueneberg ganglion neurons and induced fear-related behaviours in mice. Identification of new sources of semiochemicals is a first step towards an understanding of the interspecies danger communication that takes place in the Grueneberg ganglion.