Signal transduction in the vomeronasal organ of garter snakes: ligand-receptor binding-mediated protein phosphorylation.
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The vomeronasal (VN) system of garter snakes plays an important role in several species-typical behaviors, such as prey recognition and responding to courtship pheromones. We (X.C. Jiang et al., J. Biol. Chem. 265 (1990) 8736-8744 and Y. Luo et al., J. Biol. Chem. 269 (1994) 16867-16877) have demonstrated previously that in the snake VN sensory epithelium, the chemoattractant ES20, a 20-kDa glycoprotein derived from electric shock-induced earthworm secretion, binds to its receptor which is coupled to PTX-sensitive G-proteins. Such binding results in elevated levels of IP3. We now report that ES20-receptor binding regulates the phosphorylation of two membrane-bound proteins with molecular masses of 42- and 44-kDa (p42/44) in both intact and cell-free preparations of the VN sensory epithelium. ES20 and DAG regulate the phosphorylation of p42/44 in a similar manner. ES20-receptor binding-mediated phosphorylation of p42/44 is rapid and transient, reaching a peak value within 40 seconds and decaying thereafter. Phosphorylation of p42/44 appears to be regulated by the countervailing actions of a specific membrane-bound protein kinase and a protein phosphatase. The phosphorylation of these membrane-bound proteins significantly reduces the activity of G-proteins as evidenced by a decrease in GTPase activity, but has little effect on ligand-receptor binding. These findings suggest that p42/44 play a role in modulating the signal transduction induced by ES20 in the vomeronasal system. (+info)
Functional dichotomy within the vomeronasal system: distinct zones of neuronal activity in the accessory olfactory bulb correlate with sex-specific behaviors.
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Chemosensory neurons in the vomeronasal organ (VNO) detect pheromones that elicit social and reproductive behaviors in most terrestrial vertebrates. Vomeronasal receptor neurons are chemoarchitecturally divided into two populations based on their position in the VNO, the type of G-protein subunit expressed, the family of putative pheromone receptor expressed, and termination site of their axons in the accessory olfactory bulb (AOB). To investigate the functional implications of these two segregated VNO-AOB pathways, we stimulated mice with pheromonal cues associated with different behavioral contexts and examined cellular activation patterns in the AOB. Exposure of ICR male mice to BALB/c males resulted in aggressive behavior, accompanied by a VNO-dependent increase in c-fos immunoreactivity in a cluster of cells located almost exclusively in the caudal AOB in both strains. This caudal cluster of activated cells did not appear to require the overt display of aggressive behavior because it was present in both the dominant and submissive males and could be evoked when the stimulus animal was anesthetized. In contrast, exposure of an ICR male to an ICR female in diestrus resulted in activation of cells located predominantly in the rostral AOB. Our findings indicate that male-to-male interactions involving interstrain recognition activate a separate population of vomeronasal receptor neurons than chemosensory cues detected in a sexual context. The results suggest that the dichotomy in the peripheral vomeronasal system serves to separate pheromones based on the behaviors they drive. As such, the results provide a bioassay for identifying pheromone molecules. (+info)
G(o) protein-dependent survival of primary accessory olfactory neurons.
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Extensive G protein-coupled receptor families in both the main and accessory olfactory systems have been implicated in axonal targeting, sensory function, and cell survival. Although sensory function seems to be mediated by G proteins, axonal guidance and cell survival may be G protein-independent processes. In the accessory olfactory system, the G(o)-containing neurons in the basal vomeronasal organ (VNO) project to the posterior accessory olfactory bulb (AOB), whereas more apically located VNO neurons contain G(i2) and project to the anterior AOB. Herein, we investigate the organization of the accessory olfactory system in mice with a targeted deletion in the G(o)alpha gene. The accessory olfactory system seems normal at birth; however, postnatally, the number of G(o)-receptor-containing VNO neurons decreases by half, and apoptotic neurons are detected. The axons of VNO neurons remain restricted to the posterior AOB. The posterior AOB is reduced in size but contains a synaptophysin-positive layer with the normal number of glomeruli. The posterior AOB has reduced mitral cell c-Fos immunoreactivity, consistent with decreased sensory activation of G(o) protein-coupled VNO receptor neurons. Thus, in the accessory olfactory system, receptor-coupled G proteins are required for cell survival. (+info)
The vomeronasal organ in the human embryo, studied by means of three-dimensional computer reconstruction.
