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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.
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
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
Bone Marrow Stromal and Vascular Smooth Muscle Cells Have Chemosensory Capacity via Bitter Taste Receptor Expression  [PDF]
Troy C. Lund, Amanda J. Kobs, Ashley Kramer, Mick Nyquist, Marcos T. Kuroki, John Osborn, Diane S. Lidke, Shalini T. Low-Nam, Bruce R. Blazar, Jakub Tolar
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0058945
Abstract: The ability of cells to detect changes in the microenvironment is important in cell signaling and responsiveness to environmental fluctuations. Our interest is in understanding how human bone marrow stromal-derived cells (MSC) and their relatives, vascular smooth muscle cells (VSMC), interact with their environment through novel receptors. We found, through a proteomics screen, that MSC express the bitter taste receptor, TAS2R46, a protein more typically localized to the taste bud. Expression was also confirmed in VSMCs. A prototypical bitter compound that binds to the bitter taste receptor class, denatonium, increased intracellular calcium release and decreased cAMP levels as well as increased the extracellular release of ATP in human MSC. Denatonium also bound and activated rodent VSMC with a change in morphology upon compound exposure. Finally, rodents given denatonium in vivo had a significant drop in blood pressure indicating a vasodilator response. This is the first description of chemosensory detection by MSC and VSMCs via a taste receptor. These data open a new avenue of research into discovering novel compounds that operate through taste receptors expressed by cells in the marrow and vascular microenvironments.
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.
Oxytocin Signaling in Mouse Taste Buds  [PDF]
Michael S. Sinclair,Isabel Perea-Martinez,Gennady Dvoryanchikov,Masahide Yoshida,Katsuhiko Nishimori,Stephen D. Roper,Nirupa Chaudhari
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0011980
Abstract: The neuropeptide, oxytocin (OXT), acts on brain circuits to inhibit food intake. Mutant mice lacking OXT (OXT knockout) overconsume salty and sweet (i.e. sucrose, saccharin) solutions. We asked if OXT might also act on taste buds via its receptor, OXTR.
Sweet taste signaling and the formation of memories of energy sources  [PDF]
Ivan E. de Araujo
Frontiers in Systems Neuroscience , 2011, DOI: 10.3389/fnsys.2011.00099
Abstract: The last decade witnessed remarkable advances in our knowledge of the gustatory system. Application of molecular biology techniques not only determined the identity of the membrane receptors and downstream effectors that mediate sweetness, but also uncovered the overall logic of gustatory coding in the periphery. However, while the ability to taste sweet may offer the obvious advantage of eliciting rapid and robust intake of sugars, a number of recent studies demonstrate that sweetness is neither necessary nor sufficient for the formation of long-lasting preferences for stimuli associated with sugar intake. Furthermore, uncoupling sweet taste from ensuing energy utilization may disrupt body weight control. This minireview examines recent experiments performed in both rodents and Drosophila revealing the taste-independent rewarding properties of metabolizable sugars. Taken together, these experiments demonstrate the reinforcing actions of sugars in the absence of sweet taste signaling and point to a critical role played by dopamine systems in translating metabolic sensing into behavioral action. From a mechanistic viewpoint, current evidence favors the concept that gastrointestinal and post-absorptive signals contribute in parallel to sweet-independent sugar acceptance and dopamine release.
Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25
Tod R Clapp, Kathryn F Medler, Sami Damak, Robert F Margolskee, Sue C Kinnamon
BMC Biology , 2006, DOI: 10.1186/1741-7007-4-7
Abstract: Depolarization with high K+ resulted in an increase in intracellular Ca2+ in a small subset of non-GFP labeled cells of both transgenic mouse lines. In contrast, no depolarization-evoked Ca2+ responses were observed in GFP-expressing taste cells of either genotype, but GFP-labeled cells responded to the PLC activator m-3M3FBS, suggesting that these cells were viable. Whole cell recording indicated that the GFP-labeled cells of both genotypes had small voltage-dependent Na+ and K+ currents, but no evidence of Ca2+ currents. A subset of non-GFP labeled taste cells exhibited large voltage-dependent Na+ and K+ currents and a high threshold voltage-gated Ca2+ current. Immunocytochemistry indicated that SNAP-25 was expressed in a separate population of taste cells from those expressing T1R3 or TRPM5. These data indicate that G protein-coupled taste receptors and conventional synaptic signaling mechanisms are expressed in separate populations of taste cells.The taste receptor cells responsible for the transduction of bitter, sweet, and umami stimuli are unlikely to communicate with nerve fibers by using conventional chemical synapses.Taste buds, the transducing elements of gustatory sensation, contain a heterogeneous population of 50 to 100 elongate taste receptor cells, which extend from the basal lamina to the surface of the epithelium. Taste stimuli interact with receptors on the apical membrane, while the basolateral membranes of some taste cells associate with gustatory nerve fibers to transmit taste information to the brain.Several types of taste cells have been identified morphologically. Type I cells, also known as "dark" cells, generally comprise about half of the taste bud. These cells are not believed to have a receptive function, but to play a more glial-like role in the taste bud [1,2]. About 35% of the cells are Type II cells, which are also known as "light" cells due to the electron lucent nature of their cytoplasm. Type II cells express T1R and T2R taste re
Expression and Secretion of TNF-α in Mouse Taste Buds: A Novel Function of a Specific Subset of Type II Taste Cells  [PDF]
Pu Feng, Hang Zhao, Jinghua Chai, Liquan Huang, Hong Wang
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0043140
Abstract: Taste buds are chemosensory structures widely distributed on the surface of the oral cavity and larynx. Taste cells, exposed to the oral environment, face great challenges in defense against potential pathogens. While immune cells, such as T-cells and macrophages, are rarely found in taste buds, high levels of expression of some immune-response-associated molecules are observed in taste buds. Yet, the cellular origins of these immune molecules such as cytokines in taste buds remain to be determined. Here, we show that a specific subset of taste cells selectively expresses high levels of the inflammatory cytokine tumor necrosis factor-α (TNF-α). Based on immuno-colocalization experiments using taste-cell-type markers, the TNF-α-producing cells are predominantly type II taste cells expressing the taste receptor T1R3. These cells can rapidly increase TNF-α production and secretion upon inflammatory challenges, both in vivo and in vitro. The lipopolysaccharide (LPS)-induced TNF-α expression in taste cells was completely eliminated in TLR2?/?/TLR4?/? double-gene-knockout mice, which confirms that the induction of TNF-α in taste buds by LPS is mediated through TLR signaling pathways. The taste-cell-produced TNF-α may contribute to local immune surveillance, as well as regulate taste sensation under normal and pathological conditions.
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.
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