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Arthropod 5-HT2 receptors: a neurohormonal receptor in decapod crustaceans that displays agonist independent activity resulting from an evolutionary alteration to the DRY motif.

ABSTRACT: The stomatogastric nervous system (STNS) is a premiere model for studying modulation of motor pattern generation. Whereas the cellular and network responses to monoamines have been particularly well characterized electrophysiologically, the transduction mechanisms that link the different monoaminergic signals to specific intracellular responses are presently unknown in this system. To begin to elucidate monoaminergic signal transduction in pyloric neurons, we used a bioinformatics approach to predict the existence of 18 monoamine receptors in arthropods, 9 of which have been previously cloned in Drosophila and other insects. We then went on to use the two existing insect databases to clone and characterize the 10th putative arthropod receptor from the spiny lobster, Panulirus interruptus. This receptor is most homologous to the 5-HT2 subtype and shows a dose-dependent response to 5-HT but not to any of the other monoamines present in the STNS. Through a series of pharmacological experiments, we demonstrate that this newly described receptor, 5-HT2betaPan, couples with the traditional G(q) pathway when expressed in HEK293 cells, but not to G(s) or G(i/o). Moreover, it is constitutively active, because the highly conserved DRY motif in transmembrane region 3 has evolved into DRF. Site-directed mutagenesis that reverts the motif back to DRY abolishes this agonist-independent activity. We further demonstrate that this receptor most likely participates in the modulation of stomatogastric motor output, because it is found in neurites in the synaptic neuropil of the stomatogastric ganglion as well as in the axon terminals at identified pyloric neuromuscular junctions.

SUBMITTER: Clark MC

PROVIDER: S-EPMC6730010 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

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Arthropod 5-HT2 receptors: a neurohormonal receptor in decapod crustaceans that displays agonist independent activity resulting from an evolutionary alteration to the DRY motif.

Clark Merry C MC Dever Timothy E TE Dever John J JJ Xu Ping P Rehder Vincent V Sosa Maria A MA Baro Deborah J DJ

The Journal of neuroscience : the official journal of the Society for Neuroscience 20040301 13

The stomatogastric nervous system (STNS) is a premiere model for studying modulation of motor pattern generation. Whereas the cellular and network responses to monoamines have been particularly well characterized electrophysiologically, the transduction mechanisms that link the different monoaminergic signals to specific intracellular responses are presently unknown in this system. To begin to elucidate monoaminergic signal transduction in pyloric neurons, we used a bioinformatics approach to pr ...[more]

PMID: 15056722

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Project description:BackgroundThe White Spot Syndrome Virus (WSSV) is an important pathogen that infects a variety of decapod species and causes a highly contagious disease in penaeid shrimps. Mass mortalities caused by WSSV have pronounced commercial impact on shrimp aquaculture. Until now WSSV is the only known member of the virus family Nimaviridae, a group with obscure phylogenetic affinities. Its isolated position makes WSSV studies challenging due to large number of genes without homology in other viruses or cellular organisms.ResultsHere we report the discovery of an unusually large amount of sequences with high similarity to WSSV in a genomic library from the Jamaican bromeliad crab Metopaulias depressus. De novo assembly of these sequences allowed for the partial reconstruction of the genome of this endogenized virus with total length of 200 kbp encompassed in three scaffolds. The genome includes at least 68 putative open reading frames with homology in WSSV, most of which are intact. Among these, twelve orthologs of WSSV genes coding for non-structural proteins and nine genes known to code for the major components of the WSSV virion were discovered. Together with reanalysis of two similar cases of WSSV-like sequences in penaeid shrimp genomic libraries, our data allowed comparison of gene composition and gene order between different lineages related to WSSV. Furthermore, screening of published sequence databases revealed sequences with highest similarity to WSSV and the newly described virus in genomic libraries of at least three further decapod species. Analysis of the viral sequences detected in decapods suggests that they are less a result of contemporary WSSV infection, but rather originate from ancestral infection events. Phylogenetic analyses suggest that genes were acquired repeatedly by divergent viruses or viral strains of the Nimaviridae.ConclusionsOur results shed new light on the evolution of the Nimaviridae and point to a long association of this viral group with decapod crustaceans.