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The human vomeronasal organ is of interest because of its potential role in sex pheromone detection. Due to the scarcity of early human material, studies of its development have concentrated on fetal rather than embryonic stages. The availability of embryonic specimens in the Walmsley Collection has enabled us to study the development of the vomeronasal organ (VNO) in human embryos between Carnegie Stages 17 and 23. Embryos at Carnegie Stage 17 or below showed no evidence of a VNO. One embryo with characteristics intermediate between Carnegie stages 17 and 18 was the earliest to show evidence of a VNO, in the form of a shallow indentation. All embryos at Carnegie Stages 18 or later had VNOs. Three-dimensional computer reconstructions were made of the VNO in each specimen where this was possible. This in part depended on the plane of section. The total volume and lumen volume were measured from these reconstructions and the volume of the vomeronasal epithelium was calculated by subtraction. A generally consistent increase in total volume and epithelial volume was observed with increasing developmental stage. The lumen contributed rather little to the total volume at these stages. (+info)
The vomeronasal organ of the South American armadillo Chaetophractus villosus (Xenarthra, Mammalia): anatomy, histology and ultrastructure.
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The vomeronasal organ (VNO) is a chemoreceptive structure that has not been extensively studied in the Xenarthran order. Tissue samples from the VNO of the armadillo Chaetophractus villosus were prepared for light and electron microscopy. The VNO is located in the anterior part of the base of the nasal septum. It is tubular in shape, approximately 18 mm in length and opens in the rostral region of the nasal cavity and with a blind caudal end. Its lumen is lined by sensory (SE) and nonsensory (NSE) epithelium. The SE shows sensory, supporting and basal cells whereas the NSE contains ciliated and nonciliated secretory cells and basal cells. At the ultrastructural level, the sensory cells appear as bipolar neurons with conspicuous microvilli on their free surface. The supporting cells of the SE contain numerous membrane-bound vesicles in their apical regions. A peculiar feature not found in other mammals, is the presence of concentric whorls of RER cisterns frequently observed in their basal expansions. Infiltrating plasma cells can be detected in the SE basal region close to the dorsal junctional area. This region also exhibits an unusual type of basal cell, probably responsible for the generation of new vomeronasal receptor neurons. The ciliated NSE cells exhibit numerous ovoids or irregularly shaped membranous protrusions projecting from the plasma membrane of the cilia. As far as we know, this is the first study reporting the presence of this feature in ciliated NSE cells. The nonciliated cells are characterised by scarce large secretory granules and apical microvilli. The vomeronasal glands are compound-branched tubuloacinar glands with serous acinar cells. Four types of secretory granules are present. The ducts of these glands reach the lumen in the dorsolateral region between the NSE and SE. Hypolemmal nerve terminals were observed contacting secretory cells. Fenestrated and nonfenestrated capillaries constitute the vascular supply to these glands. Plasma cells, intimately associated with acinar cells, were frequently observed. (+info)
Chemosensitive conductance and inositol 1,4,5-trisphosphate-induced conductance in snake vomeronasal receptor neurons.
