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PubMed2005

Down regulation of Kv3.4 channels by chronic hypoxia increases acute oxygen sensitivity in rabbit carotid body.

The carotid body (CB) chemoreceptors participate in the ventilatory responses to acute and chronic hypoxia (CH). Arterial hypoxaemia increases breathing within seconds, and CB chemoreceptors are the principal contributors to this reflex hyperventilatory response. Acute hypoxia induces depolarization of CB chemoreceptors by inhibiting certain K+ channels, but the role of these channels in CH, as in high-altitude acclimatization, is less known. Here we explored the effects of prolonged (24-48 h) hypoxic exposure of rabbit CB chemoreceptor cells in primary cultures on the voltage-dependent K+ currents and on their response to acute hypoxia. We found that CH induces a decrease in the amplitude of outward K+ currents due to a reduction in a fast-inactivating BDS- and highly TEA-sensitive component of the current. In spite of this effect, acute hypoxic inhibition of K+ currents is increased in CH cultures, as well as hypoxia-induced depolarization. These data suggest that downregulation of this component (that does not contribute to the oxygen-sensitive K+ current (IKO2) participates in the hypoxic sensitization. Pharmacological, immunocytochemical and quantitative PCR (qPCR) experiments demonstrate that CH-induced decrease in outward K+ currents is due to a downregulation of the expression of Kv3.4 channels. Taken together, our results suggest that CH sensitization in rabbit CB could be achieved by an increase in the relative contribution of IKO2 to the outward K+ current as a consequence of the decreased expression of the oxygen-insensitive component of the current. We conclude that acute and chronic hypoxia can exert their effects acting on different molecular targets.

Algorithms↗
PubMed2001

Proteolysis of the Caulobacter McpA chemoreceptor is cell cycle regulated by a ClpX-dependent pathway.

Proteolysis is involved in cell differentiation and the progression through the cell cycle in Caulobacter crescentus. We have constitutively expressed the transmembrane chemoreceptor McpA from a multicopy plasmid to demonstrate that McpA degradation is modulated during the cell cycle. The level of McpA protein starts to decrease only when the swarmer cells differentiate into stalked cells. The reduction in McpA protein levels is maintained until the stalked cells develop into predivisional cells, at which point the level returns to that observed in swarmer cells. The cell-cycle-regulated degradation of McpA does not require the last 12 C-terminal amino acids, but it does require three amino acids (AAL) located 15 residues away from the C terminus. The ClpXP protease is essential in C. crescentus for viability, and thus, we tested McpA degradation in xylose conditional mutants. The effect on McpA degradation occurred within two generations from the start of ClpX depletion. The conditional mutants' growth rate was only slightly affected, suggesting that ClpX is directly involved in McpA proteolysis.

ATPases Associated with Diverse Cellular Activitie↗
PubMed1999

Protein kinase C--a potential modifier of carotid body function.

This article deals with the potential role of protein kinase C (PKC) in signal transduction in the carotid body. The carotid body is a chemosensory organ which, by sensing reductions in arterial blood oxygen tension, is primarily responsible for the hyperventilation of hypoxia. The mechanisms of transduction of the hypoxic stimulus into a neural signal regulating respiration are not clear. Hypoxia increases the phosphoinositide-specific phospholipase C (PLC) activity in the carotid body. The PLC-derived signalling molecules are known to activate PKC. The enzyme might, thus, have the potential to interact with the process of chemoreception. This article demonstrates that PKC is present in the chemoreceptor cells of the cat carotid body and discusses the biology of the enzyme relevant to chemosensory function. This gives rise to the hypothesis that PKC-mediated mechanisms alter chemoreceptor cell function to a sufficient extent to metamorphose the hypoxic signal into an increased discharge frequency in the apposed sinus nerve endings.

Animals↗
PubMed2004

Laryngeal chemosensory clusters.

