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PLOS ONE  2012 

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

DOI: 10.1371/journal.pone.0044220

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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.


[1]  Bourlat SJ, Nielsen C, Lockyer AE, Littlewood DTJ, Telford MJ (2003) Xenoturbella is a deuterostome that eats molluscs. Nature 424: 925–928.
[2]  Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, et al. (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470: 255?+.
[3]  Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, et al. (2006) A genomic view of the sea urchin nervous system. Developmental Biology 300: 434–460.
[4]  Angerer LM, Yaguchi S, Angerer RC, Burke RD (2011) The evolution of nervous system patterning: insights from sea urchin development. Development 138: 3613–3623.
[5]  Burke RD (2011) Deuterostome neuroanatomy and the body plan paradox. Evolution & Development 13: 110–115.
[6]  Hyman LH (1955) The Invertebrates: Echinodermata. New York: McGraw-Hill.
[7]  Cobb JLS (1987) Neurobiology of the echinodermata. In: Ali MA, editor. Invertebrate Nervous Systems. New York: Plenum Press. 483–525.
[8]  Cobb JLS, Stubbs TR (1981) The giant-neuron system in Ophiuroids. 1. The general morphology of the radial nerve cords and circumoral nerve ring. Cell and Tissue Research 219: 197–207.
[9]  Cobb JLS, Stubbs TR (1982) The giant-neuron system in Ophiuroids. 3. The detailed connections of the circumoral nerve ring. Cell and Tissue Research 226: 675–687.
[10]  Stubbs TR, Cobb JLS (1981) The giant-neuron system in Ophiuroids. 2. The hyponeural motor tracts. Cell and Tissue Research 220: 373–385.
[11]  Peters BH (1985) The innervation of spines in the sea-urchin Echinus esculentus L - an electron-microscopic study. Cell and Tissue Research 239: 219–228.
[12]  Heinzeller T, Welsch U (2001) The echinoderm nervous system and its phylogenetic interpretation. In: Roth G, Wullimann MF, editors. Brain Evolution and Cognition. New York: John Wiley & Sons, Inc. 41–75.
[13]  Mashanov VS, Dolmatov IY (2004) Functional morphology of the developing alimentary canal in the holothurian Eupentacta fraudatrix (Holothuroidea, Dendrochirota). Acta Zoologica 85: 29–39.
[14]  Mashanov VS, Zueva OR, Heinzeller T, Dolmatov IY (2006) Ultrastructure of the circumoral nerve ring and the radial nerve cords in holothurians (Echinodermata). Zoomorphology 125: 27–38.
[15]  Mashanov VS, Zueva OR, Garcia-Arraras JE (2010) Organization of glial cells in the adult sea cucumber central nervous system. Glia 58: 1581–1593.
[16]  Vandenspiegel D, Flammang P, Fourmeau D, Jangoux M (1995) Fine-structure of the dorsal papillae in the holothurioid Holothuria forskali (Echinodermata). Tissue & Cell 27: 457–465.
[17]  Garcia-Arraras JE, Rojas-Soto M, Jimenez LB, Diaz-Miranda L (2001) The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analysis. Journal of Experimental Biology 204: 865–873.
[18]  Diaz-Balzac CA, Santacana-Laffitte G, Miguel-Ruiz JES, Tossas K, Valentin-Tirado G, et al. (2007) Identification of nerve plexi in connective tissues of the sea cucumber Holothuria glaberrima by using a novel nerve-specific antibody. Biological Bulletin 213: 28–42.
[19]  Diaz-Balzac CA, Abreu-Arbelo JE, Garcia-Arraras JE (2010) Neuroanatomy of the tube feet and tentacles in Holothuria glaberrima (Holothuroidea, Echinodermata). Zoomorphology 129: 33–43.
[20]  Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Dolmatov IY (2007) Developmental origin of the adult nervous system in a holothurian: an attempt to unravel the enigma of neurogenesis in echinoderms. Evolution & Development 9: 244–256.
[21]  Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197: 670–671.
