Vomeronasal Glands Research Articles

The vomeronasal organ of the South American armadillo Chaetophractus villosus (Xenarthra, Mammalia): anatomy, histology and ultrastructure.

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.

A developmental study using three antibodies (VOBM1, VOBM2, and VOM2): immunocytochemical and electron microscopical analysis of the luminal surface of the rat vomeronasal sensory epithelium.

The development of the rat vomeronasal organ was studied morphologically and immunocytochemically, using the monoclonal antibodies (MAbs) VOBM1, VOBM2 and VOM2 that react with the luminal surface of the vomeronasal sensory epithelium. Postnatal day (P) 7, 14, 21, 28, 35 and adult animals were examined. The vomeronasal organ and the blood vessel of the organ markedly increased in size and the vomeronasal glands increased in number between P7 and P14. At P35, the shape of the vomeronasal organ was similar to that of the adult but its size was slightly smaller. Electron microscopy showed that only a few scattered microvilli were present on supporting cells, and receptor cells were immature at P7. At P21, well-branched microvilli of the receptor cells and many microvilli of the supporting cells were observed on the luminal surface of the sensory epithelium. At P35, most apical endings of supporting cells and receptor cells were covered with numerous microvilli. Less developed areas were also present at the luminal surface of the epithelium at P35. At P7, immunoreactivities of the three antibodies were observed as discontinuous thin-layered bands only on the luminal surface of the sensory epithelium and no immunoreactivity was observed in other regions of the vomeronasal organ. Immunoreactivities of the VOBM1, VOBM2 and VOM2 increased with age and were observed as continuous thin-layered bands on the luminal surface of the epithelium by P35. These finding suggest that the development of the vomeronasal organ continues after birth and that the organ may reach maturity just before puberty (P42-49).

Vomeronasal organ and its associated structures in the opossum Monodelphis domestica.

The opossum Monodelphis domestica possesses a well-developed vomeronasal system. Uptake of chemical stimuli into the vomeronasal organ (VNO) involves a stereotypical "nuzzling" behavior. In the present study, ten animals were examined by light and electron microscopy. The peripheral oro-nasal structures that apparently enhance access of solutes into the VNO include: (1) two lateral grooves of the ventral rhinarium and a network of channels leading into them, (2) dental gap adjacent to the grooves, (3) butterfly-shaped incisive papilla, and (4) unique bristle/cup-shaped filiform papillae on the tongue. The longitudinal axis of the vomeronasal complex is composed of the VNO proper at its rostral end, and an extensive compound serous gland at its caudal end with a distinct transition zone in between. The transition zone is characterized by the following features: merging of the main excretory duct of the large vomeronasal gland with the VNO lumen and drainage of auxiliary glandular clusters into the lumen, irregularities in the sensory epithelium ("rosette" appearance), and the ending of the cartilaginous support surrounding the VNO. Multiple elongated bundles of smooth muscle are positioned between the sensory epithelium and the cartilaginous capsule and more caudally are intertwined with the glandular parenchyma. These bundles become more numerous at the transition zone. Contraction and extension of these muscles may function to enhance the flow of solutes and glandular secretion within the lumen. Two extensive venous sinuses are associated with the opossum VNO complex: the internal vein bordering the sensory epithelium at its rostral end, and the external vein alongside the nonsensory epithelium. This arrangement suggests a unique dual pumping mechanism.

Prenatal development of the mammalian vomeronasal organ.

