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J. Biol. Chem., Vol. 282, Issue 48, 35098-35103, November 30, 2007

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A Peptide-gated Ion Channel from the Freshwater Polyp Hydra^*

Andjelko Golubovic, Anne Kuhn, Michael Williamson^¶, Hubert Kalbacher^||, Thomas W. Holstein, Cornelis J. P. Grimmelikhuijzen^¶, and Stefan Gründer¹

From the Institute of Physiology II, University of Würzburg, D-97070 Würzburg, Germany, Molecular Evolution and Genomics, Heidelberg Institute of Zoology, D-69120 Heidelberg, Germany, ^¶Department of Cell Biology and Comparative Zoology, Institute of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark, and ^||Interfakultäres Institut für Biochemie, University of Tübingen, D-72074 Tübingen, Germany

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.

Received for publication, August 16, 2007 , and in revised form, September 21, 2007.

The nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AM393879 [GenBank] , AM393878 [GenBank] , AM393880 [GenBank] , and AM393881 [GenBank] .

^* This work was supported by the Deutsche Forschungsgemeinschaft SFB 488 (to T. W. H.) and the Danish Research Agency (to C. J. P. G.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Dept. of Physiology II, Röntgenring 9, D-97070 Würzburg, Germany. Tel.: 49-931-31-6046; Fax: 49-931-31-2741; E-mail: stefan.gruender{at}uni-wuerzburg.de.

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