Calcium modulates the rapid kinetics of the odorant-induced cyclic AMP signal in rat olfactory cilia

Jaworsky, D. E.; Matsuzaki, Osamu; Borisy, FF; Ronnett, GV

doi:10.1523/jneurosci.15-01-00310.1995

Cited by 36 publications

(42 citation statements)

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“…Individual lobster olfactory receptor neurons seem to express two different transduction channels: odorant-induced opening of cyclic nucleotide-gated channels results in a hyperpolarizing conductance, whereas odorant-induced opening of plasma membrane IP 3 -gated channels results in a depolarizing conductance (Fadool and Ache, 1992;Ache and Zhainazarov, 1995). Vertebrate olfactory receptor neurons have odorant-stimulated IP 3 signaling pathways (Boekhoff et al, 1990;Miyamoto et al, 1992), but their function is unclear (Jaworsky et al, 1995;Brunet et al, 1996). In addition, bitter-tasting compounds stimulate the production of IP 3 in vertebrate taste cell membranes (Spielman et al, 1996).…”

Section: Discussionmentioning

confidence: 99%

OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans

1997

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Although cyclic nucleotide-gated channels mediate sensory transduction in olfaction and vision, other forms of sensory transduction are independent of these channels. Caenorhabditis elegans cyclic nucleotide-gated channel mutants respond normally to some olfactory stimuli and to osmotic stimuli, suggesting that these chemosensory responses use an alternative sensory transduction pathway. One gene that may act in this pathway is osm-9, which is required for each of these responses as well as a mechanosensory response to nose touch. osm-9 encodes a protein with ankyrin repeats and multiple predicted transmembrane domains that has limited similarity to the Drosophila phototransduction channels transient receptor potential (TRP) and TRP-like (TRPL). The sequence of OSM-9 and other TRP-like genes reveals a previously unsuspected diversity of mammalian and invertebrate genes in this family. osm-9 is required for the activity of the predicted G-proteincoupled odorant receptor ODR-10, which acts in the AWA olfactory neurons; its similarity to other G-protein-regulated transduction channels suggests that OSM-9 is involved in AWA signaling. osm-9::GFP fusion genes are expressed in a subset of chemosensory, mechanosensory, and osmosensory neurons. osm-9 also affects olfactory adaptation within neurons that require the cyclic nucleotide-gated channel for olfaction; in these neurons, the gene has a regulatory function and not a primary role in sensory transduction.Key words: olfaction; C. elegans; mechanosensation; sensory transduction; signaling pathways; olfactory adaptation; TRP channels Sensory neurons transduce environmental stimuli via the activation of channels that differ by organism and by sensory system. One important class of sensory channels includes cAMP-and cGM P-gated channels. In the vertebrate visual system, photoactivation of the G-protein-coupled receptor rhodopsin results in closure of cGM P-gated channels (Stryer, 1991). Olfactory transduction in vertebrates also begins with the activation of Gprotein-coupled receptors and is mediated by opening of cAM P-gated channels (Reed, 1992). Mice mutant for the olfactory cyclic nucleotide-gated channel fail to generate electrical responses to all tested odorants, although the olfactory neurons are present and have normal passive membrane properties (Brunet et al., 1996). C yclic nucleotide-gated channels have also been implicated in chemosensation in the nematode Caenorhabditis elegans. C. elegans senses a large number of volatile attractants with two pairs of olfactory neurons designated AWA and AWC (Bargmann et al., 1993). AWC olfactory responses may be mediated by a putative cyclic nucleotide-gated channel encoded by the tax-2 and tax-4 genes (Coburn and Bargmann, 1996;Komatsu et al., 1996). The TAX-2/TAX-4 channel also participates in chemotaxis to water-soluble attractants (Dusenbery et al., 1975) and in thermotaxis (Mori and Ohshima, 1995). TAX-2 and TAX-4 gene fusions are expressed in the sensory neurons that mediate these responses.By contrast, sensory tr...

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Section: Discussionmentioning

confidence: 99%

OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans

1997

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“…Levels of PDE1 activity and protein in cells are regulated transcriptionally and post-translationally; cAMPand Ca 2ϩ -dependent signaling both contribute. Roles for PDE1C have been demonstrated in human VSMC proliferation (Rybalkin et al, 1997), olfactory fatigue (Jaworsky et al, 1995), and insulin-secretion (Han et al, 1999). In addition, increased PDE1A expression was reported to contribute to the development of nitroglycerin tolerance, a multifactorial phenomenon leading to reduced efficacy of this important antianginal drug (Kim et al, 2001).…”

Section: Pde1mentioning

confidence: 99%

Cyclic Nucleotide Phosphodiesterase Activity, Expression, and Targeting in Cells of the Cardiovascular System

