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TRPM5-expressing microvillous cells in the main olfactory epithelium
Weihong Lin, Ejiofor AD Ezekwe, Zhen Zhao, Emily R Liman, Diego Restrepo
BMC Neuroscience , 2008, DOI: 10.1186/1471-2202-9-114
Abstract: We show that the GFP-positive microvillous cells were morphologically diversified and scattered throughout the entire MOE. These cells immunoreacted to an antibody against TRPM5, confirming the expression of this ion channel in these cells. In addition, they showed a Ca2+-activated non-selective cation current in electrophysiological recordings. They did not immunoreact to antibodies that label cell markers and elements of the transduction pathways from olfactory sensory neurons and solitary chemosensory cells of the nasal cavity. Further, the TRPM5-expressing cells did not display axon-like processes and were not labeled with a neuronal marker nor did trigeminal peptidergic nerve fibers innervate these cells.We provide morphological and immunocytochemical characterization of the TRPM5-expressing microvillous cells in the main olfactory epithelium. Our data demonstrate that these cells are non-neuronal and in terms of chemosensory transduction do not resemble the TRPM5-expressing olfactory sensory neurons and nasal solitary chemosensory cells.The peripheral olfactory epithelium in mammal is made up of four types of cells, ciliated olfactory sensory neurons (OSNs), basal cells, supporting cells and microvillious cells, which together form a pseudostratified epithelium [1-3]. The olfactory sensory neurons are specialized in detecting diverse odor molecules and transmitting information to the olfactory bulb through their axonal projections [4-6]. Mature OSNs are ciliated bipolar neurons, with cell bodies that are located in the middle layers of the epithelium[1,7-9]. Each of the mature OSNs sends an apical dendrite to the luminal surface where the dendrite terminates in an oval structure, the olfactory knob, bearing approximately 20 cilia where olfactory receptor proteins and the elements of the olfactory transduction cascade are localized [10-12]. A single axon protruding from the basal end of the soma of the OSN penetrates the basal lamina and projects to the olfacto
TRPM5, a taste-signaling transient receptor potential ion-channel, is a ubiquitous signaling component in chemosensory cells
Silke Kaske, Gabriele Krasteva, Peter K?nig, Wolfgang Kummer, Thomas Hofmann, Thomas Gudermann, Vladimir Chubanov
BMC Neuroscience , 2007, DOI: 10.1186/1471-2202-8-49
Abstract: Here, we systematically investigated the expression of TRPM5 in rat and mouse tissues. Apart from taste buds, where we found TRPM5 to be predominantly localized on the basolateral surface of taste receptor cells, TRPM5 immunoreactivity was seen in other chemosensory organs – the main olfactory epithelium and the vomeronasal organ. Most strikingly, we found solitary TRPM5-enriched epithelial cells in all parts of the respiratory and gastrointestinal tract. Based on their tissue distribution, the low cell density, morphological features and co-immunostaining with different epithelial markers, we identified these cells as brush cells (also known as tuft, fibrillovesicular, multivesicular or caveolated cells). In terms of morphological characteristics, brush cells resemble taste receptor cells, while their origin and biological role are still under intensive debate.We consider TRPM5 to be an intrinsic signaling component of mammalian chemosensory organs, and provide evidence for brush cells being an important cellular correlate in the periphery.Transient receptor potential (TRP) proteins form a large gene family of ion channels characterized by distinct activation mechanisms and biophysical properties. By sequence homology, members of the family fall into six subfamilies (TRPC, TRPV, TRPM, TRPML, TRPP, and TRPA). There is mounting evidence that TRP channels are involved in thermosensation, mechanosensation, smell and taste. A subset of TRP channels, called 'thermo-TRPs' (TRPV1-TRPV4, TRPA1 and TRPM8), have been found to be highly temperature dependent and are directly involved in heat and cold sensation in the peripheral nervous system [1]. Several TRP channels are mechanosensitive or activated by hypotonic challenge (TRPV4, TRPA1, TRPM3, PKD1 and TRPP2) [2]. TRPC2 is specifically expressed in the rodent sensory epithelium of the vomeronasal organ (VNO) where it plays a critical role in signaling processes triggered by pheromones [3,4]. More recently, evidence was obtai
Olfactory and solitary chemosensory cells: two different chemosensory systems in the nasal cavity of the American alligator, Alligator mississippiensis
Anne Hansen
BMC Neuroscience , 2007, DOI: 10.1186/1471-2202-8-64
