Anatomy and development of the nervous system of <i>Nematostella vectensis</i>, an anthozoan cnidarian

Marlow, Heather; Srivastava, Mansi; Matus, David Q.; Rokhsar, Daniel S.; Martindale, Mark Q.

doi:10.1002/dneu.20698

Cited by 232 publications

(312 citation statements)

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“…More recently, GABA immunoreactivity was found in interneurons of the cubozoan jellyfish Carybdea marsupialis (Martin, 2004) and in the ectodermal nerve net of the anthozoan sea anemone Nematostella vectensis (Marlow et al, 2009). GABA immunogold labelling was found in putative neural processes within the neural plexus of the sea anemone Phymactis papillosa (Delgado et al, 2010).…”

Section: Inhibitory Transmitters and Receptors: Gaba And Glycinementioning

confidence: 99%

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

Pierobon

2012

Int. J. Dev. Biol.

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Cnidarians lack well developed organs, but they have evolved the molecular and cellular components needed to assemble a nervous system. The apparent 'simplicity' of the cnidarian nervous net does not occur at the cellular level, but rather in the organisation of conducting systems. Cnidarian neurons are in fact electrically excitable, show the typical extended morphology and are connected by chemical synapses or gap junctions. They have been regarded as peptidergic, given the wealth of neuropeptides generally distributed along neurites and in cell bodies, supporting the hypothesis of a modulatory role in neurotransmission. However, the presence of clear-cored, as well as dense-cored synaptic vesicles in cnidarian neurons suggests both fast and slow synaptic transmission mechanisms. In fact, biochemical and functional evidence indicates that classical neurotransmitters and their metabolic partners are present in cnidarian tissues, where they are involved in coordinating motility and behavior. We have identified and characterized in Hydra tissues receptors to the inhibitory and excitatory amino acid neurotransmitters, GABA, glycine and NMDA, that are similar to mammalian ionotropic receptors in terms of their biochemical and pharmacological properties. These receptors appear to regulate pacemaker activities and their physiological correlates; in the live animal, they also affect feeding behavior, namely the duration and termination of the response elicited by reduced glutathione, with opposite actions of GABA and glycine or NMDA, respectively. These results suggest that modulation of cellular signaling through ligand-gated-ion channels is an ancient characteristic in the animal kingdom, and that the pharmacological properties of these receptors have been highly conserved during evolution.

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Section: Inhibitory Transmitters and Receptors: Gaba And Glycinementioning

confidence: 99%

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

Pierobon

2012

Int. J. Dev. Biol.

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“…N. vectensis constitutes an ectodermal and endodermal nerve net making it a simple and diffuse nervous system that runs throughout the animal's body (Marlow et al, 2009;Nakanishi et al, 2012). Also, recently, the ctenophore (M. leidyi) genome has been sequenced and the organism also possesses a peripheral subepithelial nerve net, neurons and nerves associated with the tentacles (Jager et al, 2011;Richter and King, 2013;Ryan et al, 2013).…”

Section: Reviewmentioning

confidence: 99%

“…Also, the list was cross verified with whole-genome analysis and comparative genomic studies (Anctil, 2009;Moroz et al, 2014;Nikitin, 2014;Putnam et al, 2007;Riesgo et al, 2014;Ryan et al, 2013;Srivastava et al, 2008;Srivastava et al, 2010). Marlow et al, 2009;Nakanishi et al, 2012;Niimura, 2009). These findings provide insights that the prebilaterians exhibit a GPCR-mediated sensory system and suggested that the genetic complexity commonly assumed to have arisen much later in animal evolution is actually an ancestral feature.…”

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confidence: 99%

“…However, N. vectensis is regarded as one of the earliest organisms in animal evolution possessing a nervous system (Putnam et al, 2007;Technau and The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system Arunkumar Krishnan* and Helgi B. Schiöth* Steele, 2011). N. vectensis constitutes an ectodermal and endodermal nerve net making it a simple and diffuse nervous system that runs throughout the animal's body (Marlow et al, 2009;Nakanishi et al, 2012). Also, recently, the ctenophore (M. leidyi) genome has been sequenced and the organism also possesses a peripheral subepithelial nerve net, neurons and nerves associated with the tentacles (Jager et al, 2011;Richter and King, 2013;Ryan et al, 2013).…”