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Snake vomeronasal receptor neurons in slice preparations were studied using the patch-clamp technique in the conventional and nystatin-perforated whole-cell configurations. The mean resting potential was approximately -70 mV; the average input resistance was 3 GOmega. Neurons required current injection of only 1-10 pA to display a variety of spiking patterns. Intracellular dialysis of 100 microM inositol 1,4,5-trisphosphate (IP(3)) evoked an inward current in 38% of neurons, with an average peak amplitude of 16.4 +/- 2.8 pA at a holding potential of -70mV. Application of 100 microM 3-deoxy-3-fluoro-D-myo-inositol 1,4,5-trisphosphate (F-IP(3)), a derivative of IP(3), also evoked an inward current in 4/8 (50%) neurons (32.6 +/- 58 pA at -70 mV, n = 4). The reversal potentials of the induced components were estimated to be -14 +/- 5 mV for IP(3) and -17 +/- 3 mV for F-IP(3). Bathing the neurons in 10 microM ruthenium red solution greatly reduced the IP(3)-evoked inward current to 1.6 +/- 1.1 pA at -70 mV (n = 6). With Cs(+)-containing internal solution, neither the Ca(2+)-ATPase inhibitor thapsigargin (1-50 microM) nor the Ca(2+)-ionophore ionomycin (10 microM) evoked a significant current response, suggesting that IP(3) can elicit current response in the neurons without mediation by intracellular Ca(2+) stores. Intracellular application of 1 mM cAMP evoked no detectable current response. Extracellular application of chemoattractant for snakes evoked a very large inward current. The reversal potential of the chemoattractant-induced current was similar to that of the IP(3)-induced current. The present results suggest that IP(3) may act as a second messenger in the transduction of chemoattractants in the garter snake vomeronasal organ. (+info)
A descriptive and comparative lectin histochemical study of the vomeronasal system in pigs and sheep.
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The accessory olfactory bulb (AOB) is the primary target of the sensory epithelium of the vomeronasal organ (VNO), and thus constitutes a fundamental component of the accessory olfactory system, which is involved in responses to behaviour-related olfactory stimuli. In this study we investigated the characteristics of the AOB, VNO, vomeronasal nerves (VNNs) and caudal nasal nerve (CdNN) in pigs and sheep, species in which olfaction plays a key behavioural role both in the neonatal period and in adulthood. The patterns of staining of the AOB by the Bandeiraea simplicifolia and Lycopersicon esculentum lectins were the same in the 2 species, whereas the Ulex europeus and Dolichos biflorus lectins gave different patterns. In both species, lectin staining of the AOB was consistent with that of the VNNs, while the CdNN did not label any of the structures studied. The entire sensory epithelium of the pig was labelled by Ulex europeus and Lycopersicum esculentum lectins, and all 4 lectins used labelled the mucomicrovillar surface of the sensory epithelium in sheep. (+info)
Random expression of main and vomeronasal olfactory receptor genes in immature and mature olfactory epithelia of Fugu rubripes.
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Main olfactory receptor genes were isolated from a seawater fish, Fugu rubripes (pufferfish), and characterized. Two subfamilies of genes encoding seven transmembrane receptors were identified; one consists of five or more members, termed FOR1-1 to 5 of FOR1 subfamily, and the other appears to be a single copy gene, termed the FOR2 subfamily. FOR1 members show extremely high amino acid sequence similarities of about 95% to one another, and are distantly related to catfish-1 with the highest similarity of 37%. FOR2 shows 43% similarity to goldfish-A28. Phylogenically, both FOR members are categorized among pedigrees of the fish main olfactory receptor family outside the mammalian receptor family, although similarities between Fugu receptors and those of fresh-water fishes are lower than those among fresh-water fishes. In situ hybridization shows that both subfamilies of receptor genes are expressed randomly over the olfactory epithelium throughout all developmental stages, and no segregation of the signals was found. On the other hand, when three members of a vomeronasal olfactory receptor gene family, related to the Ca(2+)-sensing receptor, were used as probes, they were also randomly expressed over the same epithelium as the main olfactory receptors. This is in contrast to the expression profiles observed for zebrafish and goldfish, where the main or vomeronasal olfactory receptors are expressed in segregated patterns. It is thus suggested that the expression pattern of fish olfactory receptors varies depending on the species, although fish olfactory receptors are highly related to one another in their primary structures, and are phylogenically distinct from those of mammals. (+info)