[22]  Walker RJ, Papaioannou S, Holden-Dye L (2009) A review of FMRFamide- and RFamide-like peptides in metazoa. Invertebrate Neuroscience 9: 111–153.
[23]  Elphick MR, Newman SJ, Thorndyke MC (1995) Distribution and action of SALMFamide neuropeptides in the starfish Asterias rubens. Journal of Experimental Biology 198: 2519–2525.
[24]  Muneoka Y, Morishita F, Furukawa Y, Matsushima O, Kobayashi M, et al. (2000) Comparative aspects of invertebrate neuropeptides. Acta Biologica Hungarica 51: 111–132.
[25]  Diaz-Miranda L, Price DA, Greenberg MJ, Lee TD, Doble KE, et al. (1992) Characterization of two novel neuropeptides from the sea cucumber Holothuria glaberrima. The Biological Bulletin 182: 241–247.
[26]  Birenheide R, Tamori M, Motokawa T, Ohtani M, Iwakoshi E, et al. (1998) Peptides controlling stiffness of connective tissue in sea cucumbers. Biological Bulletin 194: 253–259.
[27]  Inoue M, Birenheide R, Koizumi O, Kobayakawa Y, Muneoka Y, et al. (1999) Localization of the neuropeptide NGIWYamide in the holothurian nervous system and its effects on muscular contraction. Proceedings of the Royal Society B-Biological Sciences 266: 993–1000.
[28]  Garcia-Arraras JE, Enamorado-Ayala I, Torres-Avillan I, Rivera V (1991) FMRFamide-like immunoreactivity in cells and fibers of the holothurian nervous system. Neuroscience Letters 132: 199–202.
[29]  Witte I, Kreienkamp HJ, Gewecke M, Roeder T (2002) Putative histamine-gated chloride channel subunits of the insect visual system and thoracic ganglion. Journal of Neurochemistry 83: 504–514.
[30]  McCoole MD, Baer KN, Christie AE (2011) Histaminergic signaling in the central nervous system of Daphnia and a role for it in the control of phototactic behavior. Journal of Experimental Biology 214: 1773–1782.
[31]  Weiss KR, Chiel HJ, Koch U, Kupfermann I (1986) Activity of an Identified Histaminergic Neuron, and Its Possible Role in Arousal of Feeding-Behavior in Semi-Intact Aplysia. Journal of Neuroscience 6: 2403–2415.
[32]  Jacobs EH, Yamatodani A, Timmerman H (2000) Is histamine the final neurotransmitter in the entrainment of circadian rhythms in mammals? Trends in Pharmacological Sciences 21: 293–298.
[33]  Emanuel MB (1999) Histamine and the antiallergic antihistamines: a history of their discoveries. Clinical and Experimental Allergy 29: 1–11.
[34]  Smith SL (1992) Investigation of histamine in echinoderms. University of South Florida: 89.
[35]  Leguia M, Wessel GM (2006) The histamine H1 receptor activates the nitric oxide pathway at fertilization. Molecular Reproduction and Development 73: 1550–1563.
[36]  Swanson RL, Williamson JE, De Nys R, Kumar N, Bucknall MP, et al. (2004) Induction of settlement of larvae of the sea urchin Holopneustes purpurascens by histamine from a host alga. Biological Bulletin 206: 161–172.
[37]  Swanson RL, Marshall DJ, Steinberg PD (2007) Larval desperation and histamine: how simple responses can lead to complex changes in larval behaviour. Journal of Experimental Biology 210: 3228–3235.
[38]  Sutherby J, Giardini J-L, Nguyen J, Wessel G, Leguia M, et al. (2012) Histamine is a modulator of metamorphic competence in Strongylocentrotus purpuratus (Echinodermata: Echinoidea). BMC Developmental Biology 12: 14.
[39]  Lambert P (1997) Sea cucumbers of British Columbia, southeast Alaska and Puget Sound. Vancouver: University of British Columbia Press.
[40]  Sewell MA (1994) Birth, recruitment and juvenile growth in the intraovarian brooding sea-cucumber Leptosynapta clarki. Marine Ecology-Progress Series 114: 149–156.
[41]  Rasband WS (1997–2011) ImageJ. U.S. National Institutes of Health, Bethedsa, Maryland, USA.
[42]  Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International. 36–42.
[43]  Muneoka Y, Iwakoshi E, Ohtani M, Takahashi T, Teranishi H, et al. (1995) Bioactive peptides isolated from the sea cucumber Stichopus japonicus: I. Actions on muscle tissues. Zoological Science (Tokyo) 12: 105.
