Chemoreception in Hydra vulgaris (attenuata): initial characterization of two distinct binding sites for l-glutamic acid

Bellis, Susan L.; Grosvenor, William; Kass-Simon, G.; Rhoads, Dennis E.

doi:10.1016/0005-2736(91)90272-a

Cited by 48 publications

(31 citation statements)

References 23 publications

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“…These findings indicate that these receptors are functionally activated by their specific ligands; the ability of GSH to potentiate [ 3 H]MK-801 binding is consistent with data obtained in rat (Ogita et al, 1995) and Hydra (Bellis et al, 1991) membrane preparations.…”

Section: Excitatory Transmitters and Receptors: Glutamatesupporting

confidence: 88%

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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: Excitatory Transmitters and Receptors: Glutamatesupporting

confidence: 88%

“…Binding studies show that glutamate binds to crude membrane fractions of Hydra (Bellis et al, 1991 (Grosvenor et al, 1992).…”

Section: Excitatory Transmitters and Receptors: Glutamatementioning

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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“…Recently, calcium and potassium channels were characterised in jellyfish with functional features similar to those measured in vertebrate counterparts Jeziorski et al (1999), Grigoriev et al (1999), while GABAreceptors were pharmacologically identified Pierobon et al (2001). Neurotransmitters like glycine Pierobon et al (2001), nitric oxide Colasanti et al (1997), endocannabinoid De Petrocellis et al (1999 and glutamate Bellis et al (1991) are likely playing a physiological role in the feeding response.…”

Section: Figmentioning

confidence: 91%

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

2004

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Cnidarians represent the first animal phylum with an organized nervous system and a complex active behavior. The hydra nervous system is formed of sensory-motoneurons, ganglia neurons and mechanoreceptor cells named nematocytes, which all differentiate from a common stem cell. The neurons are organized as a nerve net and a subset of neurons participate in a more complex structure, the nerve ring that was identified in most cnidarian species at the base of the tentacles. In order to better understand the genetic control of this neuronal network, we analysed the expression of evolutionarily-conserved regulatory genes in the hydra nervous system. The PRD-CLASS homeogene, prdl-b, and the nuclear orphan receptor, hyCOUP-TF, are expressed at strong levels in proliferating nematoblasts, a lineage where they were found repressed during patterning and morphogenesis, and at low levels in distinct subsets of neurons. Interestingly, PRD-CLASS homeobox and COUP-TF genes are also expressed during neurogenesis in bilaterians, suggesting that mechanoreceptor and neuronal cells derive from a common ancestral cell. Moreover, the PRD-CLASS homeobox gene prdl-a, the ANTP-CLASS homeobox gene msh, and the thrombospondin-related gene TSP1, which are expressed in distinct subset of neurons in the adult polyp, are also expressed during early budding and/or head regeneration. These data strengthen the fact that two distinct regulations, one for neurogenesis and another for patterning, already apply to these regulatory genes, a feature also identified in bilaterian related-genes.

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“…In contrast to glutamate (Bellis et al, 1991), these ligands do not modify times of mouth opening, suggesting that their effect is exerted on the neuromuscular circuitry underlying the feeding behaviour, rather than on the GSH receptor itself (reviewed in Pierobon, 2012). Therefore, neurotransmitter modulation of the feeding behaviour seems to be attained by multiple complex chemical and/or cellular pathways.…”

Section: Introductionmentioning

confidence: 99%

Regional modulation of the response to glutathione in Hydra vulgaris (Pallas, 1766).

Pierobon

2015

Journal of Experimental Biology

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In the presence of prey, or upon exposure to reduced glutathione (GSH), Hydra polyps open a mouth to ingest the captured prey and close it after feeding; at rest the mouth is not evident. In previous papers we have shown that GABA, glycine and NMDA modulate the mechanisms of mouth closure through ligand-gated-ion-channel receptors that are similar to their mammalian analogues in terms of biochemical and pharmacological properties. In order to study the regional distribution of these receptors, we have applied the GSH assay to polyps amputated at different levels of the body column. The response to 1-10 µmol l −1 GSH of polyps lacking either peduncle and foot or the entire body columns (heads) was not different from control, whole animals. In the presence of GABA or muscimol, duration of the response was significantly decreased in heads; the decrease was suppressed by the GABA antagonists gabazine and bicuculline. By contrast, in animals lacking peduncle and foot, duration of the response did not vary upon GABA administration. Conversely, in the presence of glycine, duration of the response in heads preparations was similar to control, whereas in footless polyps, it was significantly reduced. The decrease was mimicked by the glycine agonists taurine and β-alanine, and counteracted by strychnine. These results suggest a regional distribution of receptors to GABA and glycine in the neuromuscular circuitry modulating the feeding behaviour.

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Chemoreception in Hydra vulgaris (attenuata): initial characterization of two distinct binding sites for l-glutamic acid

Cited by 48 publications

References 23 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)

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

Regional modulation of the response to glutathione in Hydra vulgaris (Pallas, 1766).

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