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Syed AS
,
Sansone A
,
Nadler W
,
Manzini I
,
Korsching SI
.
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Mammalian olfactory receptor families are segregated into different olfactory organs, with type 2 vomeronasal receptor (v2r) genes expressed in a basal layer of the vomeronasal epithelium. In contrast, teleost fish v2r genes are intermingled with all other olfactory receptor genes in a single sensory surface. We report here that, strikingly different from both lineages, the v2r gene family of the amphibian Xenopus laevis is expressed in the main olfactory as well as the vomeronasal epithelium. Interestingly, late diverging v2r genes are expressed exclusively in the vomeronasal epithelium, whereas "ancestral" v2r genes, including the single member of v2r family C, are restricted to the main olfactory epithelium. Moreover, within the main olfactory epithelium, v2r genes are expressed in a basal zone, partially overlapping, but clearly distinct from an apical zone of olfactory marker protein and odorant receptor-expressing cells. These zones are also apparent in the spatial distribution of odor responses, enabling a tentative assignment of odor responses to olfactory receptor gene families. Responses to alcohols, aldehydes, and ketones show an apical localization, consistent with being mediated by odorant receptors, whereas amino acid responses overlap extensively with the basal v2r-expressing zone. The unique bimodal v2r expression pattern in main and accessory olfactory system of amphibians presents an excellent opportunity to study the transition of v2r gene expression during evolution of higher vertebrates.
Fig. 1.
A phylogenetic tree of the X. tropicalis V2R repertoire was generated by a modified maximum-likelihood method (aLRT-ML). Colored branches refer to the nearest X. tropicalis orthologs of cloned X. laevis genes analyzed here. Note that amphibian v2r-C is a single gene, orthologous to the mammalian V2R-C family (8). (Inset) X. laevis genes analyzed here, as well as their closest orthologs in X. tropicalis and an estimate for the number of cross-reacting v2r genes (≥80% amino acid sequence identity to the X. laevis clones). *No close ortholog of v2r-A2b in X. tropicalis. Accession numbers have been deposited with the European Nucleotide Archive.
Fig. 2.
Bimodal expression for the V2R family in MOE and VNO. (A) RT-PCR (40 cycles) was performed under stringent conditions; specificity does not change at higher cycle numbers. Lanes from left to right: VNO, MOE, olfactory bulb, brain, heart, and genomic DNA (in Bottom panel only). A β-actin intron-spanning probe was used as control for absence of genomic DNA contamination (Bottom). Arrows, 400-bp bands of molecular weight marker. (B) Cryosections of larval X. laevis were hybridized with antisense probes for seven v2r genes and omp2 as depicted. Note the bimodal expression of v2r genes in either MOE (Left) or VNO (Right). Micrographs shown are from ventral horizontal sections of larval head tissue, which contain both VNO and MOE. VNO is above and/or to the right of the MOE, see also the colored overlay in C. Most probes cross-react with several to many other genes (Fig. 1), resulting in higher abundance of labeled cells. Scale bar for v2r-C valid for all panels except v2r-A3 E1. (C) Percentage of v2r-expressing cells in MOE (red bars) and VNO (green bars). Axis is shown on top; note the logarithmic scale. Over 100 to 350 cells (corresponding to 1�10 tissue sections) were analyzed per gene. For MOE-specific v2r genes, not a single cell was observed in the VNO, whereas very rare exceptions (2 of 677 cells) were seen for VNO-specific v2r genes.
Fig. 3. A basal zone of the MOE is edicated to v2r gene expression. In situ hybridization was performed for the three MOE-specific v2r genes and omp2 using dorsal horizontal sections of larval head tissue. Enlargements from regions delineated by blue or cyan rectangles are shown to the right of each complete section. A ring of dark brown melanophores delineates the basal border of the epithelium; apical is toward the lumen. All v2r genes are enriched basally, whereas omp2-expressing cells are preferentially localized in an apical region. Forskolin- and amino acid-responsive cells were identified by calcium imaging (green and red ovals, respectively). Forskolin-responsive cells are apically enriched, very similar to omp2-expressing cells, whereas amino acid-responsive cells show a preferentially basal location.
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