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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
Taste and pheromone perception in mammals and flies
Hiroaki Matsunami, Hubert Amrein
Genome Biology , 2003, DOI: 10.1186/gb-2003-4-7-220
Abstract: Feeding is initiated in terrestrial animals with the detection of volatile (airborne) chemicals. Generally referred to as odorants, these chemicals are released from food sources towards which animals move by monitoring the concentration gradient of a particular odor. Naturally, noxious volatile substances are also detected by the same sensory epithelia, in this case leading to avoidance of the odor source. In both mammals and insects, volatile cues are detected by odorant receptor proteins, which are G-protein-coupled receptors (GPCRs) encoded by a single large gene family expressed in the cognate olfactory epithelia in the nose and antenna of mammals and insects, respectively. The odorant receptor gene family consists of about 1,000 genes in mice and 60 in Drosophila. Surprisingly, the odorant receptor genes in mammals and insects are not related to each other at the sequence level (beyond encoding GPCRs), even though they recognize a largely overlapping array of chemical compounds. The olfactory systems of insects and mammals have analogous anatomical features and use similar molecular logic for olfactory coding, however [1].Once a potential food source is identified, animals taste it by means of contact between chemicals from the source and chemosensory receptors located in the gustatory (taste) organs, predominantly the tongue in mice and the labellum (proboscis) in Drosophila (both species also have secondary taste organs). Distinct sets of taste-receptor proteins in specific taste cells allow the organism to discriminate between 'delicious' food, generally associated with rich nutrition, and bitter-tasting substrates, typically present in contaminated, non-edible food sources.Courtship and mating are also initiated by chemosensory signals, better known as pheromones, although other sensory systems are also important for these behaviors. Pheromones are sometimes sex-specific and are secreted by specialized glands or cells to trigger distinct behavioral and end
Sensing the Underground – Ultrastructure and Function of Sensory Organs in Root-Feeding Melolontha melolontha (Coleoptera: Scarabaeinae) Larvae  [PDF]
Elisabeth J. Eilers, Giovanni Talarico, Bill S. Hansson, Monika Hilker, Andreas Reinecke
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0041357
Abstract: Introduction Below ground orientation in insects relies mainly on olfaction and taste. The economic impact of plant root feeding scarab beetle larvae gave rise to numerous phylogenetic and ecological studies. Detailed knowledge of the sensory capacities of these larvae is nevertheless lacking. Here, we present an atlas of the sensory organs on larval head appendages of Melolontha melolontha. Our ultrastructural and electrophysiological investigations allow annotation of functions to various sensory structures. Results Three out of 17 ascertained sensillum types have olfactory, and 7 gustatory function. These sensillum types are unevenly distributed between antennae and palps. The most prominent chemosensory organs are antennal pore plates that in total are innervated by approximately one thousand olfactory sensory neurons grouped into functional units of three-to-four. In contrast, only two olfactory sensory neurons innervate one sensillum basiconicum on each of the palps. Gustatory sensilla chaetica dominate the apices of all head appendages, while only the palps bear thermo-/hygroreceptors. Electrophysiological responses to CO2, an attractant for many root feeders, are exclusively observed in the antennae. Out of 54 relevant volatile compounds, various alcohols, acids, amines, esters, aldehydes, ketones and monoterpenes elicit responses in antennae and palps. All head appendages are characterized by distinct olfactory response profiles that are even enantiomer specific for some compounds. Conclusions Chemosensory capacities in M. melolontha larvae are as highly developed as in many adult insects. We interpret the functional sensory units underneath the antennal pore plates as cryptic sensilla placodea and suggest that these perceive a broad range of secondary plant metabolites together with CO2. Responses to olfactory stimulation of the labial and maxillary palps indicate that typical contact chemo-sensilla have a dual gustatory and olfactory function.
Hedonic Taste in Drosophila Revealed by Olfactory Receptors Expressed in Taste Neurons  [PDF]
Makoto Hiroi, Teiichi Tanimura, Frédéric Marion-Poll
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0002610
Abstract: Taste and olfaction are each tuned to a unique set of chemicals in the outside world, and their corresponding sensory spaces are mapped in different areas in the brain. This dichotomy matches categories of receptors detecting molecules either in the gaseous or in the liquid phase in terrestrial animals. However, in Drosophila olfactory and gustatory neurons express receptors which belong to the same family of 7-transmembrane domain proteins. Striking overlaps exist in their sequence structure and in their expression pattern, suggesting that there might be some functional commonalities between them. In this work, we tested the assumption that Drosophila olfactory receptor proteins are compatible with taste neurons by ectopically expressing an olfactory receptor (OR22a and OR83b) for which ligands are known. Using electrophysiological recordings, we show that the transformed taste neurons are excited by odor ligands as by their cognate tastants. The wiring of these neurons to the brain seems unchanged and no additional connections to the antennal lobe were detected. The odor ligands detected by the olfactory receptor acquire a new hedonic value, inducing appetitive or aversive behaviors depending on the categories of taste neurons in which they are expressed i.e. sugar- or bitter-sensing cells expressing either Gr5a or Gr66a receptors. Taste neurons expressing ectopic olfactory receptors can sense odors at close range either in the aerial phase or by contact, in a lipophilic phase. The responses of the transformed taste neurons to the odorant are similar to those obtained with tastants. The hedonic value attributed to tastants is directly linked to the taste neurons in which their receptors are expressed.
