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Cited by 36Ion channel regulation and functionMarine Invertebrate Physiology and EcologyIon Transport and Channel Regulation

Ether-à-go-go family voltage-gated K+ channels evolved in an ancestral metazoan and functionally diversified in a cnidarian–bilaterian ancestor

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Li, Xiaofan, Martinson, Alexandra S., Layden, Michael J., Diatta, Fortunay H., Sberna, Anna P., Simmons, David K., Martindale, Mark Q., Jegla, Timothy J.·2015·Journal of Experimental Biology
DOI 10.1242/jeb.110080PMC PMC4334144
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Abstract

We examined the evolutionary origins of the ether-à-go-go (EAG) family of voltage-gated K(+) channels, which have a strong influence on the excitability of neurons. The bilaterian EAG family comprises three gene subfamilies (Eag, Erg and Elk) distinguished by sequence conservation and functional properties. Searches of genome sequence indicate that EAG channels are metazoan specific, appearing first in ctenophores. However, phylogenetic analysis including two EAG family channels from the ctenophore Mnemiopsis leidyi indicates that the diversification of the Eag, Erg and Elk gene subfamilies occurred in a cnidarian/bilaterian ancestor after divergence from ctenophores. Erg channel function is highly conserved between cnidarians and mammals. Here we show that Eag and Elk channels from the sea anemone Nematostella vectensis (NvEag and NvElk) also share high functional conservation with mammalian channels. NvEag, like bilaterian Eag channels, has rapid kinetics, whereas NvElk activates at extremely hyperpolarized voltages, which is characteristic of Elk channels. Potent inhibition of voltage activation by extracellular protons is conserved between mammalian and Nematostella EAG channels. However, characteristic inhibition of voltage activation by Mg(2+) in Eag channels and Ca(2+) in Erg channels is reduced in Nematostella because of mutation of a highly conserved aspartate residue in the voltage sensor. This mutation may preserve sub-threshold activation of Nematostella Eag and Erg channels in a high divalent cation environment. mRNA in situ hybridization of EAG channels in Nematostella suggests that they are differentially expressed in distinct cell types. Most notable is the expression of NvEag in cnidocytes, a cnidarian-specific stinging cell thought to be a neuronal subtype.

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  • All three EAG subfamilies seem to have at least partially conserved molecular functions, when tested in vitro.

    “All three subfamilies seem to have at least partially conserved molecular functions, when tested in vitro [79,81].”

    From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [79]

  • Cnidocytes express one of the three subfamilies of the EAG family of voltage-gated K+ channels.

    “Interestingly, cnidocytes express one of the three subfamilies of the ether-à-go-go (EAG) family of voltage-gated K+ channels [79].”

    From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [79]

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Cited by

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Authors
Li, X., Martinson, A. S., Layden, M. J., Diatta, F. H., Sberna, A. P., Simmons, D. K., Martindale, M. Q., & Jegla, T. J.
Affiliations
  • Pennsylvania State University (US)
  • University of Florida (US)
Corresponding author
Jegla, Timothy J.
ORCID
Venue
Journal of Experimental Biology
Publisher
The Company of Biologists
Published
2015-02-15
Volume
218
Issue
4
Pages
526-536
ISSN
  • 0022-0949 (ISSN-L)
  • 1477-9145
DOI
10.1242/jeb.110080
PMC
PMC4334144
OpenAlex
W2170150201
Cited by
36
References
10
Citations by year
2026: 3 · 2025: 3 · 2024: 4 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 1 · 2016: 3 · 2015: 5
FWCI
2.17
Type
journal article
Language
en
Open access
Locations
  • Journal of Experimental Biology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation
  • National Institute of General Medical Sciences (R01GM093116)
  • National Institute of Neurological Disorders and Stroke (R01NS069842, NS069842)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Keywords
voltage-gated potassium channels, Nematostella vectensis, ctenophores, Mnemiopsis leidyi, proton inhibition, divalent cation inhibition, differential gene expression, neuronal excitability
MeSH terms
Animals, Base Sequence, Cnidaria, Phylogeny, Sea Anemones, Xenopus, In Situ Hybridization, Evolution, Molecular, Potassium Channels, Voltage-Gated

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