The vomeronasal organ (VNO) originates from the medial wall of the olfactory pit shortly after the middle of the embryonic period in mammals. The Anlage stage consists of a cellular bud that grows dorsally, caudally, and towards the midline leaving a groove. The following stage, Early Morphogenesis, includes the closure of the vomeronasal groove to form a parasagittal blind-ended tube in the nasal septum, which opens into the nasal and/or oral cavities. The lumen adopts a crescent shape while the epithelial lining differentiates into an increasingly wider epithelium on the concave side and a gradually thinner epithelium on the convex side. The former goes on to occupy a medial position and develops neuroblasts among supporting and undifferentiated cells, with supporting cell nuclei tending to align in the upper rows. The lateral "non-sensory" epithelium furrows, giving a kidney-shaped appearance to the VNO cross section. The next stage, Late Morphogenesis is extended up to a difference in thickness between both epithelia becomes similar to the adult, generally by birth. An increasing number of ciliary generation complexes, larger and more abundant microvilli, and an evident glycocalyx are observed in the neuroepithelium at the luminal surface, while enzymatic activities become more intense. The non-sensory epithelium appears quite mature save for its luminal surface, which is still devoid of cilia. Blood capillaries penetrate the most basal region of the neuroepithelium and vomeronasal glands are very few and immature. At birth, some neurons appear well developed to support certain functionality; however, persistence of architectural, histochemical, and ultrastructural signs of immaturity, suggests that full performance of the VNO does not occur in newborn mammals, but in prepubertal ages.

Differential expression of odorant-binding protein genes in rat nasal glands: implications for odorant-binding proteinII as a possible pheromone transporter.

We examined the distribution and ontogeny of two odorant-binding proteins in the rat at various stages of development from newborn to adult using northern blot and in situ hybridization methods. Our results demonstrated spatial segregation between odorant-binding protein and odorant-binding proteinII in nasal glandular tissues. Odorant-binding protein messenger RNA was expressed in the glandular system opening into the nasal vestibule, whereas odorant-binding proteinII messenger RNA was seen in the posterior glands of the nasal septum and in the vomeronasal glands. In addition, odorant-binding protein and odorant-binding proteinII messenger RNA levels increased during early postnatal stages with time courses that paralleled the anatomical development of the main olfactory system and the vomeronasal system, respectively. Our results suggest that odorant-binding proteinII functions as a pheromone transporter in the vomeronasal system.

Differential expression of vomeromodulin and odorant-binding protein, putative pheromone and odorant transporters, in the developing rat nasal chemosensory mucosae.

Expression of the putative pheromone and odorant transporter, vomeromodulin, was characterized in developing rat nasal mucosae using in situ hybridization and immunocytochemistry. Initial expression of vomeromodulin mRNA and protein was detected at embryonic day (E)16 in the maxillary sinus component of the lateral nasal glands. The abundance of mRNA and protein in the lateral nasal glands increased with age and reached a peak at postnatal day (P)27. Also at P27, vomeromodulin mRNA and protein expression was initiated in vomeronasal glands and posterior glands of the nasal septum. Comparison of the developmental expression of odorant-binding protein, another carrier protein synthesized in the lateral nasal glands, with that of vomeromodulin demonstrated major differences. In contrast to vomeromodulin, odorant-binding protein was not detected until postnatal day 2 in the ventral component of the lateral nasal glands and anterior glands of the nasal septum. These results suggest that the expression of vomeromodulin and odorant-binding protein is developmentally and differentially regulated and confirms the suggestion that vomeromodulin may function in olfactory and vomeronasal perireceptor processes as a transporter for pheromones and odorants. In addition, the embryonic expression of vomeromodulin suggests its involvement in olfactory perireceptor processes in utero.

Expression of the putative pheromone and odorant transporter vomeromodulin mRNA and protein in nasal chemosensory mucosae

In nasal chemosensory systems, glandular proteins associated with the vomeronasal and olfactory epithelia perform specific perireceptor functions associated with sensory transduction. Vomeromodulin, a recently identified glycoprotein synthesized by the lateral nasal glands, is proposed to be a pheromone transporter (Khew-Goodall et al., FASEB J 5:2976-2982, 1991). In our study, we have investigated its expression in vomeronasal, olfactory, and respiratory nasal mucosae of rats and humans using in situ hybridization and immunocytochemical techniques. In the rat, vomeromodulin mRNA and protein were localized abundantly in the glandular acini of the maxillary sinus component of the lateral nasal glands. In addition, the vomeronasal and posterior glands of the nasal septum also expressed vomeromodulin mRNA and protein. Vomeromodulin immunoreactivity was localized extracellularly in the mucus of the sensory and non-sensory epithelia of the vomeronasal organ, and in the mucociliary complex of the olfactory, respiratory, and associated nasal epithelia. In human nasal mucosae, vomeromodulin immunoreactivity was localized in the mucociliary complex of the vomeronasal and respiratory epithelia. Comparison of the localization of vomeromodulin with that of odorant-binding protein, which is also synthesized in the lateral nasal glands of rats, revealed that odorant-binding protein was expressed in a completely separate glandular region, namely the ventral component. In the septal glands, vomeromodulin was expressed in the posterior glands whereas odorant-binding protein was localized in the anterior glands. Odorant-binding protein immunoreactivity was not observed in the vomeronasal glands. In contrast, both proteins were localized in the mucus of vomeronasal, olfactory, and respiratory epithelia. Our results suggest that vomeromodulin, like odorant-binding protein, functions as a chemosensory stimulus transporter associated with perireceptor processes in vomeronasal and olfactory transduction.

