A peptide-gated ion channel from the freshwater polyp Hydra
Open accessAbstract
Chemical transmitters are either low molecular weight molecules or neuropeptides. As a general rule, neuropeptides activate only slow metabotropic receptors. To date, only one exception to this rule is known, the FMRFamide-activated Na(+) channel (FaNaC) from snails. Until now FaNaC has been regarded as a curiosity, and it was not known whether peptide-gated ionotropic receptors are also present in other animal groups. Nervous systems first evolved in cnidarians, which extensively use neuropeptides. Here we report cloning from the freshwater cnidarian Hydra of a novel ion channel (Hydra sodium channel, HyNaC) that is directly gated by the neuropeptides Hydra-RFamides I and II and is related to FaNaC. The cells expressing HyNaC localize to the base of the tentacles, adjacent to the neurons producing the Hydra-RFamides, suggesting that the peptides are the natural ligands for this channel. Our results suggest that neuropeptides were already used for fast transmission in ancient nervous systems.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [38]
Cites
Kellenberger, S. B., & Schild, L. (2002) · Physiological Reviews · doi:10.1152/physrev.00007.2002 · Cited by 1,017 · see citing works
Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel
Lingueglia, É., Champigny, G., Lazdunski, M., & Barbry, P. (1995) · Nature · doi:10.1038/378730a0 · Cited by 392 · see citing works
A new member of acid-sensing ion channels from pituitary gland
Gründer, S., Geissler, H.-S., Bässler, E.-L., et al. (2000) · Neuroreport · doi:10.1097/00001756-200006050-00003 · Cited by 233 · see citing works
Self-citationAskwith, C. C., Cheng, C., Ikuma, M., Benson, C. J., Price, M. P., & Welsh, M. J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81144-7 · Cited by 221 · see citing works
Gründer, S., Firsov, D., Chang, S. S., et al. (1997) · The EMBO Journal · doi:10.1093/emboj/16.5.899 · Cited by 216 · see citing works
Self-citationAntisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps
Grimmelikhuijzen, C. J. P. (1985) · Cell and Tissue Research · doi:10.1007/bf00214639 · Cited by 189 · see citing works
Self-citationPeptides in the Nervous Systems of Cnidarians: Structure, Function, and Biosynthesis
Grimmelikhuijzen, C. J. P., Leviev, I., & Carstensen, K. (1996) · International review of cytology · doi:10.1016/s0074-7696(08)61345-5 · Cited by 180 · see citing works
Self-citationAn ancient Wnt-Dickkopf antagonism inHydra
Guder, C., Pinho, S., Nacak, T. G., Schmidt, H. A., Hobmayer, B., Niehrs, C., & Holstein, T. W. (2006) · Development · doi:10.1242/dev.02265 · Cited by 171 · see citing works
Self-citationKellenberger, S. B., Gautschi, I., & Schild, L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.4170 · Cited by 144 · see citing works
On the Molecular Basis of Ion Permeation in the Epithelial Na+ Channel
Kellenberger, S. B., Hoffmann-Pochon, N., Gautschi, I., et al. (1999) · The Journal of General Physiology · doi:10.1085/jgp.114.1.13 · Cited by 128 · see citing works
Permeating protons contribute to tachyphylaxis of the acid‐sensing ion channel (ASIC) 1a
Chen, X., & Gründer, S. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.120733 · Cited by 103 · see citing works
Self-citationA Pore Segment in DEG/ENaC Na+ Channels
Snyder, P. M., Olson, D. R., & Bucher, D. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.40.28484 · Cited by 102 · see citing works
The Phe-Met-Arg-Phe-amide-activated Sodium Channel Is a Tetramer
Coscoy, S., Lingueglia, É., Lazdunski, M., & Barbry, P. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.14.8317 · Cited by 102 · see citing works
Characterization of the Selectivity Filter of the Epithelial Sodium Channel
Sheng, S., Li, J., McNulty, K. A., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.12.8572 · Cited by 90 · see citing works
A Family of Acid-sensing Ion Channels from the Zebrafish
Paukert, M., Sidi, S., Russell, C. L., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401477200 · Cited by 81 · see citing works
Ultrastructure of synapses in the first-evolved nervous systems
Westfall, J. A. (1996) · Journal of Neurocytology · doi:10.1007/bf02284838 · Cited by 78 · see citing works
