New insights on ctenophore neural anatomy: Immunofluorescence study in <i>Pleurobrachia pileus</i> (Müller, 1776)

Jager, Muriel; Chiori, Roxane; Alié, Alexandre; Dayraud, Cyrielle; Quéinnec, Éric; Manuel, Michaël

doi:10.1002/jez.b.21386

Cited by 102 publications

(151 citation statements)

References 60 publications

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“…FMRFamide-like and vasopressin-like immunereactivities were reported in some Pleurobrachia neurons (Grimmelikhuijzen, 1983;Jager et al, 2011), but none of these neuropeptide classes were found in the recent genomic studies . Cholinergic and monoaminergic control of bioluminescent flashes were proposed for Mnemiopsis (Anctil, 1985) but neither effector neurons nor specific transmitter synthetic enzymes were identified.…”

Section: Tripartite Synapses In Ctenophoresmentioning

confidence: 97%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

114

139

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Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers -features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuronspecific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamineconsistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

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Section: Tripartite Synapses In Ctenophoresmentioning

confidence: 97%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

114

139

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“…However, we have to recognize that those genes could also have been co-opted several times in evolution (in toto or a fraction of them; see, for instance, [83]) or used for the general patterning of the neuroepithelia, instead of being devoted to the specification of concrete neural areas/ structures [84 -86]. The alternative hypothesis is the multiple origin of centralized NSs, which states that they have evolved, independently, more than once [84,85,101,102]. The hypothesis relies on the observation that there is a 'patchy' rstb.royalsocietypublishing.org Phil.…”

Section: Independent Events In Nervous System Centralization Across Mmentioning

confidence: 99%

Xenacoelomorpha: a case of independent nervous system centralization?

Gavilán

Perea-Atienza

Martı́nez

2016

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Centralized nervous systems (NSs) and complex brains are among the most important innovations in the history of life on our planet. In this context, two related questions have been formulated: How did complex NSs arise in evolution, and how many times did this occur? As a step towards finding an answer, we describe the NS of several representatives of the Xenacoelomorpha, a clade whose members show different degrees of NS complexity. This enigmatic clade is composed of three major taxa: acoels, nemertodermatids and xenoturbellids. Interestingly, while the xenoturbellids seem to have a rather 'simple' NS (a nerve net), members of the most derived group of acoel worms clearly have ganglionic brains. This interesting diversity of NS architectures (with different degrees of compaction) provides a unique system with which to address outstanding questions regarding the evolution of brains and centralized NSs. The recent sequencing of xenacoelomorph genomes gives us a privileged vantage point from which to analyse neural evolution, especially through the study of key gene families involved in neurogenesis and NS function, such as G protein-coupled receptors, helixloop-helix transcription factors and Wnts. We finish our manuscript proposing an adaptive scenario for the origin of centralized NSs (brains).

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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). Here, we analyse the large expansions of GPCRs, and present the evidence accumulated so far for the presence of neurotransmitters and their roles in early metazoans.…”

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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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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New insights on ctenophore neural anatomy: Immunofluorescence study in Pleurobrachia pileus (Müller, 1776)

Cited by 102 publications

References 60 publications

Convergent evolution of neural systems in ctenophores

Convergent evolution of neural systems in ctenophores

Xenacoelomorpha: a case of independent nervous system centralization?

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

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