Maurice¹,

Palmer²,

Tilley³

et al. 2003

Mol Pharmacol

292

255

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Cyclic AMP (cAMP) and cGMP regulate a myriad of cellular functions, such as metabolism, contractility, motility, and transcription in virtually all cell types, including those of the cardiovascular system. Considerable effort over the last 20 years has allowed identification of the cellular components involved in the synthesis of cyclic nucleotides, as well as effectors of cyclic nucleotide-mediated signaling. More recently, a central role for cyclic nucleotide phosphodiesterase (PDE) has also been elaborated in many cell types, including those involved in regulating the activities of the cardiovascular system. In this review, we introduce the PDE families whose members are expressed in cells of the cardiovascular system including cardiomyocytes, vascular smooth muscle cells, and vascular endothelial cells. Because cell behavior is a dynamic process influenced by numerous factors, we will attempt to emphasize how changes in the activity, expression, and targeting of PDE influence cyclic nucleotide-mediated regulation of the behavior of these cells.The cyclic nucleotides cAMP and cGMP regulate a myriad of cellular functions, including metabolism, contractility, motility, and transcription in virtually all cell types, including those of the cardiovascular system (Antoni, 2000;Klein, 2002). Although early work identified cAMP and cGMP as second messengers and led to the discovery of the proteins involved in coordinating the synthesis, degradation, and cellular actions of cyclic nucleotides, early models describing how these systems allowed cyclic nucleotide-mediated regulation of multiple cellular functions underestimated the levels of flexibility and specialization involved. In this context, recent work has identified large numbers of receptor (Marchese et al., 1999;Lucas et al., 2000), adenylyl cyclase (Hanoune and Defer, 2001), guanylyl cyclase (Garbers, 1999;Lucas et al., 2000), heterotrimeric G-protein (Marchese et al., 1999), and cyclic nucleotide phosphodiesterase (PDE) (Beavo and Reifsnyder, 1990;Beavo, 1995;Conti et al., 1995;Manganiello and Degerman, 1999;Conti, 2000;Conti and Jin, 2000;Houslay and Kolch, 2000;Soderling and Beavo, 2000;Francis et al., 2001;Houslay and Adams, 2003) protein families. Although many of the cellular effects of cAMP and cGMP are coordinated through their activation of cyclic nucleotide-dependent protein kinases (Lincoln et al., 1995), several other effectors are now known. Thus, cyclic nucleotidegated ion channels (Yau, 1994), cAMP-activated guanine nucleotide exchange factors (de Rooij et al., 1998;Kawasaki et al., 1998), and cyclic nucleotide PDEs have each been shown to transduce cyclic nucleotide-encoded information (Beavo and Reifsnyder, 1990;Beavo, 1995;Conti et al., 1995;Manganiello and Degerman, 1999;Conti, 2000;Conti and Jin, 2000;Houslay and Kolch, 2000;Soderling and Beavo, 2000;Francis et al., 2001;Houslay and Adams, 2003). More recently, an appreciation of the impact of regulated anchoring/targeting of cyclic nucleotide-regulated proteins to discrete subcell...

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“…For example, the nonspecific PDE inhibitor 3-isobutyl-1-methylxanthine (IBMX) prolongs the normally transient elevation of cAMP (11) and the current elicited by odorant stimulation (14). In addition, the predominant PDE activity in olfactory cilia is Ca2+/calmodulin dependent and studies using rapid stop-flow analysis indicate that cAMP accumulation in the subsecond, time range is disproportionately enhanced in the presence of IBMX at higher concentrations of Ca2+, suggesting that th, Ca2+/calmodulin-dependent PDE (CaM-PDE) is quite active under these conditions (15,16). Finally, Ca2+ appears to be a regulator in the control of cAMP signal termination.…”

mentioning

confidence: 99%

“…The possibility that a CaM-PDE might be activated as a consequence of odorant stimulation was suggested originally by the observations that the predominant PDE activity present in olfactory cilia was stimulated by Ca2+ and had a high affinity for cAMP and cGMP (16). More recently, this CaM-PDE activity in olfactory cilia has been implicated as a modulator of the subsecond changes of cAMP after odorant stimulation (15). The facts that PDE1C2 has high affinity for cAMP and that its mRNA is highly enriched in olfactory sensory neurons suggest an important role of PDE1C2 in a Ca2+-regulated rapid termination of the olfactory cAMP signal.…”

mentioning

confidence: 99%

“…This ensures a rapid rise in intracellular cAMP concentration. However, at later stages, further increases in Ca2+ concentration may start to inhibit type III adenylyl cyclase (15,39,40) and to activate PDE1C2. By stimulating the activity of the PDE1C2 as well as perhaps inhibiting adenylyl cyclase, the higher levels of Ca2+ could cause a rapid decline in cAMP.…”

mentioning

confidence: 99%

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Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons.

Yan

Zhao

Bentley

et al. 1995

Proc. Natl. Acad. Sci. U.S.A.

165

124

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The sensing of an odorant by an animal must be a rapid but transient process, requiring an instant response and also a speedy termination of the signal. Previous biochemical and electrophysiological studies suggest that one or more phosphodiesterases (PDEs) may play an essential role in the rapid termination of the odorant-induced cAMP signal. Here we report the molecular cloning, expression, and characterization of a cDNA from rat olfactory epithelium that encodes a member of the calmodulin-dependent PDE family designated as PDE1C. This enzyme shows high affinity for cAMP and cGMP, having a K. for cAMP much lower than that of any other neuronal Ca2+/calmodulin-dependent PDE. The mRNA encoding this enzyme is highly enriched in olfactory epithelium and is not detected in six other tissues tested. However, RNase protection analyses indicate that other alternative splice variants related to this enzyme are expressed in several other tissues. Within the olfactory epithelium, this enzyme appears to be expressed exclusively in the sensory neurons. The high affinity for cAMP of this Ca2 /calmodulin-dependent PDE and the fact that its mRNA is highly concentrated in olfactory sensory neurons suggest an important role for it in a Ca2+-regulated olfactory signal termination.

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Calcium modulates the rapid kinetics of the odorant-induced cyclic AMP signal in rat olfactory cilia

Cited by 36 publications

References 50 publications

OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans

OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans

Cyclic Nucleotide Phosphodiesterase Activity, Expression, and Targeting in Cells of the Cardiovascular System

Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons.

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