Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review

Koizumi, Osamu; Sato, Nobuko; Goto, Chiaki

doi:10.1007/s10750-004-2636-x

Cited by 29 publications

(23 citation statements)

References 40 publications

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“…Cnidarians often possess both endodermal and ectodermal NSs [91]. As highlighted by Koizumi et al [82], it has been observed that nerve cells residing either in ectoderm or the endoderm express different types of peptides. These differences are also seen in different nerve cells populations.…”

Section: Transformation From Nerve Nets To Compact Brains In the Xenamentioning

confidence: 98%

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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Section: Transformation From Nerve Nets To Compact Brains In the Xenamentioning

confidence: 98%

Xenacoelomorpha: a case of independent nervous system centralization?

Gavilán

Perea-Atienza

Martı́nez

2016

Phil. Trans. R. Soc. B

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“…An immunocytochemical study performed with anti-RFamide antibodies (Koizumi et al, 1992) demonstrated the occurrence of a nerve ring at the base of the hypostome in Hydra oligactis, formed by neurites of ganglion cells running circumferentially in a bundle, providing the first anatomical evidence of the existence of a ring structure previously inferred by electrophysiological studies (Kass-Simon, 1972). Labeling with different monoclonal antibodies or antibodies raised against different Hydra neuropeptides identified distinct subsets of neurons with specific regional distributions, dependent on axial position (Koizumi andBode, 1986, 1991;Koizumi et al, 2004). A remarkable feature of the net is, in fact, its plasticity: neurons are continually migrating to be eliminated at the apical and basal ends of the polyp together with the adjacent epithelia (Dunne et al, 1985;Bode et al, 1986), thus implying that extensive synapse remodeling must occur in physiological conditions.…”

Section: The Nervous Net Of Hydra: Anatomy Ultrastructure and Physiomentioning

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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“…In contrast to most bilaterians, cnidarians often possess both endodermal and ectodermal nervous systems. The overall architecture of the adult nervous system in the hydrozoan polyp Hydra resembles a nerve net with regional differences in neuron densities (reviewed by Koizumi et al, 2004), whereas anthozoan polyps often display accumulations of neurons and neurites associated with longitudinal endodermal infoldings termed mesenteries (e.g. Batham et al, 1960).…”

Section: Introductionmentioning

confidence: 99%

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms

et al. 2012

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SUMMARYAs a sister group to Bilateria, Cnidaria is important for understanding early nervous system evolution. Here we examine neural development in the anthozoan cnidarian Nematostella vectensis in order to better understand whether similar developmental mechanisms are utilized to establish the strikingly different overall organization of bilaterian and cnidarian nervous systems. We generated a neuron-specific transgenic NvElav1 reporter line of N. vectensis and used it in combination with immunohistochemistry against neuropeptides, in situ hybridization and confocal microscopy to analyze nervous system formation in this cnidarian model organism in detail. We show that the development of neurons commences in the ectoderm during gastrulation and involves interkinetic nuclear migration. Transplantation experiments reveal that sensory and ganglion cells are autonomously generated by the ectoderm. In contrast to bilaterians, neurons are also generated throughout the endoderm during planula stages. Morpholino-mediated gene knockdown shows that the development of a subset of ectodermal neurons requires NvElav1, the ortholog to bilaterian neural elav1 genes. The orientation of ectodermal neurites changes during planula development from longitudinal (in early-born neurons) to transverse (in late-born neurons), whereas endodermal neurites can grow in both orientations at any stage. Our findings imply that elav1-dependent ectodermal neurogenesis evolved prior to the divergence of Cnidaria and Bilateria. Moreover, they suggest that, in contrast to bilaterians, almost the entire ectoderm and endoderm of the body column of Nematostella planulae have neurogenic potential and that the establishment of connectivity in its seemingly simple nervous system involves multiple neurite guidance systems.

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Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review

Cited by 29 publications

References 40 publications

Xenacoelomorpha: a case of independent nervous system centralization?

Xenacoelomorpha: a case of independent nervous system centralization?

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

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms

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