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      Novel Insights into the Echinoderm Nervous System from Histaminergic and FMRFaminergic-Like Cells in the Sea Cucumber Leptosynapta clarki

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      1 , 2 , 1 , 3 , 4 , 1 , 5 , *
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          Abstract

          Understanding of the echinoderm nervous system is limited due to its distinct organization in comparison to other animal phyla and by the difficulty in accessing it. The transparent and accessible, apodid sea cucumber Leptosynapta clarki provides novel opportunities for detailed characterization of echinoderm neural systems. The present study used immunohistochemistry against FMRFamide and histamine to describe the neural organization in juvenile and adult sea cucumbers. Histaminergic- and FMRFaminergic-like immunoreactivity is reported in several distinct cell types throughout the body of L. clarki. FMRFamide-like immunoreactive cell bodies were found in the buccal tentacles, esophageal region and in proximity to the radial nerve cords. Sensory-like cells in the tentacles send processes toward the circumoral nerve ring, while unipolar and bipolar cells close to the radial nerve cords display extensive processes in close association with muscle and other cells of the body wall. Histamine-like immunoreactivity was identified in neuronal somatas located in the buccal tentacles, circumoral nerve ring and in papillae distributed across the body. The tentacular cells send processes into the nerve ring, while the processes of cells in the body wall papillae extend to the surface epithelium and radial nerve cords. Pharmacological application of histamine produced a strong coordinated, peristaltic response of the body wall suggesting the role of histamine in the feeding behavior. Our immunohistochemical data provide evidence for extensive connections between the hyponeural and ectoneural nervous system in the sea cucumber, challenging previously held views on a clear functional separation of the sub-components of the nervous system. Furthermore, our data indicate a potential function of histamine in coordinated, peristaltic movements; consistent with feeding patterns in this species. This study on L. clarki illustrates how using a broader range of neurotransmitter systems can provide better insight into the anatomy, function and evolution of echinoderm nervous sytems.

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          Most cited references36

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          A genomic view of the sea urchin nervous system.

          The sequencing of the Strongylocentrotus purpuratus genome provides a unique opportunity to investigate the function and evolution of neural genes. The neurobiology of sea urchins is of particular interest because they have a close phylogenetic relationship with chordates, yet a distinctive pentaradiate body plan and unusual neural organization. Orthologues of transcription factors that regulate neurogenesis in other animals have been identified and several are expressed in neurogenic domains before gastrulation indicating that they may operate near the top of a conserved neural gene regulatory network. A family of genes encoding voltage-gated ion channels is present but, surprisingly, genes encoding gap junction proteins (connexins and pannexins) appear to be absent. Genes required for synapse formation and function have been identified and genes for synthesis and transport of neurotransmitters are present. There is a large family of G-protein-coupled receptors, including 874 rhodopsin-type receptors, 28 metabotropic glutamate-like receptors and a remarkably expanded group of 161 secretin receptor-like proteins. Absence of cannabinoid, lysophospholipid and melanocortin receptors indicates that this group may be unique to chordates. There are at least 37 putative G-protein-coupled peptide receptors and precursors for several neuropeptides and peptide hormones have been identified, including SALMFamides, NGFFFamide, a vasotocin-like peptide, glycoprotein hormones and insulin/insulin-like growth factors. Identification of a neurotrophin-like gene and Trk receptor in sea urchin indicates that this neural signaling system is not unique to chordates. Several hundred chemoreceptor genes have been predicted using several approaches, a number similar to that for other animals. Intriguingly, genes encoding homologues of rhodopsin, Pax6 and several other key mammalian retinal transcription factors are expressed in tube feet, suggesting tube feet function as photosensory organs. Analysis of the sea urchin genome presents a unique perspective on the evolutionary history of deuterostome nervous systems and reveals new approaches to investigate the development and neurobiology of sea urchins.
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            Structure of a molluscan cardioexcitatory neuropeptide.

            A cardioexcitatory substance from ganglia of the clam Macrocallista nimbosa, formerly designated peak C, is the tetrapeptide amide Phe-Met-Arg-Phe-NH2. Its structure was determined by the combined use of Edman dansyl degradation and tryptic digestion. The structure was confirmed by synthesis. This neuropeptide is active at about 10(-8)M when assayed on molluscan muscle.
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              The evolution of nervous system patterning: insights from sea urchin development.

              Recent studies of the sea urchin embryo have elucidated the mechanisms that localize and pattern its nervous system. These studies have revealed the presence of two overlapping regions of neurogenic potential at the beginning of embryogenesis, each of which becomes progressively restricted by separate, yet linked, signals, including Wnt and subsequently Nodal and BMP. These signals act to specify and localize the embryonic neural fields - the anterior neuroectoderm and the more posterior ciliary band neuroectoderm - during development. Here, we review these conserved nervous system patterning signals and consider how the relationships between them might have changed during deuterostome evolution.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                6 September 2012
                : 7
                : 9
                : e44220
                Affiliations
                [1 ]Friday Harbor Laboratories, University of Washington, Seattle, Washington, United States of America
                [2 ]Department of Biology, Indiana University, Bloomington, Indiana, United States of America
                [3 ]The Whitney Laboratory for Marine Bioscience, University of Florida, Gainesville, Florida, United States of America
                [4 ]Department of Neuroscience, University of Florida, Gainesville, Florida, United States of America
                [5 ]Integrative Biology, University of Guelph, Guelph, Ontario, Canada
                University of Gothenburg, Sweden
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LAH AH. Performed the experiments: LAH LLM AH. Analyzed the data: LAH AH. Contributed reagents/materials/analysis tools: LLM AH. Wrote the paper: LAH AH.

                Article
                PONE-D-12-15259
                10.1371/journal.pone.0044220
                3435416
                22970182
                8c0dfdd8-efd5-49b6-840b-eae9f88b9667
                Copyright @ 2012

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 25 May 2012
                : 3 August 2012
                Page count
                Pages: 11
                Funding
                The authors acknowledge funding from the Washington Research Foundation to LAH, the NSERC Discovery Grant (400230) and McKnight Brain Research Foundation Funds to AH, as well as UF Opportunity Funds, NSF IOS-1146575, NSF CNS-0821622, United States National Institutes of Health (NIH) 5R01GM097502, NIH 5R21RR025699 and NIH 5R21DA030118 to LLM. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Neurological System
                Motor Systems
                Nerve Tissue
                Nervous System Components
                Nervous System Physiology
                Neuroanatomy
                Sensory Physiology
                Marine Biology
                Neuroscience
                Cellular Neuroscience
                Neuronal Morphology
                Sensory Systems
                Gustatory System
                Olfactory System
                Neurotransmitters
                Zoology
                Animal Behavior
                Animal Physiology
                Comparative Anatomy

                Uncategorized
                Uncategorized

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