The expression of molecules involved in the transductory cascade of the sense of taste (TRs, alpha-gustducin, PLCbeta2, IP3R3) has been described in lingual taste buds or in solitary chemoreceptor cells located in different organs. At the laryngeal inlet, immunocytochemical staining at the light and electron microscope levels revealed that alpha-gustducin and PLCbeta2 are mainly localized in chemosensory clusters (CCs), which are multicellular organizations differing from taste buds, being generally composed of two or three chemoreceptor cells. Compared with lingual taste buds, CCs are lower in height and smaller in diameter. In laryngeal CCs, immunocytochemistry using the two antibodies identified a similar cell type which appears rather unlike the alpha-gustducin-immunoreactive (IR) and PLCbeta2-IR cells visible in lingual taste buds. The laryngeal IR cells are shorter than the lingual ones, with poorly developed basal processes and their apical process is shorter and thicker. Some cells show a flask-like shape due to the presence of a large body and the absence of basal processes. CCs lack pores and their delimitation from the surrounding epithelium is poorly evident. The demonstration of the existence of CCs strengthens the hypothesis of a phylogenetic link between gustatory and solitary chemosensory cells.

Animals↗
PubMed1997

Comparative aspects of central CO2 chemoreception.

We compare and contrast the putative mechanisms underlying CO2 chemoreceptor function in air breathing vertebrates and terrestrial pulmonate snails. We discuss the role of intracellular pH (pHi) in central respiratory responses to CO2 and describe a variety of patterns of pHi regulation in chemosensory areas. One pattern, in which pHi retains a fixed relationship to the CO2 stimulus over time, seems well suited to chemoreceptor cells. Alphastat regulation of ventilation is apparent in both air breathing vertebrates and terrestrial pulmonate snails. Diethyl pyrocarbonate inhibits respiratory responses to hypercapnia in both groups of animals. The neuronal basis of chemosensitivity is similar, in that putative chemoreceptor cells depolarize during hypercapnic stimulation, but the ionic basis of excitability appears to be a potassium conductance in the vertebrates studied to date and a calcium conductance in the snails. Despite divergent evolutionary histories, chemosensory responses and mechanisms are remarkably similar in air breathing vertebrates and terrestrial pulmonate snails.

Animals↗
PubMed2004

Identification and characterization of a specific sensory epithelium in the rat larynx.

A specific laryngeal sensory epithelium (SLSE), which includes arrays of solitary chemoreceptor cells, is described in the supraglottic region of the rat. Two plates of SLSE were found, one on each side of the larynx. The first plate was located in the ventrolateral wall of the larynx, and the second was located in the interarytenoidal region. In SLSE, immunoblotting showed the presence of alpha-gustducin and phospholipase C beta2 (PLCbeta2), which are two markers of chemoreceptor cells. At immunocytochemistry, laryngeal immunoreactivity for alpha-gustducin was localized mainly in solitary chemosensory cells. Double-label immunocytochemistry using confocal microscopy demonstrated that alpha-gustducin-expressing cells in large part colocalize type III IP3 receptor (IP3R3), another key molecule in bitter taste perception. However, some IP3R3-expressing cells do not colocalize alpha-gustducin. At ultrastructural immunocytochemistry, these cells showed packed apical microvilli, clear cytoplasmic vesicles, and cytoneural junctions. SLSE was characterized by high permeability to a tracer due to poorly developed junctional contacts between superficial cells. Junctions were short in length and showed little contact with the terminal web. Ultrastructural analysis showed deep pits among the superficial cells. In SLSE, high density of intraepithelial nerve fibers was found. The lamina propria of the SLSE appeared thicker than that in other supraglottic regions. It was characterized by the presence of a well-developed subepithelial nerve plexus. The immunocytochemical and ultrastructural data suggested that SLSE is a chemoreceptor located in an optimal position for detecting substances entering the larynx from the pharynx or the trachea.

Animals↗
PubMed2001

Nitric oxide enhances Ca(2+)-dependent K(+) channel activity in rat carotid body cells.

The nitric oxide (NO) donor S-nitroso-acetylpenicillamine (SNAP) enhanced Ca(2+)-dependent K(+) channel activity in rat carotid body chemoreceptor cells. Ca(2+)-dependent K(+) channel activity was enhanced by SNAP in 38% (whole-cell configuration) and 67% (cell-attached mode) of the cells tested and was not affected by intracellular Ca(2+) chelation with BAPTA-AM. Enhancement of Ca(2+)-dependent K(+) channel activity by SNAP was blocked by the cGMP-dependent protein kinase G inhibitor 8-[(4-chlorophenyl)thio]-guanosine 3',5'-cyclic monophosphothioate Rp diastereomer (Rp-8-pCPT-cGMPS). NO thus enhances Ca(2+)-dependent K(+) channel activity through cGMP-dependent protein kinase G. The NO-mediated increase in Ca(2+)-dependent K(+) channel activity is likely to alter the function of carotid body chemoreceptor cells and could explain the decreased chemosensitivity of the carotid body in response to NO released from efferent nerves or vascular endothelial cells.

