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

Pierobon, Paola

doi:10.1387/ijdb.113464pp

Cited by 34 publications

(29 citation statements)

References 123 publications

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“…Similarly, in Hydra, there are also ample immunohistochemical, biochemical and functional data to indicate their presence (Kass-Simon and Pierobon, 2007;Pierobon, 2012) and two putative metabotropic acetylcholine receptors (mAchRs) have been identified (Collin et al, 2013). Ionotropic receptors for small-molecule transmitters have, however, not been studied at the molecular level in Hydra (see below); we will therefore concentrate our discussion of neurotransmitters on neuropeptides.…”

Section: Neurotransmitters In Hydra -Small Molecules and Peptidesmentioning

confidence: 99%

Peptide-gated ion channels and the simple nervous system of Hydra

Gründer

Assmann

2015

Journal of Experimental Biology

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Neurons either use electrical or chemical synapses to communicate with each other. Transmitters at chemical synapses are either small molecules or neuropeptides. After binding to their receptors, transmitters elicit postsynaptic potentials, which can either be fast and transient or slow and longer lasting, depending on the type of receptor. Fast transient potentials are mediated by ionotropic receptors and slow long-lasting potentials by metabotropic receptors. Transmitters and receptors are well studied for animals with a complex nervous system such as vertebrates and insects, but much less is known for animals with a simple nervous system like Cnidaria. As cnidarians arose early in animal evolution, nervous systems might have first evolved within this group and the study of neurotransmission in cnidarians might reveal an ancient mechanism of neuronal communication. The simple nervous system of the cnidarian Hydra extensively uses neuropeptides and, recently, we cloned and functionally characterized an ion channel that is directly activated by neuropeptides of the Hydra nervous system. These results demonstrate the existence of peptide-gated ion channels in Hydra, suggesting they mediate fast transmission in its nervous system. As related channels are also present in the genomes of the cnidarian Nematostella, of placozoans and of ctenophores, it should be considered that the early nervous systems of cnidarians and ctenophores have co-opted neuropeptides for fast transmission at chemical synapses.

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Section: Neurotransmitters In Hydra -Small Molecules and Peptidesmentioning

confidence: 99%

Peptide-gated ion channels and the simple nervous system of Hydra

Gründer

Assmann

2015

Journal of Experimental Biology

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“…But peptides are not only active as morphogens as several classes of peptides actually perform neurophysiological tasks, and for a while neurotransmission was even assumed to be predominantly peptidergic in cnidarians (Grimmelikhuijzen et al, 2002;Pierobon, 2012). In the 1990s an ambitious screen for Hydra peptides was launched in Japan, identifying both neuropeptides and epitheliopeptides .…”

Section: Peptide Signaling In Hydramentioning

confidence: 99%

“…In this issue, Paola Pierobon proposes a scenario whereby the multipolar GABAergic neurons in the apical region provide an integrative response that regulates the initiation and the termination of the feeding response (Pierobon, 2012).…”

Section: Peptide Signaling In Hydramentioning

confidence: 99%

Hydra, a fruitful model system for 270 years

Galliot¹

2012

Int. J. Dev. Biol.

