Three homologous subunits form a high affinity peptide-gated ion channel in Hydra
Open accessAbstract
Recently, three ion channel subunits of the degenerin (DEG)/epithelial Na(+) channel (ENaC) gene family have been cloned from the freshwater polyp Hydra magnipapillata, the Hydra Na(+) channels (HyNaCs) 2-4. Two of them, HyNaC2 and HyNaC3, co-assemble to form an ion channel that is gated by the neuropeptides Hydra-RFamides I and II. The HyNaC2/3 channel is so far the only cloned ionotropic receptor from cnidarians and, together with the related ionotropic receptor FMRFamide-activated Na(+) channel (FaNaC) from snails, the only known peptide-gated ionotropic receptor. The HyNaC2/3 channel has pore properties, like a low Na(+) selectivity and a low amiloride affinity, that are different from other channels of the DEG/ENaC gene family, suggesting that a component of the native Hydra channel might still be lacking. Here, we report the cloning of a new ion channel subunit from Hydra, HyNaC5. The new subunit is closely related to HyNaC2 and -3 and co-localizes with HyNaC2 and -3 to the base of the tentacles. Coexpression in Xenopus oocytes of HyNaC5 with HyNaC2 and -3 largely increases current amplitude after peptide stimulation and affinity of the channel to Hydra-RFamides I and II. Moreover, the HyNaC2/3/5 channel has altered pore properties and amiloride affinity, more similarly to other DEG/ENaC channels. Collectively, our results suggest that the three homologous subunits HyNaC2, -3, and -5 form a peptide-gated ion channel in Hydra that could contribute to fast synaptic 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 [39]
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- Authors
- Dürrnagel, S., Kuhn, A., Tsiairis, C. D., Williamson, M., Kalbacher, H., Grimmelikhuijzen, C. J. P., Holstein, T. W., & Gründer, S.
- Affiliations
- RWTH Aachen University (DE)
- University of Copenhagen (DK)
- University of Tübingen (DE)
- Corresponding author
- Gründer, Stefan
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2010-04
- Volume
- 285
- Issue
- 16
- Pages
- 11958-11965
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2852933
- OpenAlex
- W1993150938
- Cited by
- 58
- References
- 28
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 3 · 2022: 3 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 7 · 2017: 3 · 2016: 2 · 2015: 9 · 2014: 5 · 2013: 4 · 2012: 8
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 685, SFB 488)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- Hydra magnipapillata, tentacles, fast synaptic transmission
- MeSH terms
- Amiloride, Amino Acid Sequence, Animals, Cloning, Molecular, Feeding Behavior, Female, Hydra, Ion Channels, Molecular Sequence Data, Nerve Tissue Proteins, Oocytes, Recombinant Proteins, Xenopus laevis, Ion Channel Gating, Sequence Homology, Amino Acid, In Situ Hybridization, Evolution, Molecular, Protein Subunits, Sodium Channel Blockers, Epithelial Sodium Channels, Degenerin Sodium Channels, In Vitro Techniques
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