Ancient Protostome Origin of Chemosensory Ionotropic Glutamate Receptors and the Evolution of Insect Taste and Olfaction  [PDF]
Vincent Croset equal contributor,Raphael Rytz equal contributor,Scott F. Cummins,Aidan Budd,David Brawand,Henrik Kaessmann,Toby J. Gibson,Richard Benton
PLOS Genetics , 2010, DOI: 10.1371/journal.pgen.1001064
Abstract: Ionotropic glutamate receptors (iGluRs) are a highly conserved family of ligand-gated ion channels present in animals, plants, and bacteria, which are best characterized for their roles in synaptic communication in vertebrate nervous systems. A variant subfamily of iGluRs, the Ionotropic Receptors (IRs), was recently identified as a new class of olfactory receptors in the fruit fly, Drosophila melanogaster, hinting at a broader function of this ion channel family in detection of environmental, as well as intercellular, chemical signals. Here, we investigate the origin and evolution of IRs by comprehensive evolutionary genomics and in situ expression analysis. In marked contrast to the insect-specific Odorant Receptor family, we show that IRs are expressed in olfactory organs across Protostomia—a major branch of the animal kingdom that encompasses arthropods, nematodes, and molluscs—indicating that they represent an ancestral protostome chemosensory receptor family. Two subfamilies of IRs are distinguished: conserved “antennal IRs,” which likely define the first olfactory receptor family of insects, and species-specific “divergent IRs,” which are expressed in peripheral and internal gustatory neurons, implicating this family in taste and food assessment. Comparative analysis of drosophilid IRs reveals the selective forces that have shaped the repertoires in flies with distinct chemosensory preferences. Examination of IR gene structure and genomic distribution suggests both non-allelic homologous recombination and retroposition contributed to the expansion of this multigene family. Together, these findings lay a foundation for functional analysis of these receptors in both neurobiological and evolutionary studies. Furthermore, this work identifies novel targets for manipulating chemosensory-driven behaviours of agricultural pests and disease vectors.
Is TrpM5 a reliable marker for chemosensory cells? Multiple types of microvillous cells in the main olfactory epithelium of mice
Anne Hansen, Thomas E Finger
BMC Neuroscience , 2008, DOI: 10.1186/1471-2202-9-115
Abstract: We investigated the main olfactory epithelium of mice at the light and electron microscopic level and describe several subpopulations of microvillous cells. The ultrastructure of the microvillous cells reveals at least three morphologically different types two of which express the TrpM5 channel. None of these cells have an axon that projects to the olfactory bulb. Tests with a large panel of cell markers indicate that the TrpM5-positive cells are not sensory since they express neither neuronal markers nor are contacted by trigeminal nerve fibers.We conclude that TrpM5 is not a reliable marker for chemosensory cells. The TrpM5-positive cells of the olfactory epithelium are microvillous and may be chemoresponsive albeit not part of the sensory apparatus. Activity of these microvillous cells may however influence functionality of local elements of the olfactory system.Traditionally, the main olfactory epithelium (MOE) of mammals was said to contain only basal cells, supporting cells, and ciliated olfactory receptor neurons (ORNs) that utilize OR-type receptor molecules and the canonical G-protein-coupled transduction pathway via Gαolf, adenylyl cyclase III (ACIII), and cAMP [1]. However, a review of the literature suggests that this conventional view is too simplistic, e.g. microvillous ORNs are present in the olfactory epithelium of fishes and in the vomeronasal organ of mammals. Also, microvillous cells have been reported for the MOE of some mammals including humans [2-5]. A study by Rowley et al. utilizing HRP tracing claimed that at least some microvillous cells project directly to the olfactory bulb [6]. Braun and Zimmermann [4], utilizing ecto-5'-nucleotidase as a marker, detected microvillous cells in the MOE and suggested a mechanosensory function for these elements. Carr et al. reported microvillous cells in rats and concluded that these cells were non-sensory cells [7]. Functional studies revealed that mice with a disrupted cAMP pathway of ciliated ORNs are s
Olfactory receptors in non-chemosensory tissues  [cached]
NaNa Kang & JaeHyung Koo*
BMB Reports , 2012,
Abstract: Olfactory receptors (ORs) detect volatile chemicals that lead tothe initial perception of smell in the brain. The olfactory receptor(OR) is the first protein that recognizes odorants in theolfactory signal pathway and it is present in over 1,000 genesin mice. It is also the largest member of the G protein-coupledreceptors (GPCRs). Most ORs are extensively expressed in thenasal olfactory epithelium where they perform the appropriatephysiological functions that fit their location. However, recentwhole-genome sequencing shows that ORs have been foundoutside of the olfactory system, suggesting that ORs may playan important role in the ectopic expression of non-chemosensorytissues. The ectopic expressions of ORs and their physiologicalfunctions have attracted more attention recently sinceMOR23 and testicular hOR17-4 have been found to be involvedin skeletal muscle development, regeneration, and humansperm chemotaxis, respectively. When identifying additionalexpression profiles and functions of ORs in non-olfactorytissues, there are limitations posed by the small number ofantibodies available for similar OR genes. This review presentsthe results of a research series that identifies ectopic expressionsand functions of ORs in non-chemosensory tissues toprovide insight into future research directions.