Animals↗
PubMed2006

Caffeine inhibition of rat carotid body chemoreceptors is mediated by A2A and A2B adenosine receptors.

Caffeine, an unspecific antagonist of adenosine receptors, is commonly used to treat the apnea of prematurity. We have defined the effects of caffeine on the carotid body (CB) chemoreceptors, the main peripheral controllers of breathing, and identified the adenosine receptors involved. Caffeine inhibited basal (IC50, 210 microm) and low intensity (PO2 approximately 66 mm Hg/30 mm K+) stimulation-induced release of catecholamines from chemoreceptor cells in intact preparations of rat CB in vitro. Opposite to caffeine, 5'-(N-ethylcarboxamido)adenosine (NECA; an A2 agonist) augmented basal and low-intensity hypoxia-induced release. 2-p-(2-Carboxyethyl)phenethyl-amino-5'-N-ethylcaboxamido-adenosine hydrochloride (CGS21680), 2-hexynyl-NECA (HE-NECA) and SCH58621 (A2A receptors agents) neither affected catecholamine release nor altered the caffeine effects. The 8-cycle-1,3-dipropylxanthine (DPCPX; an A1/A2B antagonist) and 8-(4-{[(4-cyanophenyl)carbamoylmethyl]-oxy}phenyl)-1,3-di(n-propyl)xanthine (MRS1754; an A2B antagonist) mimicking of caffeine indicated that caffeine effects are mediated by A2B receptors. Immunocytochemical A2B receptors were located in tyrosine hydroxylase positive chemoreceptor cells. Caffeine reduced by 52% the chemosensory discharges elicited by hypoxia in the carotid sinus nerve. Inhibition had two components with pharmacological analysis indicating that A2A and A2B receptors mediate, respectively, the low (17 x 10(-9) m) and high (160 x 10(-6) m) IC50 effects. It is concluded that endogenous adenosine, via presynaptic A2B and postsynaptic A2A receptors, can exert excitatory effects on the overall output of the rat CB chemoreceptors.

Adenosine↗
PubMed2002

Significance of ROS in oxygen sensing in cell systems with sensitivity to physiological hypoxia.

Reactive oxygen species (ROS) are oxygen-containing molecular entities which are more potent and effective oxidizing agents than is molecular oxygen itself. With the exception of phagocytic cells, where ROS play an important physiological role in defense reactions, ROS have classically been considered undesirable byproducts of cell metabolism, existing several cellular mechanisms aimed to dispose them. Recently, however, ROS have been considered important intracellular signaling molecules, which may act as mediators or second messengers in many cell functions. This is the proposed role for ROS in oxygen sensing in systems, such as carotid body chemoreceptor cells, pulmonary artery smooth muscle cells, and erythropoietin-producing cells. These unique cells comprise essential parts of homeostatic loops directed to maintain oxygen levels in multicellular organisms in situations of hypoxia. The present article examines the possible significance of ROS in these three cell systems, and proposes a set of criteria that ROS should satisfy for their consideration as mediators in hypoxic transduction cascades. In none of the three cell types do ROS satisfy these criteria, and thus it appears that alternative mechanisms are responsible for the transduction cascades linking hypoxia to the release of neurotransmitters in chemoreceptor cells, contraction in pulmonary artery smooth muscle cells and erythropoietin secretion in erythropoietin producing cells.

Animals↗
PubMed1996

Secondary connections of the dorsal and ventral facial lobes in a teleost fish, the rockling (Ciliata mustela).

