The comprehensive analysis of DEG/ENaC subunits in Hydrareveals a large variety of peptide-gated channels, potentially involved in neuromuscular transmission
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BACKGROUND: It is generally the case that fast transmission at neural synapses is mediated by small molecule neurotransmitters. The simple nervous system of the cnidarian Hydra, however, contains a large repertoire of neuropeptides and it has been suggested that neuropeptides are the principal transmitters of Hydra. An ion channel directly gated by Hydra-RFamide neuropeptides has indeed been identified in Hydra - the Hydra Na+ channel (HyNaC) 2/3/5, which is expressed at the oral side of the tentacle base. Hydra-RFamides are more widely expressed, however, being found in neurons of the head and peduncle region. Here, we explore whether further peptide-gated HyNaCs exist, where in the animal they are expressed, and whether they are all gated by Hydra-RFamides. RESULTS: We report molecular cloning of seven new HyNaC subunits - HyNaC6 to HyNaC12, all of which are members of the DEG/ENaC gene family. In Xenopus oocytes, these subunits assemble together with the four already known subunits into thirteen different ion channels that are directly gated by Hydra-RFamide neuropeptides with high affinity (up to 40 nM). In situ hybridization suggests that HyNaCs are expressed in epitheliomuscular cells at the oral and the aboral side of the tentacle base and at the peduncle. Moreover, diminazene, an inhibitor of HyNaCs, delayed tentacle movement in live Hydra. CONCLUSIONS: Our results show that Hydra has a large variety of peptide-gated ion channels that are activated by a restricted number of related neuropeptides. The existence and expression pattern of these channels, and behavioral effects induced by channel blockers, suggests that Hydra co-opted neuropeptides for fast neuromuscular transmission.
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Pharmacological evidence and the localization of RFamide neuropeptides and ionotropic RFamide receptors suggest that iRFa-Rs are involved in neuromuscular transmission in Hydra.
“The presence of RFamide neuropeptides in large-dense core vesicles at the neuromuscular junction [58] and of the ionotropic RFamide-receptors (iRFa-Rs) in epitheliomuscular cells together with pharmacological evidence suggests that the iRFa-Rs are involved in neuromuscular transmission [39,40].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [40]
Neuropeptide signaling in Hydra is mediated not only by GPCRs but also by ion channel receptors.
“neuropeptide signaling in Hydra is mediated not only by GPCRs, but also by ion channel receptors [38,40,56]”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [40]
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Regional modulation of the response to glutathione in Hydra vulgaris (Pallas, 1766).
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The Neuropeptide Nocistatin Is Not a Direct Agonist of Acid-Sensing Ion Channel 1a (ASIC1a)
Kuspiel, S., Wiemuth, D., & Gründer, S. (2021) · Biomolecules · doi:10.3390/biom11040571 · Cited by 10 · see citing works
Functional Modules within a Distributed Neural Network Control Feeding in a Model MedusaPreprint
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A conserved peptide-binding pocket in HyNaC/ASIC ion channels
Ortega-Ramírez, A., Albani, S., Bachmann, M., Schmidt, A., Pinoé-Schmidt, M., Assmann, M., Augustinowski, K., Rossetti, G., & Gründer, S. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2409097121 · Cited by 7 · see citing works
In vivo neuromodulation of animal behavior with organic semiconducting oligomers
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Evolution of neuropeptides: From diffusing molecules to modulators of synaptic transmission
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Invertebrate Bile Acid‐Sensitive Ion Channels and Their Emergence in Bilateria
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Efficient expression of a cnidarian peptide-gated ion channel in mammalian cells
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Diarylamidine activation of a brachiopod DEG/ENaC/ASIC channel
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The Drosophila DEG/ENaC PPK12 is a Na+ leak channel with a low Na+ affinity
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HySyn: A genetically-encoded synthetic synapse to rewire neural circuits in vivoPreprint
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A proton-gated channel identified in the centipede antenna
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Diversity of ligand-gated ion channels in free-living and parasitic copepods (Crustacea)
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Evolutionary principles underlying neuron subtype encoding and diversification in animalsPreprint
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Mechanosensation and the brain–body axis: From survival needs to social behaviours
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- Authors
- Assmann, M., Kuhn, A., Dürrnagel, S., Holstein, T. W., & Gründer, S.
- Affiliations
- RWTH Aachen University (DE)
- Heidelberg University (DE)
- Corresponding author
- Gründer, Stefan
- Venue
- BMC Biology
- Published
- 2014-10-14
- Volume
- 12
- Issue
- 1
- Pages
- 84-84
- ISSN
- 1741-7007 (ISSN-L)
- PMC
- PMC4212090
- OpenAlex
- W2130083593
- Cited by
- 70
- References
- 55
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 7 · 2023: 7 · 2022: 8 · 2021: 8 · 2020: 3 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 4 · 2015: 5 · 2014: 1
- FWCI
- 2.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion, other-oa)
- RWTH Publications (RWTH Aachen)
- Funders
- Deutsche Forschungsgemeinschaft (GR 1771/7-1)
- Hebrew University of Jerusalem
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- Hydra, neuromuscular transmission, epitheliomuscular cells, diminazene, cnidarian nervous system, neuropeptide signaling
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Epithelial Cells, Hydra, Molecular Sequence Data, Synaptic Transmission, Neurons, Neuropeptides, Oocytes, Phylogeny, Synapses, Xenopus, Sequence Alignment, In Situ Hybridization, Degenerin Sodium Channels
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