ECB-ART-39926
Dev Biol
2006 Dec 01;3001:434-60. doi: 10.1016/j.ydbio.2006.08.007.
Show Gene links
Show Anatomy links
A genomic view of the sea urchin nervous system.
Burke RD
,
Angerer LM
,
Elphick MR
,
Humphrey GW
,
Yaguchi S
,
Kiyama T
,
Liang S
,
Mu X
,
Agca C
,
Klein WH
,
Brandhorst BP
,
Rowe M
,
Wilson K
,
Churcher AM
,
Taylor JS
,
Chen N
,
Murray G
,
Wang D
,
Mellott D
,
Olinski R
,
Hallböök F
,
Thorndyke MC
.
Abstract
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.
PubMed ID: 16965768
PMC ID: PMC1950334
Article link: Dev Biol
Grant support: [+]
HD22619 NICHD NIH HHS , Z01 DE000712-02 Intramural NIH HHS, EY11930 NEI NIH HHS , S19916 Biotechnology and Biological Sciences Research Council , R01 HD022619 NICHD NIH HHS , R01 EY011930 NEI NIH HHS
Genes referenced: LOC100887844 LOC100888955 LOC105444438 LOC115925415 ntf5 pax6 rhol2
References [+] :
Adams,
A peptide fragment of ependymin neurotrophic factor uses protein kinase C and the mitogen-activated protein kinase pathway to activate c-Jun N-terminal kinase and a functional AP-1 containing c-Jun and c-Fos proteins in mouse NB2a cells.
2003, Pubmed
Adams, A peptide fragment of ependymin neurotrophic factor uses protein kinase C and the mitogen-activated protein kinase pathway to activate c-Jun N-terminal kinase and a functional AP-1 containing c-Jun and c-Fos proteins in mouse NB2a cells. 2003, Pubmed
Adayev, Transmembrane signaling in the brain by serotonin, a key regulator of physiology and emotion. 2005, Pubmed
Aizenberg, Calcitic microlenses as part of the photoreceptor system in brittlestars. 2001, Pubmed , Echinobase
Alioto, The odorant receptor repertoire of teleost fish. 2005, Pubmed
Araç, Close membrane-membrane proximity induced by Ca(2+)-dependent multivalent binding of synaptotagmin-1 to phospholipids. 2006, Pubmed
Avery, In vitro exocytosis in sea urchin eggs requires a synaptobrevin-related protein. 1997, Pubmed , Echinobase
Bailey, Regulation of vertebrate eye development by Rx genes. 2004, Pubmed
Baker, Vertebrate cranial placodes I. Embryonic induction. 2001, Pubmed
Bassham, The evolutionary history of placodes: a molecular genetic investigation of the larvacean urochordate Oikopleura dioica. 2005, Pubmed
Beer, Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris. 2001, Pubmed , Echinobase
Benito-Gutiérrez, The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells. 2005, Pubmed
Berghard, A novel family of ancient vertebrate odorant receptors. 1998, Pubmed
Bertrand, Proneural genes and the specification of neural cell types. 2002, Pubmed
Bisgrove, Development of Serotonergic Neurons in Embryos of the Sea Urchin, Strongylocentrotus purpuratus: (serotonergic/neural development/embryo/echinoid). 1986, Pubmed , Echinobase
Blevins, Spatial vision in the echinoid genus Echinometra. 2004, Pubmed , Echinobase
Boyl, Otx genes in the development and evolution of the vertebrate brain. 2001, Pubmed
Brown, Math5 is required for retinal ganglion cell and optic nerve formation. 2001, Pubmed
Burke, Neuron-specific expression of a synaptotagmin gene in the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Burke, The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus. 1978, Pubmed , Echinobase
Burke, A genomic view of the sea urchin nervous system. 2006, Pubmed
Cameron, Initiation of metamorphosis in laboratory cultured sea urchins. 1974, Pubmed , Echinobase
Campbell, Piecing together evolution of the vertebrate endocrine system. 2004, Pubmed
Cazzamali, Molecular cloning and functional expression of a Drosophila corazonin receptor. 2002, Pubmed
Chan, SpCOUP-TF: a sea urchin member of the steroid/thyroid hormone receptor family. 1992, Pubmed , Echinobase
Chan, Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus. 1990, Pubmed
Chang, Evidence for a cannabinoid receptor in sea urchin sperm and its role in blockade of the acrosome reaction. 1993, Pubmed , Echinobase
Chenna, Multiple sequence alignment with the Clustal series of programs. 2003, Pubmed
Clandinin, Surprising twists to exocyst function. 2005, Pubmed
Clyne, A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. 1999, Pubmed
Cobb, The significance of the radial nerve cords in asteroids and echinoids. 1970, Pubmed , Echinobase
Cobb, Anatomical studies of simple invertebrate synapses utilizing stage rotation election microscopy and densitometry. 1977, Pubmed , Echinobase
Conlon, Evolution of the insulin molecule: insights into structure-activity and phylogenetic relationships. 2001, Pubmed
Conner, Members of the SNARE hypothesis are associated with cortical granule exocytosis in the sea urchin egg. 1997, Pubmed , Echinobase