In the rockling, Ciliata mustela (Teleostei), a portion of the dorsal fin is a specialized chemosensory organ possessing solitary chemoreceptor cells innervated by a recurrent branch of the facial nerve. Previous studies have demonstrated that the specialized solitary chemoreceptor cell system is represented in the dorsal segment of the medullary facial lobe (DFL), whereas the taste buds in the remainder of the facial-nerve-innervated skin are represented in the ventral division of the lobe (VFL). The carbocyanine dye DiI was used to investigate the secondary and higher order brain connections of these two distinct subdivisions of the facial lobe. Both segments of the facial lobe sent fibers into the contralateral DFL via a dorsocaudal facial commissure and to the contralateral vagal lobes and VFL via fibers arching ventrally through the reticular formation. Ascending fibers from both facial lobe segments were traced into the secondary gustatory nucleus and into the lateral superficial facial nucleus, a small area in the dorsolateral brainstem laterally adjacent to the nucleus medialis of the octavolateral complex. Additionally, the VFL had reciprocal connections with a newly described nucleus adjacent to the incoming facial nerve root. Both DFL and VFL had descending fibers reaching two portions of the funicular nuclear complex, although the VFL contribution to this area is far more extensive than the DFL input. Thus, substantial overlap exists in the connections of the two facial subsystems; i.e., the solitary chemoreceptor information is not processed in nuclei distinct from those making up the usual gustatory lemniscus.

Animals↗
PubMed1994

A model of the role of adaptation and disadaptation in olfactory receptor neurons: implications for the coding of temporal and intensity patterns in odor signals.

Natural odors occur as turbulent plumes resulting in spatially and temporally variable odor signals at the chemoreceptor cells. Concentrations can fluctuate widely within discrete packets of odor and individual packets are very intermittent and unpredictable. Chemoreceptor cells display the temporally dynamic properties of adaptation and disadaptation, which serve to alter their responses to these fluctuating odor patterns. A computational model, modified from one previously published, was used to investigate the effect of adaptation and recovery of adaptation (disadaptation) on the spike output of model olfactory receptor cells under natural stimulus conditions. The response characteristics of model cells were based upon empirically determined dose-response, adaptation, disadaptation and flicker fusion properties of peripheral olfactory cells. The physiological properties of the model cell (adaptation and disadaptation rate and the dose-response relationship) could be modified independently, allowing assessment of the role of each in shaping the responses of the model cell. Complete adaptation and disadaptation time courses ranged from 500 ms (rapid cells) to 10 s (slow cells). The stimuli for the model cells were quantified odor plume recordings obtained under a variety of biologically relevant flow conditions. As expected, the rapidly adapting model cells displayed different response characteristics than the slowly adapting model cells to identical temporal odor profiles. Responses of the model cells depended upon their adaptation and disadaptation rates, and the frequency characteristics of the odor presentation. These results indicate that adaptation and disadaptation determine the range of concentration fluctuations over which a particular cell will respond. Thus, these properties function as an olfactory equivalent of a band-pass filter in electronics. This type of filtering has implications for the extraction of information from odor signals, such as the coding of temporal and intensity features.

Adaptation, Physiological↗
PubMed2004

Espins are multifunctional actin cytoskeletal regulatory proteins in the microvilli of chemosensory and mechanosensory cells.

Espins are associated with the parallel actin bundles of hair cell stereocilia and are the target of mutations that cause deafness and vestibular dysfunction in mice and humans. Here, we report that espins are also concentrated in the microvilli of a number of other sensory cells: vomeronasal organ sensory neurons, solitary chemoreceptor cells, taste cells, and Merkel cells. Moreover, we show that hair cells and these other sensory cells contain novel espin isoforms that arise from a different transcriptional start site and differ significantly from other espin isoforms in their complement of ligand-binding activities and their effects on actin polymerization. The novel espin isoforms of sensory cells bundled actin filaments with high affinity in a Ca(2+)-resistant manner, bound actin monomer via a WASP (Wiskott-Aldrich syndrome protein) homology 2 domain, bound profilin via a single proline-rich peptide, and caused a dramatic elongation of microvillus-type parallel actin bundles in transfected epithelial cells. In addition, the novel espin isoforms of sensory cells differed from other espin isoforms in that they potently inhibited actin polymerization in vitro, did not bind the Src homology 3 domain of the adapter protein insulin receptor substrate p53, and did not bind the acidic, signaling phospholipid phosphatidylinositol 4,5-bisphosphate. Thus, the espins constitute a family of multifunctional actin cytoskeletal regulatory proteins with the potential to differentially influence the organization, dimensions, dynamics, and signaling capabilities of the actin filament-rich, microvillus-type specializations that mediate sensory transduction in various mechanosensory and chemosensory cells.