Differential expression of alpha, mu, and pi classes of glutathione S-transferases in chemosensory mucosae of rats during development.

The expression of three classes of glutathione S-transferases (GSTs), Alpha, Mu, and Pi was investigated in the nasal mucosae of rats during development using immunohistochemical methods. GST Alpha and Mu were first detected in the supranuclear region of sustentacular cells on embryonic days 16. The Bowman's glands expressed differential patterns of immunoreactivity during development, beginning at postnatal day (P) 2 and P6 for Alpha and Mu classes, respectively and being greatest at P11 for both. The acinar cells of vomeronasal glands in the vomeronasal organ expressed Alpha and Mu classes of GSTs from P11 onwards. In the septal organ of Masera, the supranuclear region of sustentacular cells expressed GSTs from P11 with little or no variation during development. In the respiratory mucosa, Alpha and Mu classes of GSTs were detected at the brush borders of ciliated cells and in the acinar cells of posterior septal glands, but not in anterior septal or respiratory glands located on the turbinates. Compared to olfactory mucosa, the changes in immunoreactivity for GSTs were less pronounced in the respiratory mucosa during development. Specific GST Pi immunoreactivity was not detected in the nasal mucosae at any stage of development studied. The occurrence of GSTs in the nasal mucosa, including olfactory, vomeronasal, septal, and respiratory epithelia, suggests that the GSTs are actively involved in the biotransformation of xenobiotics including odorants and pheromones, and may also participate in perireceptor processes such as odorant clearance. In addition, we have developed a working model describing the cellular localization of certain phase I (e.g., cytochrome P-450s) and phase II (e.g., GSTs, gamma-glutamyl transpeptidase) biotransformation enzymes in the olfactory mucosa and their proposed roles in xenobiotic metabolism.

Observations on the Vomeronasal Organ of the Colugo <i>Cynocephalus</i> (Mammalia, Dermoptera)

This paper presents the first description of a functional vomeronasal organ in the colugo or 'flying lemur' Cynocephalus, the sole living representative of the order Dermoptera (Mammalia). The vomeronasal organ complex comprises patent nasopalatine and vomeronasal ducts, a 10-mm-long epithelial tube consisting of an 8- to 10-cell thick, 65-microns-tall neurosensory epithelium, the vomeronasal nerve, and the accessory olfactory bulb. The vomeronasal glands are sparse. Among mammals, the vomeronasal organ of the colugo is one of the relatively longest, at nearly 48% of nasal cavity length. It is exceeded among archontans (colugos, bats, primates, and tree shrews) only by that of the strepsirhine primate Microcebus murinus.

<b>DISTRIBUTION OF GALANIN IMMUNOREACTIVE FIBERS IN THE MOUSE VOMERONASAL </b><b>ORGAN </b>

Galanin (GAL)-immunohistochemical techniques were applied to the mouse vomeronasal organ. GAL-immunoreactive fibers were seen in the receptor-free epithelial region, but no fibers were found in the neuroepithelial region. Many GAL-immunoreactive fibers were distributed around the cavernous blood vessels and the vomeronasal glands, and these fibers had a large number of varicosities and branches. GAL-immunoreactive fibers were also distributed in both the olfactory epithelial area and the respiratory epithelial area. GALimmunoreactive cell bodies were seen in the trigeminal ganglion, in the sphenopalatine ganglion, and in the superior cervical ganglion

Fine structure of the vomeronasal and septal olfactory epithelia and of glandular structures.