Croce, Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. 2006, Pubmed , Echinobase
Croce, A genome-wide survey of the evolutionarily conserved Wnt pathways in the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Czerny, DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). 1995, Pubmed , Echinobase
Czerny, The characterization of novel Pax genes of the sea urchin and Drosophila reveal an ancient evolutionary origin of the Pax2/5/8 subfamily. 1997, Pubmed , Echinobase
Davis, Drosophila retinal homeobox (drx) is not required for establishment of the visual system, but is required for brain and clypeus development. 2003, Pubmed
Dehal, The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. 2002, Pubmed
Di Bernardo, Spatially restricted expression of PlOtp, a Paracentrotus lividus orthopedia-related homeobox gene, is correlated with oral ectodermal patterning and skeletal morphogenesis in late-cleavage sea urchin embryos. 1999, Pubmed , Echinobase
Donner, Conservation and non-conservation of genetic pathways in eye specification. 2004, Pubmed
Elphick, Neural control of muscle relaxation in echinoderms. 2001, Pubmed , Echinobase
Elphick, The neurobiology and evolution of cannabinoid signalling. 2001, Pubmed , Echinobase
Elphick, The invertebrate ancestry of endocannabinoid signalling: an orthologue of vertebrate cannabinoid receptors in the urochordate Ciona intestinalis. 2003, Pubmed
Elphick, The phylogenetic distribution and evolutionary origins of endocannabinoid signalling. 2005, Pubmed
Elphick, The SALMFamides: a new family of neuropeptides isolated from an echinoderm. 1991, Pubmed , Echinobase
Elphick, Nitric Oxide Function in an Echinoderm. 1998, Pubmed , Echinobase
Elphick, Molecular characterisation of SALMFamide neuropeptides in sea urchins. 2005, Pubmed , Echinobase
Ensslen, PTPmu signaling via PKCdelta is instructive for retinal ganglion cell guidance. 2004, Pubmed
Felsenstein, Phylogenies from molecular sequences: inference and reliability. 1988, Pubmed
Fernald, Evolution of eyes. 2000, Pubmed
Florey, Cholinergic motor control of sea urchin tube feet: evidence for chemical transmission without synapses. 1980, Pubmed , Echinobase
Florey, Ultrastructure of sea urchin tube feet. Evidence for connective tissue involvement in motor control. 1977, Pubmed , Echinobase
Fredriksson, The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. 2003, Pubmed
Furukawa, rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. 1997, Pubmed
Gaiddon, Brain-derived neurotrophic factor stimulates AP-1 and cyclic AMP-responsive element dependent transcriptional activity in central nervous system neurons. 1996, Pubmed
Gans, Neural crest and the origin of vertebrates: a new head. 1983, Pubmed
García-Arrarás, The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analysis. 2001, Pubmed , Echinobase
Gautam, Distinct phenotypes of mutant mice lacking agrin, MuSK, or rapsyn. 1999, Pubmed
Gehring, New perspectives on eye development and the evolution of eyes and photoreceptors. 2005, Pubmed
Glaser, Temperature synchronization of the Drosophila circadian clock. 2005, Pubmed
Grens, Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. 1995, Pubmed
Gutman, International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. 2005, Pubmed
Hallböök, Evolution of the vertebrate neurotrophin and Trk receptor gene families. 1999, Pubmed
Hargrave, Rhodopsin's protein and carbohydrate structure: selected aspects. 1984, Pubmed
Hatakeyama, Retinal cell fate determination and bHLH factors. 2004, Pubmed
Hewes, Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. 2001, Pubmed
Heyland, Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development. 2004, Pubmed , Echinobase
Heyland, Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). 2004, Pubmed , Echinobase
Hirayama, Structural and functional features of transcription factors controlling the circadian clock. 2005, Pubmed
Hoffmann, Ependymins: meningeal-derived extracellular matrix proteins at the blood-brain barrier. 1996, Pubmed
Holland, Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate? 2001, Pubmed
Howard-Ashby, Identification and characterization of homeobox transcription factor genes in Strongylocentrotus purpuratus, and their expression in embryonic development. 2006, Pubmed , Echinobase
Howard-Ashby, Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Hsu, Evolution of glycoprotein hormone subunit genes in bilateral metazoa: identification of two novel human glycoprotein hormone subunit family genes, GPA2 and GPB5. 2002, Pubmed