Project description:Crustaceans express genes for at least three classes of putative chemosensory proteins. These are: Ionotropic Receptors (IRs), derived from the heterotetrameric ionotropic glutamate receptors (iGluRs); Transient Receptor Potential (TRP) channels, a diverse set of sensor-channels that include several families of chemoreceptor channels; and Gustatory Receptor Like receptors (GRLs), ionotropic receptors that are homologues of Gustatory Receptors (GRs) of insects and are expressed sparingly in most crustaceans so far studied. IRs are typically numerically the most dominant of these receptor proteins in crustaceans and include two classes: co-receptor IRs, which are necessary for making a functional receptor-channel; and tuning IRs, whose specific combination in the IR subunits in the heterotetramer confers chemical specificity. Previous work showed that the transcriptomes from two major chemosensory organs-the lateral flagellum of the antennule (LF) and the tips of the legs (dactyls)-of the Caribbean spiny lobster Panulirus argus express four co-receptor IRs and over 100 tuning IRs. In this paper, we examined and compared the transcriptomes from the LF and dactyls of P. argus and three other decapod crustaceans-the clawed lobster Homarus americanus, red swamp crayfish Procambarus clarkii, and the blue crab Callinectes sapidus. Each species has at least ca. 100 to 250 IRs, 1 to 4 GRLs, and ca. 15 TRP channels including those shown to be involved in chemoreception in other species. The IRs show different degrees of phylogenetic conservation: some are arthropod-conserved, others are pancrustacean-conserved, others appear to be crustacean-conserved, and some appear to be species-specific. Many IRs appear to be more highly expressed in the LF than dactyl. Our results show that decapod crustaceans express an abundance of genes for chemoreceptor proteins of different types, phylogenetic conservation, and expression patterns. An understanding of their functional roles awaits determining their expression patterns in individual chemosensory neurons and the central projections of those neurons.

Project description:BackgroundThe complex life cycle of the coconut crab, Birgus latro, begins when an obligate terrestrial adult female visits the intertidal to hatch zoea larvae into the surf. After drifting for several weeks in the ocean, the post-larval glaucothoes settle in the shallow subtidal zone, undergo metamorphosis, and the early juveniles then subsequently make their way to land where they undergo further physiological changes that prevent them from ever entering the sea again. Here, we sequenced, assembled and analyzed the coconut crab genome to shed light on its adaptation to terrestrial life. For comparison, we also assembled the genomes of the long-tailed marine-living ornate spiny lobster, Panulirus ornatus, and the short-tailed marine-living red king crab, Paralithodes camtschaticus. Our selection of the latter two organisms furthermore allowed us to explore parallel evolution of the crab-like form in anomurans.ResultsAll three assembled genomes are large, repeat-rich and AT-rich. Functional analysis reveals that the coconut crab has undergone proliferation of genes involved in the visual, respiratory, olfactory and cytoskeletal systems. Given that the coconut crab has atypical mitochondrial DNA compared to other anomurans, we argue that an abundance of kif22 and other significantly proliferated genes annotated with mitochondrial and microtubule functions, point to unique mechanisms involved in providing cellular energy via nuclear protein-coding genes supplementing mitochondrial and microtubule function. We furthermore detected in the coconut crab a significantly proliferated HOX gene, caudal, that has been associated with posterior development in Drosophila, but we could not definitively associate this gene with carcinization in the Anomura since it is also significantly proliferated in the ornate spiny lobster. However, a cuticle-associated coatomer gene, gammacop, that is significantly proliferated in the coconut crab, may play a role in hardening of the adult coconut crab abdomen in order to mitigate desiccation in terrestrial environments.ConclusionThe abundance of genomic features in the three assembled genomes serve as a source of hypotheses for future studies of anomuran environmental adaptations such as shell-utilization, perception of visual and olfactory cues in terrestrial environments, and cuticle sclerotization. We hypothesize that the coconut crab exhibits gene proliferation in lieu of alternative splicing as a terrestrial adaptation mechanism and propose life-stage transcriptomic assays to test this hypothesis.

Dataset Information

Arthropod 5-HT2 receptors: a neurohormonal receptor in decapod crustaceans that displays agonist independent activity resulting from an evolutionary alteration to the DRY motif.

Publications

Arthropod 5-HT2 receptors: a neurohormonal receptor in decapod crustaceans that displays agonist independent activity resulting from an evolutionary alteration to the DRY motif.

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