155

113

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The discovery of Hydra regeneration by Abraham Trembley in 1744 promoted much scientific curiosity thanks to his clever design of experimental strategies away from the natural environment. Since then, this little freshwater cnidarian polyp flourished as a potent and fruitful model system. Here, we review some general biological questions that benefitted from Hydra research, such as the nature of embryogenesis, neurogenesis, induction by organizers, sex reversal, symbiosis, aging, feeding behavior, light regulation, multipotency of somatic stem cells, temperature-induced cell death, neuronal transdifferentiation, to cite only a few. To understand how phenotypes arise, theoricists also chose Hydra to model patterning and morphogenetic events, providing helpful concepts such as reaction-diffusion, positional information, and autocatalysis combined with lateral inhibition. Indeed, throughout these past 270 years, scientists used transplantation and grafting experiments, together with tissue, cell and molecular labelings, as well as biochemical procedures, in order to establish the solid foundations of cell and developmental biology. Nowadays, thanks to transgenic, genomic and proteomic tools, Hydra remains a promising model for these fields, but also for addressing novel questions such as evolutionary mechanisms, maintenance of dynamic homeostasis, regulation of stemness, functions of autophagy, cell death, stress response, innate immunity, bioactive compounds in ecosystems, ecotoxicant sensing and science communication. KEY WORDS: historical perspective, transplantation, modeling, developmental reactivation, Hydra regeneration, multipotency, stemness, symbiosis, environmentThe heuristic value of the Hydra model systemIn the early 18th century the word biology was not yet in use but the nature of living organisms and their evolutionary relationships was the focus of interest for philosophers and naturalists, as evidenced by their pioneering efforts to develop new tools such as microscopes that would allow finer observation (Palm, 1996). The microscopic observation of organisms taken in the field undoubtedly helped develop morphological keys to sort between the animal and vegetal kingdoms and to group them into phyla (Linnaeus, 1758). Among the ambiguous species that could not be easily classified were the seawater corals that looked like flowers (Watson, 1753;McConnell, 1990) and the freshwater Hydra polyp that was considered to exhibit both animal and vegetal features. For example, Hydra easily reproduces asexually through budding, a trait frequently assigned to plants or fungi.Having observed some Hydra polyps in a pond, Abraham Trembley (1710-1784) (who had received a PhD in mathematics from the University of Geneva (Switzerland) and was now educating the children of the Count of Bentick in the Netherlands) decided Int. J. Dev. Biol. 56: 411-423 (2012) to solve that problem by testing their capacity to regenerate, assuming that if Hydra regenerates, then it should be considered a plant, but if it does...

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“…Hydra produce a multitude of potentially bioactive compounds, including hemolysins likely involved in digestion (Sher et al, 2008, Sher et al, 2005a, Zhang et al, 2003, other potential pore-forming proteins involved in development and immunity (Amimoto et al, 2006, Miller et al, 2007, Sher and Zlotkin, 2009), neuropeptides and signaling peptides (Bosch and Fujisawa, 2001, Bottger et al, 2006, Takahashi et al, 1997, see in this issue (Fujisawa and Kayakawa, 2012;Pierobon, 2012) and several antimicrobial peptides (Augustin et al, 2009, Fraune et al, 2010. These proteins and peptides are produced by different body regions or cells, and several are secreted either into the gastrovascular cavity (Sher et al, 2008), into the developing oocyte or onto the ectodermal surface (Fraune et al, 2010).…”

Section: Can the Chemical Armament Of A Cnidarian Affect The Environmmentioning

confidence: 99%

What Hydra can teach us about chemical ecology how a simple, soft organism survives in a hostile aqueous environment

Rachamim

Sher

2012

Int. J. Dev. Biol.

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Hydra and its fellow cnidarians -sea anemones, corals and jellyfish -are simple, mostly sessile animals that depend on bioactive chemicals for survival. In this review, we briefly describe what is known about the chemical armament of Hydra, and detail future research directions where Hydra can help illuminate major questions in chemical ecology, pharmacology, developmental biology and evolution. Focusing on two groups of putative toxins from Hydra -phospholipase A2s and proteins containing ShK and zinc metalloprotease domains, we ask: how do different venom components act together during prey paralysis? How is a venom arsenal created and how does it evolve? How is the chemical arsenal delivered to its target? To what extent does a chemical and biotic coupling exist between an organism and its environment? We propose a model whereby in Hydra and other cnidarians, bioactive compounds are secreted both as localized point sources (nematocyte discharges) and across extensive body surfaces, likely combining to create complex "chemical landscapes". We speculate that these cnidarian-derived chemical landscapes may affect the surrounding community on scales from microns to, in the case of coral reefs, hundreds of kilometers.

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

Cited by 34 publications

References 123 publications

Peptide-gated ion channels and the simple nervous system of Hydra

Peptide-gated ion channels and the simple nervous system of Hydra

Hydra, a fruitful model system for 270 years

What Hydra can teach us about chemical ecology how a simple, soft organism survives in a hostile aqueous environment

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