Ishimaru, Two families of candidate taste receptors in fishes. 2005, Pubmed
Jahn, Membrane fusion. 2003, Pubmed
Janer, A comparative study on androgen metabolism in three invertebrate species. 2005, Pubmed , Echinobase
Jeffery, Migratory neural crest-like cells form body pigmentation in a urochordate embryo. 2004, Pubmed
Karnik, Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. 1988, Pubmed
Kenny, SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. 1999, Pubmed , Echinobase
Konopka, Clock mutants of Drosophila melanogaster. 1971, Pubmed
Lapraz, RTK and TGF-beta signaling pathways genes in the sea urchin genome. 2006, Pubmed , Echinobase
Leguia, Selective expression of a sec1/munc18 member in sea urchin eggs and embryos. 2004, Pubmed , Echinobase
Li, Two Otx proteins generated from multiple transcripts of a single gene in Strongylocentrotus purpuratus. 1997, Pubmed , Echinobase
Lindgens, Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. 2004, Pubmed
Lowe, Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. 2003, Pubmed
Luke, Spfkh1 encodes a transcription factor implicated in gut formation during sea urchin development. 1997, Pubmed , Echinobase
Luo, Identification of a stanniocalcin paralog, stanniocalcin-2, in fish and the paracrine actions of stanniocalcin-2 in the mammalian ovary. 2005, Pubmed
Mangelsdorf, The nuclear receptor superfamily: the second decade. 1995, Pubmed
Marsh, Neurotrophin-3 and brain-derived neurotrophic factor activate multiple signal transduction events but are not survival factors for hippocampal pyramidal neurons. 1996, Pubmed
Materna, The C2H2 zinc finger genes of Strongylocentrotus purpuratus and their expression in embryonic development. 2006, Pubmed , Echinobase
Mathers, The Rx homeobox gene is essential for vertebrate eye development. 1997, Pubmed
Mazet, Molecular evidence from ascidians for the evolutionary origin of vertebrate cranial sensory placodes. 2005, Pubmed
Mazet, Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes. 2005, Pubmed
Melarange, Comparative analysis of nitric oxide and SALMFamide neuropeptides as general muscle relaxants in starfish. 2003, Pubmed , Echinobase
Merrow, The circadian cycle: daily rhythms from behaviour to genes. 2005, Pubmed
Miljkovic-Licina, Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system. 2004, Pubmed
Minokawa, Expression patterns of four different regulatory genes that function during sea urchin development. 2004, Pubmed , Echinobase
Mire, Gap junctional communication in the vibration-sensitive response of sea anemones. 2000, Pubmed
Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed
Mu, A gene network downstream of transcription factor Math5 regulates retinal progenitor cell competence and ganglion cell fate. 2005, Pubmed
Mu, A gene regulatory hierarchy for retinal ganglion cell specification and differentiation. 2004, Pubmed
Nakajima, Divergent patterns of neural development in larval echinoids and asteroids. 2004, Pubmed , Echinobase
Nimmrich, The novel ependymin related gene UCC1 is highly expressed in colorectal tumor cells. 2001, Pubmed
Olinski, Three insulin-relaxin-like genes in Ciona intestinalis. 2006, Pubmed
Otim, SpHnf6, a transcription factor that executes multiple functions in sea urchin embryogenesis. 2004, Pubmed , Echinobase
Panchin, Evolution of gap junction proteins--the pannexin alternative. 2005, Pubmed
Pentreath, Neurobiology of echinodermata. 1972, Pubmed , Echinobase
Pentreath, Acetylcholine and cholinesterase in the radial nerve of Asterias rubens. 1968, Pubmed , Echinobase
Pereira-Leal, Evolution of the Rab family of small GTP-binding proteins. 2001, Pubmed
Piront, Inhibition of long-term memory formation by anti-ependymin antisera after active shock-avoidance learning in goldfish. 1988, Pubmed
Poustka, Generation, annotation, evolutionary analysis, and database integration of 20,000 unique sea urchin EST clusters. 2003, Pubmed , Echinobase
Poustka, On the origin of the chordate central nervous system: expression of onecut in the sea urchin embryo. 2004, Pubmed , Echinobase
Raible, Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. 2006, Pubmed , Echinobase
Reinecke, The phylogeny of the insulin-like growth factors. 1998, Pubmed
Revilla-i-Domingo, R11: a cis-regulatory node of the sea urchin embryo gene network that controls early expression of SpDelta in micromeres. 2004, Pubmed , Echinobase
Richmond, The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans. 2002, Pubmed
Roepke, Estradiol and endocrine disrupting compounds adversely affect development of sea urchin embryos at environmentally relevant concentrations. 2005, Pubmed , Echinobase