Actins↗
PubMed1993

An immuno-electron microscopic comparison of olfactory marker protein localization in the supranuclear regions of the rat olfactory epithelium and vomeronasal organ neuroepithelium.

Immuno-electron microscopy was used to examine olfactory marker protein (OMP) ultrastructural localization in the supranuclear regions of the rat olfactory epithelium (OE) and vomeronasal organ (VNO) neuroepithelium. In the OE, OMP immuno-reaction product was observed within the cytoplasm of olfactory chemoreceptor cell dendrites, vesicles and cilia. Reaction product was absent from olfactory microvillar cells and their unique microvillar projections. In the neuroepithelium of the VNO, immuno-reaction product was seen within the dendrites of the chemoreceptor cells, and in the bases of their attached microvilli; the remaining distal portions of these microvilli were unlabeled. These results demonstrate a difference in the distribution of OMP immunoreactivity over the surfaces of the rat OE and VNO. They also show that OMP immunoreactivity does not exist in the rat olfactory microvillar cells.

Animals↗
PubMed2005

Activity modulation in cockroach sensillum: the role of octopamine.

The plasticity of sensory perception is provided partially by modulation of receptor cells. The electrical activity of American cockroach chemoreceptor cells in response to sex pheromone was measured under the influence of octopamine treatment and tracheal anoxia. Both experimental procedures caused decreased electroantennograms but affected spike activity differently: octopamine treatment increased firing rate, whereas anoxia decreased it. Spike frequency under octopamine treatment was elevated in response to pheromone stimulation and at background activity. Experiments with perfusion of isolated antennae showed a direct effect of octopamine on spike activity of pheromone sensilla, and excluded the possibility of indirect effects via octopamine-dependent release of other biologically active substances. The suggested mechanism of octopamine action is receptor cell membrane depolarization.

Animals↗
PubMed2006

Cell birth and survival following seasonal periods of cell proliferation in the chemosensory epithelia of red-backed salamanders, Plethodon cinereus.

In addition to the continuous low levels of neurogenesis typical of adult vertebrates to replace damaged chemoreceptor cells, red-backed salamanders (Plethodon cinereus) experience an up-regulation of chemoreceptor epithelial cell proliferation on a seasonal basis. Significantly more cell division occurs in late spring than at any other time of the year, and we investigated the fate and life span of these newly generated cells. We used 5-bromo-2'-deoxyuridine (BrdU) immunocytochemical cell birth dating to examine cell proliferation and cell migration in the main olfactory and vomeronasal epithelia of red-backed salamanders collected in late spring who were allowed to survive for one hour or three, four, 25, 28, 42, 49 and 100 days post-injection. We examined new neuron growth in the vomeronasal and olfactory epithelia using antibodies against Growth Associated Protein-43 (GAP-43), a protein whose synthesis is up-regulated during axon growth. We also tracked apoptosis within both types of chemosensory epithelia using terminal deoxynucleotidyl transferase-mediated nick-end labeling (TUNEL). BrdU-immunoreactive cells were located extensively throughout the vomeronasal epithelia, particularly in the area posterior to the entrance of the nasolacrimal duct, not only after three days of survival, but also all of the longer experimental survival periods as well; BrdU-ir cells within the olfactory epithelia were rarely located after longer survival periods. Salamanders collected in late spring displayed extensive GAP-43 labeling in the vomeronasal epithelia posterior to the entrance of the nasolacrimal duct, indicating a large population of young vomeronasal receptor neurons. Finally, apoptotic cells were evident in this same post-nasolacrimal-duct-area of the vomeronasal organ and in the olfactory epithelium. We suggest that vomeronasal receptor neurons born in late spring function throughout the summer and may be associated with the animals' extensive territoriality during that period.

Analysis of Variance↗
PubMed2003

Pivotal role of nucleotide P2X2 receptor subunit of the ATP-gated ion channel mediating ventilatory responses to hypoxia.