The vomeronasal and septal olfactory organs are two neurosensory structures in the mammalian nasal septum which are poorly understood relative to the main olfactory system. The vomeronasal organ is a paired, blind-ending tubular structure that opens rostrally into the nasal cavity in some species and into the incisive ducts in others. When present in mammals, the septal olfactory organ is an island of olfactory mucosa positioned such that it is in the primary air pathway in the caudal portion of the nasal cavity. Mammalian nasal glands, with a diverse histochemical and ultrastructural morphology, secrete a variety of substances onto the mucosal surface. One of these substances, odorant binding protein, localized in bovine nasal glands and lateral nasal glands of rodents, may be important in the capture and conveyance of odorant molecules to olfactory receptors. The objectives of this paper are to present original data while reviewing the literature on the ultrastructure of vomeronasal and septal olfactory neuroepithelia, and of vomeronasal, bovine nasal, and lateral nasal glands. Nasal tissues from pigs, calves, and hamsters were prepared for electron microscopy. Neurosensory epithelia of the porcine vomeronasal organ and the hamster septal olfactory organ are similar to that described for the vomeronasal and septal olfactory organs of other mammals. Bovine nasal and rodent lateral nasal glands consist of subregions which differ morphologically; the most abundant acinar cell type in the bovine nasal gland contains lightly electron dense secretory granules while that of the rodent lateral nasal gland contains both small electron dense and large, electron lucent granules. The porcine vomeronasal gland contains numerous small, dense granules of a diverse morphology.

Differential distribution of gamma-glutamyl cycle molecules in the vomeronasal organ of rats.

Molecules related to the gamma-glutamyl cycle, including thiols, glutathione (GSH) and gamma-glutamyl transpeptidase (gamma-GT) were identified histochemically and immunohistochemically in the vomeronasal organ of neonatal and adult rats. Thiols and GSH were distributed in the mucomicrovillar complex (MMC), vomeronasal receptor neurons and acinar cells of vomeronasal glands (VNG). gamma-GT was localized in the MMC and in the VNG, where it was associated mainly with the luminal surface of the acinar cells and ducts. The VNO of the neonates exhibited higher staining intensities for all compounds than that of the adults. The data indicate that components of the gamma-glutamyl cycle are present in the VNO and that they are secreted into mucus, where they may be associated with perireceptor events including clearance of pheromones and detoxification of xenobiotics.

Vomeromodulin, a putative pheromone transporter: cloning, characterization, and cellular localization of a novel glycoprotein of lateral nasal gland

Vomeromodulin, a novel glycoprotein of lateral nasal gland, has been cloned by differential hybridization from nasal/olfactory tissue. The 2.2-kb mRNA directs the in vitro synthesis of a 60-kDa primary translation product in reticulocyte lysates. Differential sensitivity to endoglycosidases indicates that vomeromodulin is posttranslationally modified in vivo by N-glycosylation to form a 70-kDa glycoprotein of the complex type. Immunocytochemical localization with two different antipeptide antisera demonstrates that vomeromodulin is abundant in the lateral nasal glands and is also present in the posterior septal and vomeronasal glands. Most striking is the observation that it is highly concentrated in the mucus of the vomeronasal organ of Jacobson but is not detectable in the mucus of the main olfactory neuroepithelium. Evaluation of mRNA and protein distribution by Northern and Western analyses, respectively, indicates that vomeromodulin is absent from 15 other tissues. The glandular and mucosal distribution of this glycoprotein implies a transport function that may be related to the mechanisms by which pheromones of low volatility gain access to their receptors in the vomeronasal organ. These observations support our hypothesis that vomeromodulin participates in perireceptor events that facilitate the process of pheromone access and detection.

Morphological evidence for a direct innervation of the mouse vomeronasal glands.

The morphological evidence for a direct autonomic innervation of the mouse vomeronasal glands is presented. Axonal varicosities containing a few dense-core vesicles and numerous clear vesicles (36-60 nm in diameter) make synaptic contacts with the secretory cells at the base of the glandular acini. The axonal presynaptic membrane is associated with a distinct dense material and it is separated from the secretory cell by a synaptic cleft of about 12-14 nm. At the postsynaptical level, coated vesicles can be found. Additional postsynaptical specializations have not been observed.

