Pacemaker activity in hydra is modulated by glycine receptor ligands

Ruggieri, Rosamaria; Pierobon, Paola; Kass-Simon, G.

doi:10.1016/j.cbpb.2004.03.015

Cited by 35 publications

(25 citation statements)

References 44 publications

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“…Glycine is a major inhibitory amino acid neurotransmitter in the vertebrate CNS that works by inducing a hyperpolarising chloride current when bound to a post-synaptic receptor but it can also be a modulator in excitatory ionotropic glutamate receptors. In Hydra, glycine has been identified and localised to the nerve net where it functions in pacemaker activity of peristaltic contractions (elongations and contractions) of the muscle in the body column; it is also involved in the chemosensory response during feeding by inhibiting the closure of the mouth upon stimulation by glutathione (Pierobon et al, 2001;Ruggieri et al, 2004;Kass-Simon and Pierobon, 2006). Similar responses are observed by the application of alanine and taurine in Hydra (Kass-Simon and Pierobon, 2006).…”

Section: Neuroactive Amino Acids In Sponge Tissuementioning

confidence: 80%

Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)

Elliott

Leys

2010

Journal of Experimental Biology

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SUMMARYThe view that sponges lack tissue level organisation, epithelia, sensory cells and coordinated behaviour is challenged by recent molecular studies showing the existence in Porifera of molecules and proteins that define cell signalling systems in higher order metazoans. Demonstration that freshwater sponges can contract their canals in an organised manner in response to both external and endogenous stimuli prompted us to examine the physiology of the contraction behaviour. Using a combination of digital timelapse microscopy, high-performance liquid chromatography-mass spectrometry (HPLC-MS) analysis, immunocytochemistry and pharmacological manipulations, we tested the role of the diffusible amino acids glutamate and g-aminobutyric acid (GABA) and a short-lived diffusible gas, nitric oxide (NO), in triggering or modulating contractions in Ephydatia muelleri. We identified pools of glutamate, glutamine and GABA used to maintain a metabotropic glutamate and GABA receptor signalling system. Glutamate induced contractions and propagation of a stereotypical behaviour inflating and deflating the canal system, acting in a dosedependent manner. Glutamate-triggered contractions were blocked by the metabatropic glutamate receptor inhibitor AP3 and by incubation of the sponge in an allosteric competitive inhibitor of glutamate, Kynurenic acid. Incubation in GABA inhibited glutamate-triggered contractions of the sponge. Nitric oxide synthase, involved in the formation of the diffusible gas NO, was localised using NADPH-diaphorase to mesenchyme cells in the osculum and pinacoderm. A cGMP assay showed the same cells were labelled suggesting that the NO system is functional. Our findings suggest sponges coordinate behaviour using chemical messenger systems common to other animals. Supplementary material available online at

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Section: Neuroactive Amino Acids In Sponge Tissuementioning

confidence: 80%

Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)

Elliott

Leys

2010

Journal of Experimental Biology

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“…Some involve rhythmic contraction of the body column. In Hydra , a pacemaker system regulates this process (Passano and McCullough, 1963, 1964; Kass-Simon et al, 2003; Ruggieri et al, 2004). It is constituted by a small subset of nerve cells connected by gap junctions located near the foot, and capable of synchronous firing (Takaku et al, 2014).…”

Section: Cnidarian Muscle Functionsmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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“…Serotonin is involved in metamorphosis of the hydrozoans Phialidium gregarium and Eudendrium racemosum (McCauley, 1997;Zega et al, 2007). And, the neurotransmitter glycine affects the endodermal pacemakers and thereby regulates elongation and contraction of the hydra body column (Ruggieri et al, 2004). Similarly, electrophysiological experiments show that glutamate and GABA and their receptors are involved in pacemaker activity in Hydra (Kass-Simon et al, 2003).…”

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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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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Pacemaker activity in hydra is modulated by glycine receptor ligands

Cited by 35 publications

References 44 publications

Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)

Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

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

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