Samanta, The transcriptome of the sea urchin embryo. 2006, Pubmed , Echinobase
Sasai, Regulation of neural determination by evolutionarily conserved signals: anti-BMP factors and what next? 2001, Pubmed
Satou, A genomewide survey of developmentally relevant genes in Ciona intestinalis. V. Genes for receptor tyrosine kinase pathway and Notch signaling pathway. 2003, Pubmed
Schlosser, Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes. 2005, Pubmed
Schmidt, Neuronal plasticity depending on a glycoprotein synthesized in goldfish leptomeninx. 1992, Pubmed
Schmidt, Antibodies to ependymin block the sharpening of the regenerating retinotectal projection in goldfish. 1988, Pubmed
Schuel, Anandamide (arachidonylethanolamide), a brain cannabinoid receptor agonist, reduces sperm fertilizing capacity in sea urchins by inhibiting the acrosome reaction. 1994, Pubmed , Echinobase
Schulz, Increased association of synaptosome-associated protein of 25 kDa with syntaxin and vesicle-associated membrane protein following acrosomal exocytosis of sea urchin sperm. 1998, Pubmed , Echinobase
Selke, Serine/threonine protein phosphatases type 1, 2A and 2C in vertebrate retinae. 1998, Pubmed
Shashoua, CMX-8933, a peptide fragment of the glycoprotein ependymin, promotes activation of AP-1 transcription factor in mouse neuroblastoma and rat cortical cell cultures. 2001, Pubmed
Shashoua, Classical conditioning leads to changes in extracellular concentrations of ependymin in goldfish brain. 1989, Pubmed
Shashoua, The role of brain extracellular proteins in neuroplasticity and learning. 1985, Pubmed
Shashoua, Ependymin, a brain extracellular glycoprotein, and CNS plasticity. 1991, Pubmed
Smit, Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain. 1998, Pubmed
Sodergren, Shedding genomic light on Aristotle's lantern. 2006, Pubmed , Echinobase
Sudhof, The synaptic vesicle cycle. 2004, Pubmed
Suárez-Castillo, Ependymin, a gene involved in regeneration and neuroplasticity in vertebrates, is overexpressed during regeneration in the echinoderm Holothuria glaberrima. 2004, Pubmed , Echinobase
Südhof, Synaptotagmins: why so many? 2002, Pubmed
Tahara, Calcium can disrupt the SNARE protein complex on sea urchin egg secretory vesicles without irreversibly blocking fusion. 1998, Pubmed , Echinobase
Takacs, Expression of an NK2 homeodomain gene in the apical ectoderm defines a new territory in the early sea urchin embryo. 2004, Pubmed , Echinobase
Teng, The syntaxins. 2001, Pubmed
Thompson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. 1994, Pubmed
Wada, Ascidian otx gene Hroth activates transcription of the brain-specific gene HrTRP. 2002, Pubmed
Walldorf, Homeobrain, a novel paired-like homeobox gene is expressed in the Drosophila brain. 2000, Pubmed
Walton, Genomics and expression profiles of the Hedgehog and Notch signaling pathways in sea urchin development. 2006, Pubmed , Echinobase
Wang, Site of attachment of 11-cis-retinal in bovine rhodopsin. 1980, Pubmed
Wang, Requirement for math5 in the development of retinal ganglion cells. 2001, Pubmed
Washbourne, Cell adhesion molecules in synapse formation. 2004, Pubmed
Wasson, Progesterone metabolism in the ovaries and testes of the echinoid Lytechinus variegatus Lamarck (Echinodermata). 2000, Pubmed , Echinobase
Whalley, Membrane fusion of secretory vesicles of the sea urchin egg in the absence of NSF. 2004, Pubmed , Echinobase
Whittaker, The echinoderm adhesome. 2006, Pubmed , Echinobase
Wilkinson, Evolution of the relaxin-like peptide family. 2005, Pubmed
Wilson, Starfish insulin. 1965, Pubmed , Echinobase
Yaguchi, Initial analysis of immunochemical cell surface properties, location and formation of the serotonergic apical ganglion in sea urchin embryos. 2000, Pubmed , Echinobase
Yaguchi, Expression of tryptophan 5-hydroxylase gene during sea urchin neurogenesis and role of serotonergic nervous system in larval behavior. 2003, Pubmed , Echinobase
Yaguchi, Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos. 2006, Pubmed , Echinobase
Yuh, Brn1/2/4, the predicted midgut regulator of the endo16 gene of the sea urchin embryo. 2005, Pubmed , Echinobase
Zhu, Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. 2002, Pubmed
de Pablo, Insulin-related molecules and insulin effects in the sea urchin embryo. 1988, Pubmed , Echinobase
van Kesteren, Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis. 1992, Pubmed
van Kesteren, Early evolutionary origin of the neurotrophin receptor family. 1998, Pubmed