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

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.

Novel markers identify nervous system components of the holothurian nervous system

“…A recent report characterizing the distribution of FMRFamide- and histamine-like immunoreactivities in the nervous system of L. clarki (Hoekstra et al 2012) provides for a comparison of the results obtained in this species with our three novel markers. In general terms, the immunoreactivity of all the antibodies is found within the same structures, in small subset of cells and fibers.…”

A START-domain-containing protein is a novel marker of nervous system components of the sea cucumber Holothuria glaberrima

“…In general, the markers fall into two large categories; the first being those antibodies that recognize what are supposed to be the echinoderm homologs of the antigens recognized by the antibodies in other animal species. Here we find antibodies to neurotransmitters such as serotonin (Murabe et al 2008), GABA (Newman and Thorndyke 1994) and histamine (Hoekstra et al 2012) or to their synthesizing enzymes, such as tyrosine hydroxylase (Diaz-Balzac et al 2010). Other antibodies recognize echinoderm peptides (Diaz-Miranda et al 1995), or proteins associated with the nervous system such as synaptotagmin (Burke et al 2006), calbindin (Diaz-Balzac et al 2012) or β-tubulin (Diaz-Balzac et al 2016).…”

Evolution of basal deuterostome nervous systems

“…The nerve ring and the outer parts of the nerve cord belong to the ectonerual compartment, whereas the inner layer of the nerve cords is the hyponeural system. These two systems were thought to be separate; however, fine-structural studies and histochemistry of neurotransmitters in sea cucumbers have indicated that both systems are derived from ectoderm and are interconnected (Mashanov et al, 2007;Hoekstra et al, 2012). Moreover, Echinoderms also have numerous ectodermal sensory cells.…”