Abstract: Electron microscopy and immunocytochemistry were used to examine the sensory epithelium of the nasal cavity of the American alligator. Almost the entire nasal cavity is lined with olfactory (sensory) epithelium. Two types of olfactory sensory neurons are present. Both types bear cilia as well as microvilli at their apical endings and express the typical markers for olfactory neurons. The density of these olfactory neurons varies along the nasal cavity. In addition, solitary chemosensory cells innervated by trigeminal nerve fibres, are intermingled with olfactory sensory neurons. Solitary chemosensory cells express components of the PLC-transduction cascade found in solitary chemosensory cells in rodents.The nasal cavity of the American alligator contains two different chemosensory systems incorporated in the same sensory epithelium: the olfactory system proper and solitary chemosensory cells. The olfactory system contains two morphological distinct types of ciliated olfactory receptor neurons.The nasal cavity of all vertebrates houses multiple chemosensors. The olfactory and the vomeronasal receptors detect a variety of odours including food-related and social signals. In addition, chemically-sensitive free nerve endings of the trigeminal nerve and trigeminally innervated chemosensors that respond to irritants have been reported for some vertebrate species. The chemosensors are expressed in various cell types. In mammals, the olfactory system contains ciliated and microvillous olfactory receptor neurons (OSNs). In many mammals these neurons are segregated in two compartments: ciliated OSNs are housed in the main olfactory epithelium detecting chemicals related mostly to food and microvillous OSNs in the so-called vomeronasal organ (VNO) detecting mostly (but not limited to) social cues [1]. Fish olfactory epithelium also contains ciliated and microvillous OSNs [2], but here both cell types are intermingled in one olfactory epithelium since fish do not have a VNO. In
An IP3R3- and NPY-Expressing Microvillous Cell Mediates Tissue Homeostasis and Regeneration in the Mouse Olfactory Epithelium  [PDF]
Cuihong Jia, Sebastien Hayoz, Chelsea R. Hutch, Tania R. Iqbal, Apryl E. Pooley, Colleen C. Hegg
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0058668
Abstract: Calcium-dependent release of neurotrophic factors plays an important role in the maintenance of neurons, yet the release mechanisms are understudied. The inositol triphosphate (IP3) receptor is a calcium release channel that has a physiological role in cell growth, development, sensory perception, neuronal signaling and secretion. In the olfactory system, the IP3 receptor subtype 3 (IP3R3) is expressed exclusively in a microvillous cell subtype that is the predominant cell expressing neurotrophic factor neuropeptide Y (NPY). We hypothesized that IP3R3-expressing microvillous cells secrete sufficient NPY needed for both the continual maintenance of the neuronal population and for neuroregeneration following injury. We addressed this question by assessing the release of NPY and the regenerative capabilities of wild type, IP3R3+/?, and IP3R3?/? mice. Injury, simulated using extracellular ATP, induced IP3 receptor-mediated NPY release in wild-type mice. ATP-evoked NPY release was impaired in IP3R3?/? mice, suggesting that IP3R3 contributes to NPY release following injury. Under normal physiological conditions, both IP3R3?/? mice and explants from these mice had fewer progenitor cells that proliferate and differentiate into immature neurons. Although the number of mature neurons and the in vivo rate of proliferation were not altered, the proliferative response to the olfactotoxicant satratoxin G and olfactory bulb ablation injury was compromised in the olfactory epithelium of IP3R3?/? mice. The reductions in both NPY release and number of progenitor cells in IP3R3?/? mice point to a role of the IP3R3 in tissue homeostasis and neuroregeneration. Collectively, these data suggest that IP3R3 expressing microvillous cells are actively responsive to injury and promote recovery.
Expression of taste receptors in Solitary Chemosensory Cells of rodent airways
Marco Tizzano, Mirko Cristofoletti, Andrea Sbarbati, Thomas E Finger
BMC Pulmonary Medicine , 2011, DOI: 10.1186/1471-2466-11-3
