Cnidarians and the evolutionary origin of the nervous system

Watanabe, Hiroshi; Fujisawa, Toshitaka; Holstein, Thomas W.

doi:10.1111/j.1440-169x.2009.01103.x

Cited by 174 publications

(184 citation statements)

References 189 publications

(349 reference statements)

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“…Among these, the neuropeptide RFamide family of GPCRs is the most studied among the cnidarians. RFamide-positive neurons were found in N. vectensis, Hydra, Hydractinia and jellyfish, and they are found in all classes of cnidarians (Watanabe et al, 2009 (Churcher and Taylor, 2011;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.…”

Section: N V E C T E N S I S T a D H A E R E N S A Q U E E N S mentioning

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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Section: N V E C T E N S I S T a D H A E R E N S A Q U E E N S mentioning

confidence: 99%

“…dopamine and serotonin transmitters, as well as neuropeptides, are involved in cnidarian neurotransmission (Kass-Simon and Pierobon, 2007;Watanabe et al, 2009) (Fig. 2).…”

Section: N V E C T E N S I S T a D H A E R E N S A Q U E E N S mentioning

confidence: 99%

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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“…Individual neurons in cnidarians are highly specialized. In comparison to neurons of bilateral animals, they contain close to a complete set of signaling molecules that are involved in nervous system development, maintenance and communication (see Watanabe et al, 2009). This puts the individual neurons of cnidarians on a level of complexity similar to that of neurons of higher animals.…”

Section: Are Cnidarian Nervous Systems Made Up Of Nerve Nets?mentioning

confidence: 99%

Do jellyfish have central nervous systems?

Satterlie

2011

Journal of Experimental Biology

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Summary The traditional view of the cnidarian nervous system is of a diffuse nerve net that functions as both a conducting and an integrating system; this is considered an indicator of a primitive condition. Yet, in medusoid members, varying degrees of nerve net compression and neuronal condensation into ganglion-like structures represent more centralized integrating centers. In some jellyfish, this relegates nerve nets to motor distribution systems. The neuronal condensation follows a precept of neuronal organization of higher animals with a relatively close association with the development and elaboration of sensory structures. Nerve nets still represent an efficient system for diffuse, non-directional activation of broad, two-dimensional effector sheets, as required by the radial, non-cephalized body construction. However, in most jellyfish, an argument can be made for the presence of centralized nervous systems that interact with the more diffuse nerve nets.

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“…1B; reviewed by Galliot et al (2009)]. Although their neurons are not uniformly distributed, cnidarian polyps lack brain-like nervous system centralization and their nervous system is often described as a nerve net (Galliot et al, 2009;Watanabe et al, 2009). The cellular origin of neurons has mainly been described in hydrozoans (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…ectoderm and endoderm (Nakanishi et al, 2012). At the molecular level, Nematostella possesses many genes related to conserved bilaterian neural genes (Putnam et al, 2007;Watanabe et al, 2009), and subsets of its nervous system have been examined using antibodies against conserved neuropeptide precursor molecules [e.g. Marlow et al (2009)].…”

Section: Introductionmentioning

confidence: 99%

Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis

2014

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Bilaterian neurogenesis is characterized by the generation of diverse neural cell types from dedicated neural stem/progenitor cells (NPCs). However, the evolutionary origin of NPCs is unclear, as neurogenesis in representatives of the bilaterian sister group, the Cnidaria, occurs via interstitial stem cells that also possess broader, non-neural, developmental potential. We address this question by analysing neurogenesis in an anthozoan cnidarian, Nematostella vectensis. Using a transgenic reporter line, we show that NvSoxB(2) -an orthologue of bilaterian SoxB genes that have conserved roles in neurogenesis -is expressed in a cell population that gives rise to sensory neurons, ganglion neurons and nematocytes: the three primary neural cell types of cnidarians. EdU labelling together with in situ hybridization, and within the NvSoxB(2)::mOrange transgenic line, demonstrates that cells express NvSoxB(2) before mitosis and identifies asymmetric behaviours of sibling cells within NvSoxB (2) + lineages. Morpholino-mediated gene knockdown of NvSoxB (2) blocks the formation of all three neural cell types, thereby identifying NvSoxB(2) as an essential positive regulator of nervous system development. Our results demonstrate that diverse neural cell types derive from an NvSoxB(2)-expressing population of mitotic cells in Nematostella and that SoxB genes are ancient components of a neurogenic program. To our knowledge this is the first description of a lineage-restricted, multipotent cell population outside the Bilateria and we propose that neurogenesis via dedicated, SoxB-expressing NPCs predates the split between cnidarians and bilaterians.

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Cnidarians and the evolutionary origin of the nervous system

Cited by 174 publications

References 189 publications

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

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

Do jellyfish have central nervous systems?

Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis

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