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Vol. 32, No. 1, 2010
Issue release date: March 2010
Section title: Original Paper
Free Access
Dev Neurosci 2010;32:1–18
(DOI:10.1159/000235758)

A Putative ‘Pre-Nervous’ Endocannabinoid System in Early Echinoderm Development

Buznikov G.A.b · Nikitina L.A.b · Bezuglov V.V.a · Francisco M.E.Y.b · Boysen G.f · Obispo-Peak I.N.b · Peterson R.E.b, d · Weiss E.R.b · Schuel H.g · Temple B.R.S.e · Morrow A.L.c · Lauder J.M.b
aShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russia; bDepartment of Cell and Developmental Biology, and cDepartment of Psychiatry and Bowles Center for Alcohol Studies, University of North Carolina School of Medicine (UNCSM), and dConfocal Imaging Core, Neuroscience Center, UNCSM, and eR.L. Juliano Structural Bioinformatics Core Facility, University of North Carolina, and fDepartment of Environmental Sciences and Engineering, and Center of Environmental Health and Susceptibility, School of Public Health, University of North Carolina, Chapel Hill, N.C., and gDivision of Anatomy and Cell Biology, Department of Pathology and Anatomical Sciences, School of Medicine, State University of New York at Buffalo, Buffalo, N.Y., USA
email Corresponding Author

Abstract

Embryos and larvae of sea urchins (Lytechinus variegatus, Strongylocentrotus droebachiensis, Strongylocentrotus purpuratus, Dendraster excentricus), and starfish (Pisaster ochraceus) were investigated for the presence of a functional endocannabinoid system. Anandamide (arachidonoyl ethanolamide, AEA), was measured in early L. variegatus embryos by liquid chromatography/mass spectrometry. AEA showed a strong developmental dynamic, increasing more than 5-fold between the 8–16 cell and mid-blastula 2 stage. ‘Perturb-and-rescue’ experiments in different sea urchin species and starfish showed that AEA blocked transition of embryos from the blastula to the gastrula stage, but had no effect on cleavage divisions, even at high doses. The non-selective cannabinoid receptor agonist, CP55940, had similar effects, but unlike AEA, also blocked cleavage divisions. CB1 antagonists, AEA transport inhibitors, and the cation channel transient membrane potential receptor V1 (TrpV1) agonist, arachidonoyl vanillic acid (arvanil), as well as arachidonoyl serotonin and dopamine (AA-5-HT, AA-DA) acted as rescue substances, partially or totally preventing abnormal embryonic phenotypes elicited by AEA or CP55940. Radioligand binding of [3H]CP55940 to membrane preparations from embryos/larvae failed to show significant binding, consistent with the lack of CB receptor orthologs in the sea urchin genome. However, when binding was conducted on whole cell lysates, a small amount of [3H]CP55940 binding was observed at the pluteus stage that was displaced by the CB2 antagonist, SR144528. Since AEA is known to bind with high affinity to TrpV1 and to certain G-protein-coupled receptors (GPCRs), the ability of arvanil, AA-5-HT and AA-DA to rescue embryos from AEA teratogenesis suggests that in sea urchins AEA and other endocannabinoids may utilize both Trp and GPCR orthologs. This possibility was explored using bioinformatic and phylogenetic tools to identify candidate orthologs in the S. purpuratus sea urchin genome. Candidate TrpA1 and TrpV1 orthologs were identified. The TrpA1 ortholog fell within a monophyletic clade, including both vertebrate and invertebrate orthologs, whereas the TrpV1 orthologs fell within two distinct TrpV-like invertebrate clades. One of the sea urchin TrpV orthologs was more closely related to the vertebrate epithelial calcium channels (TrpV5-6 family) than to the vertebrate TrpV1-4 family, as determined using profile-hidden Markov model (HMM) searches. Candidate dopamine and adrenergic GPCR orthologs were identified in the sea urchin genome, but no cannabinoid GPCRs were found, consistent with earlier studies. Candidate dopamine D1, D2 or α1-adrenergic receptor orthologs were identified as potential progenitors to the vertebrate cannabinoid receptors using HMM searches, depending on whether the multiple sequence alignment of CB receptor sequences consisted only of urochordate and cephalochordate sequences or also included vertebrate sequences.

© 2009 S. Karger AG, Basel


  

Key Words

  • Anandamide
  • Arachidonoyl ethanolamide
  • Sea urchin
  • Starfish
  • Embryo/larvae
  • Development
  • Morphogens
  • Gastrulation
  • Phylogeny
  • Neurotransmitter
  • Vanilloid receptors

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Author Contacts

Dr. Jean M. Lauder
Department of Cell and Developmental Biology
University of North Carolina School of Medicine
Chapel Hill, NC 27599-7090 (USA)
Tel. +1 919 966 5020, Fax +1 919 966 1856, E-Mail unclau@med.unc.edu

  

Article Information

Received: February 6, 2009
Accepted after revision: August 17, 2009
Published online: November 12, 2009
Number of Print Pages : 18
Number of Figures : 8, Number of Tables : 3, Number of References : 102
Additional supplementary material is available online - Number of Parts : 1

  

Publication Details

Developmental Neuroscience

Vol. 32, No. 1, Year 2010 (Cover Date: March 2010)

Journal Editor: Levison S.W. (Newark, N.J.)
ISSN: 0378-5866 (Print), eISSN: 1421-9859 (Online)

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