Abstract: We utilized a combination of immunohistochemistry and molecular techniques (rtPCR and in situ hybridization) on rats and transgenic mice where the Tas1R3 or TRPM5 promoter drives expression of green fluorescent protein (GFP).Epithelial SCCs specialized for chemoreception are distributed throughout much of the respiratory tree of rodents. These cells express elements of the taste transduction cascade, including Tas1R and Tas2R receptor molecules, α-gustducin, PLCβ2 and TrpM5. The Tas2R bitter taste receptors are present throughout the entire respiratory tract. In contrast, the Tas1R sweet/umami taste receptors are expressed by numerous SCCs in the nasal cavity, but decrease in prevalence in the trachea, and are absent in the lower airways.Elements of the taste transduction cascade including taste receptors are expressed by SCCs distributed throughout the airways. In the nasal cavity, SCCs, expressing Tas1R and Tas2R taste receptors, mediate detection of irritants and foreign substances which trigger trigeminally-mediated protective airway reflexes. Lower in the respiratory tract, similar chemosensory cells are not related to the trigeminal nerve but may still trigger local epithelial responses to irritants. In total, SCCs should be considered chemoreceptor cells that help in preventing damage to the respiratory tract caused by inhaled irritants and pathogens.Chemical irritation of the respiratory and tracheal mucosa causes various reflex responses such as coughing and apnea. Similarly, chemical stimulation of the larynx results in a number of protective reflexes involved in respiratory regulation, including startle, swallowing, apnea, laryngeal constriction, hypertension, and bradycardia [1-7]. Such disturbance of respiration, if prolonged, may cause profound hypoxemia and even death [8,9]. Despite obvious physiological and clinical importance, not enough information is available regarding the means by which chemical irritants are detected.Until recently, the presump
Distribution and Organization of Different Cells Lining the Olfactory Epithelium of the Indian Minor Carp, Labeo bata (Hamilton 1822): A Light and Scanning Electron Microscopic Analysis  [PDF]
Saroj Kumar Ghosh,Padmanabha Chakrabarti
Pakistan Journal of Biological Sciences , 2011,
Abstract: The olfactory epithelium of adult Labeo bata (Hamilton) has been studied by light and scanning electron microscopy. The oval shaped olfactory rosette consists of 26 to 28 primary lamellae arranged on both side of the median leaf like raphe. The middle dorsal portion of the lamellae is provided with linguiform processes. This linguiform process is occupied by sensory epithelium and characterized by the presence of two types of receptor cells, ciliated and with microvillous cells. The apical and basal part of the olfactory lamellae are covered with non-sensory epithelium. The non-sensory epithelium is made up of stratified epithelial cells and mucous cells. The surface of the non-sensory epithelium is represented by stratified epithelial cells which are provided with unbranched microridges arranged in a concentric whorl. Variations in the cellular organization in the sensory and non-sensory olfactory epithelium have been highlighted in reference to the olfactory sense of the fish concerned.
Chemoreception Regulates Chemical Access to Mouse Vomeronasal Organ: Role of Solitary Chemosensory Cells  [PDF]
Tatsuya Ogura,Kurt Krosnowski,Lana Zhang,Mikhael Bekkerman,Weihong Lin
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0011924
Abstract: Controlling stimulus access to sensory organs allows animals to optimize sensory reception and prevent damage. The vomeronasal organ (VNO) detects pheromones and other semiochemicals to regulate innate social and sexual behaviors. This semiochemical detection generally requires the VNO to draw in chemical fluids, such as bodily secretions, which are complex in composition and can be contaminated. Little is known about whether and how chemical constituents are monitored to regulate the fluid access to the VNO. Using transgenic mice and immunolabeling, we found that solitary chemosensory cells (SCCs) reside densely at the entrance duct of the VNO. In this region, most of the intraepithelial trigeminal fibers innervate the SCCs, indicating that SCCs relay sensory information onto the trigeminal fibers. These SCCs express transient receptor potential channel M5 (TRPM5) and the phospholipase C (PLC) β2 signaling pathway. Additionally, the SCCs express choline acetyltransferase (ChAT) and vesicular acetylcholine transporter (VAChT) for synthesizing and packaging acetylcholine, a potential transmitter. In intracellular Ca2+ imaging, the SCCs responded to various chemical stimuli including high concentrations of odorants and bitter compounds. The responses were suppressed significantly by a PLC inhibitor, suggesting involvement of the PLC pathway. Further, we developed a quantitative dye assay to show that the amount of stimulus fluid that entered the VNOs of behaving mice is inversely correlated to the concentration of odorous and bitter substances in the fluid. Genetic knockout and pharmacological inhibition of TRPM5 resulted in larger amounts of bitter compounds entering the VNOs. Our data uncovered that chemoreception of fluid constituents regulates chemical access to the VNO and plays an important role in limiting the access of non-specific irritating and harmful substances. Our results also provide new insight into the emerging role of SCCs in chemoreception and regulation of physiological actions.