Histological development of the vomeronasal complex in the pre- and postnatal rat.

The vomeronasal complex of the rat was studied by means of different staining techniques and light microscopy between the 13th day of gestation and 42 days of postnatal life. The anlage of the vomeronasal organ in the 13-day-old embryo consisted of a cluster of cells proliferating from the olfactory placode towards the medial line. The vomeronasal organ was well developed by the end of gestation, showing the same ratio between receptor and receptor-free epithelium as in the adult animal. However, full development of the epithelia did not occur until the end of the second postnatal week. Glandular rudiments were observed within the vomeronasal area in 17-day-old fetuses, but the gland showed no sign of activity until the 7th day of postnatal life, when a slight PAS-positive reaction was observed in their cells' cytoplasm. This PAS-positive reaction intensified considerably during the second week and corresponded to the adult picture by the end of this time. The content of the vomeronasal glands contrasted with that of the glands flowing into the nasal fossa, which did not show any PAS-positive reaction but which stained positive for alcian blue. We also studied the evolution of the blood vessels such as the capsule of the complex. This capsule showed complete ossification by the beginning of the 3rd postnatal week, with the exception of certain regions which remained cartilaginous in the adult. Some capillaries were observed in the complex in 17-day-old fetuses, and by 20 days of gestation some of them could be observed penetrating the receptor epithelium. Subsequently, the vascularization of the complex became so profuse that one could consider the vomeronasal complex to consist of erectile tissue.

The anatomy of the rostral nasal cavity and vomeronasal organ in Tarsipes rostratus (Marsupialia: Tarsipedidae).

The rostral nasal structure of Tarsipes is described from diagrams drawn from transverse serial sections. Left and right nasal cavities are separate but nasal and oral cavities communicate freely via the nasopalatine ducts, whose oral openings lie lateral to the incisive papilla. The papilla is grooved ventrally with taste buds on the sides of the groove. The nasopalatine ducts open to the nasal cavity below a glandular swell body over the tip of the vomeronasal cartilage. The ducts of the vomeronasal organ open into the oral end of the nasopalatine ducts. The organ extends about one third of the way along the base of the septum, with sensory epithelium medially and ciliated epithelium laterally. Vomeronasal glands occupy the ventral half of the septum caudal to the sensory epithelium. It is suggested that their secretion reaches the spiny dorsal surface of the tongue, and that tongue movements may assist the presentation of odours to the vomeronasal organ. Olfactory epithelium reaches as far rostrally as the bony nasal septum in the dorsal nasal cavity. The ventral cavity is lined by ciliated epithelium with few goblet cells. The nasal vestibule receives secretion from septal glands of the dorsal swell body, from the lateral nasal gland, and from the lacrimal gland via the nasolacrimal duct.

Morphology of the nasal fossae and associated structures of the hamster (Mesocricetus auratus).

AbstractThe hamster nasal cavity consists of vestibular, non‐olfactory and olfactory portions. Much of the non‐olfactory nasal cavity surface is lined by cuboidal, stratified cuboidal, and low columnar epithelia, devoid of cilia. Goblet cells and ciliated respiratory epithelium are present over only a small portion of the nasal cavity surface.The largest glandular masses in the hamster nose are the maxillary recess glands, the vomeronasal glands and the lateral nasal gland 1; these three glands contain neutral mucopolysaccharides (PAS‐positive). Other nasal glands contain both acidic and neutral mucopolysaccharides; the staining reaction for acidic mucopolysaccharide is stronger in goblet cells and olfactory glands than in the other nasal glands.The ducts which open into the nasal vestibule are the excretory ducts of compound tubuloacinar serous glands. The one major PAS‐positive gland whose duct opens into the nasal vestibule is the lateral nasal gland 1. The ducts of the compound tubuloacinar vomeronasal glands open into the lumen of the vomeronasal organ, which is connected to the ventral nasal meatus by means of the vomeronasal duct. The ducts of the branched tubuloacinar maxillary recess glands open into the maxillary recess. Few ducts open into the caudal half of the nasal cavity.