Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

Abstract

All olfactory receptors identified in teleost fish are expressed in a single sensory surface, whereas mammalian olfactory receptor gene families segregate into different olfactory organs, chief among them the main olfactory epithelium expressing ORs and TAARs, and the vomeronasal organ expressing V1Rs and V2Rs. A transitional stage is embodied by amphibians, with their vomeronasal organ expressing more 'modern', later diverging V2Rs, whereas more 'ancient', earlier diverging V2Rs are expressed in the main olfactory epithelium.During metamorphosis the main olfactory epithelium of Xenopus tadpoles transforms into an air-filled cavity (principal cavity, air nose), whereas a newly formed cavity (middle cavity) takes over the function of a water nose. We report here that larval expression of ancient V2Rs is gradually lost from the main olfactory epithelium as it transforms into the air nose.Concomitantly, ancient v2r gene expression begins to appear in the basal layers of the newly forming water nose. We observe the same transition for responses to amino acid odorants, consistent with the hypothesis that amino acid responses may be carried by V2R receptors.3

Functional Reintegration of Sensory Neurons and Transitional Dendritic Reduction of Mitral/Tufted Cells during Injury-Induced Recovery of the Larval Xenopus Olfactory Circuit

“…Animals were chosen for this study according to their stage of larval development in order to ensure that the changes that occur in the olfactory system of larval Xenopus laevis during metamorphosis would not overlap with our time window of investigation (Dittrich et al, 2016 ). During metamorphic reorganization of the olfactory organ, whole ORN populations perish, shift locations and a substantial functional rewiring of the system takes place (Dittrich et al, 2016 ; Syed et al, 2016 ). Thus during the process of normal development, MTCs of Xenopus need to be capable of surviving an extended period with diminished axonal input.…”

Neural pathways of olfactory kin imprinting and kin recognition in zebrafish

“…Main and vomeronasal olfactory epithelium. Most amniotes, and to a certain degree amphibians (Syed et al 2017), usually have a separate main olfactory epithelium (MOE) and a vomeronasal organ (VNO). Notably, absence or reduction of a VNO is seen in humans and other primates, as well as in bats and whales (Eisthen 1992).…”

Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

“…In the case of Xenopus , the aquatic main olfactory epithelium of the tadpole transforms into a bi-modal system consisting of the MC epithelium, associated with detection of waterborne odorants, and the PC epithelium dedicated to aerial olfaction. This is supported by evidence showing that the larval PC and the adult MC both possess ciliated and microvillous ORNs (Hansen et al, 1998) and a similar set of olfactory receptors expressed (Amano and Gascuel, 2012; Syed et al, 2013, 2017) that are tuned to detect waterborne odorants like amino acids (Syed et al, 2017). The postmetamorphotic PC, on the other hand, putatively expresses receptor genes more closely related to the mammalian receptors responsive to volatile odors (Freitag et al, 1995, 1998).…”

“…During metamorphosis, major remodeling occurs in the PC of larval Xenopus caused by massive cell death and replacement of ORNs (Hansen et al, 1998;Higgs and Burd, 2001;Dittrich et al, 2016). The remodeled adult PC is eventually composed of only ciliated ORNs and expresses olfactory receptors putatively responsive to airborne odorants (Freitag et al, 1995;Mezler et al, 1999Mezler et al, , 2001, thus assuming the role of the adult 'air nose' (Föske, 1934;Hansen et al, 1998;Syed et al, 2017). In contrast, the VNO does not seem to change significantly during metamorphosis in regard to its cellular composition or function (Hansen et al, 1998;Dittrich et al, 2016).…”