[44]  Diaz-Miranda L, Blanco RE, Garcia-Arraras JE (1995) Localization of the heptapeptide GFSKLYFamide in the sea cucumber Holothuria glaberrima (Echinodermata): a light and electron microscopic study. The Journal of comparative neurology 352: 626–640.
[45]  Diaz-Miranda L, Garcia-Arraras JE (1995) Pharmacological action of the heptapeptide GFSKLYFamide in the muscle of the sea cucumber Holothuria glaberrima (Echinodermata). Comparative Biochemistry and Physiology Part C, Pharmacology, toxicology & endocrinology 110: 171–176.
[46]  Cobb JLS (1985) The neurobiology of the ectoneural hyponeural synaptic connection in an echinoderm. Biological Bulletin 168: 432–446.
[47]  Takahashi K, editor (1966) Muscle physiology. New York: Interscience. 513–527.
[48]  Hill RB, editor (1993) Comparative physiology of echinoderm muscle. Rotterdam: A.A. Balkema.
[49]  Motokawa T (1984) Connective-tissue catch in Echinoderms. Biological Reviews of the Cambridge Philosophical Society 59: 255–270.
[50]  Uexküll Jv (1900) Die physiologie des Seeigelstachels. Z Biol 39: 73–112.
[51]  Elphick MR, Melarange R (2001) Neural control of muscle relaxation in echinoderms. Journal of Experimental Biology 204: 875–885.
[52]  Wyman LC, Lutz BR (1930) The action of adrenaline and certain drugs on the isolated holothurian cloaca. Journal of Experimental Zoology 57: 441–453.
[53]  Von Euler US, Chaves N, Teodosio N (1952) Effect of acetylcholine, noradrenaline, adrenaline and histamine on isolated organs of Aplysia and Holothuria. Acta Physiologica Latino Americana 2: 101–106.
[54]  Kobzar GT (1984) Muscle chemorecptors in the Holothurian Cucumaria japonica. Zhurnal Evolyutsionnoi Biokhimii i Fiziologii 20: 419–422.
[55]  Altieri SMDL, Mendes EG (1986) The responses of the longitudinal muscles of Holothuria Grisea selenka 1867 to drugs: a quantitative approach. Boletim de Fisiologia Animal (Sao Paulo) 10: 21–40.
[56]  Mendes EG, Abbud L, Ancona Lopez AA (1970) Pharmacological studies on the invertebrate non-striated muscles Part 1: The response to drugs. Comparative and General Pharmacology 1: 11–22.
[57]  Protas LL, Muske GA (1980) Effects of some transmitter substances on the tube foot muscles of the starfish, Asterias amurensis (Lutken). General Pharmacology 11: 113–118.
[58]  Lorenz W, Matejka E, Schmal HJ, Seidel W, Reimann HJ, et al. (1973) A phylogentic study on the occurence and distribution of histamine in the gastro-intestinal tract and other tissues of man and various animals. Comparative and General Pharmacology 4: 229–250.
[59]  Reite OB (1972) Comparative physiology of histamine. Physiological Reviews 52: 778–819.
[60]  Mettrick DF, Telford JM (1965) Histamine content and histidine decarboxylase activity of some marine and terrestrial animals from West Indies. Comparative Biochemistry and Physiology 16: 547–559.
[61]  Swanson RL, de Nys R, Huggett MJ, Green JK, Steinberg PD (2006) In situ quantification of a natural settlement cue and recruitment of the Australian sea urchin Holopneustes purpurascens. Marine Ecology-Progress Series 314: 1–14.
[62]  Swanson R, Byrne M, Prowse T, Mos B, Dworjanyn S, et al. (2012) Dissolved histamine: a potential habitat marker promoting settlement and metamorphosis in sea urchin larvae. Marine Biology 159: 915–925.
[63]  Lai ZC, Maxson R, Childs G (1988) Both basal and ontogenetic promoter elements affect the timing and level of expression of a sea-urchin H-1 gene during early embryogenesis. Genes and Development 2: 173–183.
[64]  Leguia M, Wessel GM (2004) The histamine H1 receptor stimulates the nitric oxide pathway leading to calcium release at fertilization. Molecular Biology of the Cell 15: 431A–431A.


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