Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates

Abstract

The olfactory system of many terrestrial vertebrates comprises a main olfactory organ and a vomeronasal organ each containing a morphologically distinct type of olfactory receptor neuron (ORN). The two cell types also differ in the expression of G-proteins and odorant receptor molecules. Fish do not have a vomeronasal organ, and their olfactory neurons-three different morphological types-are contained in one epithelium. The olfactory organ of goldfish appears as a rosette, with the sensory epithelium lying along the proximal portion of each lamella, where it attaches to the midline raphe. Using immunocytochemistry, in situ hybridization, and electron microscopy, we tested whether a correlation exists between receptor cell morphology, distribution of cell type within the sensory epithelium, and expression of odorant receptors and G-proteins. A strong correlation exists between ORN morphology, type of odorant receptor and G-protein expressed and the distribution of sensory cells within the olfactory epithelium. The Buck and Axel type of odorant receptor and Galpha(olf) are expressed in tall ciliated ORNs distributed homogenously across the entire sensory epithelium. In contrast, microvillous ORNs expressing V2R-like receptors, and Galpha(o), Galpha(q), or Galpha(i-3), and crypt type ORNs expressing Galpha(o) and Galpha(q), are preferentially located along the dorsal margin of the epithelium and near the midline raphe. V2R- and OR-type receptor molecules do not colocalize in one cell, and only crypt-type ORNs express more than one G-protein.

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.…”

“…The RNs expressing the same receptor molecule, project their axons to the same glomerulus, synapsing with few mitral cells (Takigami et al, 2000;Firestein, 2001). Thus it has been suggested that, in the olfactory/vomeronasal system of a vertebrate, the localization of a RN, its morphology, the receptor gene family it expresses, the G-protein subtype coupled with this receptor, and the zone of projection to the OB are somehow correlated (Halpern and Martínez-Marcos, 2003;Hansen et al, 2004).…”