In mammals, the ventilatory response to decreased oxygen tension in the arterial blood is initiated by excitation of specialized O2-sensitive chemoreceptor cells in the carotid body that release neurotransmitters to activate endings of the sinus nerve afferent fibers. We investigated the role of ATP acting via ionotropic P2X receptors in the carotid body function and ventilatory response to hypoxia in mice. Mice deficient in P2X2 receptor subunit showed a markedly attenuated ventilatory response to hypoxia, whereas the response to hypoxia in P2X3-deficient mice was comparable with that seen in wild-type controls. P2X2 and P2X3 receptor subunit deficiency did not affect the ventilatory responses to hypercapnia. P2X2 subunit deficiency resulted in a dramatic reduction in the responses of the carotid sinus nerve to hypoxia in the in vitro carotid body-sinus nerve preparation. ATP and its stable analog alpha,beta-methyleneATP both evoked rapid excitation of sinus nerve afferents, and the P2 receptor antagonist PPADS (pyridoxal-5'-phosphate-6-azophenyl-2',4'-disulphonic acid) (100 microm) blocked hypoxia-induced increase in sinus nerve discharge. Immunoreactivities for P2X2 and P2X3 subunits were both detected on afferent terminals surrounding clusters of glomus cells in the wild-type animals but were absent in mice deficient in P2X2 and P2X3 receptor subunits. These observations provide the first definitive evidence that, in the carotid body, ATP is a key transmitter released by chemoreceptor cells to activate endings of the sinus nerve afferent fibers. We conclude that P2X receptors containing the P2X2 subunit play a pivotal role in carotid body function and in mediating ventilatory responses to hypoxia.

Action Potentials↗
PubMed2006

Effects of intermittent hypoxia on cat petrosal ganglion responses induced by acetylcholine, adenosine 5'-triphosphate and NaCN.

Exposure to chronic intermittent hypoxia (CIH) for 4 days enhances the cat carotid body (CB) chemosensory responses to acute hypoxia. However, it is not known if CIH enhances the responses of the petrosal ganglion (PG) neurons that innervate the CB chemoreceptor cells. Accordingly, we studied the effects of the CB putative excitatory transmitter acetylcholine (ACh) and adenosine 5 -triphosphate (ATP), and the effects of citotoxic hypoxia (NaCN) applied to the isolated PG from cats exposed to CIH for 4 days. The dose-dependent curve parameters of the frequency of discharges evoked in the carotid sinus nerve by the application of ACh, ATP and NaCN to the isolated PG in control condition were not significantly modified in the CIH-treated cats. Present results suggest that CIH enhances the chemosensory responses to acute hypoxia acting primarily at the chemoreceptor cells, without major changes in the response of PG neurons evoked by the application of putative CB excitatory transmitters to their somata.

Acetylcholine↗
PubMed2001

Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorant-binding protein PBPRP2.

In Drosophila, as in most insects, gustation is mediated by sensory hairs located on the external and internal parts of the proboscis and on the legs and wings. We describe in detail the organization and ultrastructure of the gustatory sensilla on the labellum and legs and the distribution of PBPRP2, a putative odorant-binding protein, in the gustatory organs of Drosophila. The labellum carries two kinds of sensilla: taste bristles and taste pegs. The former have the typical morphology of gustatory sensilla and can be further subdivided into three morphological subtypes, each with a stereotyped distribution and innervation. Taste pegs have a unique morphology and are innervated by two receptor cells: one mechanoreceptor and the other a putative chemoreceptor cell. PBPRP2 is abundantly expressed in all adult gustatory organs on labellum, legs, and wings and in the internal taste organs on the proboscis. In contrast to olfactory organs, where PBPRP2 is expressed in the epidermis, this protein is absent from the epidermis of labial palps and legs. In the taste bristles of the labellum and legs, PBPRP2 is localized in the crescent-shaped lumen of the sensilla, and not in the lumen where the dendrites of the gustatory neurons are found, making a function in stimulus transport unlikely in these sensilla. In contrast, PBPRP2 in peg sensilla is expressed in the inner sensillum-lymph cavity and is in contact with the dendrites. Thus, PBPRP2 could be involved as a carrier for hydrophobic ligands, e.g., bitter tastants, in these sensilla.

Animals↗