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confidence: 99%

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The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

Krishnan

Schiöth

2015

Journal of Experimental Biology

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The origin and evolution of the nervous system is one of the most intriguing and enigmatic events in biology. The recent sequencing of complete genomes from early metazoan organisms provides a new platform to study the origins of neuronal gene families. This review explores the early metazoan expansion of the largest integral transmembrane protein family, the G protein-coupled receptors (GPCRs), which serve as molecular targets for a large subset of neurotransmitters and neuropeptides in higher animals. GPCR repertories from four pre-bilaterian metazoan genomes were compared. This includes the cnidarian Nematostella vectensis and the ctenophore Mnemiopsis leidyi, which have primitive nervous systems (nerve nets), the demosponge Amphimedon queenslandica and the placozoan Trichoplax adhaerens, which lack nerve and muscle cells. Comparative genomics demonstrate that the rhodopsin and glutamate receptor families, known to be involved in neurotransmission in higher animals are also widely found in prebilaterian metazoans and possess substantial expansions of rhodopsin-family-like GPCRs. Furthermore, the emerging knowledge on the functions of adhesion GPCRs in the vertebrate nervous system provides a platform to examine possible analogous roles of their closest homologues in pre-bilaterians. Intriguingly, the presence of molecular components required for GPCR-mediated neurotransmission in pre-bilaterians reveals that they exist in both primitive nervous systems and nerve-cell-free environments, providing essential comparative models to better understand the origins of the nervous system and neurotransmission. KEY WORDS: Neuron, GPCR, Nerve net, Synapse, EvolutionIntroduction G protein-coupled receptors (GPCRs) constitute the largest superfamily among membrane bound proteins that control key physiological functions, such as, neurotransmission, hormone releases, and immune responses among others (Katritch et al., 2013; Lagerström and Schiöth, 2008;Rosenbaum et al., 2009). As such, the large range of integral transmembrane proteins in this family respond to subsequent, diverse array of ligands: including neurotransmitters, hormones, lipids, and odorants (Civelli et al., 2013;Shoichet and Kobilka, 2012). GPCRs in mammals are classified into the five main families according to the GRAFS classification: glutamate, rhodopsin, adhesion, frizzled and secretin (Fredriksson et al., 2003). These five GPCR families are associated with various physiological functions, but the roles of the glutamate and the rhodopsin families are particularly well documented for REVIEW Department of Neuroscience, Functional Pharmacology, Uppsala University, BMC, Box 593,751 24, Uppsala, Sweden.*Authors for correspondence (arunkumar.krishnan@neuro.uu.se; helgi.schioth@neuro.uu.se) neurotransmission and regulation of the nervous system (Niswender and Conn, 2010;Schoepp, 2001). Some functions include synaptic transmission, synapse formation, axon guidance and development of neuronal circuits (Collingridge et al., 2004;Hnasko and Edwards, 2012)...

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“…5A). The emergence of neural structures in metazoans leads to innovation in protein functions (50). Although the origin of nerve cells remains unknown, the Cnidaria, whose name derived from cnidocytes (i.e.…”

Section: In the Cnidarian C Hemisphaerica Two Globins (Chengb1 And mentioning

confidence: 99%

Neuroglobins, Pivotal Proteins Associated with Emerging Neural Systems and Precursors of Metazoan Globin Diversity

Lechauve

Jager

Laguerre

et al. 2013

Journal of Biological Chemistry

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Background: Neuroglobins are expressed in vertebrate neurons. Results: Neuroglobins are located in neural systems of two basal animals (acoels and jellyfish) and are ubiquitous in metazoan transcriptomes. Conclusion: Neuroglobin was recruited in neural cell prototypes and later co-opted in hemoglobin-based blood systems. Significance: The universality of neuroglobins sheds new light on the origin and evolution of globins.

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Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian

Cited by 232 publications

References 99 publications

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa)

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

Neuroglobins, Pivotal Proteins Associated with Emerging Neural Systems and Precursors of Metazoan Globin Diversity

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