Correlation between Olfactory Receptor Cell Type and Function in the Channel Catfish

Abstract

The olfactory epithelium of fish contains three intermingled types of olfactory receptor neurons (ORNs): ciliated, microvillous, and crypt. The present experiments were undertaken to test whether the different types of ORNs respond to different classes of odorants via different families of receptor molecules and G-proteins corresponding to the morphology of the ORN. In catfish, ciliated ORNs express OR-type receptors and Galpha(olf). Microvillous ORNs are heterogeneous, with many expressing Galpha(q)/11, whereas crypt ORNs express Galpha(o). Retrograde tracing experiments show that ciliated ORNs project predominantly to regions of the olfactory bulb (OB) that respond to bile salts (medial) and amino acids (ventral) (Nikonov and Caprio, 2001). In contrast, microvillous ORNs project almost entirely to the dorsal surface of the OB, where responses to nucleotides (posterior OB) and amino acids (anterior OB) predominate. These anatomical findings are consistent with our pharmacological results showing that forskolin (which interferes with Galpha(olf)/cAMP signaling) blocks responses to bile salts and markedly reduces responses to amino acids. Conversely, U-73122 and U-73343 (which interfere with Galpha(q)/11/phospholipase C signaling) diminish amino acid responses but leave bile salt and nucleotide responses essentially unchanged. In summary, our results indicate that bile salt odorants are detected predominantly by ciliated ORNs relying on the Galpha(olf)/cAMP transduction cascade. Nucleotides are detected by microvillous ORNs using neither Galpha(olf)/cAMP nor Galpha(q)/11/PLC cascades. Finally, amino acid odorants activate both ciliated and microvillous ORNs but via different transduction pathways in the two types of cells.

Immunolocalization of G‐Protein Alpha Subunits in the Olfactory System of the Cartilaginous Fish Scyliorhinus Canicula

“…Their sensory epithelia are differentially located in tetrapods, while, in fish, the two systems share the same localization and thence epithelium (Hansen et al, 2003(Hansen et al, , 2004. In mammals, the receptor neurons (RNs) in the olfactory epithelium (OE) express receptors of the olfactory receptor (OR) gene family, whereas the RNs in the vomeronasal epithelium (VE) express receptors of the vomeronasal receptors 1 and 2 (V1R and V2R) gene families (Buck and Axel, 1991;Dulac and Axel, 1995;Dryer, 2000;Halpern and Martínez-Marcos, 2003).…”

“…In mammals, the receptor neurons (RNs) in the olfactory epithelium (OE) express receptors of the olfactory receptor (OR) gene family, whereas the RNs in the vomeronasal epithelium (VE) express receptors of the vomeronasal receptors 1 and 2 (V1R and V2R) gene families (Buck and Axel, 1991;Dulac and Axel, 1995;Dryer, 2000;Halpern and Martínez-Marcos, 2003). In fish, all the receptor gene families are expressed by the RNs located into the same, unique OE (Hansen et al, 2003(Hansen et al, , 2004.…”

“…Moreover, a correlation between the morphology of the RN and the family of the expressed receptor molecule has been demonstrated in many species (Sato and Suzuki, 2001;Lipschitz and Michel, 2002;Halpern and Martínez-Marcos, 2003;Hansen et al, 2003Hansen et al, , 2004Einsthen, 2004;Hansen and Zielinski, 2005;Vielma et al, 2008). The receptor molecules belong to the gene superfamily GPCRs (G-protein coupled receptors).…”

“…The receptor molecules belong to the gene superfamily GPCRs (G-protein coupled receptors). Different types of G-protein have been shown to have a functional co-expression with different receptor molecules; in particular the distribution of different G-protein alpha subunits have been described in the olfactory/vomeronasal system of vertebrates (Takigami et al, 2000;Belanger et al, 2003;Halpern and Martínez-Marcos, 2003;Hansen et al, 2003Hansen et al, , 2004.…”

“…Studies about the organization of the olfactory system and the modality of signal transduction have been carried out in different species of bony fishes and also in jawless fishes (Freitag et al, 1999;Speca et al, 1999;Belanger et al, 2003;Hansen et al, 2003Hansen et al, , 2004Korsching, 2009), but these topics have yet to be explored in Chondrichthyes. The olfactory system of Chondrichthyes has been studied mainly from a morphological point of view (Ebbesson and Heimer, 1970;Theisen et al, 1986;Franceschini and Ciani, 1993;Takami et al, 1994;Ferrando et al, 2006aFerrando et al, ,b, 2007a; its development has been only partially described (Fishelson and Baranes, 1997;Ferrando et al, 2007b;Ferrando, 2008).…”