Heterogeneous Sensory Innervation and Extensive Intrabulbar Connections of Olfactory Necklace Glomeruli  [PDF]
Renee E. Cockerham, Adam C. Puche, Steven D. Munger
PLOS ONE , 2009, DOI: 10.1371/journal.pone.0004657
Abstract: The mammalian nose employs several olfactory subsystems to recognize and transduce diverse chemosensory stimuli. These subsystems differ in their anatomical position within the nasal cavity, their targets in the olfactory forebrain, and the transduction mechanisms they employ. Here we report that they can also differ in the strategies they use for stimulus coding. Necklace glomeruli are the sole main olfactory bulb (MOB) targets of an olfactory sensory neuron (OSN) subpopulation distinguished by its expression of the receptor guanylyl cyclase GC-D and the phosphodiesterase PDE2, and by its chemosensitivity to the natriuretic peptides uroguanylin and guanylin and the gas CO2. In stark contrast to the homogeneous sensory innervation of canonical MOB glomeruli from OSNs expressing the same odorant receptor (OR), we find that each necklace glomerulus of the mouse receives heterogeneous innervation from at least two distinct sensory neuron populations: one expressing GC-D and PDE2, the other expressing olfactory marker protein. In the main olfactory system it is thought that odor identity is encoded by a combinatorial strategy and represented in the MOB by a pattern of glomerular activation. This combinatorial coding scheme requires functionally homogeneous sensory inputs to individual glomeruli by OSNs expressing the same OR and displaying uniform stimulus selectivity; thus, activity in each glomerulus reflects the stimulation of a single OSN type. The heterogeneous sensory innervation of individual necklace glomeruli by multiple, functionally distinct, OSN subtypes precludes a similar combinatorial coding strategy in this olfactory subsystem.
The repertoire of olfactory C family G protein-coupled receptors in zebrafish: candidate chemosensory receptors for amino acids
Tyler S Alioto, John Ngai
BMC Genomics , 2006, DOI: 10.1186/1471-2164-7-309
Abstract: Using genome database mining and other informatics approaches, we identified and characterized the repertoire of 54 intact "V2R-like" olfactory C family GPCRs in the zebrafish. Phylogenetic analysis – which also included a set of 34 C family GPCRs from fugu – places the fish olfactory receptors in three major groups, which are related to but clearly distinct from other C family GPCRs, including the calcium sensing receptor, metabotropic glutamate receptors, GABA-B receptor, T1R taste receptors, and the major group of V2R vomeronasal receptor families. Interestingly, an analysis of sequence conservation and selective pressure in the zebrafish receptors revealed the retention of a conserved sequence motif previously shown to be required for ligand binding in other amino acid receptors.Based on our findings, we propose that the repertoire of zebrafish olfactory C family GPCRs has evolved to allow the detection and discrimination of a spectrum of amino acid and/or amino acid-based compounds, which are potent olfactory cues in fish. Furthermore, as the major groups of fish receptors and mammalian V2R receptors appear to have diverged significantly from a common ancestral gene(s), these receptors likely mediate chemosensation of different classes of chemical structures by their respective organisms.The vertebrate olfactory system receives and decodes sensory information from a myriad chemical cues. The first step in this process is the recognition of these cues by receptors expressed by the primary sensory neurons in the olfactory epithelium (reviewed in refs. [1,2]). Receptor-mediated activity within the population of olfactory sensory neurons is then interpreted by the brain to identify the molecular nature of the odorant stimulus. A large multigene family thought to encode odorant receptors was initially identified in the rat [3] and belong to what is now referred to as the "OR" superfamily of odorant receptors (reviewed in [4]). The predicted structure of these recept
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