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Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis
Author(s) -
Schmidt Axel,
Bauknecht Philipp,
Williams Elizabeth A.,
Augustinowski Katrin,
Gründer Stefan,
Jékely Gáspár
Publication year - 2018
Publication title -
the faseb journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.709
H-Index - 277
eISSN - 1530-6860
pISSN - 0892-6638
DOI - 10.1096/fj.201800274r
Subject(s) - ionotropic effect , g protein coupled receptor , ion channel , metabotropic receptor , biology , neuropeptide , microbiology and biotechnology , signal transduction , receptor , biochemistry , glutamate receptor
ABSTRACT Neuropeptides commonly signal by metabotropic GPCRs. In some mollusks and cnidarians, RFamide neuropeptides mediate fast ionotropic signaling by peptide‐gated ion channels that belong to the DEG/ENaC family. Here we describe a neuropeptide system with a dual mode of signaling by both a peptide‐gated ion channel and a GPCR. We identified and characterized a peptide‐gated channel in the marine annelid Platynereis dumerilii that is specifically activated by Wamide myoinhibitory peptides derived from the same proneuropeptide. The myoinhibitory peptide‐gated ion channel (MGIC) belongs to the DEG/ENaC family and is paralogous to RFamidegated ion channels. Platynereis myoinhibitory peptides also activate a previously described GPCR, MAG. We measured the potency of all Wamides on both MGIC and MAG and identified peptides that preferentially activate one or the other receptor. Analysis of a single‐cell transcriptome resource indicates that MGIC and MAG signal in distinct target neurons. The identification of a Wamide‐gated ion channel suggests that peptide‐gated channels are more diverse and widespread in animals than previously appreciated. The possibility of neuropeptide signaling by both ionotropic and metabotropic receptors to different target cells in the same organism highlights an additional level of complexity in peptidergic signaling networks.—Schmidt, A., Bauknecht, P., Williams, E. A., Augustinowski, K., Gründer, S., Jekely, G. Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis . FASEB J. 32, 5338–5349 (2018). www.fasebj.org