Three homologous subunits form a high affinity peptide-gated ion channel in Hydra

TY - JOUR

T1 - Three homologous subunits form a high affinity peptide-gated ion channel in Hydra

AU - Dürrnagel, Stefan

AU - Kuhn, Anne

AU - Tsiairis, Charisios D

AU - Williamson, Michael

AU - Kalbacher, Hubert

AU - Grimmelikhuijzen, Cornelis J P

AU - Holstein, Thomas W

AU - Gründer, Stefan

PY - 2010/4/16

Y1 - 2010/4/16

N2 - 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.

AB - 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.

KW - Amiloride

KW - Amino Acid Sequence

KW - Animals

KW - Cloning, Molecular

KW - Epithelial Sodium Channel

KW - Evolution, Molecular

KW - Feeding Behavior

KW - Female

KW - Hydra

KW - In Situ Hybridization

KW - Ion Channel Gating

KW - Ion Channels

KW - Molecular Sequence Data

KW - Nerve Tissue Proteins

KW - Oocytes

KW - Protein Subunits

KW - Recombinant Proteins

KW - Sequence Homology, Amino Acid

KW - Sodium Channel Blockers

KW - Xenopus laevis

U2 - 10.1074/jbc.M109.059998

DO - 10.1074/jbc.M109.059998

M3 - Journal article

C2 - 20159980

SN - 0021-9258

VL - 285

SP - 11958

EP - 11965

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

IS - 16

ER -