Schaefer, L., 酒井, 秀., Mattéi, M., Lazdunski, M., & Lingueglia, É. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01403-4 · Cited by 77 · see citing works
Darmer, D., Hauser, F., Nothacker, H., Bosch, T. C. G., Williamson, M. P., & Grimmelikhuijzen, C. J. P. (1998) · Biochemical Journal · doi:10.1042/bj3320403 · Cited by 76 · see citing works
Self-citationCottrell, G. A., Green, K. A., & Davies, N. W. (1990) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00382698 · Cited by 71 · see citing works
Koizumi, O., Wilson, J. D., Grimmelikhuijzen, C. J. P., & Westfall, J. A. (1989) · Journal of Experimental Zoology · doi:10.1002/jez.1402490105 · Cited by 67 · see citing works
Self-citationIsolation of Four Novel Neuropeptides, the Hydra-RFamides I–IV, fromHydra magnipapillata
Moosler, A., Rinehart, K. L., & Grimmelikhuijzen, C. J. P. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1849 · Cited by 61 · see citing works
Self-citationCoexistence of neuropeptides in hydra
Grimmelikhuijzen, C. J. P. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90272-5 · Cited by 58 · see citing works
Self-citationMetazoan Evolution: Some Animals Are More Equal than Others
Raible, F., & Arendt, D. (2004) · Current Biology · doi:10.1016/j.cub.2004.01.015 · Cited by 48 · see citing works
Hansen, G. N., Williamson, M. P., & Grimmelikhuijzen, C. J. P. (2000) · Cell and Tissue Research · doi:10.1007/s004410000240 · Cited by 45 · see citing works
Self-citationEndogenous trypsin receptors in Xenopus oocytes: linkage to internal calcium stores
Schultheiß, M., Neumcke, B., & Richter, H.-P. (1997) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050104 · Cited by 33 · see citing works
Location of a ligand recognition site of FMRFamide‐gated Na+ channels
Cottrell, G. A., Jeziorski, M. C., & Green, K. A. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02081-6 · Cited by 23 · see citing works
Richardson, M. (1999) · doi:10.1002/(sici)1521-1878(199907)21:7
Flagged first, then by citations
Cited by
Sorted by citations
The phylogenetic position of ctenophores and the origin(s) of nervous systems
Jákely, G., Paps, J., & Nielsen, C. (2015) · EvoDevo · doi:10.1186/2041-9139-6-1 · Cited by 189 · see citing works
Origins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168 · see citing works
Back to the Basics: Cnidarians Start to Fire
Bosch, T. C. G., Klimovich, A., Domazet-Lošo, T., Gründer, S., Holstein, T. W., Jékely, G., Miller, D. J., Murillo-Rincon, A. P., Rentzsch, F., Richards, G. S., et al. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2016.11.005 · Cited by 144 · see citing works
Self-citationAssmann, M., Kuhn, A., Dürrnagel, S., Holstein, T. W., & Gründer, S. (2014) · BMC Biology · doi:10.1186/s12915-014-0084-2 · Cited by 70 · see citing works
Three homologous subunits form a high affinity peptide-gated ion channel in Hydra
Dürrnagel, S., Kuhn, A., Tsiairis, C. D., Williamson, M., Kalbacher, H., Grimmelikhuijzen, C. J. P., Holstein, T. W., & Gründer, S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.059998 · Cited by 58 · see citing works
Self-citation
- Authors
- Golubovic, A., Kuhn, A., Williamson, M., Kalbacher, H., Holstein, T. W., Grimmelikhuijzen, C. J. P., & Gründer, S.
- Affiliations
- University of Würzburg (DE)
- University of Copenhagen (DK)
- University of Tübingen (DE)
- Corresponding author
- Gründer, Stefan
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2007-11
- Volume
- 282
- Issue
- 48
- Pages
- 35098-35103
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2023710681
- Cited by
- 101
- References
- 27
- Citations by year
- 2025: 6 · 2024: 3 · 2023: 8 · 2022: 9 · 2021: 6 · 2020: 6 · 2019: 6 · 2018: 7 · 2017: 5 · 2016: 7 · 2015: 8 · 2014: 5 · 2013: 7 · 2012: 4
- FWCI
- 2.77
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- Hydra, neuropeptides, ligand-gated ion channels, cnidarian nervous system, nervous system evolution, fast synaptic transmission
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Hydra, Ions, Ligands, Membrane Proteins, Molecular Sequence Data, Nerve Tissue Proteins, Peptides, Phylogeny, Sodium Channels, Sequence Homology, Amino Acid, In Situ Hybridization, Rats, Acid Sensing Ion Channels
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review