Microvillous inclusion disease (microvillous atrophy)
Frank M Ruemmele, Jacques Schmitz, Olivier Goulet
Orphanet Journal of Rare Diseases , 2006, DOI: 10.1186/1750-1172-1-22
Abstract: Microvillous inclusion diseaseMicrovillous atrophyCongenital enteropathyCongenital familial protracted diarrhea with enterocyte brush-border abnormalitiesMicrovillous inclusion disease (MVID) or microvillous atrophy (MVA) is a congenital and constitutive disorder of intestinal epithelial cells [1-6]. It is characterized by the neonatal onset of abundant watery diarrhea persisting despite total bowel rest. Onset most often occurs within the first days of life. Microvillous atrophy, first described in 1978 [7], was the first clinical entity identified on a morphological basis as being responsible for the so-called protracted or intractable diarrhea syndrome. The diagnosis is based on typical morphological abnormalities detected through a combination of light and electron microscopic (EM) analyses of small bowel biopsies [8-14]. Standard histology reveals a variable degree of villous atrophy without marked crypt hyperplasia, in addition to abnormal periodic-acid schiff (PAS) positive secretory granules accumulating in the apical cytoplasm of mature enterocytes and an altered (atrophic after PAS staining) enterocyte brush border membrane. These findings are completed by EM with the detection of atrophic or completely absent microvilli on mature enterocytes (see below) along with so-called microvillous inclusions (vacuoles lined by microvilli) and the finding of large PAS positive granules in immature enterocytes.Pregnancy and delivery are uneventful; in general, there is no notion of polyhydramnios except in rare isolated cases. Severe watery diarrhea starts within the first days of life [1-4,6,7]. This diarrhea becomes so abundant, that within 24 h the children can loose up to 30% of their body weight, resulting in profound metabolic acidosis and severe dehydration. MVID is most often severe and life-threatening. Accurate quantification of the stool volumes reveals 150 to over 300 ml/kg/d, with a high sodium content (approximately 100 mmol/L). Complete and prolonged bo
Identification of new binding partners of the chemosensory signaling protein Gγ13 expressed in taste and olfactory sensory cells  [PDF]
Zhenhui Liu,Claire Fenech,Sylvie Grall,Fabienne Laugerette,Jean-Pierre Montmayeur
Frontiers in Cellular Neuroscience , 2012, DOI: 10.3389/fncel.2012.00026
Abstract: Tastant detection in the oral cavity involves selective receptors localized at the apical extremity of a subset of specialized taste bud cells called taste receptor cells (TRCs). The identification of the genes coding for the taste receptors involved in this process have greatly improved our understanding of the molecular mechanisms underlying detection. However, how these receptors signal in TRCs, and whether the components of the signaling cascades interact with each other or are organized in complexes is mostly unexplored. Here we report on the identification of three new binding partners for the mouse G protein gamma 13 subunit (Gγ13), a component of the bitter taste receptors signaling cascade. For two of these Gγ13 associated proteins, namely GOPC and MPDZ, we describe the expression in taste bud cells for the first time. Furthermore, we demonstrate by means of a yeast two-hybrid interaction assay that the C terminal PDZ binding motif of Gγ13 interacts with selected PDZ domains in these proteins. In the case of the PDZ domain-containing protein zona occludens-1 (ZO-1), a major component of the tight junction defining the boundary between the apical and baso-lateral region of TRCs, we identified the first PDZ domain as the site of strong interaction with Gγ13. This association was further confirmed by co-immunoprecipitation experiments in HEK 293 cells. In addition, we present immunohistological data supporting partial co-localization of GOPC, MPDZ, or ZO-1, and Gγ13 in taste buds cells. Finally, we extend this observation to olfactory sensory neurons (OSNs), another type of chemosensory cells known to express both ZO-1 and Gγ13. Taken together our results implicate these new interaction partners in the sub-cellular distribution of Gγ13 in olfactory and gustatory primary sensory cells.
Functional promiscuity in a mammalian chemosensory system: extensive expression of vomeronasal receptors in the main olfactory epithelium of mouse lemurs  [PDF]
Philipp Hohenbrink,Silke Dempewolf,Nicholas I. Mundy,Ute Radespiel
Frontiers in Neuroanatomy , 2014, DOI: 10.3389/fnana.2014.00102
Abstract: The vomeronasal organ (VNO) is functional in most terrestrial mammals, though progressively reduced in the primate lineage, and is used for intraspecific communication and predator recognition. Vomeronasal receptor (VR) genes comprise two families of chemosensory genes (V1R and V2R) that have been considered to be specific for the VNO. However, recently a large number of VRs were reported to be expressed in the main olfactory epithelium (MOE) of mice, but there is little knowledge of the expression of these genes outside of rodents. To explore the function of VR genes in mammalian evolution, we analyzed and compared the expression of 64 V1R and 2 V2R genes in the VNO and the MOE of the grey mouse lemur (Microcebus murinus), the primate with the largest known VR repertoire. We furthermore compared expression patterns in adults of both sexes and seasons, and in an infant. A large proportion (83% – 97%) of the VR loci was expressed in the VNO of all individuals. The repertoire in the infant was as rich as in adults, indicating reliance on olfactory communication from early postnatal development onwards. In concordance with mice, we also detected extensive expression of VRs in the MOE, with proportions of expressed loci in individuals ranging from 29% to 45%. TRPC2, which encodes a channel protein crucial for signal transduction via VRs, was co-expressed in the MOE in all individuals indicating likely functionality of expressed VR genes in the MOE. In summary, the large VR repertoire in mouse lemurs seems to be highly functional. Given the differences in the neural pathways of MOE and VNO signals, which project to higher cortical brain centers or the limbic system, respectively, this raises the intriguing possibility that the evolution of MOE-expression of VRs enabled mouse lemurs to adaptively diversify the processing of VR-encoded olfactory information.
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