Chemoreceptive Control of Feeding Processes in Hydra

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

doi:10.1093/chemse/21.3.313

Cited by 29 publications

(16 citation statements)

References 35 publications

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“…The suggestion made by Lenhoff (1974), based on his detailed analysis of the kinetics of the response, that mouth closure is simply derived from receptor desensitization was challenged by later studies. Grosvenor et al (1996) found that wounded prey release other substances, besides GSH, that are able to shorten response duration by competitively inhibiting GSH binding. Elevated NOinduced cGMP levels are able to trigger inhibition of the response to GSH, presumably via cGMP-activated protein kinases (Colasanti et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

Putative NMDA receptors in Hydra: a biochemical and functional study

Pierobon

Sogliano

Minei

et al. 2004

Eur J of Neuroscience

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The feeding behaviour of the freshwater polyp Hydra vulgaris (Cnidaria, Hydrozoa) is modulated by a number of molecules acting as neurotransmitters in other nervous systems. Here we present biochemical and functional evidence of the occurrence of putative NMDA receptors in Hydra tissues. Saturation experiments showed the presence of one population of binding sites with nanomolar affinity and low capacity for [3H]MK-801. Before equilibrium, [3H]MK-801 binding was increased by the agonists glutamate and glycine as well as by reduced glutathione (GSH). In vivo the glutamate receptor agonist NMDA markedly decreased the duration of the response to GSH. This effect was linearly related to ligand doses in the nanomolar concentration range and was counteracted by either the NMDAR-specific antagonist D-AP5 or by the d-serine antagonist DCKA. When NMDA concentration was increased to 10 or 100 microm, duration of the response to GSH was no longer affected unless the lectin concanavalin A, which prevents receptor desensitization in other systems, was added to the test medium. Simultaneous administration of ineffective doses of NMDA and strychnine, glycine or d-serine, an agonist at the glycine binding site of the NMDA receptor in vertebrate CNS, resulted in a strong reduction of response duration. Both D-AP5 and DCKA suppressed this effect. These results, together with the decrease in response duration produced by d-serine, support the hypothesis that NMDA-like glutamate receptors may occur in Hydra tissues where they are involved in modulation of the response to GSH with opposite actions to those of GABA and glycine.

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Section: Discussionmentioning

confidence: 99%

Putative NMDA receptors in Hydra: a biochemical and functional study

Pierobon

Sogliano

Minei

et al. 2004

Eur J of Neuroscience

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“…Lenhoff (1974) suggested that mouth closure simply derived from receptor desensitization, or unbinding of GSH from its receptor. This hypothesis was challenged by the finding that wounded prey release other substances, as well as GSH, that are able to shorten response duration by competitive inhibition of GSH binding (Grosvenor et al, 1996). Our group found that inhibitory and excitatory amino acid transmitters modulate the feeding behavior by prolonging or shortening, respectively, the duration of the response to GSH.…”

Section: The Hydra Feeding Responsementioning

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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“…The feeding behavior in Hydra is characterized by the capture of preys on the tentacles, the subsequent opening of the mouth and the coordinated movement of the tentacles to favor the ingestion of the preys through the mouth. This complex behavior is triggered by reduced glutathione release from the captured prey (Loomis, ; Grosvenor et al , ; Pierobon, ). Here animals were individually exposed to preys, that is, swimming Artemias , for 15 s and the number of preys fixed on the tentacles was counted.…”

Section: Resultsmentioning

confidence: 99%

Loss of Neurogenesis in Aging Hydra

Tomczyk

Buzgariu

Perruchoud

et al. 2019

Developmental Neurobiology

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In Hydra the nervous system is composed of neurons and mechanosensory cells that differentiate from interstitial stem cells (ISCs), which also provide gland cells and germ cells. The adult nervous system is actively maintained through continuous de novo neurogenesis that occurs at two distinct paces, slow in intact animals and fast in regenerating ones. Surprisingly Hydra vulgaris survive the elimination of cycling interstitial cells and the subsequent loss of neurogenesis if force‐fed. By contrast, H. oligactis animals exposed to cold temperature undergo gametogenesis and a concomitant progressive loss of neurogenesis. In the cold‐sensitive strain Ho_CS, this loss irreversibly leads to aging and animal death. Within four weeks, Ho_CS animals lose their contractility, feeding response, and reaction to light. Meanwhile, two positive regulators of neurogenesis, the homeoprotein prdl‐a and the neuropeptide Hym‐355, are no longer expressed, while the “old” RFamide‐expressing neurons persist. A comparative transcriptomic analysis performed in cold‐sensitive and cold‐resistant strains confirms the downregulation of classical neuronal markers during aging but also shows the upregulation of putative regulators of neurotransmission and neurogenesis such as AHR, FGFR, FoxJ3, Fral2, Jagged, Meis1, Notch, Otx1, and TCF15. The switch of Fral2 expression from neurons to germ cells suggests that in aging animals, the neurogenic program active in ISCs is re‐routed to germ cells, preventing de novo neurogenesis and impacting animal survival.

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Chemoreceptive Control of Feeding Processes in Hydra

Cited by 29 publications

References 35 publications

Putative NMDA receptors in Hydra: a biochemical and functional study

Putative NMDA receptors in Hydra: a biochemical and functional study

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

Loss of Neurogenesis in Aging Hydra

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